Abstract
A comprehensive literature review shows that 12 types of pathogens, micropredators and parasites are reported to interact with chaetognaths, mostly digenean trematodes, cestodes and nematodes larval stages. Through analysis of 78,152 chaetognaths from a monthly zooplankton time series (Jan 1996–Dec 1998) collected in the Mexican Central Pacific twelve acanthocephalan larvae parasitizing chaetognaths were discovered. This is the first record of an acanthocephalan parasitizing chaetognaths, raising to 13 the types of symbionts known to interact with them (excluding predators). Cystacanth larval specimens of Corynosoma sp. (Polymorphidae) were observed parasitizing the head, trunk and caudal cavities of three of the eight chaetognath species inhabiting this tropical coastal region (Flaccisagitta enflata, Flaccisagitta hexaptera and Zonosagitta bedoti). Because Corynosoma sp. parasitized chaetognaths during different months and years (Jan–Feb 1996, Mar and Jul 1997, Jan, Jun, Aug–Sep 1998) and because the total length of these cystacanths varied between 165–480 µm, suggesting growth inside the hosts, we conclude that chaetognaths are intermediate hosts of Corynosoma sp. The twelve parasitized chaetognaths were juveniles (without gonads) or immature adults (none in reproductively mature stage IV); therefore Corynosoma may have a negative influence on host reproduction. Marine crustaceans (amphipods, decapods, copepods, mysids and euphausiids) and fishes are common intermediate or paratenic hosts of acanthocephalans. Fish, sea birds and marine mammals are definitive hosts for marine Corynosoma species. The present discovery implies that acanthocephalans are transmitted trophically through different intermediate hosts (crustaceans, chaetognaths and/or fish); thus chaetognaths can also be part of the marine acanthocephalan life cycle.
Similar content being viewed by others
References
Alvariño A. 1963. Quetognatos epiplanctónicos del Mar de Cortés. Revista de la Sociedad Mexicana de Historia Natural, 24, 97–203
Alvariño A. 1965. Distributional atlas of chaetognaths in the California Current region. California Cooperative Oceanic Fisheries Investigations Atlas, 3, 1–291
Ambriz-Arreola I., Gómez-Gutiérrez J., Franco-Gordo M.C., La-vaniegos B.E., Godínez-Domínguez E. 2012. Influence of coastal upwelling-downwelling variability on tropical eu-phausiid abundance and community structure in the inshore Mexican central Pacific. Marine Ecology Progress Series, 451, 119–136. DOI: 10.3354/meps09607
Amin O.M. 1998. Marine flora and fauna of the eastern United States. Acanthocephala. National Oceanic and Atmospheric Administration Technichal Report National Marine Fisheries Service, 135, 1–32
Anderson R.M., Schad G.A. 1985. Hookworm burdens and faecal egg counts: an analysis of the biological basis of variation. Transactions of the Royal Society of Tropical Medicine and Hygiene, 79, 812–825. DOI: 10.1016/0035-9203(85)90128-2
Aznar F.J., Pérez-Ponce de León G., Raga J.A. 2006. Status of Corynosoma (Acanthocephala: Polymorphidae) based on anatomical, ecological, and phylogenetic evidence, with the erection of Pseudocorynosoma n. gen. Journal of Parasitology, 92, 584–564. DOI: 10.1645/GE-715R.1
Barnes R.D. 1982. Invertebrate Zoology. Philadelphia, PA: Holt-Saunders International. pp. 1046–1050. ISBN 0-03-056747-5
Bieri R. 1991a. Systematics of the Chaetognatha. In: (Eds. Bone Q., Kapp H. and Pierrot-Bults A.C.). The Biology of Chaetog-naths. Oxford Science Publications, USA, pp. 122–136
