Haemogregarina Daviesensis Sp. Nov. (Apicomplexa: Haemogregarinidae)

Total Page:16

File Type:pdf, Size:1020Kb

Haemogregarina Daviesensis Sp. Nov. (Apicomplexa: Haemogregarinidae) Parasitology Research (2019) 118:2773–2779 https://doi.org/10.1007/s00436-019-06430-7 FISH PARASITOLOGY - ORIGINAL PAPER Haemogregarina daviesensis sp. nov. (Apicomplexa: Haemogregarinidae) from South American lungfish Lepidosiren paradoxa (Sarcopterygii: Lepidosirenidae) in the eastern Amazon region Pedro Hugo Esteves-Silva1 & Maria Regina Lucas da Silva2 & Lucia Helena O’Dwyer2 & Marcos Tavares-Dias3 & Lúcio André Viana1 Received: 10 February 2019 /Accepted: 15 August 2019 /Published online: 27 August 2019 # Springer-Verlag GmbH Germany, part of Springer Nature 2019 Abstract Based on morphology and morphometry of gametocytes in blood and molecular phylogenetic analysis, we described a new species of hemoparasite from the genus Haemogregarina isolated from Lepidosiren paradoxa in the eastern Amazon region. Haemogregarina daviesensis sp. nov. is characterized by monomorphic gametocytes of varying maturity stage and their dimen- sions were 16 ± 0.12 μm(range13–18) in length and 6 ± 0.97 μm(range5–8) in width. The morphological and morphometric data were not identical with other haemogregarine species from fish. All specimens of L. paradoxa analyzed were infected by H. daviesensis sp. nov. and the parasitemia level was moderate (1–28/2000 blood erythrocytes). Two sequences were obtained from L. paradoxa, and these constituted a monophyletic sister clade to the Haemogregarina species. In addition, H. daviesensis sp. nov. detected here grouped with Haemogregarina sp. sequences isolated from chelonian Macrochelys temminckii,with99% bootstrap support. This study provides the first data on the molecular phylogeny of an intraerythrocytic haemogregarine of freshwater fish and highlights the importance of obtaining additional information on aspects of the general biology of these hemoparasites in fish populations, in order to achieve correct taxonomic classification. Keywords Haemogregarine . Lungfish . Morphology . 18S rRNA gene . Hemoparasites Introduction (Machado et al. 2010; Nelson et al. 2016). This species is primarily a carnivorous fish, feeding on arthropods and snails, Lepidosiren paradoxa Fitzinger, 1837 (lungfish) is a mono- and it inhabits hypoxic shallow swamps and lakes. Lungfish type of Lepidosirenidae, which is a family of Dipnoi fish with are obligate air-breathers, but during the dry season, they are distribution restricted to South America. In Brazil, its distri- able to burrow into the mud, undergo physiological changes, butionisonlyintheAmazonandParanáRiversystems and decrease their metabolic rates, thereby inducing aestiva- tion (Almeida-Val et al. 2010). Section Editor: Astrid Holzer Haemogregarina lepidosirenis Jepps, 1927 was described by Jepps (1927)inL. paradoxa in the Gran Chaco, in * Lúcio André Viana Paraguay. Haemogregarinidae Léger, 1911 is a family of pro- [email protected] tozoa comprising three genera: Haemogregarina Danilewsky, 1885; Cyrillia Lainson, 1981; and Desseria Siddall, 1995. 1 Departamento de Ciências Biológicas e da Saúde, Universidade The species in these genera are intraerythrocytic and have Federal do Amapá. Rodovia Juscelino Kubitscheck, KM 02, S/N, Jardim Marco Zero, Macapá, Amapá 68903-419, Brazil heteroxenous life cycles (Siddall 1995). Currently, these gen- era are regarded as differing in oocyst formation and sporozo- 2 Departamento de Parasitologia, Instituto de Biociências, Universidade Estadual Paulista Júlio de Mesquita Filho, Distrito de ite numbers in invertebrate hosts (vectors) and vertebrate hosts Rubião Junior, Botucatu, São Paulo 18618-970, Brazil (fish and chelonians). The vectors for haemogregarines of fish 3 Embrapa Amapá, Rodovia Juscelino Kubitscheck, Km 5, 2600, are usually isopods of the family Gnathiidae (Davies and Smit Universidade, Macapá, Amapá 68903-419, Brazil 2001) and leeches of the families Glossiphoniidae and 2774 Parasitol Res (2019) 118:2773–2779 Piscicolidae (Lainson 1981; Siddall and Desser 1993). municipality of Santana, state of Amapá, in the eastern Transmission of these intracellular parasites occurs through Amazon region of Brazil (0° 02′ 10.91″ S; 51° 09′ 39.42″ sporozoite inoculation during vector hematophagy (Davies W). Blood samples of euthanized specimens by means of 1995;Siddall1995; Davies and Johnston 2000). medullary sectioning were taken by puncturing the ventral In Brazil, the only existing records of haemogregarines in pulmonary artery using insulin syringes containing 10% fish are Desseria mugili (Carini, 