Abstract
Phototaxis is the common behavioral response exhibited by the oncomiracidia of various monogeneans. However, the changes in the oncomiracidial swimming behavior in response to light cues are not well understood. Here, we investigated the light responses of four monogeneans that are important pathogens in mariculture, namely Benedenia epinepheli, Benedenia seriolae, Neobenedenia girellae, and Heteraxine heterocerca. The swimming trajectory and speed of oncomiracidia of each species were assessed in a glass Petri dish with an LED light placed adjacent to it, based on three different light responses: LED light in the off position (normal swimming), LED light in the on position (phototactic behavior), and immediately (< 5 s) after switching the LED light off (photophobic behavior). The oncomiracidia of all four species exhibited positive phototactic and photophobic responses; however, the change in swimming speed between each response differed among the species. The oncomiracidia of three species (B. epinepheli, N. girellae, and H. heterocerca) exhibited high swimming speed, as a phototactic response; in contrast, the oncomiracidia of B. seriolae exhibited reduced swimming speed when moving toward the light source. Benedenia epinepheli and H. heterocerca exhibited the highest swimming speed during the phototaxis phase, whereas B. seriolae and N. girellae exhibited the highest swimming speed during the photophobic phase. These light responses are considered adaptive traits to increase the chance of encountering and infecting suitable hosts in nature, and such responses could potentially be applied to the control of parasite infections in aquaculture.
This is a preview of subscription content, log in via an institution to check access.
source during normal, phototaxis, and photophobic phases. Different letters indicate statistically significant difference (Steel–Dwass, p < 0.05). Abbreviation body length, BL
Similar content being viewed by others
Data availability
Not applicable.
Code availability
Not applicable.
References
Brazenor AK, Bertozzi T, Miller TL, Whittington ID, Hutson KS (2018) DNA profiling reveals Neobenedenia girellae as the primary parasitic monogenean in global fisheries and aquaculture. Mol Phylogenet Evol 129:130–137. https://doi.org/10.1016/j.ympev.2018.05.012
Diehn B, Feinleib M, Haupt W, Hildebrand E, Lenci F, Nultsch W (1977) Terminology of behavioral responses of motile microorganisms. Photochem Photobiol 26:559–560. https://doi.org/10.1111/j.1751-1097.1977.tb07532.x
Fields DM, Skiftesvik AB, Browman HI (2018) Behavioural responses of infective-stage copepodids of the salmon louse (Lepeophtheirus salmonis, Copepoda:Caligidae) to host-related sensory cues. J Fish Dis 41(6):875–884. https://doi.org/10.1111/jfd.12690
Hargis WH Jr (1955) A new species of Benedenia (Trematoda: Monogenea) from Girella nigricans, the opaleye. J Fish Parasitol 41:48–50. https://doi.org/10.2307/3273995
Kearn G (1980) Light and gravity responses of the oncomiracidium of Entobdella soleae and their role in host location. Parasitology 81(1):71–89. https://doi.org/10.1017/S0031182000055050
Kearn GC (1982) Rapid hatching induced by light intensity reduction in the monogenean Entobdella diadema. J Parasitol 68:171–172. https://doi.org/10.1017/S0025315400031015
Kearn GC, Ogawa K, Maeno Y (1992) Hatching patterns of the monogenean parasites Benedenia seriolae and Heteraxine heterocerca from the skin and gills, respectively, of the same host fish Seriola Quinqueradiata. Zool Sci 9(2):451–455
Koesharyani I, Zafran YK, Hatai K (1999) Two species of Capsalid monogeneans infecting cultured humpback grouper Cromileptes altivelis in Indonesia. Fish Pathol 34(3):165–166. https://doi.org/10.3147/jsfp.34.165
Matsusato T (1968) Axine (Heteraxine) heterocerca, an ectoparasitic trematode on cultured yellowtail. Fish Pathol 2(2):105–111. https://doi.org/10.3147/jsfp.2.105
Nordtug T, Kvæstad B, Hagemann (2021) Responses and preferences of salmon louse (Lepeophtheirus salmonis Krøyer 1836) copepodids to underwater artificial light sources Aquaculture. 532:736036. https://doi.org/10.1016/j.aquaculture.2020.736036
