From mammals back to birds: Host-switch of the acanthocephalan Corynosoma australe from pinnipeds to the Magellanic penguin Spheniscus magellanicus

. 2017 ; 12 (10) : e0183809. [epub] 20171005

Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid28981550

Trophically-transmitted parasites are regularly exposed to potential new hosts through food web interactions. Successful colonization, or switching, to novel hosts, occur readily when 'donor' and 'target' hosts are phylogenetically related, whereas switching between distantly related hosts is rare and may result from stochastic factors (i.e. rare favourable mutations). This study investigates a host-switching event between a marine acanthocephalan specific to pinnipeds that is apparently able to reproduce in Magellanic penguins Spheniscus magellanicus from Brazil. Detailed analysis of morphological and morphometrical data from acanthocephalans from penguins indicates that they belong to Corynosoma australe Johnston, 1937. Partial fragments of the 28S rRNA and mitochondrial cox1 genes were amplified from isolates from penguins and two pinniped species (i.e. South American sea lion Otaria flavescens and South American fur seal Arctocephalus australis) to confirm this identification. Infection parameters clearly differ between penguins and the two pinniped species, which were significantly lower in S. magellanicus. The sex ratio of C. australe also differed between penguins and pinnipeds; in S. magellanicus was strongly biased against males, while in pinnipeds it was close to 1:1. Females of C. australe from O. flavescens were smaller than those from S. magellanicus and A. australis. However, fecundity (i.e. the proportion of fully developed eggs) was lower and more variable in females collected from S. magellanicus. At first glance, the occurrence of reproductive individuals of C. australe in Magellanic penguins could be interpreted as an adaptive colonization of a novel avian host through favourable mutations. However, it could also be considered, perhaps more likely, as an example of ecological fitting through the use of a plesimorphic (host) resource, since the ancestors of Corynosoma infected aquatic birds.

Zobrazit více v PubMed

Agosta SJ, Janz N, Brooks DR. How generalists can be specialists: resolving the ‘parasite paradox’ and implications for emerging disease. Zoologia. 2010;27:151–162.

Futuyma DJ,. Moreno G. The evolution of ecological specialization. Ann. Rev. Ecol. Syst. 1988;19:207–233.

Gemmill AW, Vinet ME, Read AF. The evolutionary ecology of host-specificity: experimental studies with Strongyloides ratti. Parasitology. 2000;120:429–437. PubMed

Via S, Hawthorne DJ. The genetic architecture of ecological specialization: Correlated gene effects on host use and habitat choice in pea aphids. Amer. Nat. 2002;159:S76–S88. PubMed

Agosta SJ. On ecological fitting, plant–insect associations, herbivore host shifts, and host plant selection. Oikos. 2006;114:556–565.

Brooks DR, Hoberg EP. Darwin's necessary misfit and the sloshing bucket: the evolutionary biology of emerging infectious diseases. Evol Educ Outreach. 2008;1:2–9.

Combes C. Ethological aspects of parasite transmission. Am Nat. 1991;138:866–880.

Hoberg EP. Congruent and synchronic patterns in biogeography and speciation among seabirds, pinnipeds and cestodes. J Parasitol. 1992;78:601–615. PubMed

Hoberg EP, Adams A. Phylogeny, history and biodiversity: understanding faunal structure and biogeography in the marine realm. Bull Scand Soc Parasitol. 2000;10:19–37.

McQuaid CF, Britton NF. Trophic structure, stability, and parasite persistence threshold in food webs. Bull Math Biol. 2013;75:2196–207. doi: 10.1007/s11538-013-9887-5 PubMed DOI

Ward SA, Leather SR, Pickup J, Harrington R. Mortality during dispersal and the cost of host-specificity in parasites: how many aphids find hosts? J. Anim. Ecol. 1998;67:763–773.

Raga JA, Fernández M, Balbuena JA, Aznar FJ. Parasites In: Perrin WF, Thewissen HGM, Würsing B. San Diego: editors. Encyclopedia of Marine Mammals, second Ed. Academic Press/Elsevier Inc.; 2009:821–830.