Bieri R. 1991b. Six new genera in the chaetognath family Sagittidae. Gulf Research Reports, 8, 221–226. DOI: 10.18785/grr.0803.01
Braicovich P.E., González R.A., Tanzola R.D. 2005. First record of Corynosoma australe (Acanthocephala, Polymorphidae) parasitizing seahorse, Hippocampus sp. (Pisces, Syngnathidae) in Patagonia (Argentina). Acta Parasitologica, 50, 145–149
Bush A.O., Lafferty K.D., Lotz J.M., Shostak A.W. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology, 83, 575–583. DOI: 10.2307/3284227
Busch M.W., Kuhn T., Munster J., Klimpel S. 2012. Chapter 14 Marine crustaceans as potential host and vectors for metazoan parasites. (In: Ed. H. Melhorn), Arthropods as vectors of emerging diseases, Parasitology Research Monographs 3, 329–360
Busch W. 1851. Beobachtungen uber Anatomie und Entwicklung einiger wirbellosen Seethiere. Berlin, pp. 99–100
Chatton É. 1912. Diagnoses préliminaires de Péridiniens parasites nouveaux. Bulletin de la Société Zoologique de France, 37, 85–93
Daponte M.C., Gil de Pertierra A.A., Palmieri M.A., Ostrowski de Nuñez M. 2008. Monthly occurrence of parasites of the chaetognath Sagitta friderici off Mar del Plata, Argentina. Journal of Plankton Research, 30, 567–576. DOI: 10.1093/plank/fbn019
Delaymure S.L. 1955. Helminthofauna of marine mammals (Ecology and Phylogeny). Academy of Sciences of the U. S. S. R. Laboratory of Helminthology, pp. 522. (In Russian)
Flores-Cascante L., Gendron D. 2012. Application of McMaster´s technique in live blue whales. Veterinary Record, 171, 220. DOI: 10.1135/vr.100749
Franco-Gordo C., Ambriz-Arreola I., Kozak E.R., Gómez-Gutiérrez J., Plascencia-Palomera V., Godínez-Domínguez E., Hino-josa-Larios A. 2015. Seasonal succession of zooplankton taxonomic group assemblages in surface waters of Bahía de Navidad, Mexico (November 2010–December 2011). Hidro-biológica, 25, 335–345
Franco-Gordo C., Godínez-Domínguez E., Suárez-Morales E., Freire J. 2008. Interannual and seasonal variability of the diversity and structure of ichthyoplankton assemblages in the central Mexican Pacific. Fisheries Oceanography, 17, 178–190. DOI: 10.1111/j.1365-2419.2008.00463x
García-Prieto L., García-Varela M., Mendoza-Garfías B. 2014. Biodiversidad de Acanthocephala en México. Revista Mexicana de Biodiversidad. Suplemento 85, S177–S182. DOI: 10.7550/rmb.31684. (In Spanish)
García-Prieto L., García-Varela M., Mendoza-Garfias B., Pérez-Ponce de León G. 2010. Checklist of the Acanthocephala in wildlife vertebrates of Mexico. Zootaxa, 2419, 1–50
Gasca R., Franco-Gordo C., Godínez-Domínguez E., Suárez-Mora-les E. 2012. Hyperiid amphipods community in the eastern tropical Pacific before, during, and after El Niño 1997–1998. Marine Ecology Progress Series, 455, 123–139. DOI: 10.3354/meps09571
George-Nascimento M.A., Marin S.L. 1992. Efecto de dos especies hospedadoras, el lobo fino austral Arctocephalus australis (Zimmerman) y el lobo marino común Otaria byronia (Blainville) (Carnivora; Otariidae), sobre la morfología y la fecundidad de Corynosoma sp. (Acanthocephala; Polymorphidae) en Uruguay. Revista Chilena de Historia Natural, 65, 183–193. (In Spanish)
Ghirardelli E. 1968. Some aspects of the biology of the chaetognaths. Advances in Marine Biology, 6, 271–375
Gibson D. 2016. World list of marine Acanthocephala. Accessed through: World Register of Marine Species at http://www.marine-species.org/aphia.php?p=taxdetails&id=20331 on 2016–07–29
