Mapping a brain parasite: occurrence and spatial distribution in fish encephalon

. 2023 Aug ; 21 () : 22-32. [epub] 20230311

Status PubMed-not-MEDLINE Jazyk angličtina Země Anglie, Velká Británie Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid37081833
Odkazy

PubMed 37081833
PubMed Central PMC10111940
DOI 10.1016/j.ijppaw.2023.03.004
PII: S2213-2244(23)00019-6
Knihovny.cz E-zdroje

Parasites, especially brain-encysting trematodes, can have an impact on host behaviour, facilitating the transmission to next host and completion of the life cycle, but insufficient research has been done on whether specific brain regions are targeted. Using Cardiocephaloides longicollis as a laboratory model, the precise distribution of metacercariae in experimentally-infected, wild and farmed fish was mapped. The brain regions targeted by this parasite were explored, also from a histologic perspective, and potential pathogenic effects were evaluated. Experimental infections allowed to reproduce the natural infection intensity of C. longicollis, with four times higher infection intensity at the higher dose (150 vs 50 cercariae). The observed metacercarial distribution, similar among all fish groups, may reflect a trematode species-specific pattern: metacercariae occur with highest density in the optic lobe area (primarily infecting the periventricular gray zone of optic tectum) and the medulla oblongata, whereas other areas such as the olfactory lobes and cerebellar lobes may be occupied when the more frequently invaded parts of the brain were crowded. Mono- and multicysts (i.e. formed either with a single metacercaria, or with 2-25 metacercariae encapsulated together) may be formed depending on the aggregation and timing of metacercariae arrival, with minor host inflammatory response. Larvae of C. longicollis colonizing specific brain areas may have an effect on the functions associated with these areas, which are generally related to sensory and motor functions, but are also related to other host fitness traits such as school maintenance or recognition of predators. The detailed information on the extent and distribution of C. longicollis in fish encephalon sets the ground to understand the effects of brain parasites on fish, but further investigation to establish if C. longicollis, through purely mechanical damage (e.g., occupation, pressure and displacement), has an actual impact on host behaviour remains to be tested under controlled experimental conditions.

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Achatz T.J., Chermak T.P., Martens J.R., Pulis E.E., Fecchio A., Bell J.A., Greiman S.E., Cromwell K.J., Brant S.V., Kent M.L., Tkach V.V. Unravelling the diversity of the Crassiphialinae (Digenea: Diplostomidae) with molecular phylogeny and descriptions of five new species. Curr. Res. Parasitol. Vector-Borne Dis. 2021;1 doi: 10.1016/j.crpvbd.2021.100051. PubMed DOI PMC

Barber I., Crompton D.W.T. The distribution of the metacercariae of Diplostomum phoxini in the brain of minnows, Phoxinus phoxinus. Folia Parasitol. 1997;44:19–25. PubMed

Bartoli P., Boudouresque C.F. Effect of the digenean parasites of fish on the fauna of Mediterranean lagoons. Parassitologia. 2007;49:111–117. PubMed

Bartón K. MuMIn: multi-model inference. 2022. https://CRAN.R-project.org/package=MuMIn Package ‘MuMin’ 1.47.1.

Bernstein J. In: Fish Physiology. Hoar W.S., Randall D.J., editors. Academic Press; New York: 1970. Anatomy and physiology of the central nervous system; pp. 1–90.

Bibby M.C., Rees G. The ultrastructure of the epidermis and associated structures in the metacercaria, cercaria and sporocyst of Diplostomum phoxini (Faust, 1918) Z. Für Parasitenkd. Parasitol. Res. 1971;37:169–186. PubMed

Born-Torrijos A., Poulin R., Pérez-del-Olmo A., Culurgioni J., Raga J.A., Holzer A.S. An optimised multi-host trematode life cycle: fishery discards enhance trophic parasite transmission to scavenging birds. Int. J. Parasitol. 2016;46:745–753. doi: 10.1016/j.ijpara.2016.06.005. PubMed DOI

Bouwmeester M.M., Goedknegt M.A., Poulin R., Thieltges D.W. Collateral diseases: aquaculture impacts on wildlife infections. J. Appl. Ecol. 2021;58:453–464. doi: 10.1111/1365-2664.13775. DOI

Bush A.O., Fernández J.C., Esch G.W., Seed J.R. Cambridge University Press; U.K: 2001. Parasitism: the Diversity and Ecology of Animal Parasites.