Novales Flamarique I, Gulbransen C, Galbraith M, Stucchi D (2009) Monitoring and potential control of sea lice using an LED-based light trap. Can J Fish Aquat Sci 66:1371–1382. https://doi.org/10.1139/F09-094
Nultsch W, Häder DP (1988) Photomovement in motile microorganisms II. Photochem Photobiol 47:837–869. https://doi.org/10.1111/j.1751-1097.1988.tb01668.x
Ogawa K, Bondadreantaso MG, Fukudome M, Wakabayashi H (1995a) Neobenedenia girellae (Hargis, 1955) Yamaguti, 1963 (Monogenea, Capsalidae) from cultured marine fishes of Japan. J Parasitol 81(2):223–227. https://doi.org/10.2307/3283923
Ogawa K, Bondadreantaso MG, Wakabayashi H (1995b) Redescription of Benedenia epinepheli (Yamaguti, 1937) meserve, 1938 (monogenea, capsalidae) from cultured and aquarium marine fishes of Japan. Canadian J Fish Aquat Sci 52:62–70. https://doi.org/10.1139/f95-509
Ogawa K, Egusa S (1981) Redescription of the development of Heteraxine heterocerca (Monogenea: Heteraxinidae) with a note on the relationship between the asymmetry and the site of attachment to the gill. Bull Jap Soc Sci Fish 47:1–7. https://doi.org/10.2331/SUISAN.47.1
Ogawa K, Shirakashi S (2017) Skin fluke infection of cultured marine fish. Fish Pathol 52(4):186–190. (in Japanese with English abstract) https://doi.org/10.3147/jsfp.52.186
Shirakashi S, Nakatsuka S, Udagawa A, Ogawa K (2010) Oncomiracidial behavior of Heterobothrium okamotoi (Monogenea: Diclidophoridae). Fish Pathol 45(2):51–57. https://doi.org/10.3147/jsfp.45.51
Skilton DC, Saunders RJ, Hutson KS (2020) Parasite attractants: identifying trap baits for parasite management in aquaculture. Aquaculture 516:734557. https://doi.org/10.1016/j.aquaculture.2019.734557
Udagawa, A. (2002) Researches on the behavioral characetristics and dispersion of oncomiracidia of the monogenean Heterobothrium okamotoi infecting Takifugu rubripes. PhD. thesis, University of Tokyo, pp. 179. (in Japanese)
Whittington ID, Kearn G (1986) Rhythmical hatching and oncomiracidial behaviour in the hexabothriid monogenean Rajonchocotyle emarginata from the gills of Raja spp. J Mar Biol Assoc U K 66(1):93–111. https://doi.org/10.1017/S0025315400039679
Whittington ID, Kearn GC (1989) Rapid hatching induced by light-intensity reduction in the polyopisthocotylean monogenean Plectanocotyle gurnardi from the gills of gurnards (triglidae), with observations on the anatomy and behavior of the oncomiracidium. J Mar Biol Assoc U K 69(3):609–624. https://doi.org/10.1017/s0025315400031015
Whittington ID, Kearn GC (1990) A comparative study of the anatomy and behaviour of the oncomiracidia of the related monogenean gill parasites Kuhnia scombri, K. sprostonae and Grubea cochlear from mackerel, Scomber scombrus. J Mar Biol Assoc U K 70(1):21–32. https://doi.org/10.1017/S0025315400034160
Whittington ID, Chisholm LA, Rohde K (2000) The larvae of Monogenea (Platyhelminthes). In: Baker JR, Muller R, Rollinson D (eds) Adv Parasitol, vol 44, p 139–232. https://doi.org/10.1016/S0065-308X(08)60232-8
Yamamoto S, Fukushima A, Ishimaru K, Shirakashi S (2014) Shading of net cage is an effective control measure against skin fluke Neobenedenia girellae infection in chub mackerel Scomber japonicus. Fish Sci 80(5):1021–1026. https://doi.org/10.1007/s12562-014-0781-3
Acknowledgements
The authors would like to thank the members of the Fish Pathology Laboratory of the Aquaculture Research Institute, Kindai University, for helping maintain parasite-infected fish and for collecting monogenean eggs.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Section Editor: Guillermo Salgado-Maldonado
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Supplementary file1 (MP4 24909 kb)
Supplementary file2 (MP4 25308 kb)
Rights and permissions
About this article
Cite this article
Shirakashi, S., Asai, N. & Miura, M. Phototactic responses in four monogenean oncomiracidia. Parasitol Res 120, 3173–3180 (2021). https://doi.org/10.1007/s00436-021-07280-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-021-07280-y