Geographical distribution and phoretic associations of the viviparous nematode Tokorhabditis atripennis with Onthophagus dung beetles in Japan

Ikeda, Yuya; Koike, Yuto; Shinya, Ryoji; Hasegawa, Koichi

Geographical distribution and phoretic associations of the viviparous nematode Tokorhabditis atripennis with Onthophagus dung beetles in Japan

Journal of Nematology

Volume 56 (2024): Issue 1 (March 2024)

By:

Yuya Ikeda, Yuto Koike, Ryoji Shinya and Koichi Hasegawa

Open Access

|Apr 2024

Figures & Tables

The body parts of beetles examined the number of Tokorhabditis atripennis associated.

Geographical distribution of Tokorhabditis atripennis in Japan. The numbers in the figure are the proportions of test beetles that were associated with T. atripennis.

Primer list used in this study_

Description	Primer sequence 5′-3′	Target	Reference
D2a	ACA AGT ACC GTG AGG GAA AGT TG	D2/D3 extension segments of the 28S ribosomal RNA	Nunn, 1992
D3b	TCG GAA GGA ACC AGC TAC TA	D2/D3 extension segments of the 28S ribosomal RNA	Nunn, 1992
D1F	AAG GAT TCC CTT AGT AAC GGC GAT TG	D1/D4 extension segments of the 28S ribosomal RNA	Kanzaki et al., 2021
D4R	GCG GTA TTT GCT ACT ACC AYY AMG ATC TG	D1/D4 extension segments of the 28S ribosomal RNA	Kanzaki et al., 2021
SSUF07	AAA GAT TAA GCC ATG CAT G	18S ribosomal RNA	Floyd et al., 2005
SSUR26	CAT TCT TGG CAA ATG CTT TCG		Floyd et al., 2005
18S-CL-F3	CTT GTC TCA AAG ATT AAG CCA TGC AT		Carta et al., 2018
18S-CL-R1	ACC TTG TTA CGA C T TTT G		Carta et al., 2018

Percentage of dung beetles associated with Tokorhabditis atripennis_

Host		% beetles associated with nematodes to total examined beetles (no. associated/no. examined)
Genus	Species
Aphodius		0.00 (0/103)
Ataenius		0.00 (0/8)
Copris		0.00 (0/25)
Caccobius		1.69 (2/118)
	Caccobius jessoensis		1.22 (1/82) ^a
	Caccobius unicornis		3.13 (1/32) ^ab
Onthophagus		8.33 (23/276)
	Onthophagus apicetinctus		23.3 (10/43) ^bc
	Onthophagus atripennis		14.9 (7/47) ^bc
	Onthophagus lenzii		6.67 (2/30) ^abc
	Onthophagus ohbayashii		4.11 (3/73) ^abc
	Onthophagus viduus		5.26 (1/19) ^abc
Phelotrupes		2.35 (2/85)
	Phelotrupes laevistriatus		2.47 (2/81) ^a

Total		4.07 (27/615)

