Central Annals of Aquaculture and Research

Review Article *Corresponding author Carmen Sarasquete, Department of Biotechnology & Aquaculture, Instituto de Ciencias Marinas de Updated of the Pathologies Andalucía-ICMAN.CSIC-, 11510-Puerto Real, Cádiz, Spain, Tel: 34-956832612; Email:

Affecting Cultured Gilthead Submitted: 22 March 2017 Accepted: 12 April 2017 Seabream, Sparus aurata Published: 14 April 2017 ISSN: 2379-0881 Juan J. Borrego1, Alejandro M. Labella1, Dolores Castro1, Juan B. Copyright 2 2 Ortiz-Delgado , and Carmen Sarasquete * © 2017 Sarasquete et al. 1Departamento de Microbiología, Universidad de Málaga, Spain 2Department of Biotechnology & Aquaculture, Instituto de Ciencias Marinas de OPEN ACCESS Andalucía, Spain Keywords • Gilthead seabream Abstract • Aquaculture Among other , the gilthead seabream Sparus aurata is the most • Pathologies important species in the Mediterranean aquaculture, achieving good growth • Diseases performances and progressive increased production. However, health management • Infectious agents remains as one of the major concerns of the gilthead seabream culture, because • Skeletal disorders diseases can cause major losses to commercial crops. In suboptimal conditions of • Malformational alterations intensive rearing systems, the danger of disease outbreaks is always present. Since quarantine restrictions were rarely adopted, several microbial have been transmitted to other geographic locations, and frequently they have colonized new fish hosts and/or new environments. In this work, we have updated some of the most important and also serious pathologies and diseases that from many years ago and presently affect to reared gilthead seabream specimens, mainly those with uncertain or complex aetiology (genetic, nutritional, zootechnic, among others), such as malformations-vertebral deformities, as well as those more classical and emergent parasitic and infectious pathologies and diseases. In addition, avalaible treatment and/or prophylactic measures are also discussed.

INTRODUCTION An Gilthead seabream (Sparus aurata), a member of the family adequate aquaculture practice must also consider other matters and expansion of the ornamental fish trade to name a few [3]. Sparidae, is found in the Mediterranean Sea and extends into the Atlantic Ocean from the British Isles south to Senegal. Most that are not directly related to fish health because public concerns countries around the Mediterranean culture gilthead seabream; Thus, the environmental impacts of the culture operation, the have a significant influence on how and where fish are cultured. Greece, Turkey, and Spain are the major producers in the region, accounting for over 70% of total production. The culturing of S. welfare are other important factors taking into account to achieve safety of cutured product for human consumption, and the fish aurata has achieved impressive strides in much less than two a sustainable practice of the aquaculture [4]. Most of the diseases that cause serious problems in than 173,000 Tm in 2013 [1,2]. This success is the result of strong researchdecades, goingand development from an estimated programs 110 in Tm many of fish of thein 1985 countries, to more in fromcultured another fish are geographic provoked area. by exotic Thus, pathogens; an effective that biosecurity is, they species. However, the rapid development of gilthead seabream programmewere inadvertently is vital to introduced maintaining into healthy a region via and infected to reduce fish farmingconjuction has with not a persistently been paralleled strong by market adequate demand progress for this in fish the veterinary aspects of its culture. to the implementation of methods to prevent the spread of the risk of adquiring disease in a fish facility. Biosecurity refers Fish diseases are a primary constraint to the culture of many infectious diseases within a farm, and to avoid their transmission aquatic species, avoiding both economic and social development in producer countries. This situation can be attributed to used to maintain biosecurity are inactivation strategies to wild fish populations or to adjacent fish farms. Key methods a variety of interconnected factors such as, the increased globalization of trade in live aquatic animals and their products; and avoiding fish-to-fish transmission by mean of. geographic isolation of affected farms, separation of diseased fish, specific- In order to minimize the risks of pathogens/diseases the intensification of aquaculture through the translocation of pathogen-free stocks, and quarantine measures [5] broodstock, postlarvae, fry and fingerlings; and the development Cite this article: Borrego JJ, Labella AM, Castro D, Ortiz-Delgado JB, Sarasquete C (2017) Updated of the Pathologies Affecting Cultured Gilthead Seabream, Sparus aurata. Ann Aquac Res 4(2): 1033. Sarasquete et al. (2017) Email: Central associated with aquatic movements, there are a number in gilthead seabream is due to environmental factors. Therefore, of existing global instruments, agreements, codes of practice and environmental conditions, nutritional imbalances and genetic guidelines (International Codes) that, if implemented, provide factors or their interaction, is believed to be on the basis of most certain levels of protection. Some of the provisions in the current skeletal alterations S. aurata international protocols are not always practically applicable Interestingly, by using specimens histological, [9,10,14,17-23]. histochemistry and immunohistochemistry approaches, recently we have been regionally adopted health management programme is considered registered two types of opercular anomalies in reared gilthead ato practical the diseases approach. of concern Subasinghe to a etspecific al. [6], region. recommended Therefore, that a seabream specimens [13], which were described according to the development of standardized methods for disease diagnosis and screening of pathogens, along with regular evaluation of their effectiveness as compared with other diagnostic methods should gillclassification chamber, previouslystarting at reportedthe upper by corner Beraldo of theet al. branchial [24], Type cleft I: be a priority task. is another established, proven and the folding of the operculum (opercle and sub-opercle) into the lack of the operculum (lack of development of the opercle, in cultured marine animals. decrease the severity subopercle,and extending interopercle down to its and lower preopercle) third; and with Type a II: regression the partial of ofcost-effective disease losses, method reduce for controlling the need for certain antibiotic infectious use, leavediseases no the loose edge extending down to its lower third. The overall residues in the product and do not induce pathogen resistance. In conjunction with good health management and good husbandry opercular abnormalities unilaterally affected both sides of the practices, there is great potential for the use of technology incidence of fish with deformed operculum was 6.3%. These bilateral abnormality in the operculum only affected 1.1% of the head: the right (3.3%) and left (3.0%) equally; whereas the for specificIn this work, use in we marine have revisedaquaculture. the main infectious pathologies affecting to both wild and reared gilthead seabream; and in showed internal lesions characterised by an accentuated ventral addition, some pathologies provoked by physiological (i.e. curvaturereared fish. (lordosis) Fish with of the a severe vertebral external column. body The shape degree deformity of these nutritional disorders), not optimal or inadequate rearing or pathological symptoms varied along the vertebral column axis environmental conditions, and potential genetic factors have also been updated. Future perspectives on welfare, treatment haemal and haemal areas of the vertebral column (position 11 and prophylactic measures to improve the Mediterranean and mainly affected vertebrae located between the limit of pre- aquaculture are also discussed. lordosis was 10.1%. These histological and histopathological disordersto 15 from indicated urostyle upwards). that the reduced The incidence opercular of fish surface affected in theby Malformational and skeletal disorders Type I deformity in gilthead seabream was mainly due to the The presence of morphological abnormalities in reared folding of the edge of the opercle from the superior corner gilthead seabream is an important problem for current towards the gill chamber. The conservation of the different opercular bones that compose the operculum suggested an effect Malformations can affect different aspects of the morphology of of the rearing conditions during sensitive developmental periods, aquaculture and it entails significant economic losses. coinciding with the beginning of skeletogenesis of the opercular reducesthe fish such the as market pigmentation, value of shape, the species scales, commercializedskeleton and swim as bladder. The high incidence of some malformations significantly thecomplex, supportive which tissue is formed of the by operculum intramembranous was not yet ossification formed at from this earlya condensed developmental core of mesenchymal period, mechanical cells [24,25]. damage Considering (i.e. excessive that whole fish and implies an additional effort at farms to eliminate water movements) could cause this opercular malformation [26]. noticeableabnormal fish quantitative [7]. The variations incidence ofcan vertebral be attributed deformities, to several i.e. Nevertheless, in the opercular deformity (Type II) described in differentopercular variable anomalies zootechnnical can vary fromconditions, 6 to 80%optimization [8-14]. in These the gilthead seabream specimens [13], the coalescence between rearing procedures and feeding protocols, and the application of genetic improvement programmes (i.e. bloodstock selection fusion of the opercular structures, giving the appearance of and breeding) during the last two decades. Skeletal deformities underdevelopedopercular bone areas or incomplete might have tissue. caused These semi-rigidity opercular and disorders tissue are the most relevant malformations and they include head might be mechanically induced by forced opercular movements and vertebral column anomalies. Lack of operculum and occurring during ventilation or food ingestion processes [26], lordosis, scoliosis, kyphosis and vertebral fusions are the most although the putative involvement of nutritional factors and/or frequent skeletal anomalies in gilthead seabream, particularly in environmental pollutants should not be negleted [7]. association with inbreeding has been reported on skeleton reared fish, but also in wild populations [15]. Similarly, a slight complex, multifactorial and still not completely known. Genetic, environmental,The aetiology zootechnical of vertebral malformations and nutritional in fish factors species have is Báez et al. [14], reported inheritance of skeletal deformities been frequently associated with different or similar vertebral inabnormalities gilthead seabream, by Astorga such et as al. lack [16], of and operculum, in addition, lordosis Negrín- and vertebral fusions, among others. Nevertheless, Castro et al. [10], that vertebral deformities might appear during the notochord reported only a slight familiar association when comparing segmentationabnormalities andin various vertebral fish centrumspecies. Several differentiation authors processesindicated seabream specimens lacking operculum, but neither between [22,27]. However, others suggested that these deformities lordotics nor between normal ones and, they suggested that most are a consequence of disfunction in collagen at phenotypic variation observed for lordosis and lack of operculum notochordal and perinotochordal collagen sheets during early

