Abstract
Data available on the peculiarities of the tegument structure and encapsulation of the acanthocephalans Corynosoma strumosum (Palaeacanthocephala, Polymorphidae) and Sphaerirostris picae (Palaeacanthocephala, Centrorhynchidae) in paratenic hosts are summarized. Corynosomes are shown to have a capsule structure varying from fibroblastic to leukocytal depending on the species of the paratenic host (sea fish). The characteristic thick glycocalix layer may or may not develop on the tegument surface of corynosomes surrounded by the leukocytal capsule in the hosts of different species. The acanthocephalan S. picae in a paratenic host (lizard) is also surrounded by a leukocytal capsule; however, no characteristic glycocalyx layer is formed on its tegument surface. Such a glycocalyx supposedly represents a protective reaction of the parasite to cellular encapsulation, but in the case of its absence the protective mechanism remains unclear. Based on these results, a hypothesis about two strategies of interrelations between acanthocephalans and paratenic hosts is advanced. According to the first strategy, the acanthocephalan (C. strumosum in the fish of the majority of the species studied), regardless of the structure of the capsule formed around it, is covered with a thick layer of glycocalyx, while the cells of the inner part of the capsule are destroyed. When invading paratenic hosts of other species (C. strumosum in flatfishes, as well as in experimentally infested aquarium fish and lizards, S. picae in lizards), the second strategy is realized: the acanthocephalan is surrounded by a leukocytal capsule; however, a thick layer of glycocalyx on its surface is not formed and the capsule’s cells are not destroyed.
Similar content being viewed by others
REFERENCES
Amin, O.M., Heckmann, R.A., Mesa, R., and Mesa, E., Description and host relationships of cystacanths of Polymorphus spindlatus (Acanthocephala: Polymorphidae) from their paratenic fish hosts in Peru, J. Helminthol. Soc. Washington, 1995, vol. 62, no. 2, pp. 249–253.
Amin, O.M., Heckmann, R.A., Inchausty, V., and Vasquez, R., Immature Polyacanthorhynchus rhopalorhynchus (Acanthocephala: Polyacanthorhynchidae) in venton, Hoplias malabaricus (Pisces) from Moca Vie River, Bolivia, with notes in its apical organ and histopathology, J. Helminthol. Soc. Washington, 1996, vol. 63, no. 1, pp. 115–119.
Atrashkevich, G.I., Acanthocephalans of the genus Corynosoma Luhe, 1904 (Acanthocephales: Polymorphidae) in the Sea of Okhotsk and the parasitic system of the dominant species C. strumosum (Rudolphi, 1802), in IV Vserossiiskii s’’ezd Parazitologicheskogo obshchestva pri RAN “Parazitologiya v XXI veke – problemy, metody, resheniya”, 20–25 oktyabrya 2008 g. (IV All-Russia Congr. Parasitol. Soc. Russ. Acad. Sci. “Parasitology in the 21st Century: Challenges, Methods, and Solutions,” October 20–25, 2008), St. Petersburg: Lema, 2008, vol. 1, pp. 38–42.
Khokhlova, I.G., Akantotsefaly nazemnykh pozvonochnykh fauny SSSR (Acanthocephalans of Terrestrial Vertebrates of the Fauna of the USSR), Moscow: Nauka, 1986.
Marchand, B. and Grita-Timoulali, Z., Comparative ultrastructural study of the cuticle of larvae and adults of Centrorhynchus milvus Ward, 1956 (Acanthocephala, Centrorhynchidae), J. Parasitol., 1992, vol. 78, no. 2, pp. 355–359.
Nikishin, V.P., Morphofunctional diversity of glycocalyx in tapeworms, Biol. Bull. Rev., 2017, vol. 7, no. 2, pp. 160–178.
Nikishin, V.P., Glycocalyx modifications in acanthocephalans, Biol. Bull. (Moscow), 2018, vol. 45, no. 1, pp. 35–46.
Nikishin, V.P. and Skorobrechova, E.M., Encapsulation of acanthocephalans Corynosoma sp. in two reservoir host species, Dokl. Biol. Sci., 2007, vol. 417, no. 4, pp. 462–464.
Nikishin, V.P. and Skorobrechova, E.M., Relationships of acanthocephalans with hosts (morphological aspect), Usp. Sovrem. Biol., 2015, vol. 135, no. 2, pp. 203–221.
Parker, G.A., Ball, M.A., and Chubb, J.C., To grow or not to grow? Intermediate and paratenic hosts as helminth life cycle strategies, J. Theor. Biol., 2009, vol. 258, no. 1, pp. 135–147.