Information on all Tokorhabditis atripennis strains obtained in this study_

Strain	Date	Collection Site	Host	Beetles’ body site
KHA602	2016.6.5	Chubu Univ, Kasugai, Aichi	O. atripennis	-
KHA603	2016.6.5	Chubu Univ, Kasugai, Aichi	O. atripennis	-
KHA604	2016.6.5	Chubu Univ, Kasugai, Aichi	O. atripennis	-
KHA605	2017.5.10	Chubu Univ, Kasugai, Aichi	O. atripennis	1), 2)
KHA606	2017.5.27	Kasugano Enchi, Nara Park, Nara	O. lenzii	2), 4)
KHA607	2017.5.28	Asajigahara, Nara Park, Nara	O. ohbayashii	3)
KHA608	2017.5.28	Asajigahara, Nara Park, Nara	O. lenzii	1), 2), 3)
KHA612	2017.7.2	Toino misaki, Kushima, Miyazaki	C. unicornis	2)
KHA611	2017.7.7	Ishigaki, Okinawa	O. apicetinctus	2)
KHA609	2017.7.7	Ishigaki, Okinawa	O. apicetinctus	2)
KHA610	2017.7.7	Ishigaki, Okinawa	O. viduus	3)
KHA613	2018.5.11	Morioka, Iwate	C. jessoensis	3)
KHA614	2018.7.24	Asajigahara, Nara Park, Nara	O. ohbayashii	2)
KHA615	2018.7.24	Asajigahara, Nara Park, Nara	O. ohbayashii	3)
KHA616	2018.12.3	Tonoshiro Park, Ishigaki, Okinawa	O. apicetinctus	2)
KHA619	2018.12.2	Shinsakae Park, Ishigaki, Okinawa	O. apicetinctus	3)
KHA620	2018.12.2	Tonoshiro Park, Ishigaki, Okinawa	O. apicetinctus	3)
KHA617	2018.12.2	Tonoshiro Park, Ishigaki, Okinawa	O. apicetinctus	3)
KHA621	2018.12.2	Tonoshiro Park, Ishigaki, Okinawa	O. apicetinctus	3)
KHA622	2018.12.2	Tonoshiro Park, Ishigaki, Okinawa	O. apicetinctus	3)
KHA623	2018.12.2	Tonoshiro Park, Ishigaki, Okinawa	O. apicetinctus	2)
KHA618	2018.12.2	Tonoshiro Park, Ishigaki, Okinawa	O. apicetinctus	3)
SHR9	2021.5.14	Meiji Univ, Kawasaki, Kanagawa	O. atripennis	2)
SHR12	2021.8.3	Meiji Univ, Kawasaki, Kanagawa	P. laevistriatus	1)
SHR21	2021.8.4	Meiji Univ, Kawasaki, Kanagawa	O. atripennis	3)
SHR24	2021.8.4	Meiji Univ, Kawasaki, Kanagawa	P. laevistriatus	6)
SHR16	2021.9.30	Kurokawa Field Science Center, Kawasaki, Kanagawa	O. atripennis	2), 3)

The number of beetles collected for each attractant and collection site, with the exception of pit-hole traps_

Attractant	Date	Collecting site	Beetles number
Extensive raising deer dropping	2017.5.27	Araike, Nara Park, Nara	35
		Kasugano Enchi, Nara Park, Nara	26
	2017.5.28	Araike, Nara Park, Nara	8
		Asajigahara, Nara Park, Nara	19
	2018.7.24	Araike, Nara Park, Nara	19
		Asajigahara, Nara Park, Nara	74
Extensive raising cow dropping	2017.6.24	Chausuyama, Kitashitara, Aichi	47
Wild horse dropping	2017.7.2	Toino misaki, Kushima, Miyazaki	8
Domestic cow dropping	2017.7.4	Yakushima, Kagoshima	15
Dog or Cat dropping	2017.7.7	Ishigaki, Okinawa	7
	2018.12.1	Matsuo Park, Naha, Okinawa	1
		Chuo Park, Naha, Okinawa	2
		Midorigaoka Park, Naha, Okinawa	14
	2018.12.3	Tonoshiro Park, Ishigaki, Okinawa	4
	2018.12.2	Tonoshiro Park, Ishigaki, Okinawa	25
		Tonoshiro Park, Ishigaki, Okinawa	20
		Shogyo ji, Ishigaki, Okinawa	3
Hand catch	2017.8.28	Kurama, Kyoto	2
	2021.9.16	Meiji Univ, Kawasaki, Kanagawa	2
Wild deer dropping	2017.9.26	Kamaishi, Iwate	6
	2017.10.16	Kagoshima Univ, Takakuma, Kagoshima	2
	2017.11.1	Shiriyazaki, Aomori	17
	2018.5.11	Morioka, Iwate	13
	2018.8.29	Asahisashi, Kamaishi, Iwate	39
		Ogawa, Kamaishi, Iwate	29
Domestic sheep dropping	2018.8.22	Nakasatsunai, Hokkaido	5
Vending machine light	2018.8.28	Morioka, Iwate	2
Extensive raising horse dropping	2018.9.4	Aso, Kumamoto	35
Streetlight	2021.6.25	Atsuma, Hokkaido	4
	2021.7.17	Uehara, Taketomi, Yaeyama, Okinawa	8

Total			491

Percentage of dung beetles associated with Tokorhabditis atripennis in each prefecture_

Prefecture	% associated (no. associated site/no. examined)

