Abstract
Phoresy is a passive transportation behavior where one organism (phoront) disperses to a new location by attaching to another organism. Pseudoscorpions are arthropod predators that mainly live in soil, subterranean habitats, and under tree bark. Some species also live in animal nests and engage in phoresy on small mammals, suggesting close associations with these animals. However, the relationship between phoretic pseudoscorpions and hosts as well as the ecological significance of phoresy remain largely unexplored. Here, to understand the function of phoresy of Megachernes ryugadensis, phoretic on small mammals, their phoretic behavior was investigated in a deciduous forest in northern Japan; individual-level dynamics of phoresy were examined by over 3-year mark-recapture surveys that concurrently marked the host and phoront; and host characteristics, such as sex and age class, were analyzed based on a 2-year small mammal trapping survey. The primary host species was the abundant Japanese wood mouse Apodemus speciosus. Out of 132 pseudoscorpions marked, 5 were recaptured approximately 1 month later. No pseudoscorpions were recaptured within the same census period (3–4 days) when they were marked, indicating that phoresy events last less than one night, and pseudoscorpions are unlikely to engage in phoresy again within a few weeks of their initial engagement. Furthermore, analysis of host characteristics revealed a tendency for female mice and adult individuals to have a higher probability of being hosts compared with males and subadults, respectively. Based on the findings in this and previous studies, the function of phoresy in this species is discussed.
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Data availability
The datasets generated and analyzed during the current study are available from the corresponding author on reasonable request.
References
Bartlow AW, Agosta SJ (2021) Phoresy in animals: review and synthesis of a common but understudied mode of dispersal. Biol Rev 96:223–246. https://doi.org/10.1111/brv.12654
Barton PS, Weaver HJ, Manning AD (2014) Contrasting diversity dynamics of phoretic mites and beetles associated with vertebrate carrion. Exp Appl Acarol 63:1–13. https://doi.org/10.1007/s10493-013-9758-7
Bowler DE, Benton TG (2005) Causes and consequences of animal dispersal strategies: relating individual behaviour to spatial dynamics. Biol Rev 80:205–225
Durden LA (1991) Pseudoscorpions associated with mammals in Papua New Guinea. Biotropica 23:204–206. https://doi.org/10.2307/2388309
Francke O, Villegas-Guzmán GA (2006) Symbiotic relationships between pseudoscorpions (Arachnida) and packrats (Rodentia). J Arachnol 34:289–298. https://doi.org/10.1636/04-36.1
Harvey MS (2013) Pseudoscorpions of the World, version 3.0. Western Australian Museum, Perth. http://www.museum.wa.gov.au/catalogues/pseudoscorpions. Accessed 21 June 2023
Harvey MS, Ratnaweera PB, Udagama PV, Wijesinghe MR (2012) A new species of the pseudoscorpion genus Megachernes (Pseudoscorpiones: Chernetidae) associated with a threatened Sri Lankan rainforest rodent, with a review of host associations of Megachernes. J Nat Hist 46:2519–2535. https://doi.org/10.1080/00222933.2012.707251
Hlebec D, Harms D, Kučinić M, Harvey MS (2023a) Integrative taxonomy of the pseudoscorpion family Chernetidae (Pseudoscorpiones: Cheliferoidea): evidence for new range-restricted species in the Dinaric Karst. Zool J Linn Soc zlad083. https://doi.org/10.1093/zoolinnean/zlad083
Hlebec D, Podnar M, Kučinić M, Harms D (2023b) Molecular analyses of pseudoscorpions in a subterranean biodiversity hotspot reveal cryptic diversity and microendemism. Sci Rep 13:430. https://doi.org/10.1038/s41598-022-26298-5
Keum E, Takaku G, Lee K, Jung C (2016) New records of phoretic mites (Acari: Mesostigmata) associated with dung beetles (Coleoptera: Scarabaeidae) in Korea and their ecological implication. J Asia-Pac Entomol 19:353–357. https://doi.org/10.1016/j.aspen.2016.04.002
Levi HW (1953) Observations on two species of pseudoscorpions. Can Entomol 85:55–62. https://doi.org/10.4039/Ent8555-2
Morikawa K (1954) On some pseudoscorpions in Japanese limegrottoes. Memoirs of the Ehime University Sect II Ser B 2:79–87
Muchmore WB (1971) Phoresy by north and central American pseudoscorpions. Proc Rochester Acad Sci 12:79–97
Murakami O (1974) Growth and development of the Japanese wood mouse (Apodemus speciosus) I. The breeding season in the field. Jap J Ecol 24:194–206
Murienne J, Harvey MS, Giribet G (2008) First molecular phylogeny of the major clades of Pseudoscorpiones (Arthropoda: Chelicerata). Mol Phylogenet Evol 49:170–184. https://doi.org/10.1016/j.ympev.2008.06.002
Muster C, Spelda J, Rulik B et al (2021) The dark side of pseudoscorpion diversity: the German Barcode of Life campaign reveals high levels of undocumented diversity in European false scorpions. Ecol Evol 11:13815–13829. https://doi.org/10.1002/ece3.8088
Ohdachi SD, Ishibashi Y, Fukui D, Saitoh T (eds) (2015) The wild mammals of Japan, 2nd edn. Shokado, Kyoto