Janz N, Nylin S. Butterflies and plants: a phylogenetic study. Evolution. 1998;52:486–502. doi: 10.1111/j.1558-5646.1998.tb01648.x PubMed DOI

Brooks DR, McLennan DA, León-Règagnon V, Zelmer D. Ecological fitting as a determinant of parasite community structure. Ecology. 2006;87:S76–S85. PubMed

Agosta SJ, Klemens JA. Ecological fitting by phenotypically flexible genotypes: implications for species associations, community assembly and evolution. Ecol. Lett. 2008;11:1123–1134. doi: 10.1111/j.1461-0248.2008.01237.x PubMed DOI

Brooks DR, Hoberg EP. The emerging infectious disease crisis and pathogen pollution: a question of ecology and evolution In: Rohde K. editor. The balance of nature and human impact. Cambridge: Cambridge University Press; 2013. pp. 215–229.

Janzen DH. On ecological fitting. Oikos. 1985;45:308–310.

Aznar FJ, Pérez-Ponce de León G, Raga JA. Status of Corynosoma (Acanthocephala: Polymorphidae) based on anatomical, ecological, and phylogenetic evidence, with the erection of Pseudocorynosoma. J Parasitol. 2006;92:548–564. doi: 10.1645/GE-715R.1 PubMed DOI

Amin OM. Classification of the Acanthocephala. Folia Parasitol. 2013;60:273–305. PubMed

Machado-Filho DA. Nova espécie do gênero Corynosoma Lühe, 1904 (Acanthocephala, Echinorhynchidea). Rev Brasil Biol. 1970;30:377–379.

Noronha D. Corynosoma clementei Giovannoni and Fernandes, 1965 and its synonym Corynosoma seropedicus Machado Filho, 1970, an accidental parasite of Canis familiaris L., 1758. Arq Flum Med Vet. 1988;3:119–120.

Valtonen ET, Niinimaa A. Dispersion and frequency distribution of Corynosoma spp. (Acanthocephala) in the fish of the Bothnian Bay. Aquilo Ser Zool. 1983;22:1–11.

Zdzitowiecki K, Presler P. Occurrence of Acanthocephala in intermediate hosts, Amphipoda, in Admiralty Bay, South Shetland Islands, Antarctica. Polish Polar Res. 2001;22:205–212.

Laskowski Z, Zdzitowiecki K. The helminth fauna of some notothenioid fishes collected from the shelf of Argentine Islands, West Antarctica. Pol Polar Res. 2005;26:315–324.

Hernández-Orts JS. Taxonomy and ecology of metazoan parasites of otariids from Patagonia, Argentina: adult and infective stages. PhD thesis. Valencia, Spain: University of Valencia; 2013.

Petrochenko, 1958 Petrochenko VI. Acanthocephala of Domestic and Wild Animals. Vol. I Izdatel’stvo Akademii Nauk SSSR: Moscow; 1958.

Yamaguti S. Systema Helminthum Volume V: Acanthocephala. Interscience Publisher: New York; 1963.

Aznar FJ, Hernández-Orts J, Suarez AA, García-Varela M, Raga JA, Cappozzo HL. A ssessing host-parasite specificity through coprological analysis: a case study with species of Corynosoma (Acanthocephala: Polymorphidae) from marine mammals. J Helminthol. 2012;86:156–164. PubMed

Hoberg EP. Aspects of ecology and biogeography of Acanthocephala in Antarctic seabirds. Ann Parasitol Hum Comp. 1986;61:199–214.

Zdzitowiecki K. Acanthocephala of the Antarctic. Polish Polar Res. 1986;7:79–117.

Margolis L, Groff JM, Johnson SC, McDonald TE, Kent ML, Blaylock RB. Helminth parasites of sea otters (Enhydra lutris) from Prince William Sound, Alaska: comparisons with other populations of sea otters and comments on the origin of their parasites. J Helminthol Soc Wash. 1997;64:161–168.

Schmidt G. Acanthocephalan infections of man, with two new records. J Parasitol. 1971;57:582–584. PubMed

Richardson DJ, Cole RA. Acanthocephala of the bald eagle (Haliaeetus leucocephalus) in North America. J Parasitol. 1997;83:540–541. PubMed

Smales LR. Polymorphidae (Acanthocephala) from Australian mammals with descriptions of two new species. Syst Parasitol. 1986;8:91–100.