Pronina, S.V. and Pronin, N.M., Vzaimootnosheniya v sistemakh gel’minty-ryby (na tkanevom, organnom i organizmennom urovnyakh) (Relationships in Helminths–Fish Systems (at the Tissue, Organ, and Organismal Levels)), Shul’man, S.S., Ed., Moscow: Nauka, 1988.
Sharpilo, V.P., Paraziticheskie chervi presmykayushchikhsya fauny SSSR (Parasitic Worms of the Reptile Fauna of the USSR), Kiev: Naukova Dumka, 1976.
Sharpilo, V.P. and Salamatin, R.V., Paratenic parasitism: the formation and development of the concept, in Istoricheskii ocherk, bibliografiya (Historical Essay, Bibliography), Kiev: LOGOS, 2005.
Sharpilo, V.P., Sonin, M.D., and Lisitsyna, O.I., Paratenic parasitism: the distribution and manifestation patterns, Vestn. Zool., 1996, no. 6, pp. 3–10.
Sharpilo, V.P., Kornyushin, V.V., and Lisitsyna, O.I., On the evolutionary conservatism of acanthocephalan life cycles and the relationship of this phenomenon with the prevalence of paratenic parasitism in them, Vestn. Zool., 1998, vol. 32, nos. 1–2, pp. 12–17.
Shul’ts, R.S. and Davtyan, E.A., Forms of host–parasite relationships in helminthology, Zool. Zh., 1954, vol. 6, pp. 1201–1205.
Skorobrechova, E.M., Morphology of the relationships of the acanthocephalan Corynosoma strumosum (Acanthocephales: Polymorphidae) and paratenic hosts in nature and experiment, Cand. Sci. (Biol.) Dissertation, St. Petersburg: Zool. Inst. Ross. Akad. Nauk, 2014.
Skorobrechova, E.M. and Nikishin, V.P., Structure of capsule surrounding acanthocephalans Corynosoma strumosum in paratenic hosts of three species, Parasitol. Res., 2011, vol. 108, no. 2, pp. 467–475.
Skorobrechova, E.M. and Nikishin, V.P., Encapsulation of the acanthocephalan Corynosoma strumosum parasite in fish Hemichromis bimaculatus: a preliminary experimental study, Vestn. Sev.-Vost. Nauchn. Tsentra Dal’nevost. Otd. Ross. Akad. Nauk, 2012, no. 3, pp. 52–58.
Skorobrechova, E.M. and Nikishin, V.P., Dependence of the structure of the capsule surrounding the acanthocephalan Corynosoma strumosum on the species of its natural paratenic host, Biol. Bull. (Moscow), 2014, vol. 41, no. 4, pp. 333–348.
Skorobrechova, E.M. and Nikishin, V.P., The morphological peculiarities of the acanthocephalan Corynosoma strumosum (Rudolphi, 1802) (Polymorphidae) in paratenic hosts, the eelpout Zoarces elongatus (Kner, 1868) (Zoarcidae) and the halibut Hippoglossus stenolepis (Schmidt, 1904) (Pleuronectidae), Russ. J. Mar. Biol., 2017, vol. 43, no. 1, pp. 49–56.
Skorobrechova, E.M., Nikishin, V.P., and Lisitsyna, O.I., Structure of capsule around acanthocephalan Corynosoma strumosum from uncommon paratenic hosts—lizards of two species, Parasitol. Res., 2012, vol. 110, no. 1, pp. 459–467.
Skorobrekhova, E.M. and Nikishin, V.P., Encapsulation of the acanthocephalan Sphaerirostris picae in its natural paratenic host, J. Parasitol., 2016, vol. 102, no. 5, pp. 556–558.
Vitomskova, E.A., Gel’minty promyslovykh ryb severnoi chasti basseina Okhotskogo morya, opasnye dlya cheloveka i zhivotnykh (Helminths of the Commercially Valuable Fishes of the Northern Part of the Okhotsk Sea Basin That Are Harmful to Humans and Animals), Magadan: ZNIISKh RASKhN, 2003.
Ward, H.L., Studies on the life history of Neoechinorhynchus cylindratus (Van Cleave, 1913) (Acanthocephala), Transact. Am. Microsc. Soc., 1940, vol. 59, pp. 327–347.
Funding
This study was supported by the Russian Foundation for Basic Research (project no. 15-04-01418) and the Presidium of the Far East Branch of the Russian Academy of Sciences (project no. 15-I-6-015 о).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.
Additional information
Translated by N. Smolina
Rights and permissions
About this article
Cite this article
Nikishin, V.P., Skorobrekhova, E.M. Two Strategies of Acanthocephalan Interrelations with Paratenic Hosts. Biol Bull Russ Acad Sci 46, 814–822 (2019). https://doi.org/10.1134/S1062359019080090
Received:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S1062359019080090