Trichodina mutabilis (Protozoa: Ciliophora: Trichodinidae) from the characid fish Astyanax mexicanus in the Cuatro Ciénegas region, northern Mexico
Trichodina mutabilis (Protozoa: Ciliophora: Trichodinidae) en el pez carácido Astyanax mexicanus de la región de Cuatro Ciénegas, norte de México
Alma Gabriela Islas-Ortega, Rogelio Aguilar-Aguilar
Departamento de Biología Comparada, Facultad de Ciencias, Universidad Nacional Autónoma de México. Apartado postal 70–399, 04510 México, D. F., Mexico
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A, población de la especie en la zona de estudio; B, hábito de la planta; C, tallo dicotómico; e= enación, s= sinangio.</p>" ] ] ] "autores" => array:1 [ 0 => array:2 [ "autoresLista" => "Victoria Hernández-Hernández, María Guadalupe Segovia-Ramírez, Sergio Argüelles-Marmolejo" "autores" => array:3 [ 0 => array:2 [ "nombre" => "Victoria" "apellidos" => "Hernández-Hernández" ] 1 => array:2 [ "nombre" => "María Guadalupe" "apellidos" => "Segovia-Ramírez" ] 2 => array:2 [ "nombre" => "Sergio" "apellidos" => "Argüelles-Marmolejo" ] ] ] ] ] "idiomaDefecto" => "es" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S1870345314707870?idApp=UINPBA00004N" "url" => "/18703453/0000008500000002/v1_201501071639/S1870345314707870/v1_201501071639/es/main.assets" ] "en" => array:17 [ "idiomaDefecto" => true "titulo" => "<span class="elsevierStyleItalic">Trichodina mutabilis</span> (Protozoa: Ciliophora: Trichodinidae) from the characid fish <span class="elsevierStyleItalic">Astyanax mexicanus</span> in the Cuatro Ciénegas region, northern Mexico" "tieneTextoCompleto" => true "paginas" => array:1 [ 0 => array:2 [ "paginaInicial" => "613" "paginaFinal" => "616" ] ] "autores" => array:1 [ 0 => array:3 [ "autoresLista" => "Alma Gabriela Islas-Ortega, Rogelio Aguilar-Aguilar" "autores" => array:2 [ 0 => array:2 [ "nombre" => "Alma Gabriela" "apellidos" => "Islas-Ortega" ] 1 => array:3 [ "nombre" => "Rogelio" "apellidos" => "Aguilar-Aguilar" "email" => array:1 [ 0 => "raguilar@ciencias.unam.mx" ] ] ] "afiliaciones" => array:1 [ 0 => array:2 [ "entidad" => "Departamento de Biología Comparada, Facultad de Ciencias, Universidad Nacional Autónoma de México. Apartado postal 70–399, 04510 México, D. F., Mexico" "identificador" => "aff0005" ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "<span class="elsevierStyleItalic">Trichodina mutabilis</span> (Protozoa: Ciliophora: Trichodinidae) en el pez carácido <span class="elsevierStyleItalic">Astyanax mexicanus</span> de la región de Cuatro Ciénegas, norte de México" ] ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0020" "etiqueta" => "Figure 4" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr4.jpeg" "Alto" => 730 "Ancho" => 973 "Tamanyo" => 160918 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Scanning electron micrograph of <span class="elsevierStyleItalic">T. mutabilis</span>, adoral view.</p>" ] ] ] "textoCompleto" => "<span class="elsevierStyleSections"><p id="par0005" class="elsevierStylePara elsevierViewall">Ciliates of the genus <span class="elsevierStyleItalic">Trichodina</span> Ehrenberg, 1831 are epibionts and often ectoparasites on animals including fish, where they are pathogenic, causing damage to skin and gills (<a class="elsevierStyleCrossRef" href="#bib0100">Sleigh, 1991</a>), often leading to death of the infested fish (<a class="elsevierStyleCrossRef" href="#bib0040">Hoffman, 1999</a>). Its proliferation might be promoted by changes in the relationship among host, parasite, and environment caused by nutritional deficiency, poor water quality, and infectious or parasitic diseases, causing severe epidermal lesions and disease outbreaks (<a class="elsevierStyleCrossRef" href="#bib0055">Khan, 2004</a>; <a class="elsevierStyleCrossRef" href="#bib0075">Martins et al., 2010</a>).