Ann Aquac Res 4(1): 1033 (2017) 2/14 Sarasquete et al. (2017) Email: Central also occur later in ontogeny, for instance during the ongrowing period,development at which [28]. point However, they are many generally vertebral induced deformities by mechanical may cycle has three main phases: a parasitic feeding stage (trophont), an encysted reproductive stage (tomont), and a free-swimming or by a combination of both situations [31,32]. According to death.infective The stage dinospores (dinospore) are susceptible [41]. Damages to various of the chemotherapies gill epithelium overloads [29], or by curvature of the vertebral axis [30], [41,42],and osmoregulatory but trophonts impairmentand tomonts are more the likely resistant. causes Treatment of fish lordotic gilthead seabream specimens, a change in chondrocyte Ortiz-Delgado et al. [13], in the affected vertebral region of the calcium deposition were evidenced, suggesting that a metaplastic with 100-200 mg/L formalin for 6-9 h detaches trophonts from shiftmorphology, was involved from [33].vacuolated Furthermore, to hyper-dense, in these seabream and an increased lordotic fish, but as tomonts, they resume division after the removal of specimens, a disorganization of the intervertebral region, with acquireformalin a [41]. certain A copper degree sulfate of immunity treatment [43]. (0.75 mg/L) for 14 d is a complete loss of notochordal sheath integrity was evidenced. also effective, although toxic for juvenile fish [41]. Survivor fish irritans In addition, imbalanced cycling (proliferation vs. apoptosis) detected in deformed vertebral centra showing higher cell skin, and eyes, compromising (Class the ) physiological produced functions the “Marineof these proliferation activity, which could explain the presence of dense White Spot disease”, is a that invades the epithelium of gills, packaged chondrocytes, occupying most of the intervertebral on the skin, epithelial hyperplasia, mucus hypersecretion, skin space without vacuolization. Moreover, a higher remodelling discoloration,organs. The clinical corneal signs cloudiness, include pinhead-sized and mainly disruptionwhitish “blisters” of the process may occur in lordotic specimens, such as was evidenced gill lamellar structure and severe respiratory distress [40]. In by using chondrogenic and osteogenic immunomarkers [7,13,34]. Mediterranean cultures of S. aurata, the ciliate has been reported In general a preferential accumulation of osteocalcin in compact in Israel, Italy and Spain [44]. The life cycle of this parasite bone and notochord cells was detected in notochordal tissues of seabream specimens with deformed vertebrae. It is suggested d of growth, it leaves its , loses its cilia (protomont), encysts, that lordotic vertebrae should be more fragile that those normal andconsists starts of four dividing phases: (tomont), the first eventually is parasitic producing (trophont), up after to 2003-7 fish Awith new non-deformed type of vertebral axial structures. malformation, named haemal life span of 24 h, but their ability to infect a host decreases rapidly vertebral compression and fusion haemal VCF), was described free-swimming infectiveStudies on vaccination (theront). against Theronts Cryptocaryon have a neural and haemal processes and the compression and fusion aftervaccines 6-8 areh [45,46]. still available. ofby vertebral Lozoides bodies, et al. [35].affecting It consists the posterior of deformed part of the cartilaginous vertebral have produced interesting results [47,48], but no commercial Trichodina spp. has been observed often infesting the gills column in combination with lordosis. The early anatomical signs of reared seabream specimens and also in wild and culture of the haemal VCF consist of abnormal centrum mineralization, malformed cartilaginous neural and haemal processes and Brooklynella hostilis is a ciliate easily recognizable by its oval, developing lordotic alterations. The histological examination of sparids in Mediterranean and Atlantic areas [40,49-51]. the deformed individuals reveals that haemal VCF is preceded by B. hostilis can cause serious skin notochord abnormalities. In older animals suggests that haemal lesionsdorsoventrally [4], destroying flattened the shape, tissue by surfaceits notched of the oral hosts area, by and mean by VCF is linked to high mortality rates. its sizecytopharyngeal [52]. As a gill armature, pathogen, feeding on tissue debris, ingesting Pathologies provoked by parasitic microorganisms B. hostilis was diagnosed in cagecultured gilthead seabream in the Red Sea Parasitic diseases, also known as parasitosis, are infectious blood cells, and causing hemorrhages in the gills [52]. (or not) diseases caused or transmitted by eukaryotic organisms. [53].Microsporidiosis is a disease provoked by eukaryotic many parasitic organisms do not cause diseases. They can induce parasites belonging to the phylum . This phylum stressParasites and canimmunodepression, affect practically and all-living as a consequence organisms; secondary however, includes obligate intracellular parasites that infect a wide range of infections, pathologies and severe disorders diseases, are more and invertebrate hosts. Microsporidians have evolved an elaborate mechanism for invading animal host cells, but have otherwise greatly reduced biological complexity. Although frequentThe mostin those frequent parasited parasites fish. that affected during the last decade to reared gilthead seabream were Amyloodinium controversial, they are now known to either fall within the Fungi spp., Cryptocarion spp., Ichthyobodo spp. and Trichodina spp. the taxonomic affiliation of the Microsporidia has . longEconomic been [36,37]. In addition, these parasites are very good indicators losses were recorded in aquaculture due to microsporidian of contamination in aquatic ecosystems. In fact, high rates of or to be extremely closely related to the Fungi [54,55] the host, for example, the genus develops a special type of specimens reared under highly stressed aquatic ecosystems infection of fish [55], establishing a complex coexistence with mortality and infestations about 80% in gilthead seabream hypertrophy forming a , several of which may aggregate have been scored, with presence of inorganic and organic into a large pseudotumoral structure, the most adequate the most devasting parasitic diseases in temperate mariculture contaminants [38]. Amyloodiniosis or “ disease” is one of Mediterranean region, a microsporidian infection was described Amyloodinium ocellatum intreatment juveniles is ofthe cultured oral administration gilthead seabream of fumagillin in the [4,55]. French In coast the attributed to Glugea in[39,40]. a wide range of salinities and temperatures, a (17 to 30 protozooaºC). Its life highly adapted to , is able to infect different fish species sp. [56]. Abela et al. [57], observed lesions by Ann Aquac Res 4(1): 1033 (2017) 3/14 Sarasquete et al. (2017) Email: Central microsporidian parasites (genus Pleistophora) in the muscle of shows variable incidence and severity, possibly indicating a S. genetically based susceptibility to the disease [74], and direct aurata provoked by Microsporidium aurata was also reported by Polysporoplasma cultured gilthead seabream juveniles, and xenome-infections in sparis, has occasionally been associated with poor growth and infections in the musculature of gilthead seabream have been chronictransmission mortality, [85]. Other affecting myxosporean mainly to parasite, glomerular capillaries of Morsy et al. [58], in the Red Sea. Similar cases of microsporidian

Piscine apicomplexans, belonging to the classes Coccidea and reported in Greece [59], Italy [60], and Spain [40,61]. the kidney (glomerular disease) [86]. It was reportedEnterospora in Spain, nucleophilain the Adriatic is aSea, microsporidium and in fish farms responsible all over forGreece, an emaciative with high the intestine, swim bladder, liver, spleen, testes, kidney, gills, and prevalence during the warmest season [81,86-89]. Haematozoa, can parasitize a broad spectrum of fish cell types in syndrome observed in farmed gilthead seabream. The parasite is mainly found in the intestinal mucosa with clinical signs or chronic diseases, they may have been overlooked. However, blood [62,63]. Since coccidiosis provoked in fish subclinical and/ Several histopathological damages occur in severe infections and seabream cultured in Israel [64]. sparis and Goussia sparis thisincluding microsporidium anorexia, cachexia,is considered and a paleserious internal emerging organs threat [57]. in werehaemogregarine-like recorded in the intestine organisms of gilthead were observed seabream inin different gilthead gilthead seabream production [61]. According to Martins et al. facilities in Spain, indicating a wide distribution and a potential three applications of formalin solution (10 mL/m3 molnari d were adequate to control the disease caused by the protozoa. is another species described in gilthead seabream, detecting [90], ) for 15 inresponsibility its gastric epithelia,in mortalities with [49,65,66]. a particularly high prevalence in showed abdominal swelling, Cellular effectors (, granulocytes, phagocytes, non- ascitis, whitish feces, and with necrosis of the gut epithelial specific cytotoxic cells, and rodlet cells), and also humoral factors juveniles [67-70]. Affected fish lining. In vitro treatment with bronopol (100 mg/L for 30 min) (lysozyme, peroxidases, antiproteases, complement, and specific antibodies) seem to be the main fish immune components 100% of protomonts [71]. involved in the response against myxosporoses [91]. has demonstrated to be effective, killing 50% of theronts and Myxosporeans are endoparasites that either can reside in FlukesClass either draw or is feed comprised off the host of mostly tissues, ectoparasites causing irritation, fluxes, visceral cavities such as the gall bladder, the swim bladder, and hyperplasia,the most frequently haemorrhage encountered and anaemia. worm Furnestinia in mariculture echeneis [92]. is frequently observed on gilthead seabream in the Mediterranean intracellular parasites in the blood, in muscle, or in connective tissuethe urinary (histozoic tract (celozoic species). species) The myxozoans or can settle are includedas inter- or in three orders Malacovalvulida, Multivalvulida, and Bivalvulida [93], and they are usually presented at the distal extremities of the gill lamellae [94,95]. The rates of infestation are very low, genera Myxobolus, Ceratomyxa, Enteromyxum and Sphaerospora depending on the temperature [96], and the fish appareared to [72]. The main myxozoans that affect to fish specimens are the Sparicotyle chrysophrii is other common monogenean parasite for (Bivalvulida), genus Kudoa (Multivalvulida), and genus be in good health and no evident symptoms were exhibited [97]. activity produce severe anaemic conditions in the cold seasons not always display clinical signs; in fact, an important number culturedGyrodactylus gilthead seabream [92,94,98], and its haematophagus of myxosporidian(Malacovalvulida) parasites coexist [73,74]. with their Infected asymptomatic fish do gilthead seabream cultured in several Mediterranean regions [97]. Other monogenoideanwas found on parasites the fins detectedand body in surface gilthead of the genus Kudoa were found in the viscera of gilthead seabream seabream are the belonging to the species Encotyllabe vallei, culturedhost without in the causing Red Sea obvious [76], but damage this parasite [75]. Sporescauses typicalrelatively of Lamellodiscus[40,92]. echeneis, L. ignoratus, and Polylabris tubicirrus benign infections, one usually limited to a few individuals. However, under some particular stress conditions or when (200 mg/L, 30 min) are good methods of treatment. Eggs,[92]. highly pathogenic species (Ceratomyxa shasta, Myxobolus however,A 1-h formalin may survivetreatment the (150-200 therapies, mg/L) so that or repeated hydrogen treatments peroxide cerebralis, Tetracapsuloides bryosalmonae) are involved, may be required to disrupt these parasites. Neobenedenia melleni virulence is enhanced and expressed. General clinical signs are often emaciation, swollen abdomen, and gall bladder full of unreleased bile. Most myxozoan infections elicit only moderate theis very eggs sensitive may also to survive freshwater the treatment and, a 3-min [40]. freshwaterRecently, Chagas dip is host reactions at least during the early stages of infection, normally sufficient to free the fish from this infestation, but, although plasmodia with mature spores can later induce with mebendazole controls the monogenean infestations in the Enteromyxum leei (formely et al. [99], haveColossoma described macroporum that the supplementation. of the diet Myxidium leei) and other enteromyxosporidan parasites are one considerable [4]. of the major disease problems in marine aquaculture, since the freshwater fish Monorchis monorchis and Telosentis exiquus, comprises endoparasitic platyhelminths that require at leastClass one Digenea, intermediate such as host to complete their life cycle. In bodyinfection shape has and a chronicbloated abdomen, course. Affected and the fish extensive become necrosis anorexic of S. aurata, the parasite Bucephalus minimus has been found as and emaciated, and eventually die with a typical “knife edge” encysted larval or juvenile stages, and as free adults [100], and description of E. leei in cultured gilthead seabream from Cyprus Neobenedenia melleni has been detected on the body of gilthead [77],the intestine the parasite produces was a foul found odor. associated Following with the first morbidity report and seabream cultured in the Red Sea [101]. Acute infections by the cercariae have occasionally been observed due to severe damage In gilthead seabream, the infection in the host tissues during penetration and migration because the mortality in Israel [78], Greece [79-81], France [82], Italy [83], Spain [84], and Tunez [37]. Ann Aquac Res 4(1): 1033 (2017) 4/14 Sarasquete et al. (2017) Email: Central active feeding of the monogeneans on mucus and on epithelial are strongly required by the industry because could help reducing handling and improving welfare, but they are not enough of mucus [102,103]. Parasites often settle on or around the eyes, developed. Good animal husbandry and adequate nutrition damagingcells leads to the hemorrhage, cornea and inflammation, causing blindness and the [103,104].over-production Once are essential to prevent the development of the disease and, encysted, metacercariae do not produce further tissue damage, subsequently, the use of antibiotics. Combination of the suitable except intense melanization reaction around the cyst. Cardicola aurata were reported affected gilthead seabream in Spain, Italy, effect balance. The emerging crisis of resistance to antibiotics has ledand to available sporadic vaccinationapplication of protocols probiotics has in aS. aurata real benefit culture in [126], cost- miracidia caused clogging of the gill capillaries and severe local tissueCroatia, damage, and Greece while the [60,105]. adult individuals Massive presence could be offound eggs in andthe bacterial diseases and also inhibit the colonization of potential vessels of the renal parenchyma or in the afferent vessel of single pathogensin order to indevelop the digestive immunocompetance tract through incompetition fish to combat exclusion with gill arches [106,107]. principle. However, in general probiotics are low immunogenic A large number of copepods belonging to the families in application. Phage therapy can be described as the use of Caligidae and Ergasilidae in nature, temperature- and salinity-sensitive and cumbersome parasitize the itegument of fish [108]. bacteria. Experimental results with marine animal models have typically occurring in heavily infestations, although copepod bacteriophages to control specific pathogenic or problematic presenceGill filaments on S. can aurata be severely damaged and skin haemorrhages diseases caused by Vibrio harveyi, V. parahaeamolyticus, V. Several treatment agents have been suggested for anguillarumdemonstrated, and the V. efficacyalginolyticus of phage therapy against infectious control of copepods, including has only formaldehyde,rarely been associated organophosphate with fish mortalities [97]. insecticides, hydrogen peroxide, ivermectin, pyrethrum, carbaryl, Photobacteriosis is provoked [127-130]. by two subspecies of di ubenzuron, to name a few. However, the therapeutic dosage Photobacterium damselae, one of them P. damselae sub sp. may be toxic for the hosts, and other measures, such as exposures piscicida tofl freshwater, are applied. Family constitutes the caused the “pseudotuberculosis” that is recognized as isopods are grossly visible on skin, mouth and gills of the infected conditiongranulomatous-like characterized lesions by in conspicuousthe spleen and splenomegaly, kidney of affected and great majority of isopod parasites in fish [109]. These S.parasitic aurata highfish. mortalities This disease have develops been observed rapidly in into gilthead an acute seabream septicemic from is susceptible to the larvae of the Gnathiidae family, of which Gnathiafish, causing piscivora considerable constitutes damages a potentially [110]. dangerousIn addition, risk [111]. of the pathogenic bacteria can be vertical, through the gonadal The most common isopod affecting gilthead seabream in the Atlantic and Mediterranean areas [118,131-135]. Transmission Mediterranean are paralella [112] and C. oestroides route the bacteria is able to infect its host through the gills, the [113,114]. digestivefluids, as system well as and horizontal the skin through [131,136]. the The water other route, subspecies by this of P. damselae is P. damselae subsp. damselae (formerly Vibrio Bacterial, viral, and fungi pathologies damsela or Listonella damsela). This microorganism causes Vibrio spp. has been isolated frequently from diseased gilthead seabream in several farms around the Mediterranean skin ulcers or systemic disease in a wide range of fish, including gilthead seabream [137-140], and can also cause skin ulcers in associated with V. alginolyticus, V. parahaemolyticus, V. vulnificus, humans [141]. Antibiotics have been the first line of defense in basinV. harveyi, [115]. V. ordalii Mortalities, V. salmonicida, of cultured and gilthead V. anguillarum seabream were only a few years the pathogens acquired resistance to various 121]. Vibriosis is characterized by a systemic hemorrhagic antibiotics,fish aquaculture such to ascontrol kanamycin, photobacteriosis sulphonamide, outbreaks, tetracycline, but after septicemia. Lethargy, skin darkening, exophthalmia, anemic [40,116- gills, Efforts have been focused on gaining a better understanding of and ulcers are the typical external signs. Internally, congested theampicillin, biology chloramphenicol, of these pathogenic florfenicol, microorganisms and erythromycin with the aim[142]. of visceralpetechia blood on the vessels, skin and intestinal the base hemorrhages, of the fins, and accumulationinflammation developing effective vaccination strategies to control the disease. Conventional vaccinology has thus far yielded unsatisfactory of vibriosis [122,123]. Vibrio spp. produces a wide variety of results, and recombinant technology has been applied to identify ofproteases, ascitis fluid hemolysins, in the abdominal and other cavity extracellular are the most common that signs are new antigen candidates for the development of subunit vaccines responsible for the extensive tissue damage [124]. In advanced [142]. cases, congestion and liquefaction of the spleen, liver, and kidney Pseudomonas anguilliseptica infections have been described can also be observed. Factors such as transport stress, water in gilthead seabream [143] associated with a hemorrhagic temperature changes, handling, and low oxygen induced vibriosis in S. aurata conditionsepticaemia exclusively named “winter affecting syndrome” gilthead seabream or “winter reared disease” at are still eating. [125]. Flumequine, Treatment of oxytetracyclines, vibriosis with medicated sulfonamides feed can (+ (WD) [40] in the Mediterranean areas. WD refers to a be effective if done at the initial stage of the disease, while the fish low temperatures. The disease is considered as a multifactorial problem brought about by the physiological, metabolic, and for vibriosis treatment. Vaccination as preventive measure is the trimethoprim) and florfenicol are the main antimicrobials used immunological disturbances associated with the poor tolerance best option since its effectiveness has been demonstrated about ºC 100% during the protection period using both immersion and injection procedures. Oral formulations with good effectiveness unresolvedof this species aspects to rearing of its conditions etiology, theat temperatures recurrent isolation below of15 P. [144-148]. Although the WD is probably multifactorial with