	*Aphodius*	*Ataenius*	*Copris*	*Caccobius*	*Onthophagus*	*Phelotrupes*	Total
Hokkaido	0.00 (0/5)		0.00 (0/4)				0.00 (0/9)
Aomori	0.00 (0/17)						0.00 (0/17)
Iwate	0.00 (0/9)		0.00 (0/7)	1.79 (1/56)	0.00 (0/17)		1.12 (1/89)
Kanagawa					7.69 (3/39)	3.92 (3/51)	5.56 (5/90)
Gifu						0.00 (0/2)	0.00 (0/2)
Aichi	0.00 (0/6)			0.00 (0/17)	8.89 (4/45)	0.00 (0/13)	4.94 (4/81)
Kyoto						0.00 (0/2)	0.00 (0/2)
Nara	0.00 (0/62)			0.00 (0/11)	5.26 (5/95)	0.00 (0/13)	2.76 (5/181)
Miyazaki				12.5 (1/8)			12.5 (1/8)
Kumamoto	0.00 (0/4)		0.00 (0/14)	0.00 (0/10)	0.00 (0/5)	0.00 (0/2)	0.00 (0/35)
Kagoshima					0.00 (0/15)	0.00 (0/2)	0.00 (0/17)
Okinawa		0.00 (0/8)		0.00 (0/16)	18.3 (11/60)		13.1 (11/84)

Total	0.00 (0/103)	0.00 (0/8)	0.00 (0/25)	1.69 (2/118)	8.33 (23/276)	2.35 (2/85)	4.39 (27/615)