Silva RZ, Cousin JCB, Pereira J Jr. Corynosoma cetaceum Johnston & Best, 1942 (Acanthocephala, Polymorphidae) in Arctocephalus australis Zimmermann, 1783 (Mammalia: Pinnipedia): Histopathology, parasitological indices, seasonality and host gender influences. Estud Biol. 2013;35:121–134.

Stryukov AA. Invasion of Antarctic phocids seals by acanthocephals. Vestn Zool. 2004;38:23–29 (In Russian).

Zdzitowiecki K. Some antarctic acanthocephalans of the genus Corynosoma parasitizing Pinnipedia, with description of three new species. Acta Parasitol. 1984;29:359–377.

Nickol BB, Helle E, Valtonen ET. Corynosoma magdaleni in gray seals from the Gulf of Bothnia, with emended descriptions of Corynosoma strumosum and Corynosoma magdaleni. J Parasitol. 2002;88:1222–1229. doi: 10.1645/0022-3395(2002)088[1222:CMIGSF]2.0.CO;2 PubMed DOI

Hernández-Orts JS, Smales LR, Pinacho-Pinacho CD, García-Varela M, Presswell B. Novel morphological and molecular data for Corynosoma hannae Zdzitowiecki, 1984 (Acanthocephala: Polymorphidae) from teleosts, fish-eating birds and pinnipeds from New Zealand. Parasitol Int. 2017;66:905–916. doi: 10.1016/j.parint.2016.10.007 PubMed DOI

Mattiucci S, Nascetti G. Advances and trends in the molecular systematics of anisakid nematodes, with implications for their evolutionary ecology and host-parasite co-evolutionary processes. Adv Parasit. 2008;66:47–148. PubMed

Sardella NH, Mattiucci S, Timi JT, Bastida RO, Rodríguez DH, Nascetti G. Corynosoma australe Johnston, 1937 and C. cetaceum Johnston & Best, 1942 (Acanthocephala: Polymorphidae) from marine mammals and fishes in Argentinian waters: allozyme markers and taxonomic status. ‎Syst Parasitol. 2005;61:143–156. doi: 10.1007/s11230-005-3131-0 PubMed DOI

Van Cleave HJ. A preliminary analysis of the acanthocephalan genus Corynosoma in mammals of North America. J Parasitol. 1953;39:1–13. PubMed

Hernández-Orts JS, Montero FE, Juan-García A, García NA, Crespo EA, Raga JA, Aznar FJ. Intestinal helminth fauna of the South American sea lion Otaria flavescens and fur seal Arctocephalus australis from northern Patagonia, Argentina. J Helminthol. 2013;87:336–347. doi: 10.1017/S0022149X12000454 PubMed DOI

Schiavini A, Yorio P, Gandini P, Raya Rey A, Dee Boersma P. Los pingüinos de las costas argentinas: estado poblacional y conservación. Hornero 2005;20:5–23.

Aznar FJ, Cappozzo HL, Taddeo D, Montero FE, Raga JA. Recruitment, population structure, and habitat selection of Corynosoma australe (Acanthocephala) in South American fur seals, Arctocephalus australis, from Uruguay. Can J Zool. 2004;82:741–748.

Hernández-Orts JS, Timi JT, Raga JA, García-Varela M, Crespo EA, Aznar FJ. Patterns of trunk spine growth in two congeneric species of acanthocephalan: investment in attachment may differ between sexes and species. Parasitology. 2012;7:945–955. PubMed

Aznar FJ, Bush AO, Balbuena JA, Raga JA. Corynosoma cetaceum in the stomach of franciscanas, Pontoporiablainvillei (Cetacea): an exceptional case of habitat selection by an acanthocephalan. J Parasitol. 2001;87:536–541. doi: 10.1645/0022-3395(2001)087[0536:CCITSO]2.0.CO;2 PubMed DOI