</p><p id="par0010" class="elsevierStylePara elsevierViewall">Studies of <span class="elsevierStyleItalic">Trichodina</span> in Mexico are scarce. Most have been carried out on exotic cultured fishes such as <span class="elsevierStyleItalic">Carassius auratus</span> (L.), <span class="elsevierStyleItalic">Ctenopharyngodon idella</span> (Valenciennes), <span class="elsevierStyleItalic">Cyprinus carpio</span> (L.) (Cyprinidae), and <span class="elsevierStyleItalic">Oreochromis niloticus</span> (L.) (Cichlidae) (<a class="elsevierStyleCrossRef" href="#bib0010">Aladro-Lubel et al., 2006</a>). To date there are not records of this ciliate in native populations of freshwater fishes inhabiting natural localities.</p><p id="par0015" class="elsevierStylePara elsevierViewall">Cuatro Ciénegas is a small intermontane valley edge of the Sierra Madre Oriental in the Mexican state of Coahuila, northern Mexico. The approximately 1 000<span class="elsevierStyleHsp" style=""></span>km<span class="elsevierStyleSup">2</span> desert valley of Cuatro Ciénegas possess the greatest number of endemic species of any place in North America (<a class="elsevierStyleCrossRef" href="#bib0105">Stein et al., 2000</a>), holding a large biodiversity and more than 70 endemic species. Its springs, marshes, rivers, and lakes support a diverse fish fauna for a North American desert region, including at least 16 native fish species, 8<a name="p614"></a> of which are endemic (<a class="elsevierStyleCrossRef" href="#bib0080">Minckley, 1984</a>). A wide inventory of the helminth species parasitizing these fish taxa have been provided recently by <a class="elsevierStyleCrossRef" href="#bib0005">Aguilar-Aguilar et al. (2014)</a>; however, the occurrence of protozoan parasites of these fishes has not been documented. During a prospective study addressed to establish the diversity of ciliate parasites of freshwater fishes occurring in arid regions of Mexico, particularly associated with the Cuatro Ciénegas region, we analyzed several fish species. This paper provides the record of <span class="elsevierStyleItalic">Trichodina mutabilis</span><a class="elsevierStyleCrossRef" href="#bib0050">Kazubski and Migala, 1968</a> for the freshwater fish <span class="elsevierStyleItalic">Astyanax mexicanus</span> (De Filippi, 1853), which represents the first record of this trichodinid in Mexico and the second in North America.</p><p id="par0020" class="elsevierStylePara elsevierViewall">With this aim, freshwater fishes of the species <span class="elsevierStyleItalic">Astyanax mexicanus</span> (n<span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>85) (Characidae), <span class="elsevierStyleItalic">Gambusia marshi</span> Minckley and Craddock, 1962 (Poeciliidae) (n<span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>122), <span class="elsevierStyleItalic">Cyprinodon atrorus</span> Miller, 1968 (n= 108), <span class="elsevierStyleItalic">C. bifasciatus</span> Miller, 1968 (n<span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>28) (Cyprinodontidae), and <span class="elsevierStyleItalic">Herichthys minckleyi</span> (Kornfield and Taylor, 1983) (n<span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>19) (Cichlidae), were collected from several localities in the Cuatro Ciénegas region. Fish were kept alive and studied for ectoparasitic ciliates no more than 6 hours after capture. Squash slides of skin and gills were made from live specimens. Slides were impregnated by silver-nitrate to observe the adhesive disc, as described by <a class="elsevierStyleCrossRef" href="#bib0065">Lom (1958)</a>. Air-dried slides of trichodinids were stained with either Harris-Lillie's hematoxylin or Ehrlich's acid hematoxylin to studying the nuclear apparatus. Voucher slides were deposited at the Colección del Grupo de Trabajo en Parasitología de Organismos Acuáticos at the Facultad de Ciencias, UNAM, Mexico (No. CPOA-012 to 038). All measurements are presented in micrometers following the recommendations of <a class="elsevierStyleCrossRef" href="#bib0065">Lom (1958)</a> and <a class="elsevierStyleCrossRef" href="#bib0110">Van As and Basson (1989)</a>. They were made on photomicrographs obtained using an Olympus BX40® photomicroscope equipped with a Leica Pixlink PL-A662® image capture system. The measurements of the parasites were made with the aid of the Image-Pro Plus® 4.1 software. For SEM study, samples of gills and skin were fixed using glutaraldehyde 3%, and post fixed in 1% OsO4 for 1<span class="elsevierStyleHsp" style=""></span>hr, dehydrated through a graded series of ethyl alcohol and then critical point dried with CO<span class="elsevierStyleInf">2</span>. Specimens were mounted on metal stubs, coated with gold, and examined in a Hitachi Stereoscan Model S-2469N.