Beetle number_

Date	Name	Number
2016.6.5	Onthophagus atripennis	10
2016.6.5	Onthophagus viduus	3
2016.6.5	Phelotrupes laevistriatus	1
2016.5.22	Phelotrupes laevistriatus	2
2016.7.5	Onthophagus atripennis	1
2016.11.15	Phelotrupes laevistriatus	1
2017.5.8	Onthophagus atripennis	1
2017.5.10	Onthophagus atripennis	1
2017.5.26	Onthophagus atripennis	5
2017.5.27	Phelotrupes laevistriatus	2
2017.5.27	Aphodius urostigma	2
2017.5.27	Aphodius rugosostriatus	2
2017.5.27	Aphodius botulus Balthasar	1
2017.5.27	Aphodius pusillus	3
2017.5.27	Aphodius superatratus	21
2017.5.27	Onthophagus ater	3
2017.5.27	Aphodius atratus	2
2017.5.27	Onthophagus ohbayashii	19
2017.5.27	Aphodius variabilis	1
2017.5.27	Aphodius sublimbatus	1
2017.5.27	Caccobius unicornis	1
2017.5.27	Onthophagus lenzii	2
2017.5.27	Aphodius uniplagiatus	1
2017.5.28	Phelotrupes laevistriatus	6
2017.5.28	Aphodius pusillus	1
2017.5.28	Aphodius superatratus	11
2017.5.28	Onthophagus ohbayashii	5
2017.5.28	Caccobius unicornis	2
2017.5.28	Onthophagus lenzii	2
2017.6.24	Onthophagus atripennis	1
2017.6.24	Onthophagus ater	9
2017.6.24	Onthophagus lenzii	1
2017.6.24	Aphodius japonicus	3
2017.6.24	Aphodius rectus	3
2017.6.24	Caccobius jessoensis	17
2017.6.24	Onthophagus nitidus	13
2017.7.2	Caccobius unicornis	5
2017.7.2	Caccobius brevis	3
2017.7.4	Onthophagus lenzii	15
2017.7.7	Onthophagus viduus	4
2017.7.7	Onthophagus apicetinctus	3
2017.8.28	Phelotrupes laevistriatus	2
2017.9.26	Caccobius jessoensis	5
2017.9.26	Onthophagus nitidus	1
2017.10.16	Phelotrupes auratus	2
2017.11.1	Aphodius botulus Balthasar	2
2017.11.1	Aphodius rectus	15
2018.5.11	Onthophagus ohbayashii	2
2018.5.11	Caccobius jessoensis	11
2018.7.24	Onthophagus atripennis	7
2018.7.24	Phelotrupes laevistriatus	5
2018.7.24	Aphodius pusillus	8
2018.7.24	Onthophagus ohbayashii	47
2018.7.24	Caccobius unicornis	8
2018.7.24	Onthophagus lenzii	6
2018.7.24	Aphodius rectus	1
2018.7.24	Onthophagus nitidus	4
2018.7.24	Aphodius uniformis	7
2018.8.22	Aphodius pusillus	3
2018.8.22	Aphodius uniformis	2
2018.8.28	Onthophagus nitidus	2
2018.8.29	Aphodius rugosostriatus	2
2018.8.29	Caccobius jessoensis	40
2018.8.29	Onthophagus nitidus	12
2018.8.29	Aphodius igai	2
2018.8.29	Copris acutidens	7
2018.8.29	Aphodius troitzkyi	5
2018.9.4	Aphodius urostigma	4
2018.9.4	Onthophagus lenzii	4
2018.9.4	Caccobius jessoensis	9
2018.9.4	Onthophagus nitidus	1
2018.9.4	Caccobius brevis	1
2018.9.4	Phelotrupes auratus	2
2018.9.4	Copris acutidens	14
2018.12.1	Caccobius unicornis	16
2018.12.1	Onthophagus murasakinus	1
2018.12.3	Onthophagus apicetinctus	4
2018.12.2	Onthophagus viduus	12
2018.12.2	Onthophagus apicetinctus	36
2020.11.16	Phelotrupes laevistriatus	2
2020.11.21	Phelotrupes laevistriatus	4
2020.11.23	Phelotrupes laevistriatus	2
2020.11.28	Phelotrupes laevistriatus	3
2021.5.14	Onthophagus atripennis	5
2021.5.14	Phelotrupes laevistriatus	10
2021.5.14	Onthophagus nitidus	4
2021.5.15	Onthophagus atripennis	2
2021.5.15	Phelotrupes laevistriatus	1
2021.5.16	Phelotrupes laevistriatus	1
2021.6.11	Phelotrupes laevistriatus	1
2021.6.11	Onthophagus fodiens	2
2021.6.14	Onthophagus nitidus	1
2021.6.25	Copris acutidens	4
2021.7.17	Ataenius australasiae	8
2021.8.2	Onthophagus atripennis	4
2021.8.2	Phelotrupes laevistriatus	9
2021.8.3	Phelotrupes laevistriatus	12
2021.8.3	Onthophagus nitidus	1
2021.8.4	Onthophagus atripennis	2
2021.8.4	Phelotrupes laevistriatus	9
2021.9.16	Phelotrupes laevistriatus	2
2021.9.30	Onthophagus atripennis	8
2021.9.30	Phelotrupes laevistriatus	1
2021.9.30	Onthophagus nitidus	2
2021.9.30	Onthophagus fodiens	1
2021.10.20	Phelotrupes laevistriatus	2
2021.10.20	Onthophagus ater	3
2021.10.21	Phelotrupes laevistriatus	3
2021.10.21	Onthophagus ater	4

Summary of Tokorhabditis atripennis strains_

Strain	Collection site	Accession No. LSU	Accession No. SSU
KHA602	Chubu Univ, Kasugai	OR632650	OR632672
KHA603	Chubu Univ, Kasugai	OR632651	OR632673
KHA604	Chubu Univ, Kasugai	OR632652	OR632674
KHA605	Chubu Univ, Kasugai	OR632653	OR632675
KHA606	Kasugano Enchi, Nara	OR632654	OR632676
KHA607	Asajigahara, Nara	OR632655	OR632677
KHA608	Asajigahara, Nara	OR632656	OR632678
KHA612	Toino misaki, Kushima	OR632660	OR632682
KHA611	Ishigaki, Okinawa	OR632659	OR632682
KHA609	Ishigaki, Okinawa	OR632657	OR632679
KHA610	Ishigaki, Okinawa	OR632658	OR632680
KHA613	Morioka, Iwate	OR632661	OR632683
KHA614	Asajigahara, Nara	OR632662	OR632684
KHA615	Asajigahara, Nara	OR632663	OR632685
KHA616	Tonoshiro Park, Ishigaki	OR632664	OR632686
KHA619	Shinsakae Park, Ishigaki	OR632667	OR632689
KHA620	Tonoshiro Park, Ishigaki	OR632668	OR632690
KHA617	Tonoshiro Park, Ishigaki	OR632665	OR632687
KHA621	Tonoshiro Park, Ishigaki	OR632669	OR632691
KHA622	Tonoshiro Park, Ishigaki	OR632670	OR632692
KHA623	Tonoshiro Park, Ishigaki	OR632671	OR632693
KHA618	Tonoshiro Park, Ishigaki	OR632666	OR632688
SHR9	Meiji Univ, Kawasaki	OR681495	-
SHR12	Meiji Univ, Kawasaki	OR681496	-
SHR21	Meiji Univ, Kawasaki	OR681497	-
SHR24	Meiji Univ, Kawasaki	OR681498	OR717327
SHR16	Kurokawa, Kawasaki	OR681499	-