1932) Siddall, 1995, in Mugil EDTA. These samples were used to prepare blood smear liza Cuvier and Valenciennes, 1836; Haemogregarina slides, which were air-dried, fixed using absolute methanol platessae Lebailly, 1905, in Paralichthys orbignyanus for 3 min, and stained with 10% Giemsa for 30 min. The blood Valenciennes, 1839; and Cyrilia lignieresi Lainson, 1981, in smear slides were examined under optical microscopy using a Synbranchus marmoratus Bloch, 1795 (Siddall 1995; Davies calibrated ocular micrometer at × 1000 magnification under et al. 2008; Eiras et al. 2012); and Cyrilia sp. in cururu sting- oil immersion for morphological and morphometric character- ray (Potamotrygon cf. histrix) and Potamotrygon wallacei, ization of the haemogregarines. The following measurements from Mariuá Archipelago, Negro River, in the Brazilian were analyzed: (1) length and width of parasites; (2) dimen- Amazon Basin (Magro et al. 2016; Oliveira et al. 2017). sions of infected and non-infected erythrocytes; and (3) di- These descriptions of intracellular parasites were made mensions of the nuclei of infected and non-infected erythro- using only the morphological aspects of the hemoparasites; cytes. The parasitemia level was estimated based on examina- however, the morphological descriptions are improper and tion of 2000 erythrocytes, in 20 replicates of 100 erythrocytes uncertain because it is difficult to differentiate (Desser per field examined, on one slide from each fish from which 1993). This is a potentially important gap in the knowledge blood samples were obtained (Godfrey Jr et al. 1987, 1990). of these parasites, because there is reason to suspect that haemogregarines could be highly diversified, especially Molecular and phylogenetic analysis Haemogregarina spp. (Úngari et al. 2018). Although a recent- ly study provided the first molecular data of Haemogregarina Genomic DNA from two samples that had been found to be bigemina from marine fish (Hayes and Smit 2019), no studies positive for Haemogregarina sp. through blood smears was using molecular tools to determine the species of isolated from 200 μL of blood, using the illustra blood Haemogregarina in freshwater fish have been conducted genomicPrep Mini Spin Kit (GE Healthcare), following the and reported. There is a need to use molecular markers to manufacturer’sinstructions. delimit the species of haemogregarines and thus distinguish DNA samples were screened for the presence of the taxa and clarify the biodiversity of this group, so as to set Haemogregarina spp., using the primers HepF300 and future taxonomic work on a firm footing. Hep900, which amplify 600 bp of the 18S rRNA gene Hence, the aim of the present study was to describe a new (Ujvarietal.2004). The PCR conditions were 94 °C for species of Haemogregarina in L. paradoxa, from the eastern 3 min, 35 cycles at 94 °C for 45 s, 56 °C for 1 min, 72 °C Amazon region of Brazil, using the features of its morphology for 1 min, and a final extension step at 72 °C for 7 min. For and molecular biology. additional sequencing and phylogenetic analysis, the two pos- itive samples in the first PCR were also amplified using the 4558/2733 primer pair (Mathew et al. 2000), which target a Materials and methods larger fragment (1120 bp) of the 18S rRNA gene. The PCR conditions of the secondary PCR consisted of a pre-PCR step Authorization at 94 °C for 3 min, followed by 40 cycles of 94 °C for 1 min, 55 °C for 2 min, an extension at 72 °C for 2 min, and a final This study was developed according to the principles adopted extension at 72 °C for 10 min. A negative control (distilled by the Brazilian College of Animal Experimentation water) and a positive control (Hepatozoon canis DNA isolated (COBEA) and with the participation of the Embrapa Amapá from naturally infected dogs) were used in each reaction. The Animal Use Committee (#004-CEUA/CPAFAP) and ICMBio PCR products were purified and sequenced using the (Chico Mendes Institute of Biodiversity; SISBIO number: BigDye™ Terminator v.3.1 cycle sequencing ready reaction 37846-1). kit (Applied Biosystems, Foster City, CA, USA) and the ABI 3500 genetic analyzer (Applied Biosystems, Foster City, CA, Site of collection, fish capture, and haemogregarine USA). survey procedures The DNA sequences obtained in this study were edited using the BioEdit software v7.2.5 (Hall 1999) and were com- In June and July 2016 and February 2017, four specimens of pared for similarity to the sequences available in GenBank® L. paradoxa (three males and one female) were caught using using BLAST. Multiple alignment, for the two sequences ob- hooks and dip nets in the Igarapé Fortaleza basin, in the tained here and 25 sequences retrieved from GenBank®, was Parasitol Res (2019) 118:2773–2779 2775 performed using the MUSCLE algorithm and the GENEIOUS A phylogenetic tree (Fig. 2), inferred from a 1020 bp frag- v.7.1.3 software. Only the sequences with at least 1000 bp ment of the 18S rRNA gene from 27 sequences, showed that were used for the multiple alignment. The best evolutionary H. daviesensis sp. nov. obtained