Ann Aquac Res 4(1): 1033 (2017) 5/14 Sarasquete et al. (2017) Email: Central anguilliseptica similar epitheliocystis disease that affected to gilthead seabream included a moderate of WD-afeccted abdominal fish distension indicates and a significantkeratitis, anemia, role of reported by several authors [50,169]. Nevertheless, recently this microorganism in the disease [143,149,150]. External signs agents, such as Ichthyocystis hellenicum and I. sparus [170]. and sometimes petechial haemorrhages on skin [143]. Internally, Epthyteliocystisspecimens was associated appears to with be a seasonal intracellular disease beta-proteobacteria in Mediterranean hepaticlethargy pallor and fish and become severe darker distension and withof the the intestines typical stress are evident; bands, farmed gilthead seabream, occurring during the warmer months mortality of this disease is higher in the second stage (early epitheliocystis outbreaks have occurred in aquaculture systems usually the diseasedºC), where fish P.develop anguilliseptica meningoencephalitis. is recorded frequently The fish associatedand when juveniles with high are stocking first introduced densities, into presence seacages. of nutrients,However, springgentamycin, at 15-16 oxytetracycline, tetracycline, streptomycin or might be involved in an outbreak and since diagnosis [143,149,150]. Treatment with ciprofloxacin, erythromycin, canseason, be problematic, temperature there and fish is no age established [171]. Since treatment more than for thisone pathology. Alternative husbandry methods, such as decreasing usedtrimethoprim-sulphamethoxazole a bath treatment with extract gives of the a goodplant responseCassia alata [151- to stress factors and increasing water quality, around the time of control153]. Recently, the P. anguilliseptica Phumkhachorn infection. & Rattanachaikunsopon There are no commercial [154] outbreaks times has been recommended [172], together with vaccines available for this disease agent, although several ultraviolet irradiation of water supplies [173]. Antimicrobial therapy has been attempted in control of this microbial pathogen, using tetracycline and macrolide antimicrobials [174]. However, experimentalTenacibaculum vaccines maritimum have been tested [151,155,156]. found in seawater and formerly known as Cytophaga marina the most appropriate treatment to treat the disease or mitigate or Flexibacter marinus or F. maritimus [157] is . a It bacterium is an opportunistic commonly theSomridhivej heavy infection. et al. [175], demonstrated that water exchange was also known as pathogen responsible for “flexibacteriosis,” USA,“gliding and bacterial Japan affecting disease,” mainly “eroded to larval mouth or juvenile syndrome,” of a high and IridoviridaeLymphocystis family [176], disease which (LCD) is characterized is a well-known by hypertrophy fish viral “black patch necrosis.” Flexibacteriosis was described in Europe, infection provoked by a DNA virus (LCDV) belonging to the stressors and skin abrasions may trigger the development of the disease.variety of The fish mouthspecies. appears An increase eroded in water and hemorrhagic,temperature, various lesions of fibroblastic cells in the dermis connective tissue of affected S.fish, aurata occasionally proliferating as true epithelial tumours [177]. gill rot may develop followed rough handling during grading This viral disease affects a wide variety of fish species, including andmay other open in netting the skin, procedures fins and in tail nurseries appear frayed, [40]. The and disease foci of . Paperna et al. [178], reported for the first time the can become systemic, involving different internal organs. T. viraloccurrence disease of was LCD disseminated in gilthead seabreamto several rearedaquaculture in the nurseries red Sea, maritimum has been described in gilthead seabream associated aroundbut imported Mediterranean as fingerlings basin, from where Mediterranean the virus probably Sea. Later, become this with coinfection with monogenean gill parasites (Sparicotyle endemic, including Italy, Spain, Greece, Turkey, France, and and Furnestinia In vitro studies on the susceptibility of T. maritimum to various chemotherapeutic agents indicate showing the characteristic symptoms cannot be commercialized, that all bacterial) [158,159].strains isolated from different sources exhibit Portugal [179-186]. Although this disease is rarely fatal, fish

[160]. The administration of amoxycillin and trimethoprim causing important economic losses [179]. The main characteristic a similar pattern [158], but field results were not always similar of LCD is the appearance of small cream-coloured nodular lesions on the fish skin and fins [187,188]. Each nodule consists of an and enrofloxacine are effective antimicrobial therapies against LCDV-infected cell, named lymphocyst or lymphocystis cell, of bythis immersion, pathogen in such field as trials formalin, [158,161]. potassium An alternative permanganate, to drugs and appearance.up to 1 mm inThese diameter cellular [178]. aggregates These hypertrophied are usually whitish cells may in would be the use of surface-acting disinfectants administered occur singly or grouped in raspberry-like clusters of tumour stresshydrogen conditions, peroxide and [158]. avoiding Modifying overfeeding) husbandry decrease parameters the Lesscolour, frequently, and in heavily they have affected also fish,been lymphocysts described on may eyes, cover causing the (temperature and/or salinity, controlling fish densities, reducing exophthalmia,entire body, spreading and internally from the over gills theto the mesenteries, fins [178,182,189,190]. peritoneum there is a general agreement that a vaccine would considerably helpoccurrence to control of tencibaculosis tenacibaculosis in and fish several farms [158,162]. research programs To date, have been established [163], although at present, only one and environmentalseveral internal conditions, organs [187,190,191]. may persist LCDfor a is variable a chronic period and bacterin is commercially available to prevent turbot mortalities self-limiting disease that, depending on the host fish species caused by T. maritimum, but may not be effective in preventing of time [192]. Thus, the LCD-associated lesions may be evident for 1 year in cold-water fish, whereas they disappear after the tenacibaculosis in other fish species [164]. Other vaccine removalseveral weeks of heavily in warm-water infected individuals species [178,193]. are the only There measures is no developmentsEpitheliocystis are under is an trial infectious experimentations disease yet caused [155,165]. by the effective therapy for LCD; reduction in stocking density and the obligate intracellular bacteria Chlamydia, and it was described that can be adopted to reduce the impact of this disease [194]. The maintaining LCDV-free populations should be prioritizied in cultured gilthead seabream in Israel [166,167], in Italy [168], such as monogeneans, Trichodina and Vibrio spp. have been for sustainable aquaculture in endemic areas [195]. Vaccine and in Spain [94,169]. Co-infections with other fish pathogens, against LCDV has focused on the development of a recombinant Ann Aquac Res 4(1): 1033 (2017) 6/14 Sarasquete et al. (2017) Email: Central