Georgieva S, Selbach C, Faltýnková A, Soldánová M, Sures B, Skírnisson K, Kostadinova A. New cryptic species of the “revolutum” group of Echinostoma (Digenea: Echinostomatidae) revealed by molecular and morphological data. Parasit Vectors. 2013;6:64 doi: 10.1186/1756-3305-6-64 PubMed DOI PMC

Bray RA, Waeschenbach A, Cribb TH, Weedall GD, Dyal P, Littlewood DTJ. The phylogeny of the Lepocreadioidea (Platyhelminthes, Digenea) inferred from nuclear and mitochondrial genes: Implications for their systematics and evolution. Acta Parasitol. 2009;54:310–329.

Tkach VV, Grabda-Kazubska B, Pawlowski J, Swiderski Z. Molecular and morphological evidences for close phylogenetic affinities of the genera Macrodera, Leptophallus, Metaleptophallus and Paralepoderma (Digenea, Plagiorchioidea). Acta Parasitol. 1999;44:170–179.

Nadler SA, Bolotin E, Stock SP. Phylogenetic relationships of Steinernema Travassos, 1927 (Nematoda: Cephalobina: Steinernematidae) based on nuclear, mitochondrial and morphological data. Syst Parasitol. 2006;63:161–181. doi: 10.1007/s11230-005-9009-3 PubMed DOI

Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol. 1994;3:294–299. PubMed

Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol. 2016;33:1870–1874. doi: 10.1093/molbev/msw054 PubMed DOI PMC

García-Varela M, Pérez-Ponce de León G, Aznar FJ, Nadler SA. Phylogenetic relationship among genera of Polymorphidae (Acanthocephala), inferred from nuclear and mitochondrial gene sequences. Mol Phylogenet Evol. 2013;68:176–184. doi: 10.1016/j.ympev.2013.03.029 PubMed DOI

García-Varela M, Nadler SA. Phylogenetic relationships of Palaeacanthocephala (Acanthocephala) inferred from SSU and LSU rDNA gene sequences. J Parasitol. 2005;91:1401–1409. doi: 10.1645/GE-523R.1 PubMed DOI

García-Varela M, Nadler SA. Phylogenetic relationships among Syndermata inferred from nuclear and mitochondrial gene sequences. Mol Phylogenet Evol. 2006;40:61–72. doi: 10.1016/j.ympev.2006.02.010 PubMed DOI

García-Varela M, Pérez-Ponce de León G, Aznar FJ, Nadler SA. Systematic position of Pseudocorynosoma and Andracantha (Acanthocephala, Polymorphidae) based on nuclear and mitochondrial gene sequences. J Parasitol. 2009;95:178–185. doi: 10.1645/GE-1538.1 PubMed DOI

García-Varela M, Pérez-Ponce de León G. Validating the systematic position of Profilicollis Meyer, 1931 and Hexaglandula Petrochenko, 1950 (Acanthocephala: Polymorphidae) using cytochrome c oxidase (cox1). J Parasitol. 2008;94:212–217. doi: 10.1645/GE-1257.1 PubMed DOI

Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30:772–80. doi: 10.1093/molbev/mst010 PubMed DOI PMC

Li W, Cowley A, Uludag M, Gur T, McWilliam H, Squizzato S, et al. The EMBL-EBI bioinformatics web and programmatic tools framework. Nucleic Acids Res. 2015;43:W580–584. doi: 10.1093/nar/gkv279 PubMed DOI PMC

Telford MJ, Herniou EA, Russell RB, Littlewood DTJ. Changes in mitochondrial genetic codes as phylogenetic characters: two examples from the flatworms. Proc Natl Acad Sci USA. 2000;97:11359–11364. doi: 10.1073/pnas.97.21.11359 PubMed DOI PMC

Darriba D, Taboada GL, Doallo R, Posada D. ModelTest 2: more models, new heuristics and parallel computing. Nat Methods. 2012;9:772. PubMed PMC

Sugiura N. Further analysis of the data by Akaike’s information criterion and the finite corrections. Commun Stat Theory Methods. 1978;7:13–26.

Hurvich CM, Tsai CL. Regression and time series model selection in small samples. Biometrika. 1989;76:297–307.

Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012;61:539–542. doi: 10.1093/sysbio/sys029 PubMed DOI PMC

Miller MA, Pfeiffer W, Schwartz T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. New Orleans, United Stages: Proceedings of the Gateway Computing Environments Workshop (GCE); 2010.

Rambaut A, Drummond AJ. Tracer v1.5; 2009. Available from http://beast.bio.ed.ac.uk/Tracer.

Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate Maximum-Likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 2010;59:307–321. doi: 10.1093/sysbio/syq010 PubMed DOI

Rambaut A. FigTree v. 1.4. Molecular evolution, phylogenetics and epidemiology. Edinburgh, UK: University of Edinburgh, Institute of Evolutionary Biology; 2012. http://tree.bio.ed.ac.uk/software/figtree/.

Bush AD, Lafferty KD, Lotz JM, Shostak AW. Parasitology meets ecology on its own terms: Margolis et al. revised. J Parasitol. 1997;84:575–583. PubMed

Rózsa L, Reiczigel J, Majoros G. Quantifying parasites in samples of hosts. J Parasitol. 2000;86:228–232. doi: 10.1645/0022-3395(2000)086[0228:QPISOH]2.0.CO;2 PubMed DOI

Reiczigel J. Confidence intervals for the bionomial parameter: some new considerations. Stat. Med. 2003;22:611–621. doi: 10.1002/sim.1320 PubMed DOI

Reiczigel J, Rozsa L, Reiczigel A, Fabian I. Quantitative Parasitology v1.0.13; 2013. Available from http://www2.univet.hu/qpweb

Conover WJ. Practical Nonparametric Statics. 3rd edition New York: Wiley and Sons; 1999.

Anderson MJ, Gorley RN, Clarke KR. PERMANOVA+ for PRIMER: Guide to software and statistical methods. Plymouth: PRIMER-E; 2008.

Johnston TH, Mawson PM. Nematodes from Australian marine mammals. Rec South Aust Mus. 1941;6:429–434.

Johnston TH. Entozoa from the Australian hair seal. Proc Linn Soc NSW. 1937;62:9–16.

Johnston JT, Edmonds SJ. Acanthocephala from Auckland and Campbell islands. Rec Domin Mus. 1953;2:55–61.

Morini EG, Boero JJ. Corynosoma otariae n. sp. (Acanthocephala; Polymorphidae) parásito de un lobo marino (Otaria flavescens). Acta Trab Congr Sudam Zoología. La Plata, Argentina; 1959:229–234.

Brandão ML, Moreira J, Luque JL. Checklist of Platyhelminthes, Acanthocephala, Nematoda and Arthropoda parasitizing penguins of the world. Check List. 2014;10:562–573.

Boero JJ, Led JE, Brandetti E. Algunos parásitos de la avifauna Argentina. Analecta Vet. 1972;4:17–32.

Diaz J, Cremonte F, Navone GT. Helminths of the Magellanic penguin, Spheniscus magellanicus (Sphenisciformes), during the breeding season in Patagonian Coast, Chubut, Argentina. Comp Parasitol. 2010;77:172–177.

Spalding MD, Fox HE, Allen GR, Davidson N, Ferdaña ZA, Finlayson M et al. Marine ecoregions of the world: abioregionalization of coastal and shelf areas. Bioscience. 2007;57:573–583.

Silva RZ, Pereira J. Jr, Cousin JCB: Histological patterns of the intestinal attachment of Corynosoma australe (Acanthocephala: Polymorphidae) in Arctocephalus australis (Mammalia: Pinnipedia). J Parasit Dis. 2014;38:410–416. doi: 10.1007/s12639-013-0250-4 PubMed DOI PMC

Luque JL, Poulin R. Use of fish as intermediate hosts by helminth parasites: A comparative analysis. Acta Parasitol. 2004;49:353–361.

Koen-Alonso M, Crespo EA, Pedraza SN, García NA, Coscarella MA. Food habits of the South American sea lion, Otaria flavescens, off Patagonia, Argentina. Fish Bull. 2000;98:250–263.