Recommended publications
  • Haemogregariny Parazitující U Želv Rodu Pelusios: Fylogenetické Vztahy, Morfologie a Hostitelská Specifita
    Haemogregariny parazitující u želv rodu Pelusios: fylogenetické vztahy, morfologie a hostitelská specifita Diplomová práce Bc. Aneta Maršíková Školitel: MVDr. Jana Kvičerová, Ph.D. Školitel specialista: doc. MVDr. Pavel Široký, Ph.D. České Budějovice 2016 Maršíková A., 2016: Haemogregariny parazitující u želv rodu Pelusios: fylogenetické vztahy, morfologie a hostitelská specifita. [Haemogregarines in Pelusios turtles: phylogenetic relationships, morphology, and host specificity, MSc. Thesis, in Czech] – 68 pp., Faculty of Science, University of South Bohemia, České Budějovice, Czech Republic. Annotation: The study deals with phylogenetic relationships, morphology and host specificity of blood parasites Haemogregarina sp. infecting freswater turtles of the genus Pelusios from Africa. Results of phylogenetic analyses are also used for clarification of phylogenetic relationships between "haemogregarines sensu lato" and genus Haemogregarina. Prohlašuji, že svoji diplomovou práci jsem vypracovala samostatně pouze s použitím pramenů a literatury uvedených v seznamu citované literatury. Prohlašuji, že v souladu s § 47b zákona č. 111/1998 Sb. v platném znění souhlasím se zveřejněním své bakalářské práce, a to v nezkrácené podobě – v úpravě vzniklé vypuštěním vyznačených částí archivovaných Přírodovědeckou fakultou - elektronickou cestou ve veřejně přístupné části databáze STAG provozované Jihočeskou univerzitou v Českých Budějovicích na jejích internetových stránkách, a to se zachováním mého autorského práva k odevzdanému textu této kvalifikační práce. Souhlasím dále s tím, aby toutéž elektronickou cestou byly v souladu s uvedeným ustanovením zákona č. 111/1998 Sb. zveřejněny posudky školitele a oponentů práce i záznam o průběhu a výsledku obhajoby kvalifikační práce. Rovněž souhlasím s porovnáním textu mé kvalifikační práce s databází kvalifikačních prací Theses.cz provozovanou Národním registrem vysokoškolských kvalifikačních prací a systémem na odhalování plagiátů.
    [Show full text]
  • Identifying Heterogeneity in Rates of Morphological Evolution: Discrete Character Change in the Evolution of Lungfish (Sarcopterygii; Dipnoi)
    ORIGINAL ARTICLE doi:10.1111/j.1558-5646.2011.01460.x IDENTIFYING HETEROGENEITY IN RATES OF MORPHOLOGICAL EVOLUTION: DISCRETE CHARACTER CHANGE IN THE EVOLUTION OF LUNGFISH (SARCOPTERYGII; DIPNOI) Graeme T. Lloyd,1,2 Steve C. Wang,3 and Stephen L. Brusatte4,5 1Department of Palaeontology, Natural History Museum, Cromwell Road, London SW7 5BD, United Kingdom 2E-mail: [email protected] 3Department of Mathematics and Statistics, Swarthmore College, Swarthmore, Pennsylvania 19081 4Division of Paleontology, American Museum of Natural History, Central Park West at 79th Street, New York, New York 10024 5Department of Earth and Environmental Sciences, Columbia University, New York, New York 10025 Received February 9, 2010 Accepted August 15, 2011 Data Archived: Dryad: doi:10.5061/dryad.pg46f Quantifying rates of morphological evolution is important in many macroevolutionary studies, and critical when assessing possible adaptive radiations and episodes of punctuated equilibrium in the fossil record. However, studies of morphological rates of change have lagged behind those on taxonomic diversification, and most authors have focused on continuous characters and quantifying patterns of morphological rates over time. Here, we provide a phylogenetic approach, using discrete characters and three statistical tests to determine points on a cladogram (branches or entire clades) that are characterized by significantly high or low rates of change. These methods include a randomization approach that identifies branches with significantly high rates and likelihood ratio tests that pinpoint either branches or clades that have significantly higher or lower rates than the pooled rate of the remainder of the tree. As a test case for these methods, we analyze a discrete character dataset of lungfish, which have long been regarded as “living fossils” due to an apparent slowdown in rates since the Devonian.