Conn D.B., Goater C.P., Bray D. Developmental and functional ultrastructure of Ornithodiplostomum ptychocheilus diplostomula (Trematoda: Strigeoidea) during invasion of the brain of the fish intermediate host, Pimephales promelas. J. Parasitol. 2008;94:635–642. doi: 10.1645/GE-1421.1. PubMed DOI

Dezfuli B.S., Capuano S., Simoni E., Giari L., Shinn A.P. Histopathological and ultrastructural observations of metacercarial infections of Diplostomum phoxini (Digenea) in the brain of minnows Phoxinus phoxinus. Dis. Aquat. Org. 2007;75:51–59. doi: 10.3354/dao075051. PubMed DOI

Dezfuli B.S., Giari L., Shinn A.P. The role of rodlet cells in the inflammatory response in Phoxinus phoxinus brains infected with Diplostomum. Fish Shellfish Immunol. 2007;23:300–304. doi: 10.1016/j.fsi.2006.11.003. PubMed DOI

Dönges J. Entwicklungs- und Lebensdauer von Metacercarien. Z. Parasitenkd. 1969;31:340–366. doi: 10.1007/BF00259732. PubMed DOI

Erasmus D.A. Edward Arnold; London: 1972. The Biology of Trematodes.

Erasmus D.A. The migration of Cercaria X Baylis (Strigeida) within the fish intermediate host. Parasitology. 1959;49:173–190. doi: 10.1017/S0031182000026810. PubMed DOI

Goater C.P., Bray D., Conn D.B. Cellular aspects of early development of Ornithodiplostomum ptychocheilus metacercariae in the brain of fathead minnows, Pimephales promelas. J. Parasitol. 2005;91:814–821. doi: 10.1645/GE-3485.1. PubMed DOI

Guthrie D.M. In: The Behaviour of Teleost Fishes. Pitcher T.J., editor. Croom Helm; London: 1986. Role of vision in fish behaviour; pp. 111–121.

Haas W., Wulff C., Grabe K., Meyer V., Haeberlein S. Navigation within host tissues: cues for orientation of Diplostomum spathaceum (Trematoda) in fish towards veins, head and eye. Parasitology. 2007;134:1013–1023. doi: 10.1017/S0031182007002430. PubMed DOI

Halton D.W., Johnston B.R. Functional morphology of the metacercarial cyst of Bucephaloides gracilescens (Trematoda: Bucephalidae) Parasitology. 1982;85:45–52. doi: 10.1017/S0031182000054135. DOI

Helland-Riise S.H., Nadler L.E., Vindas M.A., Bengston E., Turner A.V., Johansen I.B., Weinersmith K.L., Hechinger R.F., Øverli Ø. Regional distribution of a brain-encysting parasite provides insight on parasite-induced host behavioral manipulation. J. Parasitol. 2020;106:188. doi: 10.1645/19-86. PubMed DOI

Hendrickson G.L. Ornithodiplostomum ptychocheilus: migration to the brain of the fish intermediate host, Pimephales promelas. Exp. Parasitol. 1979;48:245–258. doi: 10.1016/0014-4894(79)90106-1. PubMed DOI

Hoffman G.L. Studies on the life-cycle of Ornithodiplostomum ptychocheilus (Faust) (Trematoda: Strigeoidea) and the “self cure” of infected fish. J. Parasitol. 1958;44:416–421. doi: 10.2307/3274326. PubMed DOI

Hoffman G.L., Hoyme J.B. The experimental histopathology of the “tumor” on the brain of the stickleback caused by Diplostomum baeri eucaliae Hoffman and Hundley, 1957 (Trematoda: Strigeoidea) J. Parasitol. 1958;44:374. doi: 10.2307/3274318. PubMed DOI

