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BIHAREAN BIOLOGIST

Univeristy of Oradea, Faculty of Sciences, Department of Biology

Univeristatii str. No.1, Oradea – 410087, Romania

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BIHAREAN BIOLOGIST

(International journal of biology)

ACCEPTED PAPER - Online until proofing -

Authors: George KEHAYIAS; Lambros TSOUNIS Title: Argulus japonicus Thiele, 1900 (Crustacea: Branchiura) collected in light traps – First record from Greece Journal: Biharean Biologist Article number: e182204

Status: awaiting proofing How to cite: Kehayias, G., Tsounis, L., (2019): Argulus japonicus Thiele, 1900 (Crustacea: Branchiura) collected in light traps – First record from Greece. Biharean Biologist 13: art.182204 Date published:

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Argulus japonicus Thiele, 1900 (Crustacea: Branchiura) collected in light traps – First 1 

record from Greece 2 

George Kehayias & Lambros Tsounis 3 

Department of Environmental & Natural Resources Management, University of Patras, 4 

Seferi 2, 30100, Agrinio, Greece 5 

Corresponding author: Kehayias G. E-mail: gkechagi@upatras.gr 6 

Running title: Argulus japonicus from Greece 7 

Abstract 8 

The study reports the collection of 26 specimens of Argulus japonicus in Lake Trichonis 9 

using light traps with chemical light, in the first report of this species from Greece. Diagnostic 10 

morphological characters are provided. The phototactic response of this species is discussed 11 

pointing to the use of light traps for its detection and capture in aquatic ecosystems, and for 12 

field experimentation. 13 

Key words: Argulus japonicus, light traps, Lake Trichonis 14 

The family Arguilidae consists of serious pathogens of freshwater fish. Three Argulus sp. 15 

species have been reported in Europe named as Argulus coregoni Thorell, 1865, Argulus 16 

foliaceus (Linnaeus, 1758) and Argulus japonicus Thiele, 1900. Among the three, A. foliaceus 17 

and A. japonicus are very similar morphologically and their identification is based mainly on 18 

certain characteristics of the male specimens (Rushton-Mellor & Boxshall 1994, Soes et al. 19 

2010). 20 

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A. japonicus is an exotic species for Europe and it was originally described in China. Later, it 21 

has spread to Europe, Africa, Australia and North America through the importation of carp 22 

and gold fish (Avenant-Oldewage & Everts 2010). Within Europe, A. japonicus was first 23 

recorded in 1921 in Spain, while it has been found in Belgium and Fennoscandinavia, Britain, 24 

France, Germany, Italy, Poland, Bosnia, Croatia, Serbia and Slovakia (Soes et al. 2010). The 25 

present study provides the first report of A. japonicus in Lake Trichonis which is the largest 26 

natural lake of Greece. 27 

A. japonicus specimens were collected using light traps constructed according to Kehayias & 28 

Doulka (2007), in which the light was produced by 3 yellow Cyalume light sticks. Three light 29 

traps were deployed in May 2016 for 50 min in various locations in Lake Trichonis (Figure 30 

1), suspended from buoys at 2 m under the surface. After the retrieval of the light traps, their 31 

content was washed through a 50 μm mesh gauze and fixed with buffered 4% formalin. The 32 

sample analysis was made under a Leitz MZ 7.5 stereoscope and photographs were taken 33 

under an Olympus CH20 microscope. The total length and width of all specimens was 34 

measured with an ocular micrometer. 35 

Material examined: 26 specimens (14 ♀, 12 ♂), Greece, Etoloakarnania prefecture, Lake 36 

Trichonis (38o30′– 38o36′ N, 21o26′–21o39′ E), 30.05.2016, leg. G. Kehayias. 37 

Diagnosis: Species identification was made according to Rushton-Mellor (1994), Wadeh et 38 

al. (2008), Soes et al. (2010), Avenant-Oldewage & Everts (2010) and Aalberg et al. (2016). 39 

Female description: Total length 2.12 to 8.80 mm (Standard deviation: ± 2.17), total width 40 

1.32 to 6.28 mm (± 1.60). Body with oval shape, flattened dorso-ventrally (Figure 2), with 2 41 

noticeable compound eyes (dorsally) and 2 sucking discs (ventrally). There are four pairs of 42 

thoracic legs. The carapace covers the base of the fourth pair of legs. The abdomen consists of 43 

two acutely rounded lobes, in which the abdominal incision reaches more than half their 44 

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length. There is a pair of respiratory areas on the ventral surface of the lateral lobes, with the 45 

anterior region being smaller and almost circular, having less than half the size of the larger 46 

kidney-shaped posterior one (Figure 3). 47 

Male description: Total length 1.52 to 5.40 mm (± 1.32), total width 1.00 to 3.44 mm (± 0.85). 48 

The cephalic appendages and carapace structure are similar to those of females (Figure 2). 49 