    [Show full text]
  • A New Species of Hepatozoon (Apicomplexa: Adeleorina) from Python Regius (Serpentes: Pythonidae) and Its Experimental Transmission by a Mosquito Vector
    J. Parasitol., 93(?), 2007, pp. 1189–1198 ᭧ American Society of Parasitologists 2007 A NEW SPECIES OF HEPATOZOON (APICOMPLEXA: ADELEORINA) FROM PYTHON REGIUS (SERPENTES: PYTHONIDAE) AND ITS EXPERIMENTAL TRANSMISSION BY A MOSQUITO VECTOR Michal Sloboda, Martin Kamler, Jana Bulantova´*, Jan Voty´pka*†, and David Modry´† Department of Parasitology, University of Veterinary and Pharmaceutical Sciences, Palacke´ho 1-3, 612 42 Brno, Czech Republic. e-mail: [email protected] ABSTRACT: Hepatozoon ayorgbor n. sp. is described from specimens of Python regius imported from Ghana. Gametocytes were found in the peripheral blood of 43 of 55 snakes examined. Localization of gametocytes was mainly inside the erythrocytes; free gametocytes were found in 15 (34.9%) positive specimens. Infections of laboratory-reared Culex quinquefasciatus feeding on infected snakes, as well as experimental infection of juvenile Python regius by ingestion of infected mosquitoes, were performed to complete the life cycle. Similarly, transmission to different snake species (Boa constrictor and Lamprophis fuliginosus) and lizards (Lepidodactylus lugubris) was performed to assess the host specificity. Isolates were compared with Hepatozoon species from sub-Saharan reptiles and described as a new species based on the morphology, phylogenetic analysis, and a complete life cycle. Hemogregarines are the most common intracellular hemo- 3 genera (Telford et al., 2004). Low host specificity of Hepa- parasites found in reptiles. The Hemogregarinidae, Karyolysi- tozoon spp. is supported by experimental transmissions between dae, and Hepatozoidae are distinguished based on the different snakes from different families. Ball (1967) observed experi- developmental patterns in definitive (invertebrate) hosts oper- mental parasitemia with Hepatozoon rarefaciens in the Boa ating as vectors; all 3 families have heteroxenous life cycles constrictor (Boidae); the vector was Culex tarsalis, which had (Telford, 1984).
    [Show full text]
  • New Locality for Lepidosiren Paradoxa (Fitzinger, 1837)(Dipnoi
    13 3 the journal of 2118 biodiversity data 20 May 2017 Check List NOTES ON GEOGRAPHIC DISTRIBUTION Check List 13(3): 2118, 20 May 2017 https://doi.org/10.15560/13.3.2118 ISSN 1809-127X © 2017 Check List and Authors New locality for Lepidosiren paradoxa (Fitzinger, 1837) (Dipnoi: Lepidosirenidae) in Argentina Evelyn Romina Vallone Laboratorio de Paleontología de Vertebrados, Centro de Investigaciones Científicas y Transferencia de Tecnología a la Producción (CICyTTP-CONICET), Materi y España, 3105 Diamante, ER, Argentina E-mail: [email protected] Abstract. This study documents a new locality of the lungfish was caught by a local fisherman in shallow waters (depth of Lepidosiren paradoxa on the coast of the Entre Rios Province approximately 3 m) in a coastal area of the locality of Gen- in the lower Paraná River. This finding represents the third eral Alvear, Entre Ríos Province, Argentina (31°55ʹ27.60ʺ S, southern record of this species on southern of South America. 060°39ʹ45.52ʺ W) (Fig. 1). After collection, the specimen was Additionally, as this region has been relatively well sampled frozen and transported to the laboratory for identification. The both during past decades and currently, I discuss possible specimen was identified according to diagnosis of Ringuelet reasons why this new specimen has been observed only et al. (1967) then deposited in the Fish Collection of the Labo- recently. ratorio de Vertebrados, Centro de Investigaciones Científicas y Key words. South American lungfish; Entre Ríos; Paraná River Transferencia de Tecnología a la Producción (CICyTTP-V-18, Diamante, Entre Ríos, Argentina). The description follows the anatomical nomenclature proposed by Ringuelet et al.