plasmid DNA vaccine with a fragment of the major capsid have been achieved in recent years; and, therefore, fish farmers in Anotherprotein into experimental an expression vaccine vector using [196], encapsulated the plasmid microspheres is expressed Controlseveral Mediterranean of many serious countries infectious have diseases significativelly has been improved achieved in fish and induced a specific immune response [197-199]. throughtheir husbandry new chemicals practices with and greater vaccines, focus and now this on is fish especially welfare. administration [200]. true for bacterial diseases. However, new pathologic problems loaded with pDNA coded for LCDV showed efficacy after oral are emerging, and previously rare diseases becoming much The Viral Nervous Necrosis (VNN) or Viral Encephalopathy more prevalent; therefore, continued vigilance and solution development is required. the Nervous Necrosis Virus (NNV) belonging to the family Betanodaviridaeand Retinopathy (VER) is a viral fish disease provoked by invasive nature of the virus and its deleterious effect on tissues in the brain. Pathogenesis and retina. of Clinically, VER is related VER is to characterized the neuro- diseaseDue to interventions, the complex set such of interactions as timely diagnosis that facilitate and treatment,the spread by nervous symptoms, such as impaired coordination, loss of disease, multi-level interventions are necessary. Farm-level of balance, whirling swimming, blindness with consequent could address the host-pathogen relationship, while improved hyperexcitability in response to noise and light. Other general betweenfarm management farms, regional may address and national environment-pathogen policies, surveillance, and signschanges are in lack pigmentation, of appetite, lethargy, swim-bladder and anemia. hyperinflation, Mortality may and reporting,environment-host training, and issues. emergency To address response disease capabilities transmission are also reach 100%, in particular in larval and juvenile stages, within 1 needed. week from the onset of the neurological symptoms, depending also on the viral genotype. Chronic, asymptomatic infection of eliminate the need for antibiotics, pesticides, and other chemicals, VER is also frequent in older individuals, and it is transmitted Developing and promoting production methods that reduce or both vertically and horizontally routes. NNV has been detected environmental homeostasis is a need for a sustainable practice from gilthead seabream farmed in Greece, France and Spain, ofwhich aquaculture. can have For wide-ranging this, viral vaccines, impacts based on on human, the recombinant fish, and S aurata harbours the virus and acts as an asymptomatic carrier [206], recently it has described the [140,201-205]. Although, appear to be very promising. As this involves a transfer of genes, DNA technology and subsequently direct DNA vaccination, is available for VER, therefore control depends upon husbandry disease affects to this fish species [207,208]. No chemotherapy be addressed. Another approach showing promise is the use of there are significant issues of safety and consumer acceptance to within farms and also between different geographical areas. antigens and the subsequent development of peptide vaccines, Ozonepractices has that been prevent used tocontact avoid between or reduce naïve virus and contamination infected fish whichproteomics might and be epitope appropriate mapping against for the parasitic identification diseases. of Furthervaccine

viral proteins produced in yeast will potentially be use to haveon egg shown shell surface that immunisation [209], and virus using contaminated recombinant water viral maycoat pathogenmethods includecontrol. the use of virus-like particles or recombinant proteinbe effectively expressed sterilised in E. bycoli UV exposure [210]. Different studies New therapies using genomic tools appear to be promised, or virus-like particles expressed in eta baculovirus al. [214], showed expression that system primary or infection formalin-inactivated with an avirulent virus gene therapies. Antimicrobial peptides are also being studied as a aquabirnavirusmay be effective effectively in controlling suppressed the disease secondary [211-213]. Yamashita potentialfor example therapeutant. using dsRNA Aquaculture for disease dietsprotection are also and under RNA-i-based scrutiny infection, suggesting the use of the aquabirnavirus as a potential with respect to potential for delivery of immunostimulants and better understanding of interactions between gut microbiota, pathogens and micronutrients, including probiotic effects. immunomodulator. Recently, several DNA-based vaccines have beenOnly developed a few fungic against infections NNV [215,216]. have been reported affecting S. In short, this review has shown that there is a substantial aurata Ichthyophonus spp. causes ulcers and granulomatous lesions in internal Pathogens Management Strategies (IPMS) in S. aurata farming, organs. farmed Lesions in are Mediterranean most common basin in highly [217-219]. vascularized organs scientificand that nowadays and empirical integration base for of the all implementation the available preventive of Integrated and (spleen, kidney, heart, and liver), and the infection to have a chronic course, and prevalence seems to increase with host age treatment strategies is indispensable to fighting the diseases of not be underestimated since any effective treatment has been thisREFERENCES fish species. [220,221]. The potential infection from wild fish species should 1. Colloca F, Cerasi S. most prevalent fungi detected in cultured S. aurata in Egypt were FAO Fisheries and Aquaculture Department. Rome. speciesdevised of so far [221]., Abdel-Latif et, and al. [222], reported. that the Aspergillus Cladosporium Fusarium 2. Updated 8 February. 2005. FUTURE PERSPECTIVES FAO/STAT. Yearbooks of Fisheries and Aquaculture Statistics. Food 3. and Agriculture Organization of the United Nations, Rome, Italy. 2015. production in intensive culture of gilthead seabream in Millenium.Subasinghe Technical RP, Bondad-Reantaso Proceedings of MG, the McGladdery Conference SE.on Aquaculture MediterraneanDiseases have areas. provedMajor improvements major constraints in the understanding to efficient (Subasinghedevelopment, RP, health Bueno andP, Phillips wealth. MJ, In:Hough Aquaculture C, McGladdery in theSE, Arthur Third JR, eds.). Third Millenium, Bangkok, Thailand. 2001. of the aetiology and epidemiology of this fish species pathologies Ann Aquac Res 4(1): 1033 (2017) 7/14 Sarasquete et al. (2017) Email: Central

4. nd Ames, USA. 2010. Noga EJ. Fish Diseases: Diagnosis and Treatment, 2 Wiley-Blackwell, 21. AfonsoAquaculture. JM, Roo2006; FJ. 254: Anomal 54-64.ías morfoló heredabilidad y selecció ética y Genómica en Acuicultura (Martínez P, Figueras A, eds.). Publicacionesgicas enConsejo peces Superior cultivados: de 5. Bondad-Reantaso MG, Subasinghe RP, Arthur JR, Ogawa K, Chinabut S, Investigaciones Cientí n. In: Gen Adlard R, et al. Disease and health management in Asian aquaculture. 6. VetSubasinghe Parasitol. RP, 2005; McGladdery 132: 249-272. SE, Hill BJ. (eds.). Surveillance and zoning 22. ficas, Madrid. 2007; 213-240.

Rome, Italy. 2004. deformitiesFernandez I, in Hontoria farmed gilthead F, Ortiz-Delgado sea bream JB, ( Sparus Kotzamanis aurata Y,) fed Estevez with for aquatic animal diseases. FAO Fish. Tech. Paper No. 451. FAO, gradedA, Zambonino-Infante levels of Vitamin JL, A et enriched al. Larval rotifers performance (Brachionus and plicatilis skeletal). 7.

Boglione C, Gavaia P, Koumoundouros G, Gisbert E, Moren M, 23. Aquaculture. 2008; 283: 102-115. Fontagne S, et al. Skeletal anomalies in reared European fish larvae and juveniles. Part 1: normal and anomalous skeletogenic processes. Negrin-Baez D, Navarro A, Rodriguez-Ramilo ST,Sparus Afonso aurata JM, Zamorano L). Mar RevPaperna Aquacult. I. Swimbladder 2013; 5: S99-S120. and skeletal deformations in hatchery bred MJ. Identification of quantitative trait loci associated with the skeletal Sparus aurata deformity LSK complex in gilthead sea bream ( 8. 24. Biotecnol.Beraldo P, 2016; Pinosa 18: M, 98-106. Tibaldi E, Canavese B. Abnormalities of the . J Fish Biol. 1978; 12: 109-114. operculum in gilthead sea bream (Sparus aurata in larval, juvenile and adult stages of cultured gilthead sea bream 9. Andrades JA, Becerra J, Fernandez-Llebrez P. Skeletal deformities (Sparus aurata L. ): morphological 10. í í description. Aquaculture. 2003; 220: 89-99. ). Aquaculture. 1996; 141: 1-11. The opercular complex deformity in intensive gilthead sea bream Cortés LA, et al. Heritability of skeleton abnormalities (lordosis, lack 25. (KoumoundourosSparus aurata L. ) G,larviculture. Oran G, Divanach Moment of P, apparition Stefanakis and S, Kentouridescription. M. ofCastro operculum) J, Pino-Querido in gilthead A, Hermida sea bream M, Chavarr (Sparusas aurata D, Romero) supported R, Garc bya-

26. 11. Aquaculture. 1997; 156: 165-177. microsatellite family data. Aquaculture. 2008; 279: 18-22. Musetti R, et al. A preliminary histological and ultrastructural study Galeotti M, Beraldo P, de Dominis S, D’Angelo L, Ballestrazzi R, Koumoundouros G. Morpho-anatomical abnormalities in of opercular anomalies in gilthead sea bream larvae (Sparus aurata). Mediterranean marine aquaculture. In: Recent Advances in Aquaculture Research (Koumoundouros G, ed.). Transworld Research 27. Fish Physiol Biochem. 2000; 22: 151-157. 12. Network,Prestinicola Kerala, L, Boglione India. 2010;C, Makridis 125-148. P, Spanò A, Rimatori V, Palamara E, et al. Environmental conditioning of skeletal anomalies typology and Haga Y, Dominique III VJ, Du SJ. Analyzing notochord segmentation frequency in gilthead sea bream (Sparus aurata L., and intervertebral disc formation using the twhh:gfp transgenic zebrafishSantamar ímodel.a JA, Andrades Transgenic JA, HerrRes. 2009;áez P, 18:Fern 669-683.á 1758) juveniles. J. Perinotochordal connective sheet of gilthead sea bream larvae 13. ández I, Sarasquete C, Gisbert E. Normal and PlosOne. 2013; 8: e55736. 28. (Sparus aurata, ndez-Llebrez P, Becerra histopathological organization of the opercular bone and vertebrae in Ortiz-Delgado JB, Fern gilthead sea bream Sparus aurata L.) affected by axial malformations: An histochemical 14. and immunocytochemical study. Anat Rec. 1994; 240: 248-254. . Aquat Biol. 2014; 21: 67-84. Lordotic vertebrae in sea bass (Dicentrarchus labrax L.) are adapted Zamorano MJ. Inheritance of skeletal deformities in gilthead sea 29. Kranenbarg S, Waarsing JH, Muller M, Weinans H, van Leeuwen JL. breamNegrin-Baez (Sparus D, aurata Navarro) – lack A, of Lee-Montero operculum, lordosis, I, Soula vertebral M, Afonso fusion JM, 30. to increased loads. J Biomechanics. 2005; 38: 1239-1246.

and LSK complex. J Anim Sci. 2015; 93: 53-61. typeGorman spinal KF, curvature Handrigan in GR,the Jincurveback G, Wallis guppy R, Breden model. F. Scoliosis. Structural 2010; and micro-anatomical changes in vertebrae associated with idiopathic- 15. breamAfonso (JM,Sparus Montero aurata D,) Robainawith family L, Astorga structure. N, IzquierdoFish Physiol MS, Biochem. Gines R. Association of a lordosis-scoliosis-kyphosis deformity in gilthead sea 31. 5: 10. abnormalities of the vertebral column and caudal skeleton in 16. 2000; 22: 159-163. Gavaia PJ, Dinis MT, Cancela ML. Osteological developmentSolea and Aguilera C, et al. Genetic effect of the type of cross and consanguinity Astorga N, Valencia A, Fenández-Palacios H, Montero D, Zamorano MJ, senegalensis level in spawning quality of gilthead sea bream (Sparus aurata L.). larval and juvenile stages of hatchery-reared Senegal sole ( Genet Aquaculture. 2003; 32. ). Aquaculture. 2002; 211: 305-323. 17. VIII: 86. inCardeira Senegalese J, Bensimon-Brito sole (Solea senegalensis A, Pousao-Ferreira P, Cancela ML, Gavaia PJ. Lordotic-kyphotic vertebrae develop ectopic cartilage-like tissue Koumoundouros G, Gagliardi F, Divanach P, Boglione C, Cataudella S, 463. Sparus aurata L. ). J Appl Ichthyol. 2012; 28: 460- Kentouri M. Normal and abnormal osteological development of caudal 33. Boglione C, Gisbert E, Gavaia P, Witten PE, Moren M, Fontagne S, et al. fin in fry. Aquaculture. 1997; 149: 215-226. 18. Faustino M, Power DM. Development of osteological structures in the Skeletal anomalies in reared European fish larvae and juveniles. Part sea bream: vertebral column and caudal fin complex. J Fish Biol. 1998; 2: main typologies, occurrences and causative factors. Rev Aquacult. 52: 11-22. 34. Osteological development of the vertebral column and of the 2013; 5: S121-S167. effects on vertebral bone tissue homeostasis in gilthead sea bream 19. SfakianakisPagellus DG, erythrinus Koumoundouros G, Divanach P, Kentouri M. (FernandezSparus aurata I, Ortiz-Delgado JB, Sarasquete C, Gisbert E. Vitamine A fins in (L. 1758). Temperature effect on the Aquaculture. 2004; ) juveniles. J Appl Ichthyol. 2012; 28: 419-426. developmental plasticity and morpho-anatomical abnormalities. G. A new type of lordosis and vertebral body compression in Gilthead 20. 232: 407-424. 35. seaLozoides bream, M, Sparus Georgiau aurata AN, L Somarakis S, Witten PE, Koumoundouros Sfakianakis DG, Georgakopoulou E, Papadakis IE, Divanach P, Kentouri lordosis in European sea bass, Dicentrarchus labrax : aetiology, anatomy and consequences for M, Koumoundouros G. Environmental determinants of haemal survival. J Fish Dis. 2014; 37: 949-957. (Linnaeus, 1758). Ann Aquac Res 4(1): 1033 (2017) 8/14 Sarasquete et al. (2017) Email: Central