</p><p id="par0025" class="elsevierStylePara elsevierViewall">The only ectoparasitic ciliate species found was <span class="elsevierStyleItalic">Trichodina mutabilis</span> (<a class="elsevierStyleCrossRefs" href="#fig0005">Figs. 1–4</a>). This species was recovered in high numbers (more than 100 individuals per fish, prevalence= 100%) from the skin and gills of <span class="elsevierStyleItalic">Astyanax mexicanus</span> from the Anteojo San Juan spring in the Cuatro Ciénegas region (26°58'07” N, 102°07'38” W). Remaining host species were free of infection. Ciliates have a medium size disc-shaped body (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>) measuring 38.31<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>2.07 diameter, adhesive disc 36.22<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>2.07; absence of granules in silver-impregnated specimens. A horseshoe-shaped macronucleus (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>) is observed, with an external diameter of 64.5<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>6.37, and a distance between the ends of 7.67<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>2.37. Denticle ring (<a class="elsevierStyleCrossRef" href="#fig0015">Fig. 3</a>): 21.77<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>2.02, number of denticles 23 – 28, number of radial pins per denticle: 7–10,<a name="p615"></a> dimensions of denticle: length 4.85<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>0.25; blade 4.33<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>0.32; central part 1.46<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>0.15; ray 5.52<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>0.67; span 11.55<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>0.73. Adoral ciliary spiral 400° (<a class="elsevierStyleCrossRef" href="#fig0020">Fig. 4</a>).</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><elsevierMultimedia ident="fig0010"></elsevierMultimedia><elsevierMultimedia ident="fig0015"></elsevierMultimedia><elsevierMultimedia ident="fig0020"></elsevierMultimedia><p id="par0030" class="elsevierStylePara elsevierViewall">The ciliate species <span class="elsevierStyleItalic">Trichodina mutabilis</span> was first described by <a class="elsevierStyleCrossRef" href="#bib0050">Kazubski and Migala (1968)</a>. Since its original description, various records from diverse fish hosts have been published around the world (<a class="elsevierStyleCrossRef" href="#bib0020">Basson and Van As, 2006</a>), and a high morphological variability has been documented (<a class="elsevierStyleCrossRef" href="#bib0070">Lom, 1970</a>; <a class="elsevierStyleCrossRef" href="#bib0020">Basson and Van As, 2006</a>). Specimens analyzed in this study exhibit some morphological variation with respect to the size of the body, being smaller than those described from other parts of the world (see <a class="elsevierStyleCrossRef" href="#bib0050">Kazubski and Migala, 1968</a>; <a class="elsevierStyleCrossRef" href="#bib0070">Lom, 1970</a>; <a class="elsevierStyleCrossRef" href="#bib0030">Basson et al., 1983</a>; <a class="elsevierStyleCrossRef" href="#bib0095">Özer and Erdem, 1998</a>; <a class="elsevierStyleCrossRef" href="#bib0015">Albaladejo and Arthur, 1989</a>; <a class="elsevierStyleCrossRef" href="#bib0090">Özer, 2000</a>; <a class="elsevierStyleCrossRef" href="#bib0035">Dove and O'Donoghue, 2005</a>; <a class="elsevierStyleCrossRef" href="#bib0045">Hu, 2012</a>); however, in general terms our specimens fit with most of the characteristics described for <span class="elsevierStyleItalic">T. mutabilis</span> (<a class="elsevierStyleCrossRef" href="#bib0025">Basson and Van As, 1994</a>), and have a similar size to a population described by Mitra and Bandyopadhyay (2005).