    [Show full text]
  • Redalyc.Protozoan Infections in Farmed Fish from Brazil: Diagnosis
    Revista Brasileira de Parasitologia Veterinária ISSN: 0103-846X [email protected] Colégio Brasileiro de Parasitologia Veterinária Brasil Laterça Martins, Mauricio; Cardoso, Lucas; Marchiori, Natalia; Benites de Pádua, Santiago Protozoan infections in farmed fish from Brazil: diagnosis and pathogenesis. Revista Brasileira de Parasitologia Veterinária, vol. 24, núm. 1, enero-marzo, 2015, pp. 1- 20 Colégio Brasileiro de Parasitologia Veterinária Jaboticabal, Brasil Available in: http://www.redalyc.org/articulo.oa?id=397841495001 How to cite Complete issue Scientific Information System More information about this article Network of Scientific Journals from Latin America, the Caribbean, Spain and Portugal Journal's homepage in redalyc.org Non-profit academic project, developed under the open access initiative Review Article Braz. J. Vet. Parasitol., Jaboticabal, v. 24, n. 1, p. 1-20, jan.-mar. 2015 ISSN 0103-846X (Print) / ISSN 1984-2961 (Electronic) Doi: http://dx.doi.org/10.1590/S1984-29612015013 Protozoan infections in farmed fish from Brazil: diagnosis and pathogenesis Infecções por protozoários em peixes cultivados no Brasil: diagnóstico e patogênese Mauricio Laterça Martins1*; Lucas Cardoso1; Natalia Marchiori2; Santiago Benites de Pádua3 1Laboratório de Sanidade de Organismos Aquáticos – AQUOS, Departamento de Aquicultura, Universidade Federal de Santa Catarina – UFSC, Florianópolis, SC, Brasil 2Empresa de Pesquisa Agropecuária e Extensão Rural de Santa Catarina – Epagri, Campo Experimental de Piscicultura de Camboriú, Camboriú, SC, Brasil 3Aquivet Saúde Aquática, São José do Rio Preto, SP, Brasil Received January 19, 2015 Accepted February 2, 2015 Abstract The Phylum Protozoa brings together several organisms evolutionarily different that may act as ecto or endoparasites of fishes over the world being responsible for diseases, which, in turn, may lead to economical and social impacts in different countries.
    [Show full text]
  • Haemocystidium Spp., a Species Complex Infecting Ancient Aquatic Turtles of the Family Podocnemididae First Report of These
    IJP: Parasites and Wildlife 10 (2019) 299–309 Contents lists available at ScienceDirect IJP: Parasites and Wildlife journal homepage: www.elsevier.com/locate/ijppaw Haemocystidium spp., a species complex infecting ancient aquatic turtles of the family Podocnemididae: First report of these parasites in Podocnemis T vogli from the Orinoquia Leydy P. Gonzáleza,b, M. Andreína Pachecoc, Ananías A. Escalantec, Andrés David Jiménez Maldonadoa,d, Axl S. Cepedaa, Oscar A. Rodríguez-Fandiñoe, ∗ Mario Vargas‐Ramírezd, Nubia E. Mattaa, a Departamento de Biología, Facultad de Ciencias, Universidad Nacional de Colombia, Sede Bogotá, Carrera 30 No 45-03, Bogotá, Colombia b Instituto de Biotecnología, Facultad de Ciencias, Universidad Nacional de Colombia, Sede Bogotá, Carrera 30 No 45-03, Bogotá, Colombia c Department of Biology/Institute for Genomics and Evolutionary Medicine (iGEM), Temple University, Philadelphia, PA, USA d Instituto de Genética, Universidad Nacional de Colombia, Sede Bogotá, Carrera 30 No 45-03, Bogotá, Colombia e Fundación Universitaria-Unitrópico, Dirección de Investigación, Grupo de Investigación en Ciencias Biológicas de la Orinoquía (GINBIO), Colombia ARTICLE INFO ABSTRACT Keywords: The genus Haemocystidium was described in 1904 by Castellani and Willey. However, several studies considered Haemoparasites it a synonym of the genera Plasmodium or Haemoproteus. Recently, molecular evidence has shown the existence Reptile of a monophyletic group that corresponds to the genus Haemocystidium. Here, we further explore the clade Simondia Haemocystidium spp. by studying parasites from Testudines. A total of 193 individuals belonging to six families of Chelonians Testudines were analyzed. The samples were collected in five localities in Colombia: Casanare, Vichada, Arauca, Colombia Antioquia, and Córdoba. From each individual, a blood sample was taken for molecular analysis, and peripheral blood smears were made, which were fixed and subsequently stained with Giemsa.