Differences accounted for the copulatory structures located on the second, third and fourth 50 

leg. In particular, there are two projections positioned on the posterior margin on the basis of 51 

the second leg, a bubble-like socket on the first segment of the third leg, and a peg on the 52 

fourth leg being folded/rolled like a cone (Figure 4). The abdomen lobes are separated by 53 

deep sinus comprising about 40% of the total abdomen length. 54 

Ecological remarks: The present report extends the known geographic distribution of A. 55 

japonicus to the south-east of Europe. Usually Argulus sp. specimens are recovered as 56 

external parasites from fish, mainly cyprinids. Lake Trichonis is inhabited by 20 fish species, 57 

among which eleven cyprinids. However, there have been no reports of Argulus parasites 58 

from any of the fishes of the lake, either because the fishermen do not pay attention on them, 59 

or/and their density in their hosts is not alarming for the fishermen. Thus, it was a surprise to 60 

find this species in samples taken with light traps, while to our knowledge this must be the 61 

first report of capturing this species with the use of light traps. It is well known that vision is 62 

important for the Argulidae when they are searching for hosts (Mikheev et al., 1998) and that 63 

a change in the illumination level produced a clear difference in the searching behavior 64 

(Mikheev et al., 2000). Thus, it is assumed that A. japonicus specimens, being positively 65 

phototactic, swum towards the light cue and managed to find the entrances to get inside the 66 

light traps, in a time and energy consuming process, probably as an intense effort to find 67 

hosts. This behavior could be triggered by the presence of fish fry captured inside the light 68 

traps. Indeed, intense fry infestation by A. foliaceus in illuminated cages has been reported by 69 

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Ziliukiene et al. (2012). In any case, the presently reported phototactic response of A. 70 

japonicus is interesting and could stimulate future field behavioral studies using light traps. 71 

Acknowledgements 72 

We wish to thank Dr. Ole Møller and especially Professor Annemarie Avenant-Oldewage for 73 

their valuable aid in the identification of Argulus japonicus. This research received no specific 74 

grant from any funding agency in the public, commercial, or not-for-profit sectors. 75 

References 76 

Aalberg, K., Koščová, L., Šmiga, Ľ., Košuth, P., Koščo, J., Oros, M., Barčák, D., Lazar, P. 77 

(2016): A study of fish lice (Argulus sp.) infection in freshwater food fish. Folia Veterinaria 78 

60(3): 54-59. 79 

Avenant-Oldewage, A., Everts, L. (2010): Argulus japonicus: Sperm transfer by means of a 80 

spermatophore on Carassius auratus (L). Experimental Parasitology 126: 232-238. 81 

Doulka, E., Kehayias, G. (2008): Spatial and temporal distribution of zooplankton in Lake 82 

Trichonis (Greece). Journal of Natural History 42(5–8): 575–595. 83 

Kehayias, G., Doulka, E. (2007): A light trap for sampling Atherina boyeri larvae in Lake 84 

Trichonis (western Greece). Journal of Freshwater Ecology 22(3): 533-53. 85 

Mikheev, V. N., Valtonen, E. T. & Rintamäki-Kinnunen, P. (1998): Host searching in Argulus 86 

foliaceus L. (Crustacea: Branchiura): the role of vision and selectivity. Parasitology 116: 425-87 

430. 88 

Mikheev, V. N., Mikheev, A. V., Pasternak, A. F., Valtonen, E. T. (2000): Light-mediated 89 

host searching strategies in a fish ectoparasite, Argulus foliaceus L. (Crustacea: Branchiura). 90 

Parasitology 120: 409-416. 91 

Use the following type of citation: Biharean Biologist 2019: e182204

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Rushton-Mellor, S. K., Boxshall, G. A. (1994): The developmental sequence of Argulus 92 

foliaceus (Crustacea: Branchiura). Journal of Natural History 28: 763-785. 93 

Soes, D. M., Walker, P. D., Kruijt, D. B. (2010): The Japanese fish louse Argulus japonicas 94 

new for The Netherlands. Lauterbornia 70: 11-17. 95 

Wadeh, H., Yang, J. W., Li, G. Q. (2008): Ultrastructure of Argulus japonicus Thiele, 1900 96 

Crustacea: Branchiura) collected from Guangdong, China. Parasitology Research 102:765–97 

770. 98 

Ziliukiene, V., Žiliukas, V., Stankus, S. (2012): Infestation of Argulus foliaceus on fish fry 99 

reared in illuminated cages. Veterinarija ir Zootechnika 57(79): 83-88. 100 

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Figure 1. The map of Lake Trichonis in western Greece. 112 

Figure 2. Left: Adult female (7.40 length, 5.40 width). Right: Adult male (5.40 length, 3.44 113 

width). 114 

Figure 3. Respiratory areas of a female (ventral side). 115 

Figure 4. Copulatory structures located on the second, third and fourth leg of a male 116 

specimen. Two projections of the basis segment of the second leg, the socket on the third leg, 117 

the peg on the fourth leg. Magnification of the peg (pullout photo). 118 

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Figure 1. The map of Lake Trichonis in western Greece. 133 

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Figure 2. Left: Adult female (7.40 length, 5.40 width). Right: Adult male (5.40 length, 3.44 137 

width). 138 

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Figure 3. Respiratory areas of a female (ventral side). 141 

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142 

Figure 4. Copulatory structures located on the second, third and fourth leg of a male. Two 143 

projections of the basis segment of the second leg, the socket on the third leg, the peg on the 144 

fourth leg. Magnification of the peg (pullout photo). 145 

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