</p><p id="par0035" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Trichodina mutabilis</span> is a cosmopolitan species recorded from diverse host fish species, mainly cyprinids in the Europe, Asia, South Africa, and North America (<a class="elsevierStyleCrossRef" href="#bib0070">Lom, 1970</a>; <a class="elsevierStyleCrossRef" href="#bib0030">Basson et al., 1983</a>; <a class="elsevierStyleCrossRef" href="#bib0015">Albaladejo and Arthur, 1989</a>; <a class="elsevierStyleCrossRef" href="#bib0095">Özer and Erdem, 1998</a>; <a class="elsevierStyleCrossRef" href="#bib0090">Özer, 2000</a>; <a class="elsevierStyleCrossRef" href="#bib0060">Kritsky and Heckmann, 2002</a>; <a class="elsevierStyleCrossRef" href="#bib0035">Dove and O'Donoghue, 2005</a>; Mitra and Bandyopadhyay, 2005; <a class="elsevierStyleCrossRef" href="#bib0020">Basson and Van As, 2006</a>; <a class="elsevierStyleCrossRef" href="#bib0045">Hu, 2012</a>). According to <a class="elsevierStyleCrossRef" href="#bib0020">Basson and Van As (2006)</a>, this is a ciliate species with a worldwide distribution, probably attained via transcontinental introductions of fish. Particularly, this species has been dispersed to other countries together with shipments of carps (Cyprinidae) destined for aquaculture. It possesses a large dispersal capability and it is now found not only in introduced hosts but also in the native freshwater fish fauna. Similar introductions of parasitic species such as exotic digeneans and cestodes have been documented for freshwater fish species in Mexico (see <a class="elsevierStyleCrossRef" href="#bib0005">Aguilar-Aguilar et al., 2014</a>), where the low host specificity and great capability to adapt to different environmental conditions allow the invasive species to thrive and to expand its host and distributional range. The report of an additional introduced parasite species affecting freshwater fish fauna in Mexico must be considered in terms of suggesting accurate conservation strategies for this fauna.</p><p id="par0040" class="elsevierStylePara elsevierViewall">The present record of <span class="elsevierStyleItalic">Trichodina mutabilis</span> in <span class="elsevierStyleItalic">Astyanax mexicanus</span> represents a new host record and the first for Characidae. The present finding, along with previous records of this ciliate species in non-cyprinid fish (<a class="elsevierStyleCrossRef" href="#bib0060">Kritsky and Heckmann, 2002</a>; Mitra and Bandyopadhyay, 2005), throws new light on the biodiversity and host preference of the species (Mitra and Bandyopadhyay, 2005), and allows us to suggest a successful colonization from exotic cultured carps to native characid fish. Additionally, this is the first record of this ciliate species in Mexican fish and the second for North America, where it was previously recorded infesting the gills of carps of the species <span class="elsevierStyleItalic">Cyprinus carpio</span> in Utah, USA (<a class="elsevierStyleCrossRef" href="#bib0060">Kritsky and Heckmann, 2002</a>). Furthermore, this is the first record of ciliates of the genus <span class="elsevierStyleItalic">Trichodina</span> parasitizing native wild fishes in Mexico, since previous reports were for exotic cultured fishes (<a class="elsevierStyleCrossRef" href="#bib0010">Aladro-Lubel et al., 2006</a>).</p><p id="par0045" class="elsevierStylePara elsevierViewall">The authors would like to thank the financial support and facilities provided by Dra. Valeria Souza to conduct samplings during 2011 and 2013 within the research project<a name="p616"></a> financed by WWF-Fundación Carlos Slim Alliance, to Héctor Espinosa Pérez for the collection and identification of the fishes, to Berenit Mendoza Garfías for the SEM photographs, and Margarita Reyes Santos, Omar Lagunas Calvo, Eduardo Villalobos, and Berenice Lomeli Álvarez for technical assistance in the laboratory and field.