Hostname: page-component-5cf477f64f-n7lw4 Total loading time: 0 Render date: 2025-04-03T18:17:14.405Z Has data issue: false hasContentIssue false
  • English
  • Français

Morphological variety and mechanisms of formation of acanthocephalan cysts in intermediate host

Published online by Cambridge University Press:  31 March 2025

V.P. Nikishin ,
T.V. Davydenko  and
E.M. Skorobrekhova Open the ORCID record for E.M. Skorobrekhova [Opens in a new window]
V.P. Nikishin
Affiliation:
Institute of Biological Problems of the North FEB RAS, Portovaya Str. 18, 685000 Magadan, Russia
T.V. Davydenko
Affiliation:
Institute of Biological Problems of the North FEB RAS, Portovaya Str. 18, 685000 Magadan, Russia
E.M. Skorobrekhova*
Affiliation:
Institute of Biological Problems of the North FEB RAS, Portovaya Str. 18, 685000 Magadan, Russia
*
Corresponding Author: E. M. Skorobrekhova; Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

This report provides an overview of available data on the ultrathin structure and the mechanisms of formation of cysts around acanthocephalans of the classes Palaeacanthocephala and Archiacanthocephala in intermediate hosts. In most of the described cases, the cyst is bi-layered, consisting of an outer layer that is relatively thick and vesicular, and an underlying layer that is thin and amorphous. In acanthellae of some species, a lamellar layer is observed on the cyst surface, which degrades presumably at the cystacanth stage. Three probable mechanisms of cyst formation in acanthellae of different species have been identified. The first and second mechanisms involve the border of microvilli that develops on the tegument surface. In acanthellae of the first group, the cyst’s vesicular layer is formed by detachment of fragments or small vesicles from microvilli, a process resembling the micro-apocrine secretion, while the amorphous layer is composed of electron-dense material released from invaginates of the tegument’s outer membrane and the remaining microvilli. In acanthellae of the second group, the cyst is single-layered and formed presumably of whole microvilli separated from the tegument. Since acanthellae of the third group lack microvilli on the tegument surface, the vesicular layer of the cyst is formed of a few small vesicles and amorphous material synthesized deep in the tegument and in large vesicles transported to the parasite’s surface. The amorphous, electron-dense layer of the cyst is formed in the same manner as in the first group, but without microvilli.

