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

Yuya Ikeda
Yuya Ikeda
, 
Yuto Koike
Yuto Koike
, 
Ryoji Shinya
Ryoji Shinya
 y 
Koichi Hasegawa
Koichi Hasegawa
   | 25 abr 2024
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Article Category: Research Paper
Publicado en línea: 25 abr 2024
Páginas: -
Recibido: 09 nov 2023
DOI: https://doi.org/10.2478/jofnem-2024-0013
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© 2024 Yuya Ikeda et al., published by Sciendo
This work is licensed under the Creative Commons Attribution 4.0 International License.

Figure 1:

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

Figure 2:

Geographical distribution of Tokorhabditis atripennis in Japan. The numbers in the figure are the proportions of test beetles that were associated with T. atripennis.
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
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
SSUF07 AAA GAT TAA GCC ATG CAT G 18S ribosomal RNA Floyd et al., 2005
SSUR26 CAT TCT TGG CAA ATG CTT TCG
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

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 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)
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