</p></span>" "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2012-09-05" "fechaAceptado" => "2013-11-20" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Key words" "identificador" => "xpalclavsec382967" "palabras" => array:3 [ 0 => "Trichodinidae" 1 => "ciliates" 2 => "ecto-parasitism" ] ] ] "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec382968" "palabras" => array:3 [ 0 => "Trichodinidae" 1 => "ciliados" 2 => "ectoparasitismo" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "en" => array:2 [ "titulo" => "Abstract" "resumen" => "<p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">As a part of a series of ongoing studies on trichodinids of freshwater fishes of Mexico, several species from diverse localities in the Cuatro Ciénegas region, Coahuila, northern Mexico, were examined. Wet smears of gills and skin were made fresh and screened for the presence of trichodinids under light microscopy. Additional specimens were fixed for SEM. The only trichodinid species found was <span class="elsevierStyleItalic">Trichodina mutabilis</span>, a parasite of the characid fish <span class="elsevierStyleItalic">Astyanax mexicanus.</span> This ciliate protozoan has been introduced from Asia to many countries, including Mexico, with its original host, the Asian carps. The present record is the first for Mexico and the second in North America, being the first record of a <span class="elsevierStyleItalic">Trichodina</span> species for native wild freshwater fish in a natural environment in Mexico, since all previous records were from exotic cultured fishes.</p>" ] "es" => array:2 [ "titulo" => "Resumen" "resumen" => "<p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">Como parte de un proyecto de investigación a largo plazo sobre tricodínidos parásitos de peces dulceacuícolas de México, varios ejemplares de diversas especies de peces se recolectaron y examinaron en Cuatro Ciénegas, Coahuila, México. Se revisaron muestras frescas de la piel y las branquias bajo microscopio óptico. Algunas muestras adicionales se fijaron para microscopía electrónica. La única especie encontrada fue <span class="elsevierStyleItalic">Trichodina mutabilis</span>, la cual se registra por primera vez en México, parasitando al pez <span class="elsevierStyleItalic">Astyanax mexicanus</span>. Esta especie de protozoo ha sido introducida a diferentes partes del mundo con su huésped original, la carpa asiática. El presente registro es el primero para México y el segundo para Norteamérica, siendo también el primero en México de una especie de <span class="elsevierStyleItalic">Trichodina</span> en peces nativos en su ambiente natural, ya que los registros previos fueron hechos en peces exóticos cultivados.</p>" ] ] "multimedia" => array:4 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 964 "Ancho" => 972 "Tamanyo" => 212552 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Klein's silver impregnated <span class="elsevierStyleItalic">Trichodina mutabilis</span>, bar= 15<span class="elsevierStyleHsp" style=""></span>μm.</p>" ] ] 1 => array:7 [ "identificador" => "fig0010" "etiqueta" => "Figure 2" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr2.jpeg" "Alto" => 885 "Ancho" => 972 "Tamanyo" => 109812 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Ehrlich's acid hematoxylin stained nuclear apparatus of <span class="elsevierStyleItalic">T. mutabilis</span>, bar= 10<span class="elsevierStyleHsp" style=""></span>μm.</p>" ] ] 2 => array:7 [ "identificador" => "fig0015" "etiqueta" => "Figure 3" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr3.jpeg" "Alto" => 730 "Ancho" => 973 "Tamanyo" => 124306 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Scanning electron micrograph of <span class="elsevierStyleItalic">T. mutabilis</span>, view of a denticulate ring.</p>" ] ] 3 => array:7 [ "identificador" => "fig0020" "etiqueta" => "Figure 4" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr4.jpeg" "Alto" => 730 "Ancho" => 973 "Tamanyo" => 160918 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Scanning electron micrograph of <span class="elsevierStyleItalic">T. mutabilis</span>, adoral view.