Lafferty K.D., Morris A.K. Altered behavior of parasitized killifish increases susceptibility to predation by bird final hosts. Ecology. 1996;77:1390–1397. doi: 10.2307/2265536. DOI

Lafferty K.D., Shaw J.C. Comparing mechanisms of host manipulation across host and parasite taxa. J. Exp. Biol. 2013;216:56–66. doi: 10.1242/jeb.073668. PubMed DOI

Lochmiller R.L., Deerenberg C. Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos. 2000;88:87–98. doi: 10.1034/j.1600-0706.2000.880110.x. DOI

Matisz C.E., Goater C.P. Migration, site selection, and development of Ornithodiplostomum sp. metacercariae (Digenea: Strigeoidea) in fathead minnows (Pimephales promelas) Int. J. Parasitol. 2010;40:1489–1496. doi: 10.1016/j.ijpara.2010.04.018. PubMed DOI

Matisz C.E., Goater C.P., Bray D. Migration and site selection of Ornithodiplostomum ptychocheilus (Trematoda: Digenea) metacercariae in the brain of fathead minnows (Pimephales promelas) Parasitology. 2010;137:719–731. doi: 10.1017/S0031182009991545. PubMed DOI

Matisz C.E., Goater C.P., Bray D. Density and maturation of rodlet cells in brain tissue of fathead minnows (Pimephales promelas) exposed to trematode cercariae. Int. J. Parasitol. 2010;40:307–312. doi: 10.1016/j.ijpara.2009.08.013. PubMed DOI

Mitchell C.W. Ultrastructure of the metacercarial cyst of Posthodiplostomum minimum (MacCullum, 1921) J. Parasitol. 1974;60:67–74. PubMed

Moore J. Oxford University Press; Oxford: 2002. Parasites and the Behaviour of Animals.

Muzzall P.M., Kilroy A.L. Tylodelphys scheuringi (Diplostomidae) infecting the brain of the central mudminnow, Umbra limi, in silver creek, Michigan. U.S.A. Comp. Parasitol. 2007;74:164–166. doi: 10.1654/4278.1. DOI

Osset E.A., Fernández M., Raga J.A., Kostadinova A. Mediterranean Diplodus annularis (Teleostei: Sparidae) and its brain parasite: unforeseen outcome. Parasitol. Int. 2005;54:201–206. doi: 10.1016/j.parint.2005.05.002. PubMed DOI

Poulin R. Parasite manipulation of host personality and behavioural syndromes. J. Exp. Biol. 2013;216:18–26. doi: 10.1242/jeb.073353. PubMed DOI

Poulin R. Advances in the Study of Behavior. Elsevier; 2010. Parasite manipulation of host behavior; pp. 151–186. DOI

Prévot G., Bartoli P. Démonstration de l’existence d’un cycle marin chez les Strigeides: Cardiocepbalus longicollis Szidat, 1928 (Trematoda: Strigeidae) Ann. Parasitol. Hum. Comp. 1980;55:407–425. doi: 10.1051/parasite/1980554407. PubMed DOI

Radabaugh D.C. Encystment site selection in the brain-inhabiting metacercariae of Ornithodiplostomum ptychocheilus (Trematoda: Strigeoidea) J. Parasitol. 1980;66:183. doi: 10.2307/3280624. DOI

Radabaugh D.C. Changes in minnow, Pimephales promelas Rafinesque, schooling behaviour associated with infections of brainencysted larvae of the fluke, Ornithodiplostomum ptychocheilus. J. Fish Biol. 1980;16:621–628. doi: 10.1111/j.1095-8649.1980.tb03741.x. DOI

Ratanarat-Brockelman C. Migration of Diplostomum spathaceum (Trematoda) in the fish intermediate host. Z. Parasitenkd. 1974;43:123–134. doi: 10.1007/BF00329170. PubMed DOI