36. Sparus aurata in Paperna I, Baudin-Laurencin F. Parasitic infections in sea bass, 54. Dykova I. Phylum Microspora. In: Fish Diseases and Disorders, Vol. Dicentrarchus labrax and gilthead sea bream 1, Protozoan and Metazoan Infections (Woo PTK, ed.), 2nd Ed. CAB 37. Bahrimariculture S. Protozoan facilities andin France. myxozoan Aquaculture. infections 1979; in wild16: 173-175. gilthead sea International, Wallingford, Oxon, UK. 2006, pp. 205-229. bream (Sparus aurata L.) from North Lake of Tunis, Tunisia. Acta 55. Lom J. Microsporidia. In: Fish Diseases, Vol. 1 (Eiras JC, Segner H, Wahli T, Kapoor BG, eds.). Science Publishers, Enfield, USA. 2008; 351-395. Parasitol.Sarasquete 2012; C, Borrega 57: 114-121. B, Robles R, Núñez R, Bermú JB, et al. Parásitos como bioindicadores de calidad y salud en cultivos 56. Mathieu-Daude F, Faye N, Coste F, Manier JF, Marques A, Bouix G. 38. dez L, Ortiz-Delgadoías Occurrence of a microsporidiosis in marine cultured gilt-head bream branquiales en dorada, Sparus aurata from the Languedoc coast: a problem of specificity in the genus Glugea semiintensivos en esteros. Diagnosis y prognosis de histopatolog (Protozoa, Microspora). Bull Eur Assoc Fish Pathol. 1992; 12: 67-70. y lubina, Dicentrarchus labrax. histozoic microsporidian (Protozoa, Microspora) in cultured gilt head 57. Abela M, Brinch-Iversen J, Tanti J, Le Breton A. Occurrence of a new ActasBarbaro Cong A, Nac Francescon Acuicultura. A. 2013; Parassitosi 320-323. da Amyloodinium ocellatum sea bream Sparus aurata L. Sparus aurata allevate in un impiante di 39. Bull Eur Assoc Fish Pathol. 1996; 16: 196- (Dinophycea) su larve di 199. 40. riproduzione artificiale. Oebalia. 1985; 11: 2. Biology and Aquaculture of Gilthead Sea Bream and other Species 58. MicrosporidiumMorsy K, Bashtar aurataAR, Abdel-Ghaffar nov. sp., parasite F, Al-Quraishy of the S. gilthead Morphological sea bream and Colorni A, Padros F. Diseases and health management. In: Sparidae: Sparusphylogenetic aurata description of a new xenoma-inducing microsporidian,

(Pavlidis MA, Mylonas CC, eds.). Wiley-Blackwell, Oxford. 2011; 321- Athanassopoulou from F. the A Red case Sea. report Parasitol of Pleistophora Res. 2013; 112: sp. infection3905-3915. in 41. 357.Paperna I. cycle and tolerance to temperature and cultured sea bream (Sparus aurata L.) in Greece. Bull Eur Assoc Fish salinity of Amyloodinium ocellatum 59.

(Brown, 1931) (Dinoflagellida). 60. Pathol. 1998; 18: 9-21. 42. LawlerAnnal Parasitol AR. Studies Hum onComp. Amyloodinium 1984; 59: 7-30. ocellatum parasitological survey of European sea bass (Dicentrarchus labrax) andFioravanti gilthead M, sea Caffara bream M, (Sparus Florio aurata D, Gustinelli) cultured A, in Italy.Marcer Vet F. Res A (Dinoflagellata) in Mississippi Sound: natural and experimental hosts. Gulf Res Rep. 43. 1980; 6: 403-413. 61. Comm. 2006; 30: 249-252.

AmyloodiniumCobb CS, Levy ocellatum MG, Noga EJ. Development of immunity by the EnterosporaPalenzuela O, nucleophila Redondo MJ,n. sp., Cali causing A, Takvorian an emaciative PM, Alonso-Naveiro syndrome in a tomato clownfish Amphiprion frenatus to the dinoflagellate parasite piscineM, Alvarez-Pellitero host (Sparus aurata P, et ), al. prompts A new the intranuclear redescription microsporidium, of the family 44. . J Aquat Anim Hlth. 1998; 10: 259-263. like ciliate from the Mediterranean Sea. Bull Eur Assoc Fish Pathol. Diamant A, Issar G, Colorni A, Paperna I. A pathogenic Cryptocaryon- 62. Enterocytozoonidae. Int J Parasitol. 2014; 44: 189-203. 1991; 11: 122-124. Cryptocaryon Davies AJ, Ball SJ. The biology of fish . Adv Parasitol. 1993; 32: irritans 63. 294-366. 45. Yoshinaga T, Dickerson HW. Laboratory propagation of Brown, 1951 on saltwater-adapted black mollies Poecilia Steinhagen D, Davies AJ. Diseases caused by Apicomplexans. In: 46. latipinna. J Aquat Anim Hlth. 1994; 6: 197-201. Fish Diseases, (Eiras JC, Segner H, Wahli T, Kapoor BG, eds.). Science the development of Cryptocaryon irritans 64. Publishers,Paperna I. Sporozoan Enfield, USA. infection 2008; 1:in 517-567. cultured Sparus aurata L. and wild Diggles BK, Lester RJG. Influence of temperature and host species on 47. . J Parasitol. 1996; 82: 45-51. confers protection against a protozoan parasite, Cryptocaryon irritans. Siganus luridus. Annal Parasitol Hum Comp. 1979; 54: 385-392. Yambo AV, Song YL. Immunization of grouper, Epinephelus coioides, 65. fromAlvarez-Pellitero the intestine P, Palenzuela of gilthead O, sea Sitja-Bobadilla bream Sparus A. Ultrastructure aurata L. and Aquaculture. 2006; 260: 1-9. cytochemistry study of Eimeria sparis (Protozoa: ) stages immunogenicity of theronts, tomonts and trophonts of Cryptocaryon (Pisces: 48. Bai JS, Xie MQ, Zhu XQ, Dan XM, Li AX. Comparative studies on the irritans 66. Teleostei). Parasitol Res. 1997; 83: 126-136. description of Eimeria sparis sp. nov. and Goussia sparis sp. nov. in grouper. Parasitol Res. 2008; 102: 307-313. Sitja-Bobadilla A, Palenzuela O, Alvarez-PelliteroSparus aurata L. P. Light microscopic O. Protozoan parasites of gilthead sea bream, Sparus aurata L., from 49. Alvarez-Pellitero P, Sitja-Bobadilla A, Franco-Sierra A, Palenzuela (Protozoa: Apicomplexa) from (Pisces: Teleostei). 67. Parasitol Res. 1996; 82: 323-332. different culture systems in Spain. J Fish Dis. 1995; 18: 105-115. Alvarez-Pellitero P, Sitja-Bobadilla A. Cryptosporidium molnari n. 50. Cruz-Silva MP, Freitas MS, Orge ML. Co-infection by monogenetic species, Sparus aurata L. and Dicentrarchus labrax L. Int J Parasitol. sp. (Apicomplexa: Cryptosporidiidae) infection in two marine fish trematodes of the genus Microcotyle V. Beneden & Hesse 1863, Lamellodiscus ignoratus Palombi, 1943, the protozoan Trichodina Sparus aurata 2002; 32: 1007-1021. sp.L. Ehrenberg, 1838 and the presence of epitheliocystis, Vibrio alginolyticus and V. vulnificus in cultured sea bream ( 68. seaSitja-Bobadilla bream (Sparus A, Alvarez-Pelliteroaurata L.) and European P. Experimental sea bass ( Dicentrarchus transmission ) in Portugal. Bull Eur Assoc Fish Pathol. 1997; 17: 40-42. labraxof Cryptosporidium L. molnari (Apicomplexa: Coccidia) to gilthead 51. Mladineo I. Parasite communities of Adriatic cage-reared fish. Dis ). Parasitol Res. 2003; 91: 209-214. Aquat Org. 2005; 64: 77-83. Epidemiology of Cryptosporidium molnari in Spanish gilthead sea Aquaculture and Fisheries Science. Elsevier, Amsterdam, Holland. 69. Sitja-Bobadilla A, Padros F, Aguilera C, Alvarez-Pellitero P. 52. Lom J, Dykova I. Protozoan parasites of . Developments in bream (Sparus aurata L.) and European sea bass (Dicentrarchus labrax L. 1992; 26. Brooklynella hostilis (Hartmannulidae), a pathogenic ciliate from the gills of maricultured sea bream. Bull Eur Assoc Fish ) cultures: from hatchery to market size. Appl Environ Microbiol. 53. Diamant A. 70. 2005; 71: 131-139. Sitja-Bobadilla A, Pujalte MJ, Macian MC, Pascual J, Alvarez-Pellitero P, Pathol. 1998; 18: 33-36. Ann Aquac Res 4(1): 1033 (2017) 9/14 Sarasquete et al. (2017) Email: Central

Garay E. Interactions between bacteria and Cryptosporidium molnari in gilthead sea bream (Sparus aurata) under farm and laboratory Interactions and Pathogen Exchange Between Farmed and Wild 89. Athanassopoulou F. Myxosporean parasites. In: Review of Disease

71. conditions. Vet Parasitol. 2006; 142: 248-259. Finfish and Shellfish in Europe (DIPNET) (Raynard R, Wahli T, Vatsos I,Martins Mortensen ML, deS, eds.).Souza VESO VN, de Publishers, Moraes JRE, Oslo, de Norway. Moraes FR.2007; Gill 287-293. infection IchthyophthiriusShinn AP, Picon-Camacho multifiliis SM, Bron JE, Conway D, Yoon GH, Guo FC, et al. The anti-protozoal activity of bronopol on the key life-stages of 90. Anostomidae) by Henneguya leporinicola Fouquet, 1876 (Ciliophora). Vet Parasitol. of Leporinus macrocephalus (Garavello & Britski, 1988 Osteichthyes: 72. 2012; 186: 229-236. n. sp. (Myxozoa: of Animal Parasites, 2nd Ed. Cambridge University Park, Cambridge. Myxobolidae). Description, histopathology and treatment. Rev Bras Goater TM, Goater CP, Esch GW. Parasitism: The Diversity and Ecology 2014. Biol. 1999; 59: 527-534. 73. 91. Sijta-Bobadilla A. Fish immune response to Myxozoan parasites. Bivalvulida) infection in cultured gilt head sea bream, Sparus aurata Parasite.Strona G, 2008;Stefani 15: F, Galli420-425. P. Monogenoidean parasites of Italian marine Sitja-BobadillaL. A, Alvarez-Pellitero P. Sphaerospora (: 92. 74. Palenzuela: a preliminary O. Myxozoan report. J Fish infections Dis. 1992; in 15: Mediterranean 339-343. mariculture. fish:Papoutsoglou An updated S, checklist. Costello Ital MJ, J Zool. Stamou 2010; E, 77: Tziha 417-439. G. Environmental