    [Show full text]
  • Download Article (PDF)
    OCCASONAL PAPER NO. 48 RECORDS OF THE ZOOLOGICAL SURVEY OF INDIA MISCELLANEOUS PUBLICATION OCCASIONAL PAPER NO. 48 INDEX-CATALOGUE OF AVIAN HAEMATOZOA FROM INDIA By N. C. NANDI Zoological Survey of India, Kakdwip Field Station Kakd\vip, West Bengal ~ar1fI Edited by the Director, Zoological Survey of India 1984 C Copyright, Government of India, 1984 Published in May, 1984 PRICE: Inland: Rs. 27-00 Foreign: £ 3-00 S 6-00 PRINTED IN INDIA AT IMPRINTA, 243/2B, A. P. c. ROAD, CALCUTTA-6 AND PUBLISHED BY THB DIRECTOR, ZOOLOGICAL SURVEY OF INDIA, CALCUTrA RECORDS OF THE ZOOLOGICAL SURVEY OF INDIA MISCELLANEOUS PUBLICATION OCCASIONAL PAPER No. 48 1984 Pages 1-64 CONTENTS Pages INTRODUCTION ... 1 SYSTEMATIC POSITION OF THB AVIAN HABMATOZOA 1 SPECIES CATALOGUE 3 Genus Trypanosoma 3 Lankesterella 5 Toxoplasma 5 LeucocytozoOD 6 Haemoproteus 8 Plasmodium 15 Babesia 17 M i crofila ria 17 Unidentified parasites 20 HOST CATALOGUE 21 Order Ciconiformes 21 Family Ardeidae 21 Family Threskiornithidae .00 21 Order Anseriformes 21 Family Anatidae ... ... 21 Order Falconiformes ... ... 21 Family Accipitridae 00' 21 Family Falconidae 22 Order Galliformes .. , 22 Family Megapodiidae 22 Family Phasianidae .0' 22 Order Gruiformes .00 23 Family Turnicidae 23 Family Rallidae ... 23 Order Charadriiformes ." 24 Family Charadriidae 24 Order Columbiformes 24 Family Columbidae 24 ( ii ) Order Psittaciformes 25 Family Psittacidae ... 25 Order Cuculiformes 2S Family Cuculidae 25 Order Strigiformes 25 Family Strigidae 25 Order Coraciiformes 26 Family Alcedinidae 26 Family Meropidae 26 Family Coraciidae 27 Family Upupidae 27 Order Piciformes 27 Family Capitonidae 27 Family Picidae 28 Order Passeriformes 28 Family Pittidae ... 28 Alaudidae ... 29 Campephagidae 29 Dicruridae 29 Oriolidae 29 Corvidae 30 Paridae 31 Sittidae 31 Timaliidae 3L Pycnonotidae 32 Aegithinidae 33 Turdidae 33 Sylviidae 34 M uscicapidae 35 Motacillidae 36 Laniidae ..
    [Show full text]
  • Redescription, Molecular Characterisation and Taxonomic Re-Evaluation of a Unique African Monitor Lizard Haemogregarine Karyolysus Paradoxa (Dias, 1954) N
    Cook et al. Parasites & Vectors (2016) 9:347 DOI 10.1186/s13071-016-1600-8 RESEARCH Open Access Redescription, molecular characterisation and taxonomic re-evaluation of a unique African monitor lizard haemogregarine Karyolysus paradoxa (Dias, 1954) n. comb. (Karyolysidae) Courtney A. Cook1*, Edward C. Netherlands1,2† and Nico J. Smit1† Abstract Background: Within the African monitor lizard family Varanidae, two haemogregarine genera have been reported. These comprise five species of Hepatozoon Miller, 1908 and a species of Haemogregarina Danilewsky, 1885. Even though other haemogregarine genera such as Hemolivia Petit, Landau, Baccam & Lainson, 1990 and Karyolysus Labbé, 1894 have been reported parasitising other lizard families, these have not been found infecting the Varanidae. The genus Karyolysus has to date been formally described and named only from lizards of the family Lacertidae and to the authors’ knowledge, this includes only nine species. Molecular characterisation using fragments of the 18S gene has only recently been completed for but two of these species. To date, three Hepatozoon species are known from southern African varanids, one of these Hepatozoon paradoxa (Dias, 1954) shares morphological characteristics alike to species of the family Karyolysidae. Thus, this study aimed to morphologically redescribe and characterise H. paradoxa molecularly, so as to determine its taxonomic placement. Methods: Specimens of Varanus albigularis albigularis Daudin, 1802 (Rock monitor) and Varanus niloticus (Linnaeus in Hasselquist, 1762) (Nile monitor) were collected from the Ndumo Game Reserve, South Africa. Upon capture animals were examined for haematophagous arthropods. Blood was collected, thin blood smears prepared, stained with Giemsa, screened and micrographs of parasites captured. Haemogregarine morphometric data were compared with the data for named haemogregarines of African varanids.