Keywords

Cystacanthacanthellacysttegumentmicrovilli
Type
Review Article
Information
Journal of Helminthology , Volume 99 , 2025 , e49
Copyright
© The Author(s), 2025. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Amin, OM, Heckmann, RA, Inchausti, V and Vasquez, R (1996) Immature Polyacanthorhynchus rhopalorhynchus (Acanthocephala: Polyacanthorhynchidae) in venton, Hoplias malabaricus (Pisces) from Moca Vie River, Bolivia, with notes on its apical organ and histopathology. Journal of the Helminthological Society of Washington 63, 115–119.Google Scholar
Butterworth, P (1969) The development of the body wall of Polymorphus minutus (Acanthocephala) in its intermediate host Gammarus pulex. Parasitology 59, 373–388. https://doi.org/10.1017/s0031182000082342.Google ScholarPubMed
Chervy, L (2002) The terminology of larval cestodes or metacestodes. Systematic Parasitology 52, 1–33. https://doi.org/10.1023/a:1015086301717.CrossRefGoogle Scholar
Choi, C-J, Lee, H-J, Go, J-H, Park, Y-K Chai, J-Y and Seo, M (2010) Extraintestinal migration of Centrorhynchus sp. (Acanthocephala: Centrorhynchidae) in experimentally infected rats. Korean Journal of Parasitology 48, 139–143. https://doi.org/10.3347/kjp.2010.48.2.139.CrossRefGoogle ScholarPubMed
Crompton, DWT (1964) The envelope surrounding Polymorphus minutus (Goeze, 1782) (Acanthocephala) during its development in the intermediate host, Gammarus pulex. Parasitology 54, 721–735. https://doi.org/10.1017/S0031182000082731.CrossRefGoogle ScholarPubMed
Crompton, DWT (1967) Studies on the haemocytic reaction of Gammarus spp., and its relationship to Polymorphus minutus (Acanthocephala). Parasitology 57, 389–401. https://doi.org/10.1017/S0031182000072176.Google ScholarPubMed
Davydenko, TV, Nikishin, VP (2023). Features of the organization of the tegument in cystacanth and adult acanthocephalan Acanthocephalus tenuirostris (Achmerov et Dombrowskaja-Achmerova, 1941). Inland Water Biology 16, 185–192. https://doi.org/10.1134/S1995082923020049.CrossRefGoogle Scholar
Davydenko, TV and Nikishin, VP (2024) Cyst formation around Acanthocephalus tenuirostris (Palaeacanthocephala) in its intermediate host, the aquatic sowbug Asellus hilgendorfi. Zoomorphology 143, 603–611. https://doi.org/10.1007/s00435-024-00669-0.Google Scholar
Dezfuli, BS, Bosi, G and Rossi, R (1992) The ultrastructure of the capsule surrounding Pomphorhynchus laevis (Acanthocephala) in its intermediate host Echinogammarus stammeri (Amphipoda). Parassitologia 34, 61–69.Google ScholarPubMed
Dezfuli, BS, Bosi, G and Ross, R (1994) Fine structure of the envelope surrounding the cystacanths of Acanthocephalus clavula (Acanthocephala) in its intermediate host Echinogammarus stammeri (Amphipoda). Transactions of the American Microscopical Society 113, 34–42. https://doi.org/10.2307/3226577.CrossRefGoogle Scholar
Dezfuli, BS (1996) Cypria reptans (Crustacea: Ostracoda) as an intermediate host of Neoechinorhynchus rutili (Acanthocephala: Eoacanthocephala) in Italy. Journal of Parasitology 82, 503–505. https://doi.org/10.2307/3284094.CrossRefGoogle Scholar
Dezfuli, BS and Giari, L (1999) Amphipod intermediate host of Polymorphus minutus (Acanthocephala), parasite of water birds, with notes on ultrastructure of host-parasite interface. Folia Parasitologica 46, 117–122.Google Scholar
Dezfuli, BS (2000) Host-parasite interface between Asellus aquaticus (Isopoda) and larvae of Acanthocephalus anguillae (Acanthocephala). Folia Parasitologica 47, 154–156. https://doi.org/10.14411/fp.2000.030.CrossRefGoogle ScholarPubMed
Emde, S Rueckert, S Kochmann, J Knopf, K Sures, B and Klimpel, S (2014) Nematode eel parasite found inside acanthocephalan cysts – a ‘Trojan horse’ strategy? Parasites & Vectors 7, 504. https://doi.org/10.1186/s13071-014-0504-8.Google ScholarPubMed
Kusenko, KV and Nikishin, VP (2024) First information on the ultrathin structure of the tegument of the ‘cystacanth’ in Acanthocephala Neoechinorhynchus beringianus Mikhailova et Atrashkevich, (Eoacanthocephala, Neoechinorhynchidae). Biology Bulletin 51, 1286–1290. https://doi.org/10.1134/S1062359024607614.CrossRefGoogle Scholar
Lackie, JM and Rotheram, S (1972) Observations on the envelope surrounding Moniliformis dubius (Acanthocephala) in the intermediate host, Periplaneta americana. Parasitology 65, 303–308. https://doi.org/10.1017/S003118200004508x.CrossRefGoogle ScholarPubMed