93. bass, Dicentrarchus labrax Sparus aurata Parassitologia. 2006; 48: 27-29. L.conditions, at sea-cages, and ectoparasites on farmed European sea- due to Henneguya sp. (Myxozoa, Myxosporea) in gilthead sea bream (L.) and gilt-head sea-bream, 75. Caffara M, Marcer F, Florio D, Quaglio F, Fioravanti ML. Heart infection (Sparus aurata Padros at two F, farms Crespo in Greece. S. Proliferative Aquacult Res. epitheliocystis 1996; 27: 25-34. associated with monogenean infection in juvenile sea bream Sparus aurata in the ) cultured in Italy. Bull Eur Assoc Fish Pathol. 2003; 23: 94. 76. 108-112. of cultured Sparus aurata L. NorthVagianou East SF, of AthanassopoulouSpain. Bull Eur Assoc F, Ragias Fish Pathol. V. Prevalence 1995; 15: and 42-44. pathology Paperna I. Kudoa infection in the glomeruli, mesentery and peritoneum 77. J Fish Dis. 1982; 5: 539-543. 95. environmental and aquaculture conditions in Greece. J Hell Vet Med in cultured gilthead sea bream Sparus aurata L. Bull Eur Assoc Fish of ectoparasites of Mediterranean fish, reared under three different Diamant A. A new pathogenic histozoic Myxidium (Myxosporea) Soc. 2004; 55: 203-216. Pathol. 1992; 12: 64-66. myxosporean of cultured sea bream Sparus aurata. 96. Antonelli L, Quilichini Y, Marchand B. Sparicotyle chrysophril (Van 78. Diamant A, Lom J, Dykova I. Myxidium leei n. sp., a pathogenic of cultured Gilthead sea bream Sparus aurata Beneden and Hesse 1863) (Monogenea: Polypisthocotylea) parasite Dis Aquat Org. (Linnaeus 1758) (Pisces: 1994;Le Breton 20: 137-141.A, Marques A. Occurrence of a histozoic Myxidium infection Teleostei) from Corsica: ecological and morphological study. Parasitol 79. Res. 2010; 107: 389-398. Sparus aurata with in two marine cultured species: Puntazzo puntazzo C. and Pagrus 97. Schembri, R. Pathological findings in farmed major. Bull Eur Assoc Fish Pathol. 1995; 15: 210-212. special attention to parasites of the gills, fins and skin. Master Thesis, 80. Athanassopoulou F, Prapas T, Rodger H. Diseases of Puntazzo UniversitySanz F. Mortality of Malta. of cultured2015. sea bream (Sparus aurata) caused by an puntazzo Cuvier in marine aquaculture systems in Greece. J Fish Dis. infection with a trematode of the genus Microcotyle. Bull Eur Assoc 98. 1999; 22: 215-218. 81. Rigos G, Christophilogiannis P, Yiagnisi M, Andriopoulou A, FishChagas Pathol. EC, de 1992; Araú 12: 186-188. Koutsodimou M, Nengas I, et al. Myxosporean infections in Greek et al. Mebendazole dietary supplementation controls Monogenoidea 99. jo LD, Martins ML, Gomes LC, Malta JCO, Varella AB, mariculture. Aquacult Int. 1999; 7: 361-364. Colossoma macroponum 82. éelevagesSakiti N, Tarer du daurade, V, Jacquemin Sparus D, aurataMarques. Annal A. Présence Sci Nat en Zool Méditerranée Biol Anim. (Platyhelminthes: Dactylogyridae) and does not alter the physiology occidentale d’une Mixosporidie histozoique pathogène dans les of the freshewater fish (Cuvier 1818). 100.Aquaculture. 2016; 464: 185-189. 1996; 17: 123-127. (Platyhelminthes) from lagoons of the northern coast of the Western Bartoli P, Gibson DI. Synopsis of the life cycles of Digenea 83. Fioravanti ML, Caffara M, Florio D, Gustinelli A, Marcer F, Quaglio F. Parasitic diseases of marine fish: epidemiological and sanitary 101. Mediterranean.Colorni A. HyperparasitismJ Nat Hist. 2007; 41: of1553-1570. Amyloodinium ocellatum considerations. Parassitologia. 2006; 48: 15-18. Neobenedenia melleni 84. Alvarez-Pellitero P, Sitja-Bobadilla A. Pathology of myxosporea in (Dinoflagellida: Oodinidae) on (Monogenea: marine fish culture. Dis Aquat Org. 1993; 17: 229-238. 102. Capsalidae). Dis Aquat Org. 1994; 19: 157-159. 85. Diamant A. Fish-to-fish transmission of a marine myxosporean. Dis Paperna I. Diseases caused by parasites in the aquaculture of warm Aquat Org. 1997; 30: 99-105. 103. water fish. Ann Rev Fish Dis. 1991; 1: 155-194. disease associated with Polysporoplasma sparis (Myxozoa) infections 86. Palenzuela O, Alvarez-Pellitero Sparus P, Sitja-Bobadilla aurata L. A. Glomerular Egusa S. Infectious Diseases of Fish. AA Balkema Publications, 104. Rotterdam, Colorni A. Pathobiology Holland. 1992. of marine organisms cultured in the tropics. in cultured gilt-head sea bream, (Pisces: Teleostei). Parasitology. 1999; 118: 245-256. description of Polysporoplasma n.g. (Myxosporea), In: Tropical Mariculture (De Silva SS, ed.). Academic Press, San Polysporoplasma 87. Sitja-Bobadilla n.s. and A, Alvarez-Pellitero P. Lightn. sp. and from electron microscopic Eur J Diego, USA. 1998; 209-255. sparis Polysporoplasma mugilis Liza aurata L. et Recherches, Options Mediterrané 105. JL,Alvarez-Pellitero Basurco B, Berthe P. Report F, Toranzo about AE, fish eds.). parasitic CIHEAM/FAO, diseases. In:Zaragoza. Etudes ennes (Alvarez-Pellitero P, Barja Parasitol. 1995; 31: 77-89. 88. Mladineo I. Myxosporidean infections in Adriatic cage-reared fish. Bull 106. Spain. Padros 2004; F, Zarza 103-130. C, Crespo S. Histopathology of cultured sea bream Eur Assoc Fish Pathol. 2003; 23: 113-123. Ann Aquac Res 4(1): 1033 (2017) 10/14 Sarasquete et al. (2017) Email: Central

Sparus aurata

infected with sanguinicolid trematodes. Dis Aquat 123. Microbiol. 1996; 62: 3650-3654. 107. Org. 2001; 44: 47-52. characterisation and phylogenetic positioning of a new sanguinicolid Rigos G, Grigorakis K, Nengas I, Christophilogiannis P, Yiagnisi M, Holzer AS, Montero FE, Repulles-Albelda A, Sparus Raga JA.aurata Morphological L. culture. Koutsodimou M, et al. Stress-related pathology seems a significant obstacle for the intensive farming of common dentex, Dentex dentex blood fluke, a pathogen in Mediterranean 124. (Linnaeus). Bull Eur Assoc Fish Pathol. 1998; 18: 15-18. Eur Assoc Fish Pathol, 13th Int Conf Fish Shellfish Dis. Grado, Italy. Hjeltnes B, Roberts RJ. Vibriosis. In: Bacterial Diseases of Fish (Inglis 2007; 179. of impact of parasitic copepods on marine aquaculture. Zool Etud. V, Roberts RJ, Bromage NR, eds.). Halsted Press, New York. USA. 108. Johnson SC, Treasurer JW, Bravo S, Nagasawa K, Kabata Z. A review 1993; Akayh 109-121. T, Timur G. Vibriosis in gilthead sea bream (Sparus aurata L.) in farms in the Aegean Sea cost of Turkey. Turkish J Fish Aquat Sci. 125. 2004; 43: 229-243. treatments for parasitic diseases in Mediterranean aquaculture. 109. Athanassopoulou F, Bitchava K, Pappas IS. An overview of the 126. 2002; 2: 89-91. Monospecies and multispecies probiotic formulations produce Aquaculture (Rogers C, Basurco B, eds.). CIHEAM Options different Salinas I, systemicAbelli L, Bertoni and local F, Picchietti immunostimulatory S, Roque A, Furons effects D, in et the al. MediterranIn: The Useé of Veterinary Drugs and Vaccines in Mediterranean gilthead sea bream (Sparus aurata L. 110. ennes, Serie A, Zaragoza, Spain. 2009; 65-83. ). Fish Shellf Immunol. 2008; Khalil RH, Saad TT, El-Hamid TMA. Some studies on parasitic 127. 25: 114-123. infestations in some marine water fish with special reference on of Vibrio harveyi bacteriophage with a potential for biocontrol of Vinod MG, Shivu MM, Umesha KR, Rajeeva BC, Krohne G. Isolation 111. . J Arab Aquacult Soc. 2014; 9: 75-88. luminous vibriosis in hatchery environments. Aquaculture. 2006; of the Northern Red Sea, the Bitter Lakes and the Eastern Mediterranean Paperna I, Por and FD. Preliminarythe Biology data of Gnathia on the piscivora Gnathiidae n. (Isopoda) sp. Rapp

Comm Int Expl Scient Mer Mé 255: 117-124. 128. Pereira C, Silva YS, Santos AL, Cunha A, Gomes NCM, Almeida A. 112. Papapanagiotou EP, Trillesdit. JP. 1977; Cymothoid 24: 195-197. parasite Ceratothoa Sparus Bacteriophages with potential for inactivation of fish pathogenic aurata bacteria: Survival, host specificity and effect on bacterial community parallela inflicts great losses on cultured gilthead sea bream structure. Mar Drugs. 2011; 9: 2236-2237. Phage 113. Sarusic in G. Greece. Preliminary Dis Aquat report Org. of 2001; infestation 45: 237-239. by isopod Ceratothoa therapy as an approach to prevent Vibrio anguillarum infections in 129. Silva YL, Costa L, Pereira C, Mateus C, Cunha A, Calado R, et al.