Naya DE, Arim M, Vargas R. Diet of South American fur seals (Arctocephalus australis) in Isla de Lobos, Uruguay. Mar Mam Sci. 2002;18:734–745.

Knoff M, São Clemente SC, Pinto RM, Gomes DC. Digenea and Acanthocephala of elasmobranch fishes from the southern coast of Brazil. Mem Inst Oswaldo Cruz. 2001;96:1095–1101. PubMed

Scolaro JA, Badano LA. Diet of the Magellanic penguin Spheniscus magellanicus during the chick-rearing period at Punta Clara, Argentina. Cormorant. 1986;13:91–97.

Frere E, Gandini P, Lichtscheln V. Variación latitudinal en la dieta del pinguino de Magallanes (Spheniscus magellanicus) en la costa patagónica, Argentina. Ornitol Neotrop. 1996;7:35–41.

Scolaro JA, Wilson RP, Laurenti S, Kierspel MA, Gallelli H, Upton JA. Feeding preferences of the Magellanic penguin Spheniscus magellanicus over its breeding range in Argentina. Waterbirds 1999;22:104–110.

Timi JT, Poulin R. Parasite community structure within and across host populations of a marine pelagic fish: How repeatable is it? Int J Parasitol. 2003;33:1353–1362. PubMed

Carballo MC, Cremonte F, Navone GT, Timi JT. Similarity in parasite community structure may be used to trace latitudinal migrations of Odontesthes smitti along Argentinean coasts. J Fish Biol. 2012;80:15–28. doi: 10.1111/j.1095-8649.2011.03125.x PubMed DOI

González AF, Pascual S, Gestal C, Abollo E, Guerra A. What makes a cephalopod a suitable host for parasite? The case of Galician waters. Fish Res. 2003;60:177–183.

Valtonen ET, Helle E. Experimental infection of laboratory rats with Corynosoma semerme (Acanthocephala). Parasitology. 1982;85:9–19. PubMed

Crompton DW. Reproduction In: Crompton DWT, Nickol BB, editors. Biology of the Acanthocephala. Cambridge: Cambridge University Press; 1985. pp. 213–271.

Helle E, Valtonen ET. On the occurrence of Corynosoma spp. (Acanthocephala) in ringed seals (Pusahispida) in the Bothnian Bay, Finland. Can J Zool. 1980;58:298–303.

Pütz K, Schiavini A, Raya Rey A, Lüthi BH. Winter migration of magellanic penguins (Spheniscusma gellanicus) from the southernmost distributional range. Mar Biol. 2007;152:1227–1235.

García-Borboroglu P, Boersma PD, Ruoppolo V, Pinho-da-Silva-Filho R, Corrado-Adornes A, Conte-Sena D, et al. Magellanic penguin mortality in 2008 along the SW Atlantic coast. Marine Poll Bull. 2010;60:1652–1657. PubMed

Mateu P, Raga JA, Aznar FJ. Host specificity of Oschmarinella rochebruni and Brachycladium atlanticum (Digenea: Brachycladiidae) in five cetacean species from western Mediterranean waters. J Helminthol. 2011;85:12–19. doi: 10.1017/S0022149X10000180 PubMed DOI

Fraija-Fernández N, Olson PD, Crespo EA, Raga JA, Aznar FJ, Fernández M. Independent host switching events by digenean parasites of cetaceans inferred from ribosomal DNA. Int J Parasitol. 2015;45:167–173. doi: 10.1016/j.ijpara.2014.10.004 PubMed DOI

Nadler SA, D'Amelio S, Fagerholm HP, Berland B, Paggi L. Phylogenetic relationships among species of Contracaecum Railliet & Henry, 1912 and Phocascaris Høst, 1932 (Nematoda: Ascaridoidea) based on nuclear rDNA sequence data. Parasitology. 2000;121:455–463. PubMed

Gregori M, Aznar FJ, Abollo E, Roura A, González A, Pascual S. Nyctiphanes couchii as intermediate host for the acanthocephalan Bolbosoma balaenae in temperate waters of the NE Atlantic. Dis. Aquat. Org. 2012;99: 37–47. doi: 10.3354/dao02457 PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...