Reynolds E.S. The use of lead citrate at high pH as an electronopaque stain in electron microscopy. J. Cell Biol. 1963;17:208–212. PubMed PMC

Sánchez C.A., Becker D.J., Teitelbaum C.S., Barriga P., Brown L.M., Majewska A.A., Hall R.J., Altizer S. On the relationship between body condition and parasite infection in wildlife: a review and meta‐analysis. Ecol. Lett. 2018;21:1869–1884. doi: 10.1111/ele.13160. PubMed DOI

Sandland G.J., Goater C.P. Parasite-Induced variation in host morphology: brain-encysting trematodes in fathead minnows. J. Parasitol. 2001;87:267. doi: 10.2307/3285040. PubMed DOI

Seppälä O., Karvonen A., Valtonen E.T. Manipulation of fish host by eye flukes in relation to cataract formation and parasite infectivity. Anim. Behav. 2005;70:889–894. doi: 10.1016/j.anbehav.2005.01.020. DOI

Shaw J.C., Øverli Ø. Brain-encysting trematodes and altered monoamine activity in naturally infected killifish Fundulus parvipinnis. J. Fish. Biol. 2012;81:2213–2222. doi: 10.1111/j.1095-8649.2012.03439.x. PubMed DOI

Shirakashi S., Goater C. Chronology of parasite-induced alteration of fish behaviour: effects of parasite maturation and host experience. Parasitology. 2005;130:177–183. doi: 10.1017/S0031182004006432. PubMed DOI

Shirakashi S., Goater C.P. Brain-encysting parasites affect visually-mediated behaviours of fathead minnows. Ecoscience. 2001;8:289–293. doi: 10.1080/11956860.2001.11682655. DOI

Siegmund I., Franjola R., Torres P. Diplostomatid metacercariae in the brain of silversides from lake riñihue, Chile. J. Wildl. Dis. 1997;33:362–364. doi: 10.7589/0090-3558-33.2.362. PubMed DOI

So F.W., Wittrock D.D. Ultrastructure of the metacercarial cyst of Ornithodiplostomum ptychocheilus (Trematoda: Diplostomatidae) from the brains of fathead minnows. Trans. Am. Microsc. Soc. 1982;101:181. doi: 10.2307/3225772. DOI

Springer A.D., Easter S.S., Agranoff B.W. The role of the optic tectum in various visually mediated behaviors of goldfish. Brain Res. 1977;128:393–404. doi: 10.1016/0006-8993(77)90166-4. PubMed DOI

Timi J.T., Martorelli S.R., Haydeé Sardella N. Digenetic trematodes parasitic on Engraulis anchoita (Pisces: Engraulidae) from Argentina and Uruguay. Folia Parasitol. 1999;46:132–138. PubMed

van Beest G.S., Villar-Torres M., Raga J.A., Montero F.E., Born-Torrijos A. In vivo fluorescent cercariae reveal the entry portals of Cardiocephaloides longicollis (Rudolphi, 1819) Dubois, 1982 (Strigeidae) into the gilthead seabream Sparus aurata L. Parasit. Vectors. 2019;12:92. doi: 10.1186/s13071-019-3351-9. PubMed DOI PMC

van Beest G.S., Montero F.E., Padrós F., Raga J.A., Born-Torrijos A. The versatility of simplicity: structures of Cardiocephaloides longicollis used for different purposes during cercarial transmission. Integr. Comp. Biol. icac102. 2022 doi: 10.1093/icb/icac102. PubMed DOI

Vermaak A., Smit N.J., Kudlai O. Molecular and morphological characterisation of the metacercariae of two species of Cardiocephaloides (Digenea: Strigeidae) infecting endemic South African klipfish (Perciformes: Clinidae) Folia Parasitol. 2021;68 doi: 10.14411/fp.2021.007. PubMed DOI

Weale R.A. Harvard University Press; Cambridge: 1982. Focus on Vision.

Wullimann M.F., Rupp B., Reichert H. Birkhäuser Verlag; Basel: 1996. Neuroanatomy of the Zebrafish Brain: a Topological Atlas.

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