oestroides (Risso, 1826), in marine cultured fish. Bull Eur Assoc Fish 130. fish larvae production. Plos One. 2014; 9: e114197. 114. Pathol. Mladineo 1999; I. Life 19: cycle 110-112. of Ceratothoa oestroides, a cymothoid isopod characterization of two lytic bacteriophages, St2 and Grn1; phage Sparus therapyKalatzis application PG, Bastias for R,biological Kokkari control C, Katharios of Vibrio P. alginolyticus Isolation and in aurata φ φ parasite from sea bass Dicentrarchus labrax and sea bream Balebona. Dis Aquat MC, Mori Org.ñ 2003;igo MA, 57: 97-101. Borrego JJ. Role of extracellular 131. aquaculture Magariñ live feeds. Plos One. 2016; 11: e0151101. gilthead sea bream and turbot to Pasteurella piscicida infection by 115. sea bream (Sparus aurata os B, Toranzo AE, Romalde JL. Different susceptibility of products in the pathogenicity of Vibrio strainson cultured gilt-head 116. Colorni A, Paperna I, Gordin). Microbiologia H. Bacterial SEM.infections 1995; in 11: gilthead 439-446. sea 132. theMagari waterños route. B, Couso Bull Eur N, Assoc Noya M,Fish Merino Pathol. P, 1995; Toranzo 15: 88-90. AE, Lamas J. bream Sparus aurata Effect of temperature on the development of pasteurellosis in carrier 267. gilthead sea bream (Sparus aurata cultured at Elat. Aquaculture. 1981; 23: 257- 117. Balebona MC, Andreu MJ, Bordas MA, Zorrilla I, Moriñigo MA, 133. ). Aquaculture. 2001; 195: 17-21. Borrego JJ. Pathogenicity of Vibrio alginolyticus for cultured gilthead Photobacterium damselae ssp. piscicida sea bream (Sparus aurata L. Kvitt H, Ucko M, Colorni A, Batargias C, Zlotkin A, Knibb W. : detection by direct ). Appl Environ. Microbiol. 1998; 64: amplification of 16S rRNA gene sequences and genotypic variation 4269-4275. Balebona MC, Zorrilla I, Moriñigo MA, Borrego JJ. Survey of bacterial as determined by amplified fragment length polymorphism (AFLP). pathogens affecting farmed gilthead sea bream (Sparus aurata L.) 134. Dis Aquat Org. 2002; 48: 187-195. 118. Vatsos I. Photobacterium damselae subsp. piscicida. In: Review of in southwestern Spain from 1990 to 1996. Aquaculture. 1998; 166: VatsosDisease I, Interactions Mortensen S,and eds.). Pathogen VESO Publishers,Exchange between Oslo, Norway. Farmed 2007; and 19-35. Wild Finfish and Shellfish in Europe (DIPNET) (Raynard R, Wahli T, 119. Company R, Sitja-Bobadilla A, Pujalte MJ, Garay E, Alvarez-Pellitero 256-259. Essam HM, Abdellrazeq GS, Tayel SI, Torky HA, Fadel AH. P, Perez-Sanchez J. Bacterial and parasitic pathogens in cultured Pathogenesis of Photobacterium damselae subspecies infections in 120. common dentex, Dentex dentex L. J Fish Dis. 1999; 22: 299-309. 135. Kissil GW, Tandler A, Elizur A, Colorni A, Zohar Y. Gilthead sea bream 136. sea Romalde bass and JL, sea Magari bream.ñ osMicrob B, LoresPathog. F, 2016; Osorio 99: CR,41-50. Toranzo AE. culture. In: Encyclopedia of Aquaculture (Stickney R, ed.). John Wiley 121. & Haldar Sons, Inc., S, MaharajanNew York. USA. A, Chatterjee 2000; 408-416. S, Hunter SA, Chowdhury N, Assessment of a magnetic bead-EIA based kit for rapid diagnosis of bacterium for a tail rot disease of sea bream Sparus aurata from 137. fish Fouz pasteurellosis. B, Toranzo J AE,Microbiol Milan Meth. M, Amaro 1999; 38: C. Evidence147-154. that water Hinenoya A, et al. Identification of Vibrio harveyi as a causative

122. research Bordas hatchery MA, Balebona in Malta. MC, Microbiol Zorrilla Res. I, Borrego 2010; 165: JJ, Mori639-648.ñigo MA. transmits the disease caused by the fish pathogen Photobacterium damselae Vera P, Navas subsp. JI, damselae. Fouz B. First J Appl isolation Microbiol. of Vibrio 2000; damsela 88: 531-535. from sea skin mucus of gilthead sea bream (Sparus aurata L.). Appl Environ. bream (Sparus aurata Kinetics of adhesion of selected fish-pathogenic Vibrio strains to 138. ). Bull Eur Assoc Fish Pathol. 1991; 11: 112- Ann Aquac Res 4(1): 1033 (2017) 11/14 Sarasquete et al. (2017) Email: Central

113. Romalde JL, Ravelo C, Ló ño R, Magariños B, Toranzo AE. Vaccination strategies to prevent emerging diseases for 155. pez-Romalde S, Avenda S, et al. First isolation of Photobacterium damselae ssp. damselae 139. Labella A, Vida M, Alonso MC, Infante C, Cardenas S, Lopez-Romalde from cultured redbanded sea bream, Pagrus auriga Valenciennes, in Spanish aquaculture. Dev Biol. 2005; 121: 85-95. Pseudomonas anguilliseptica vaccine on immune gene expression 156. Jang YH, Subramanian D, Heo MS. EfficacyParalichthys of formalin-killed olivaceus. 140. Spain. J Fish Dis. 2006; 29: 175-179. Vaccine. and protection in farmed olive flounder, Garcia-Rosado E, Cano I, Martin-Antonio B, Labella A, Manchado M, 2014; 32: 1808-1813. Alonso MC, et al. Co-occurrence of viral and bacterial pathogens in disease outbreaks affecting newly cultured sparid fish. Int Microbiol. 157. proposalSukui M, for Nakagawa Tenacibaculum Y, Harayama gen. S, nov. Yamamoto with S. T enacibaculum Phylogenetic 141. 2007; 10: 193-199. maritimumanalysis and comb taxonomic. nov. study and ofTenacibaculum marine Cytophaga-like ovolyticum bacteria: comb. Fanning GR. Vibrio damsela, a marine bacterium, causes skin ulcers nov., description of Tenacibaculum mesophilum sp. nov. and Love M, Teebken-FisherChromis D,punctipinnis Hose JE, Farmer III JJ, Hickman FW, Tenacibaculum amylolyticum sp. nov. Int J Syst Evolut Microbiol. 1140. on the damselfish . Science. 1981; 214: 1139- 142. Avendañ ños B. Tenacibaculosis J Immunol Res. 2014. 2001; 51: 1639-1652. Andreoni F, Magnani M. Photobacteriosis: Prevention and diagnosis. Tenacibaculum maritimum 143. Pseudomonas 158. o-Herrera R, Toranzo AE, Magari anguilliseptica infection in marine fish caused by : a Berthe FCJ, Michel C, Bernardet JF. Identification of review. Dis Aquat Org. 2006; 71: 255-266. isolated from several fish species in France. Dis Aquat of Tenacibaculum maritimum 159. Kolygas MN, Gourzioti E, Vatsos IN, Athanassopoulou F. Identification 144. Org. Bovo 1995; G, Borghesan 21: 151-155. F, Comuzzi M, Ceschia G, Giorgetti G. ‘Winter strains from marine farmed fish in 160. Greece. Vet Rec. 2012; 170: 623. from disease’; in reared sea-bream: preliminary observations. Boll Soc It farmed Senegalese sole (Solea senegalensis, Cepeda C, Santos Y. First isolation of Flexibacter maritimus Patol Ittica. 1995; 17: 2-11. Sparus aurata Kaup) in Spain. Bull Eur 145. Doimi M. A new winter disease in sea-bream ( ): a 161. Assoc Soltani Fish M, Pathol. Shanker 2002; S, Munday22: 388-392. BL. Chemotherapy of Cytophaga/ 146. preliminaryPadros F, Tort report. L, Crespo Bull Eur S. Winter Assoc diseaseFish Pathol. in the 1996; gilthead 16: 17-18.sea bream Sparus aurata Flexibacter-like bacteria (CFLB) infections in fish: studies validating B, Saroglia M, :Sweetman some evidences J, Lavens of P, aeds.). multifactorial European etiology.Aquaculture In: clinical efficacies of selected antimicrobials. J Fish Dis. 1995; 18: Seabass and sea bream Culture: Problems and Prospects (Chatain 162. 555-565. to infections by Flexibacter and Flexibacter maritimus. Soltani M, Munday BL, Burke CM. The relative susceptibility of fish 147. Society, Ostende. Sweden. 1996; 305-307. Barros J, et al. Functional alterations associated with the ‘winter 163. Håstein T, Gudding R, Evensen Ø Gallardo MA, Sala-Rabanal M, Ibarz A, SparusPadros F, aurata Blanco). J, Aquaculture. Fernandez- Aquaculture. 1996; 140: 259-264. . Bacterial vaccines for fish-an syndrome’ in gilthead sea bream ( update of the current situation worldwide. In: Progress in Fish 2003; Tort L, 223: Rotllant 15-27. J, Liarte C, Acerete C, Hernandez A, Ceulemans S, et al. Effects of temperature decrease on feeding rates, immune indicators Vaccinology. Developments in Biologicals, (Midtlyng PJ, ed.). Karger, 164. ños B, Barja JL. 148. and histopathological changes of gilthead sea bream Sparus aurata Basel, Switzerland. 2005; 121: 55-74. Toranzo AE, Romalde JL, Dopazo CP, Magari Disease trends in the primary marine fish species cultured in Spain: a 20- fed with an experimental diet. Aquaculture. 2004; 229: 55-65. Sparus year study. World Aquacult. 2004; 35: 35-38. 149. Domenech A, Fernandez-Garayzabal JF, Lawson P, Garcia JA, Cutuli Dicentrarchus labrax to Tenacibaculum maritimum antigens. Fish aurata) associated with Pseudomonas anguilliseptica infection. 165. Salati F, Cubadda C, Viale I, Kusuda R. Immune response of sea bass MT, Blanco M, et al. Winter disease outbreak in sea-bream ( 166. Paperna I. Epitheliocystis infections in wild and cultured sea bream Sci. 2005; 71: 563-567. Aquaculture. 1997; 156: 317-326. (Sparus aurata, Sparidae) and grey mullets (Liza ramada, Mugilidae). M, Gibello A, et al. Association of Pseudomonas anguilliseptica 150. Domenech A, Fernandez-Garayzabal JF, Garcia Sparus JA, Cutuli aurata MT, L Blanco. J Fish 167. Aquaculture. Paperna I, Sabnai 1977; 10: I, Zachary 169-176. A. Ultrastructural studies in piscine infection with ‘winter disease’ in sea bream, Dis. 1999; 22: 69-71. septicemia caused by Pseudomonas anguilliseptica in cultured epitheliocystis: Evidence for a pleomorphic development cycle. J 151. Sakr, SFM, Abd el-Rhman,th AMM. Contribution on Pseudomonas Fish Ceschia Dis. G,1981; Makovec 4: 459-472. E. Epitheliocystis in sea bream (Sparus aurata) Oreochromis niloticus. 8 Int Symp on Tilapia in Aquaculture. 2008; 168. 1177-1196. reared Crespo in S,Italy. Zarza Boll C, Soc Padros It Patol F, Ittica. Marín 1995; de Mateo 17:18-24. M. Epitheliocystis agents in sea bream Sparus aurata 152. Vennerström P. Pseudomoniasis (P. anguilliseptica) in farmed fish. 169. ICES Identification Leaflets for Diseases and Parasites of Fish and : morphological evidence for two Shellfish. Leaflet No. 2015; 63. distinct chlamydia-like developmental cycles. Dis Aquat Org. 1999; 170. 37: 61-72. 153. Kholil I, Hossain MM, Neowajh S, Islam S, Kabir M. Comparative efficiency of some commercial antibiotics against Pseudomonas andSeth-Smith genomic HM, analysis Dourala of novel N, Fehr intracellular A, Qi W, Katharios P, Ruetten M, infection Phumkhachorn in fish. Int P, J RattanachaikunsoponFish Aquat Stud. 2015; P.2: 114-117. Use of Cassia alata et al. Emerging pathogens of gilthead sea bream: characterisation aqueous extract as a bath treatment to control Pseudomonas β-proteobacteria. ISME 154. anguilliseptica infection in tilapia (Oreochromis niloticus). Arch Biol 171. J. 2016; 10: 1791-1803. Nowak BF, LaPatra SE. Epitheliocystis in fish. J Fish Dis. 2006; 29: Sci. 2015; 67: 1165-1172. 573-578. Ann Aquac Res 4(1): 1033 (2017) 12/14 Sarasquete et al. (2017) Email: Central

172. Groff J, LaPatra S, Munn R, Anderson M, Osburn B. Epitheliocystis infection in cultured white sturgeon (Acipenser transmontanus) Xing J, Sheng X, Zhan W. Lymphocystis disease and diagnostic antigenic and ultrastructural similarities of the causative agent to Berlin. Germany. 1985; 116: 133-150. : 190. methods in China. Aquacult Asia Magazine. 2006; 11: 30-33. 173. the chlamydiae. J Vet Diagn Invest. 1996; 8: 172-180. O. 191. Wolf K. Fish Viruses and Fish Viral Diseases. Cornell University Miyaki K, Mizuta K, Yamamoto N, Yoshikoshi K, Kanai K, Tabeta Platycephalus Press, Ithaca. USA. 1988. Mass mortality of hatchery-reared juveniles of bartail flathead, sp. due to epitheliocystis-like disease. Bull Nagasaki 192. WilliamsGonzalez T.de The Canales iridoviruses. ML, Muñ Adv Virus Res. 1996; 46: 347-412. 174. Pref Instit Fish. 1998; 24: 7-10. A, Sarasquete C. Histological and histochemical characteristics of the bass, Micropterus salmoides (L.), with epitheliocystis hyperinfection. 193. lymphocystis disease in giltheadoz-Cueto sea bream, JA, Arellano Sparus J,aurata Garcia-Garcia, L. from Goodwin AE, Park E, Nowak BK. Successful treatment of largemouth