The number of Tokorhabditis atripennis isolated from each body part of dung beetles_

Host		% associated (no. associated body part/no. examined)

Genus	Species	(1)	(2)	(3)	(4)	(5)	(6)
Caccobius		0.00 (0/3)	33.3 (1/3)	33.3 (1/3)	33.3 (1/3)	0.00 (0/3)	0.00 (0/3)
	Caccobius jessoensis	0.00 (0/2)	0.00 (0/2)	50.0 (1/2)	50.0 (1/2)	0.00 (0/2)	0.00 (0/2)
	Caccobius unicornis	0.00 (0/1)	100 (1/1)	0.00 (0/1)	0.00 (0/1)	0.00 (0/1)	0.00 (0/1)
Onthophagus		8.33 (2/24)	41.7 (10/24)	45.8 (11/24)	4.17 (1/24)	0.00 (0/24)	0.00 (0/24)
	Onthophagus apicetinctus	0.00 (0/10)	40.0 (4/10)	60.0 (6/10)	0.00 (0/10)	0.00 (0/10)	0.00 (0/10)
	Onthophagus atripennis	16.7 (1/6)	50.0 (3/6)	33.3 (2/6)	0.00 (0/6)	0.00 (0/6)	0.00 (0/6)
	Onthophagus lenzii	20.0 (1/5)	40.0 (2/5)	20.0 (1/5)	20.0 (1/5)	0.00 (0/5)	0.00 (0/5)
	Onthophagus ohbayashii	0.00 (0/2)	50.0 (1/2)	50.0 (1/2)	0.00 (0/2)	0.00 (0/2)	0.00 (0/2)
	Onthophagus viduus	0.00 (0/1)	0.00 (0/1)	100 (1/1)	0.00 (0/1)	0.00 (0/1)	0.00 (0/1)
Phelotrupes		50.0 (1/2)	0.00 (0/2)	0.00 (0/2)	0.00 (0/2)	0.00 (0/2)	50.0 (1/2)
Phelotrupes	Phelotrupes laevistriatus	50.0 (1/2)	0.00 (0/2)	0.00 (0/2)	0.00 (0/2)	0.00 (0/2)	50.0 (1/2)

Total		10.3 (3/29)	37.9 (11/29)	41.4 (12/29)	6.90 (2/29)	0.00 (0/29)	3.45 (1/29)

DOI: https://doi.org/10.2478/jofnem-2024-0013 | Journal eISSN: 2640-396X | Journal ISSN: 0022-300X

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Language: English

Submitted on: Nov 9, 2023

Published on: Apr 25, 2024

Published by: Society of Nematologists, Inc.

In partnership with: Paradigm Publishing Services

Publication frequency: 1 times per year

Keywords:

insect-nematode interaction,

Related subjects:

© 2024 Yuya Ikeda, Yuto Koike, Ryoji Shinya, Koichi Hasegawa, published by Society of Nematologists, Inc.
This work is licensed under the Creative Commons Attribution 4.0 License.

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Geographical distribution and phoretic associations of the viviparous nematode Tokorhabditis atripennis with Onthophagus dung beetles in Japan

Figures & Tables

Figure 1:

Figure 2:

Primer list used in this study_

Percentage of dung beetles associated with Tokorhabditis atripennis_

Information on all Tokorhabditis atripennis strains obtained in this study_

The number of beetles collected for each attractant and collection site, with the exception of pit-hole traps_

Percentage of dung beetles associated with Tokorhabditis atripennis in each prefecture_

Beetle number_

Summary of Tokorhabditis atripennis strains_

The number of Tokorhabditis atripennis isolated from each body part of dung beetles_

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