Lackie, AM and Lackie, JM (1979) Evasion of the insect immune response by Moniliformis dubius (Acanthocephala): further observations on the origin of the envelope. Parasitology 79, 297–301. https://doi.org/10.1017/S0031182000053361.CrossRefGoogle ScholarPubMed
Marchand, B and Grita-Timoulali, Z (1992) Comparative ultrastructural study of the cuticle of larvae and adults of Centrorhynchus milvus Ward, 1956 (Acanthocephala, Centrorhynchidae). Journal of Parasitology 78, 355–359. https://doi.org/10.1134/S1062359024607614.CrossRefGoogle ScholarPubMed
Mercer, EH and Nicholas, WL (1967) The ultrastructure of the capsule of the larval stages of Moniliformis dubius (Acanthocephala) in the cockroach Periplaneta americana. Parasitology 57, 169–174. https://doi.org/10.1017/S0031182000071973.CrossRefGoogle Scholar
Nikishin, VP (1985) Ultrastructure of exodermis in the late acanthella Arhythmorhynchus petrochenkoi (Schmidt, 1969) (Acanthocephala, Polymorphidae). Parazitologiya 19, 306–313.Google Scholar
Nikishin, VP (1986) Fine structure of the wall of metasoma of the cystacanths Polymorphus strumosoides (Acanthocephala, Polymorphidae). Parazitologiya 20, 403–408.Google Scholar
Nikishin, VP (1992) Formation of the capsule around Filicollis anatis in its intermediate host. Journal of Parasitology 78, 127–137. https://doi.org/10.2307/3283699.Google ScholarPubMed
Nikishin, VP (1999) A cyst around acanthocephalans larvae as an element of host-parasite area. In Scientific studies in the North-East of Russia. Magadan, NESCFEB RAS, 139–149.Google Scholar
Nikishin, VP (2004) Cytomorphology of acanthocephalans. Moscow: GEOS.Google Scholar
Nikishin, VP (2011) Convergence of the cyst in cysticercoids (Cestoda, Hymenolepidata) and the tegument in cystacanths (Acanthocephala). Biology Bulletin 38, 195–202. https://doi.org/10.1134/S1062359011020099.CrossRefGoogle Scholar
Nikishin, VP and Skorobrekhova, EM (2015) Host-parasite interactions in Acanthocephala (a morphological aspect). Uspekhi sovremennoy biologii 135, 203–221 (in Russian).Google Scholar
Nikishin, VP (2018) Glycocalyx modifications in acanthocephalans. Biology Bulletin 45, 35–46. https://doi.org/10.1134/S1062359018010090.Google Scholar
Nikishin, VP and Skorobrekhova, EM (2020) The acanthocephalan Corynosoma strumosum in paratenic hosts interactions at the organism level under natural and experimental level. Moscow: KMK Scientific press Russian.Google Scholar
Nikishin, VP (2022) Terminological confusion in the designation of capsules and cysts surrounding tissue helminthes. Biology Bulletin 49, 1022–1023. https://doi.org/10.1134/S1062359022080143.Google Scholar
Olson, RE and Pierce, JR (1991) Histopathology of the trematode Stephanostomum sp. in rex sole, Glyptocephalus zachirus. Transactions of the American Microscopical Society 110, 75–79. https://doi.org/10.2307/3226743.Google Scholar
Petrochenko VI (1956) Acanthocephala of Domestic and Wild Animals. Vol. 1. Moscow: Izdatelʼstvo Akademii Nauk SSSR.Google Scholar
Petrochenko VI (1958) Acanthocephala of Domestic and Wild Animals. Vol. 2. Moscow: Izdatelʼstvo Akademii Nauk SSSR.Google Scholar
Quist, MC, Bower, MR and Hubert, WA (2007) Infection by a black spot-causing species of Uvulifer and associated opercular alterations in fishes from a high-desert stream in Wyoming. Diseases of Aquatic Organisms 78, 129–136. https://doi.org/10.3354/dao01875.CrossRefGoogle Scholar
Rotheram, S and Crompton, DWT (1972) Observations on the early relationship between Moniliformis dubius (Acanthocephala) and the hemocytes of the intermediate host, Periplaneta americana. Parasitology 64, 15–21. https://doi.org/10.1017/S0031182000044607.Google Scholar
Skorobrekhova, EM and Nikishin, VP (2019) Encapsulation of the acanthocephalan, Corynosoma strumosum (Rudolphi, 1802) Lühe, 1904, in the intermediate host, Spinulogammarus ochotensis. Journal of Parasitology 105, 567–570. https://doi.org/10.1645/19-22.CrossRefGoogle ScholarPubMed
Taraschewski, H (2000) Host-parasite interactions in Acanthocephala: a morphological Approach. Advances in Parasitology 46, 1–179. https://doi.org/10.1016/s0065-308x(00)46008-2.Google ScholarPubMed
Walker, DJ and Wittrock, DD (1992) Histochemistry and ultrastructure of the metacercarial cyst of Bolbogonotylus corkumi (Trematoda: Cryptogonimidae). Journal of Parasitology 78, 725–730. https://doi.org/10.2307/3283551Google ScholarPubMed
Zhao, B and Wang, MX (1992) Ultrastructural study of the defense reaction against the larvae of Macracanthorhynchus hirudinaceus in laboratory-infected beetles. Journal of Parasitology 78, 1098–1101. https://doi.org/10.2307/3283240.CrossRefGoogle Scholar