JSomridhivej Fish Dis. 2005; B, Taveekijakarn 28: 623-625. P, Meanan C, Somsiri T. Treatment of the South-Atlantic coast of Spain. Eur J Histochem. 1996; 40: 143- th epitheliocystis in juvenile tilapia. Proc 47 152. 175. Kasetsart Univ Ann Conf. 194. Hick P, Becker J, Whittington R. Iridoviruses of fish. In: Aquaculture 176. 2009; 1-8. Virology (Kibenge FSB, Godoy MG, eds.). Academic Press, London. . UK. 2016; 127-152. Borrego JJ, Valverde EJ, Labella AM, Castro D. Lymphocystis disease 177. virus: its importance in aquaculture. Rev Aquacult. 2016 195. Tak Seng I, Colorni A. Infectious diseases of warm water fish in marine and brackish waters. In: Diseases and Disorders of Finfish in Samalecos CP. Analysis of the structure of fish lymphocystis disease Cage Culture (Woo PTK, Bruno DW, Lin LHS, eds.). Cab International, virions from skin tumours of Pleuronectes. Arch Virol. 1986; 91: Wallingford, UK. 2002; 193-230. Study on the distribution 1-10. Paperna I, Sabnai I, Colorni A. An outbreak of lymphocystis in Sparus aurata L. 196. Zheng FR, Sun XQ, Wu X, Liu HZ, Zhang JX. 178. Paralichthys olivaceus). Aquaculture. 2006; and expression of a DNA vaccine against lymphocystis disease virus Masoero L,in Ercolinithe Gulf C, of Caggiano Aqaba, Red M, RossaSea. J FishA. Osservazioni Dis. 1982; 5: preliminary 433-437. sulla linfocisti in una maricoltura intensive italiana. Riv It Piscicolt in Japanese flounder ( 179. 261: 1128-1134. 197. Zheng F, Sun X, Liu H, Wu X, Zhong N, Wang B, et al. Distribution and Ittiopatol. 1986; 21: 70-74. Paralichthys olivaceus). Chin J in Sparus aurata from Ria Formosa, south coast of Portugal. expression in vitro and in vivo of DNA vaccine against lymphocystis 180. Menezes J, Ramos A, Pereira TG. Lymphocystis disease: an outbreak disease virus in Japanese flounder ( Oceanol Limnol. 2010; 28: 67-74. Aquaculture. Moate RM, 1987; Harris 67: JE, 222-225. McMahon S. Lymphocystis infections in Sparus aurata) in the Aegean Sea. Bull 198. Zheng F, Sun X, Wu X, Liu H, Li J, Wu S, et al. Immune efficacy of 181. a genetically engineered vaccine against Lymphocystis Disease cultured gilt-head sea bream ( Virus: Analysis of different immunization strategies. Evid Based Eur Assoc Fish Pathol. 1992; 12: 134-136. Complement Alternat Med. 2011; 2011: 729216. bream, Sparus aurata against lymphocystis disease virus and expression analysis of 182. Le Deuff RM, Renault T. Lymphocystis outbreaks in farmed sea 199. Zheng FR, Sun XQ, Xing MQ, Liu H. Immune response of DNA vaccine , first report on French Mediterranean coast. Bull Eur Assoc Fish Pathol. 1993; 13: 130-133. immune-related genes after vaccination. Aquaculture Res. 2013; 41: 200. 1444-1451. 183. Garcia-Rosado E, CastroSparus D, Rodriguezaurata, L.) S,using Perez-Prieto a new homologous SI, Borrego cell JJ. Isolation and characterization of lymphocystis virus (FLDV) from Tian JY, Sun XQ, Chen XG. Formation and oral administration of gilt-head sea bream ( alginate microspheres loaded with pDNA for lymphocystis disease line. Bull Eur Assoc Fish Pathol. 1999; 19: 53-56. virus (LCDV) to Japanese flounder. Fish Shellf Immunol. 2008; 24: 201. 592-599. 184. Bovo G, Florio D. Viral diseases of cultured fish. In: Fish Diseases bream, Sparus aurata (Eiras JC, Segner H, Wahli T, Kapoor BG, eds.). Science Publishers, Comps M, Raymond JC. Virus-like particles in the retina of the sea Enfield, USA. 2008; 185-238. 202. . Bull Eur Assoc Fish Pathol. 1996; 16: 161-163. 185. Haddad-Boubaker S, Bouzgarou N, Fakhfakh E, Khayech M, Dalla Valle L, Zanella L, Patarnello P, Paolucci L, Belvedere P, Mohamed SB, Megdich A, et al. Detection and Sparus genetic aurata characterization in Tunisia. Colombo L. Development of a sensitive diagnostic assay for fish of lymphocystis disease virus (LCDV) isolated during disease nervous necrosis virus based on RT-PCR plus nested PCR. J Fish Dis. outbreaks in cultured gilt-head sea bream 203. 2000; 23: 321-327. FishMuthuramalingam Pathol. 2013; 48: US, 101-104. Marudhupandi T, Haq MAB, Thankappan Dalla Valle L, Toffolo V, Lamprecht M, Maltese C, Bovo G, Belvedere 186. Amphiprion ocellaris (Cuvier, P, et al. Development of a sensitive and quantitative diagnostic assay T, Kumar A. HistopathologicalAmphiprion study of perculalymphocystis disease virus for fish nervous necrosis virus based on two-target real-time PCR. (LCDV) in cultured false clownfish, 204. Vet Microbiol. 2005; 110: 167-179. 1830) and true clownfish, (Lacepede, 1802). J Beraldo P, De Nigris G, Rogato F, Galeotti M. Histological and Coast Life Med. 2014; 2: 264-269. in gilthead sea bream larvae (Sparus aurata Sciaenops ocellatus Eurimmunohistochemistry Assoc Fish Pathol, 13 findingsth of viral encephalopathyretinopathy 187. Colorni A, Diamant A. Splenic and cardiac lymphocystis in red drum, 2007; 140. , L. 1578) reared in Italy. (L.). J Fish Dis. 1995; 18: 467-471. Int Conf Fish Shellfish Dis. Grado, Italy.

188. diseaseSarasquete in skin C, Gonzalezof gilthead de sea Canales bream, ML, Sparus Arellano aurata J, ,Perez-Prieto from the South SI, Attanassopoulou M, Sabatakou O. First incidence of clinical signs of Garcia-Rosado E, Borrego JJ. Histochemical study of lymphocystis 205. nodavirusBitchava infection K, Xylouri in sea E, bream, Fragkiadaki Sparus auratus E, Attanassopoulou L. Isr J Aquacult F,–

Atlantic coast of Spain. Histol Histopathol. 1998; 13: 37-45. 206. Bamidgeh. 2007; 59: 3-9. 189. Flügel RH. Lymphocystis disease virus. In: Current Topics in Microbiology and Immunology, (Willis DB, ed.). Springer-Verlag, Castric J, Thiery R, Jeffroy J, de Kinkelin P, Raymond JC. Sea bream Ann Aquac Res 4(1): 1033 (2017) 13/14 Sarasquete et al. (2017) Email: Central

Sparus aurata and inactivated betanodavirus in sevenband grouper, Epinephelus septemfasciatus , an asymptomatic contagious fish host for nodavirus. 207. Dis Cutrin Aquat JM, Org. Thiery 2001: R, Leao 47: 33-38. P, Olveira JG, Barja JL, Bandin I. Emergence (Thunberg). J Fish Dis. 2009; 32: 201-210. of pathogenic betanodaviruses belonging to SJNNV genogroup in 215. Vimal S, Farook MA, Madan N, Abdul Majeed S, Nambi KSN, Taju G, et al. Development, distribution and expression of a DNA vaccine farmed fish species from the Iberian Peninsula. J Fish Dis. 2007; 30: against nodavirus in Asian seabass, Lates calcarifier (Bloch, 1790). 225-232. 216. Aquac Res. 2014; 47: 1209-1220. Comparative analysis of both genomic segments of betanodaviruses J, et al. 208. Olveira JG, Souto S, Dopazo CP, Thiery R, Barja JL, Bandin I. Valero Y, Awad E, Buonocore F, Arizcun M, Esteban MA, Meseguer An oral chitosan DNA vaccine against nodavirus improves isolated from epizootic outbreaks in farmed fish species provides transcription of cell-mediated cytotoxicity and interferon genes in evidence for genetic reassortment. J Gen Virol. 2009; 90: 2940-2951. the European sea bass juveniles gut and survival upon infection. Dev 217. Comp Athanassopoulou Immunol. 2016; F. Ichthyophoniasis 65: 64-72. in sea bream, Sparus aurata 209. nodavirusGrotmol S,and Totland increases GK. survival Surface of disinfectionthe larvae. of Atlantic halibut (L.), and , Oncorhynchus mykiss (Walbaum) from Hippoglossus hippoglossus eggs with ozonated sea-water inactivates Greece. Dis Aquat Org. 2000; 210. 39:Frerichs 89-96. GN, Tweedie A, Starkey WG, Richards RH. Temperature, pH J Fish Dis. 1992; 15: 437-441. and electrolyte sensitivity, and heat, UV and disinfectant inactivation of sea bass (Dicentrarchus labrax) neuropathy nodavirus. 218. Franco-Sierra A, Sitja-Bobadilla A, Alvarez-Pellitero P. Ichthyophonus infection in cultured marine fish from Spain. J Fish Biol. Giarratana 1997; 51:F, Filiciotto 830-839. F. Grave episodio di ittiofonosi muscolare in 211. Aquaculture. 2000; 185: 13-24. Sparus aurata of seven band grouper, Epinephelus septemfasciatus Thunberg, 219. Tanaka S, Mori K, Arimoto M, Iwamo T, Nakai T. Protective immunity d’allevamento: descrizione di un caso e considerazioni 220. igienistiche. Ittiopatologia. 2007; 4: 41-48. against experimental viral nervous necrosis. J Fish Dis. 2001; 24: 221. Elatta MEA. Some bacterial and fungal affections causing disease 212. Thiery R, Cozien J, Cabon J, Lamour F, Baud M, Schneemann A. Yanong RP. Fungal diseases of fish. Vet Clin N Am. 2003; 6: 377-400. 15-22. problems in cultured sea bream Induction of a protective immune response against viral nervous Sparus aurata in Damietta Governorate and trials for control. J Arab Aquacult Soc. 2013; 8: necrosis in the European sea bass Dicentrarchus labrax by using 222. 213. 357-372. betanodavirus virus-like particles. J Virol. 2006; 80: 10201-10207. Epidemiological investigations of mycotic infections of cultured inactivated virus vaccine against viral nervous necrosis (VNN). Fish Abdel-Latif HMR, Khalil RH, El-hofi HR, Saad TT, Zaied SMA. Yamashita Y, Fujita Y, Kawakami H, Nakai T. The efficacy of gilthead sea bream, Sparus aurata at Marriott Lake, Egypt. Int J Fish

214. Pathol. 2005; 40: 15-21. necrosis conferred by simultaneous inoculation of aquabirnavirus Aquat Stud. 2014; 2: 5-13. Yamashita Y, Mori K, Nakai T. Protection against viral nervous

Cite this article Borrego JJ, Labella AM, Castro D, Ortiz-Delgado JB, Sarasquete C (2017) Updated of the Pathologies Affecting Cultured Gilthead Seabream, Sparus aurata. Ann Aquac Res 4(2): 1033.

Ann Aquac Res 4(1): 1033 (2017) 14/14