Oishi K, Arakaki T, Nakamura M et al (2018) Spatial arrangement and size of home ranges of Apodemus speciosus inhabiting evergreen broad-leaved forest and adjacent cedar plantation, and migration between these stands. Mamm Sci 58:23–31
Okabe K, Makino S, Shimada T et al (2018) Tick predation by the pseudoscorpion Megachernes ryugadensis (Pseudoscorpiones: Chernetidae), associated with small mammals in Japan. J Acarol Soc Japan 27:1–11. https://doi.org/10.2300/acari.27.1
Okabe K, Shimada T, Makino S (2020) Preliminary life history observations of the pseudoscorpion Megachernes ryugadensis (Pseudoscorpiones: Chernetidae) phoretic on wood mice in Japan. J Arachnol 48:155–160. https://doi.org/10.1636/0161-8202-48.2.155
Poinar GO, Curcuc BPM, Cokendolpher JC (1998) Arthropod phoresy involving pseudoscorpions in the past and present. Acta Arachnol 47:79–96. https://doi.org/10.2476/asjaa.47.79
R Core Team (2022) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Accessed 21 June 2023
Sato JJ, Kyogoku D, Komura T et al (2019) Potential and pitfalls of the DNA metabarcoding analyses for the dietary study of the large Japanese wood mouse Apodemus speciosus on Seto Inland Sea islands. Mamm Study 44:221–231. https://doi.org/10.3106/ms2018-0067
Sato JJ, Shimada T, Kyogoku D et al (2018) Dietary niche partitioning between sympatric wood mouse species (Muridae: Apodemus) revealed by DNA meta-barcoding analysis. J Mammal 99:952–964. https://doi.org/10.1093/jmammal/gyy063
Shimada T (2001) Hoarding behaviors of two wood mouse species: different preference for acorns of two Fagaceae species. Ecol Res 16:127–133
Shimada T, Takahashi A, Shibata M, Yagihashi T (2015) Effects of within-plant variability in seed weight and tannin content on foraging behaviour of seed consumers. Funct Ecol 29:1513–1521. https://doi.org/10.1111/1365-2435.12464
Szymkowiak P, Górski G, Bajerlein D (2007) Passive dispersal in arachnids. Biol Lett 44:75–101
Tapia-Ramírez G, Villegas-Guzmán GA, Lorenzo C, Hernández-Núñez A (2022) Phoretic relationship between rodents and pseudoscorpions (Arachnida) in Chiapas, México. Therya Notes 3:46–50. https://doi.org/10.12933/therya_notes-22-68
Tatsukawa K, Murakami O (1976) On the food utilization of the Japanese wood mouse Apodemus speciosus (Mammalia: Muridae). Physiol Ecol Jpn 17:133–144
Tizo-Pedroso E, Del-Claro K (2007) Cooperation in the neotropical pseudoscorpion, Paratemnoides nidificator (Balzan, 1888): feeding and dispersal behavior. Insect Soc 54:124–131. https://doi.org/10.1007/s00040-007-0931-z
Weygoldt P (1969) The biology of pseudoscorpions. Harvard University Press, Cambridge, Massachusetts
White PS, Morran L, de Roode J (2017) Phoresy. Curr Biol 27:R578–R580. https://doi.org/10.1016/j.cub.2017.03.073
World Pseudoscorpiones Catalog (WPC) (2022) World Pseudoscorpiones Catalog, Version 2022. Natural History Museum Bern. http://wac.nmbe.ch. Accessed 21 June 2023
Yoshikawa T (2023) The large japanese field mouse (Apodemus speciosus) as a consumer and potential disperser of seeds of the neurotoxic Japanese star anise (Illicium anisatum). Mamm Study 48:131–135. https://doi.org/10.3106/ms2022-0042
Zeh DW, Zeh JA (1992a) On the function of harlequin beetle-riding in the pseudoscorpion, Cordylochernes scorpioides (Pseudoscorpionida: Chernetidae). J Arachnol 20:47–51
Zeh DW, Zeh JA (1992b) Dispersal-generated sexual selection in a beetle-riding pseudoscorpion. Behav Ecol Sociobiol 30:135–142. https://doi.org/10.1007/BF00173949
Zeh DW, Zeh JA (1992c) Emergence of a giant fly triggers phoretic dispersal in the neotropical pseudoscorpion, Semeiochernes armiger (Balzan)(Pseudoscorpionida: Chernetidae). Bull Br Aracnol Soc 9:43–46
Zeh DW, Zeh JA (1992d) Failed predation or transportation? Causes and consequences of phoretic behavior in the pseudoscorpion Dinocheirus arizonensis (Pseudoscorpionida: Chernetidae). J Insect Behav 5:37–49
Acknowledgements
We are grateful to H. Sato (Tokyo Kasei University) for his valuable comments on our study. We also thank the staff of the Takizawa Research Forest of Iwate University for providing the study site and two anonymous reviewers for their constructive comments on the manuscript.
Funding
This work was supported by Japan Society for the Promotion of Science (JSPS) KAKENHI grants (nos. 16K07794, 19H03005, 22K19882 for TS; nos. 17H00807 and 20H00652 for KO).
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This study was conceived and designed by TS, KO, and SM. All authors contributed to the field surveys. Data analyses were conducted by TS. The first draft of the manuscript was written by TS, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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The methods applied in the field were approved by the local government (Iwate Prefecture, Japan).
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Communicated by: Matjaž Gregorič
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Shimada, T., Okabe, K., Makino, S. et al. Phoretic behavior of the pseudoscorpion Megachernes ryugadensis on the Japanese wood mouse Apodemus speciosus. Sci Nat 110, 51 (2023). https://doi.org/10.1007/s00114-023-01881-6
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DOI: https://doi.org/10.1007/s00114-023-01881-6