Gómez del Prado-Rosas M.C., Álvarez-Cadena J.N., Segura-Puertas L., Lamothe-Argumedo R. 2005. Hemiurid meta-cercariae (Trematoda) in chaetognaths from the Mexican Sea. Comparative Parasitology, 72, 230–233. DOI: 10.1654/4157
Gómez-Gutiérrez J., Robinson C.J., Kawaguchi S., Nicol S. 2010. Parasite diversity of Nyctiphanes simplex and Nematoscelis difficilis along the Northwestern coast of Mexico. Diseases of Aquatic Organisms, 88, 249–266. DOI: 10.3354/dao02155
Grassi G. 1881. Alcuni protisti endoparassitici. Atti della Società Italiana di Scienze Naturali, 24, 62–67. (In Italian)
Gregori M., Aznar F.J., Abollo E., Roura A., González A.F., Pascual S. 2012. Nyctiphanes couchii as intermediate host for the acanthocephalan Bolbosoma balaenae in temperate waters of the NE Atlantic. Diseases of Aquatic Organisms, 99, 37–47. DOI: 10.3354/dao02457
Gregori M., Aznar F.J., Abollo E., Roura A., González A.F., Pascual S. 2013. Nyctiphanes couchii as intermediate host for Rhadinorhynchus sp. (Acanthocephala, Echinorhynchidae) from NW Iberian Peninsula waters. Diseases of Aquatic Organisms, 105, 9–20. DOI: 10.3354/dao02611
Hovasse R. 1924. Trypanoplasma sagittae sp. nov. Compte Rendu des Séances de la Société de Biologie Paris, 91, 1254–1255. (In French)
Huys R., Bodin P. 1997. First record of Acanthocephala in marine copepods. Ophelia, 46, 217–231. DOI: 10.1080/00785326.1997.10432880
Ikeda I. 1917. A new astomatous ciliate Metaphrya sagittae gen. et sp. nov., found in the coelom of Sagitta. Annotationes Zoo-logicae Japonenses, 9, 317–324
Kozak E.R., Franco-Gordo C., Suárez-Morales E., Palomares-García J.R. 2014. Seasonal and interannual variability of the calanoid copepod community structure in shelf waters of the eastern Tropical Pacific. Marine Ecology Progress Series, 507, 95–110. DOI: 10.3354/meps10811
Laskowski Z., Jezewski W., Zdzitowiecki K. 2008. Cystacanths of Acanthocephala in notothenioid fish from the Beagle Channel (sub-Antarctica). Systematic Parasitology, 70, 107–117. DOI: 10.1007/s11230-008-9131-0
Lebour M.V. 1917. Some parasites of Sagitta bipunctata. Journal of the Marine Biological Association of the United Kingdom, 11, 201–206
Leuckart R. 1861. Bericht Uber die wiss. Leistungen in der Naturgeschichte der niederen Thiere wahrend des Jahres 1859. Archiv für Naturgeschichte, 26 pt, 2, 103–264. (In German)
Leuckart R., Pagenstecher A. 1858. Untersuchugen uber niedere Seethiere. Archiv für Anatomie und Physiologie. Leipzig, 569. (In German)
Marcogliese D.J. 1994. Aeginina longicornis (Amphipoda: Capre-llidae), new intermediate hosts for Echinorhynchus gadi (Acanthocephala: Echinorhynchidae). Journal of Parasito-logy, 80, 1043–1045
Marcogliese D.J. 1995. The role of zooplankton in the transmission of helminth parasites to fish. Reviews in Fish Biology and Fisheries, 5, 336–371. DOI: 10.1007/BF00043006
Morales-Ávila J.R., Gómez-Gutiérrez J., Gómez del Prado-Rosas M.C., Robinson C.J. 2015. Trematode larval stage of Paronatrema mantae and Copiatestes sp. parasitize Nyctiphanes simplex and Nematoscelis difficilis krill in the Gulf of California. Diseases of Aquatic Organisms, 116, 23–35. DOI: 10.3354/dao02901
Moravec F., Vidal-Martínez V.M., Aguirre-Macedo L. 1995. Some helminth parasites of Epinephelus morio (Pisces: Serranidae) from the Peninsula of Yucatan, Mexico. Studies on the Natural History of the Caribbean Region, 72, 55–66