    [Show full text]
  • A Lungfish Survivor of the End-Devonian Extinction and an Early Carboniferous Dipnoan
    1 A Lungfish survivor of the end-Devonian extinction and an Early Carboniferous dipnoan 2 radiation. 3 4 Tom J. Challands1*, Timothy R. Smithson,2 Jennifer A. Clack2, Carys E. Bennett3, John E. A. 5 Marshall4, Sarah M. Wallace-Johnson5, Henrietta Hill2 6 7 1School of Geosciences, University of Edinburgh, Grant Institute, James Hutton Road, Edinburgh, 8 EH9 3FE, UK. email: [email protected]; tel: +44 (0) 131 650 4849 9 10 2University Museum of Zoology Cambridge, Downing Street, Cambridge CB2 3EJ, UK. 11 12 3Department of Geology, University of Leicester, Leicester LE1 7RH, UK. 13 14 4School of Ocean & Earth Science, University of Southampton, National Oceanography Centre, 15 European Way, University Road, Southampton, SO14 3ZH , UK. 16 17 5Sedgwick Museum, Department of Earth Sciences, University of Cambridge, Downing St., 18 Cambridge CB2 3EQ, UK 1 19 Abstract 20 21 Until recently the immediate aftermath of the Hangenberg event of the Famennian Stage (Upper 22 Devonian) was considered to have decimated sarcopterygian groups, including lungfish, with only 23 two taxa, Occludus romeri and Sagenodus spp., being unequivocally recorded from rocks of 24 Tournaisian age (Mississippian, Early Carboniferous). Recent discoveries of numerous 25 morphologically diverse lungfish tooth plates from southern Scotland and northern England indicate 26 that at least ten dipnoan taxa existed during the earliest Carboniferous. Of these taxa, only two, 27 Xylognathus and Ballgadus, preserve cranial and post-cranial skeletal elements that are yet to be 28 described. Here we present a description of the skull of a new genus and species of lungfish, 29 Limanichthys fraseri gen.
    [Show full text]
  • I Ecomorphological Change in Lobe-Finned Fishes (Sarcopterygii
    Ecomorphological change in lobe-finned fishes (Sarcopterygii): disparity and rates by Bryan H. Juarez A thesis submitted in partial fulfillment of the requirements for the degree of Master of Science (Ecology and Evolutionary Biology) in the University of Michigan 2015 Master’s Thesis Committee: Assistant Professor Lauren C. Sallan, University of Pennsylvania, Co-Chair Assistant Professor Daniel L. Rabosky, Co-Chair Associate Research Scientist Miriam L. Zelditch i © Bryan H. Juarez 2015 ii ACKNOWLEDGEMENTS I would like to thank the Rabosky Lab, David W. Bapst, Graeme T. Lloyd and Zerina Johanson for helpful discussions on methodology, Lauren C. Sallan, Miriam L. Zelditch and Daniel L. Rabosky for their dedicated guidance on this study and the London Natural History Museum for courteously providing me with access to specimens. iii TABLE OF CONTENTS ACKNOWLEDGEMENTS ii LIST OF FIGURES iv LIST OF APPENDICES v ABSTRACT vi SECTION I. Introduction 1 II. Methods 4 III. Results 9 IV. Discussion 16 V. Conclusion 20 VI. Future Directions 21 APPENDICES 23 REFERENCES 62 iv LIST OF TABLES AND FIGURES TABLE/FIGURE II. Cranial PC-reduced data 6 II. Post-cranial PC-reduced data 6 III. PC1 and PC2 Cranial and Post-cranial Morphospaces 11-12 III. Cranial Disparity Through Time 13 III. Post-cranial Disparity Through Time 14 III. Cranial/Post-cranial Disparity Through Time 15 v LIST OF APPENDICES APPENDIX A. Aquatic and Semi-aquatic Lobe-fins 24 B. Species Used In Analysis 34 C. Cranial and Post-Cranial Landmarks 37 D. PC3 and PC4 Cranial and Post-cranial Morphospaces 38 E. PC1 PC2 Cranial Morphospaces 39 1-2.