</p>" ] ] ] "bibliografia" => array:2 [ "titulo" => "Literatute cited" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0005" "bibliografiaReferencia" => array:22 [ 0 => array:3 [ "identificador" => "bib0005" "etiqueta" => "Aguilar-Aguilar et al., 2014" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Helminth parasites of freshwater fishes from Cuatro Ciénegas, Coahuila, in the Chihuahuan desert of Mexico: inventory and biogeographical implications" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:4 [ 0 => "R. 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Khan" ] ] ] ] ] "host" => array:1 [ 0 => array:1 [ "Revista" => array:6 [ "tituloSerie" => "Journal of Fish Diseases" "fecha" => "2004" "volumen" => "27" "paginaInicial" => "181" "paginaFinal" => "184" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/15009245" "web" => "Medline" ] ] ] ] ] ] ] ] 11 => array:3 [ "identificador" => "bib0060" "etiqueta" => "Kritsky and Heckmann, 2002" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Species of <span class="elsevierStyleItalic">Dactylogyrus</span> (Monogenoidea: Dactylogyridae) and <span class="elsevierStyleItalic">Trichodina mutabilis</span> (Ciliata) infesting koi carp, <span class="elsevierStyleItalic">Cyprinus carpio</span>, during mass mortality at a commercial rearing facility in Utah, USA" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:2 [ 0 => "D.C. Kritsky" 1 => "R. 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| Year/Month | Html | Total | |
|---|---|---|---|
| 2024 November | 12 | 3 | 15 |
| 2024 October | 91 | 5 | 96 |
| 2024 September | 142 | 15 | 157 |
| 2024 August | 84 | 2 | 86 |
| 2024 July | 85 | 4 | 89 |
| 2024 June | 72 | 5 | 77 |
| 2024 May | 82 | 4 | 86 |
| 2024 April | 84 | 9 | 93 |
| 2024 March | 128 | 14 | 142 |
| 2024 February | 84 | 8 | 92 |
| 2024 January | 142 | 4 | 146 |
| 2023 December | 113 | 12 | 125 |
| 2023 November | 160 | 16 | 176 |
| 2023 October | 189 | 27 | 216 |
| 2023 September | 51 | 14 | 65 |
| 2023 August | 74 | 13 | 87 |
| 2023 July | 84 | 5 | 89 |
| 2023 June | 77 | 19 | 96 |
| 2023 May | 93 | 10 | 103 |
| 2023 April | 87 | 21 | 108 |
| 2023 March | 86 | 4 | 90 |
| 2023 February | 81 | 11 | 92 |
| 2023 January | 76 | 9 | 85 |
| 2022 December | 70 | 13 | 83 |
| 2022 November | 94 | 11 | 105 |
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| 2020 December | 26 | 10 | 36 |
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| 2020 October | 24 | 5 | 29 |
| 2020 September | 19 | 7 | 26 |
| 2020 August | 44 | 1 | 45 |
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| 2020 May | 36 | 3 | 39 |
| 2020 April | 28 | 3 | 31 |
| 2020 March | 11 | 5 | 16 |
| 2020 February | 23 | 6 | 29 |
| 2020 January | 22 | 11 | 33 |
| 2019 December | 17 | 6 | 23 |
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| 2019 October | 16 | 5 | 21 |
| 2019 September | 33 | 6 | 39 |
| 2019 August | 23 | 3 | 26 |
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| 2019 June | 94 | 15 | 109 |
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| 2019 March | 21 | 4 | 25 |
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| 2018 December | 31 | 2 | 33 |
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| 2018 October | 63 | 14 | 77 |
| 2018 September | 34 | 7 | 41 |
| 2018 August | 38 | 13 | 51 |
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| 2018 May | 17 | 10 | 27 |
| 2018 April | 7 | 8 | 15 |
| 2018 March | 11 | 12 | 23 |
| 2018 February | 6 | 1 | 7 |
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| 2017 August | 7 | 17 | 24 |
| 2017 July | 8 | 5 | 13 |
| 2017 June | 14 | 12 | 26 |
| 2017 May | 12 | 13 | 25 |
| 2017 April | 7 | 19 | 26 |
| 2017 March | 16 | 42 | 58 |
| 2017 February | 35 | 11 | 46 |
| 2017 January | 16 | 5 | 21 |
| 2016 December | 16 | 11 | 27 |
| 2016 November | 34 | 7 | 41 |
| 2016 October | 37 | 13 | 50 |
| 2016 September | 40 | 16 | 56 |
| 2016 August | 33 | 51 | 84 |
| 2016 July | 28 | 26 | 54 |
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