Moravec F., Vidal-Martínez V.M., Vargas-Vázquez J., Vivas-Ro-dríguez C., González-Solis D., Mendoza-Franco E., Simá-Ál-varez R., Guemez-Ricalde J. 1997. Helminth parasites of Epinephelus morio (Pisces: Serranidae) of the Yucatan Peninsula, southeastern Mexico. Folia Parasitologica, 44, 255–266
Nagasawa S. 1991. Chapter 8 Parasitism and diseases in Chaetognaths. In: (Eds. Bone Q., Kapp H. and Pierrot-Bults A.C.) The Biology of Chaetognaths. Oxford Science Publications, U.S.A., 76–168
Nagasawa S., Marumo R. 1979. Parasites in chaetognaths in Suruga Bay, Japan. La Mer, 17, 127–136
Nagasawa S., Simidu U., Nemoto T. 1984. Bacterial invasion of Chaetognaths under laboratory and natural conditions. Journal of the Oceanographical Society of Japan, 40, 327–333
Nickol B.B. 1985. Epizootiology. In: (Eds. Crompton D.W.T. and Nickol B.B.) Biology of the Acanthocephala. Cambridge University Press, Cambridge, 307–346
Ohtsuka S., Nagasawa K., Gejima K. 2000. Review of parasites of marine zooplankton. Bulletin of the Plankton Society of Japan, 47, 1–16
Petrochenko V.I. 1958. Acanthocephala of domestic and wild animals. Vol. 2. Izdatelstvo Akademii Nauk SSSR, Moscow, pp. 478 pp. (In Russian)
Pierrot-Bults A.C. 1990. Diseases of chaetognatha. In: (Ed. O. Kinne) Diseases of marine animals. Vol. III. Biologische Anstalt Helgoland, Germany, 425–437
Poulin R. 2007. Are there general laws in parasite ecology? Parasitology, 134, 763–776. DOI: 10.1017/S0031182006002150
Rakusa-Suszczewski S. 1968. Predation of Chaetognatha by Tomopteris helgolandica Greff. ICES Journal of Marine Science, 32, 226–231
Santos C.P., Gibson D.I., Tavares L.E.R., Luque J.L. 2008. Checklist of Acanthocephala associated with the fishes of Brazil. Zootaxa, 1938, 1–22
Sars G.O. 1885. Report on the Schizopoda collected by H.M.S. Challenger, during the years 1873–1876. In: (Eds C.W. Thomson and J. Murray) Report on the scientific results of the voyage of H.M.S. Challenger, during the years 1873–76. Zoology, 37, 1–228
Schmidt G.D. 1985. Development and life cycles. In: (Eds Crompton D.W.T. and Nickol B.B.) Biology of the Acanthocephala. Cambridge University Press, Cambridge, 273–286
Schmidt G.D., MacLean S.A. 1978. Polymorphus (Profilicollis) major Lundstrom 1942 juveniles in rock crabs, Cancer irro-ratus, from Maine. Journal of Parasitology, 64, 953–954
Slankis A., Schevchenko G.G. 1974. Data on the infestation of planktonic invertebrates with helminth larvae in the western part of the equatorial zone of the Pacific. Canadian Translation of Fisheries and Aquatic Sciences Series No. 5596. Originally published in TINRO, 88, 129–138
Smith P., Richardson S. 1977. Standard techniques for pelagic fish egg and larva surveys. FAO Fishery Technical Papers, 175, 1–107
Théodoridès J. 1989. Parasitology of marine zooplankton. Advances in Marine Biology, 25, 117–177. DOI: 10.1016/S0065-2881 (08)60189-3
Thomson J.M. 1947. The chaetognaths of south-eastern Australia. Council for Scientific and Industrial Research (Division of Fisheries), 222, 4–43
Ulianin V. 1871. Über die pelagische fauna des Schwarzen Meeres. Verhandlungen der Moskauer. Freunde der Natur. (In German)
Yamaguti S. 1963. Systema helminthum. Vol. V., Acanthocephala. Interscience Publishers, New York, pp. 423
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Lozano-Cobo, H., Gómez-Gutiérrez, J., Franco-Gordo, C. et al. The discovery of acanthocephalans parasitizing chaetognaths. Acta Parasit. 62, 401–411 (2017). https://doi.org/10.1515/ap-2017-0048
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1515/ap-2017-0048