    [Show full text]
  • D070p001.Pdf
    DISEASES OF AQUATIC ORGANISMS Vol. 70: 1–36, 2006 Published June 12 Dis Aquat Org OPENPEN ACCESSCCESS FEATURE ARTICLE: REVIEW Guide to the identification of fish protozoan and metazoan parasites in stained tissue sections D. W. Bruno1,*, B. Nowak2, D. G. Elliott3 1FRS Marine Laboratory, PO Box 101, 375 Victoria Road, Aberdeen AB11 9DB, UK 2School of Aquaculture, Tasmanian Aquaculture and Fisheries Institute, CRC Aquafin, University of Tasmania, Locked Bag 1370, Launceston, Tasmania 7250, Australia 3Western Fisheries Research Center, US Geological Survey/Biological Resources Discipline, 6505 N.E. 65th Street, Seattle, Washington 98115, USA ABSTRACT: The identification of protozoan and metazoan parasites is traditionally carried out using a series of classical keys based upon the morphology of the whole organism. However, in stained tis- sue sections prepared for light microscopy, taxonomic features will be missing, thus making parasite identification difficult. This work highlights the characteristic features of representative parasites in tissue sections to aid identification. The parasite examples discussed are derived from species af- fecting finfish, and predominantly include parasites associated with disease or those commonly observed as incidental findings in disease diagnostic cases. Emphasis is on protozoan and small metazoan parasites (such as Myxosporidia) because these are the organisms most likely to be missed or mis-diagnosed during gross examination. Figures are presented in colour to assist biologists and veterinarians who are required to assess host/parasite interactions by light microscopy. KEY WORDS: Identification · Light microscopy · Metazoa · Protozoa · Staining · Tissue sections Resale or republication not permitted without written consent of the publisher INTRODUCTION identifying the type of epithelial cells that compose the intestine.
    [Show full text]
  • Histology of Juvenile Skin of Lepidosiren Paradoxa Fitzinger, 1837 (Sarcopterygii, Dipnoi)
    Anais da Academia Brasileira de Ciências (2019) 91(4): e20190822 (Annals of the Brazilian Academy of Sciences) Printed version ISSN 0001-3765 / Online version ISSN 1678-2690 http://dx.doi.org/10.1590/0001-3765201920190822 www.scielo.br/aabc | www.fb.com/aabcjournal Histology of juvenile skin of Lepidosiren paradoxa Fitzinger, 1837 (Sarcopterygii, Dipnoi) LUIS ALBERTO ROMANO1, ANDREA I.H. LÓPEZ1, JUAN RAFAEL BUITRAGO2 and VIRGÍNIA F. PEDROSA1 1Institute of the Oceanography, University Federal of the Rio Grande, Laboratory of the de Immunology and Pathology of the Aquatic Organisms, Rua do Hotel, 2, Cassino, 96210-030 Rio Grande, RS, Brazil 2University Federal of the Rio Grande, Laboratory of the Biochemistry Functional of Aquatic Organisms, Rua do Hotel, 2, Cassino, 96210-030 Rio Grande, RS, Brazil Manuscript received on July 20, 2019; accepted for publication on September 24, 2019 How to cite: ROMANO LA, LÓPEZ AIH, BUITRAGO JR AND PEDROSA VF. 2019. Histology of juvenile skin of Lepidosiren paradoxa Fitzinger, 1837 (Sarcopterygii, Dipnoi). An Acad Bras Cienc 91: e20190822. DOI 10.1590/0001-3765201920190822. Abstract: The skin of three juvenile Lepidosiren paradoxa specimens was examined. The epidermis was composed of a polystratified epithelium resting on a basement membrane, including mucus-secreting cells, and a cuticle of mucopolysaccharides on the surface. Two types of skin receptors, electroreceptors and mechanoreceptors, were found; the first type was located in the dermoepidermal junction, and the second type was completely intraepiderma. The skin structure of these fish, suggests the possibility of the skin participating in the breath. Key words: electroreceptors, lungfish, mechanoreceptors, Paraná River basin, pirambóia.
    [Show full text]