Tick Predation by the Pseudoscorpion Megachernes Ryugadensis (Pseudoscorpiones: Chernetidae), Associated with Small Mammals in Japan*

J. Acarol. Soc. Jpn., 27(1): 1-11. May 25, 2018 © The Acarological Society of Japan http://www.acarology-japan.org/ 1

Tick predation by the pseudoscorpion Megachernes ryugadensis (Pseudoscorpiones: Chernetidae), associated with small mammals in Japan*

Kimiko OKABE1†, Shun’ichi MAKINO1, Takuya SHIMADA2‡, Takuya FURUKAWA1,

Hayato IIJIMA1 and Yuya WATARI1 1Forestry and Forest Products Research Institute, 1 Matsunosato, Tsukuba, Ibaraki, 305-8687 Japan 2Tohoku Research Center, Forestry and Forest Products Research Institute, 92-25 Nabeyashiki, Shimokuriyagawa, Morioka, Iwate, 020-0123 Japan

(Received 7 January 2018; Accepted 11 March 2018)

ABSTRACT

Ticks are obligate blood feeders that parasitize a variety of vertebrates and can be serious pests for these animals. Due to public concerns about the risk of chemical controls, there is a high demand for biological control agents to reduce tick populations and the spread of tick-borne diseases. In this study, we observed tick predation by the pseudoscorpion Megachernes ryugadensis in a laboratory for the first time. Adult and tritonymphal M. ryugadensis were collected in the field during phoresis on Japanese wood mice and transferred to a Petri dish. These pseudoscorpions preyed on larval Haemaphysalis ticks and nymphal and adult Haemaphysalis megaspinosa. Most pseudoscorpions fed on two to three larval ticks on the first day following tick transfer. There were no significant differences between male and female pseudoscorpions in the numbers of larval ticks consumed or the numbers of days required to consume all ticks. Although there was no significant difference between the numbers of days to consume nymphal and adult male ticks, male pseudoscorpions consumed adult female ticks significantly faster than did female pseudoscorpions. Although the sample sizes in this study were small, the tritonymphal pseudoscorpion displayed similar trends in the predation of larval and nymphal ticks. Further study is required to obtain detailed information on the life history traits of the tick and pseudoscorpion and the impacts of the tick on small rodents and their nest fauna to determine the role of M. ryugadensis as a natural enemy of ticks. Key words: biological control, natural enemy, nidicolous species, rodent, symbiosis

* Supplementary videos are available on the website of the Acarological Society of Japan (http://www/acarology- japan.org/). † Corresponding author: email: [email protected] ‡ Present address: Forestry and Forest Products Research Institute, Tsukuba. DOI: 10.2300/acari.27.1 2 Kimiko OKABE et al.

INTRODUCTION

Ixodida or ticks are obligate blood feeders that parasitize a variety of vertebrates and can be serious pests for these animals through blood reduction, disease transmission, or injuries caused by primary and/or secondary irritation at the attachment site (Oliver, 1989). In wild animals, especially those that are small and/or slender, blood loss to parasites such as ticks is not trivial; thus, they have developed avoidance strategies including grooming and cleaning (Hart, 1992; Schmid-Hempel, 2014; Loker and Hofkin, 2015). Large numbers of ticks can cause substantial economic losses in livestock and transmit various kinds of human disease agents including Lyme disease, Japanese spotted fever, and severe fever with thrombocytopenia syndrome (SFTS) (Fukunaga et al., 1995; Ishikura et al., 2002; Jongejan and Uilenberg, 2004; Parola et al., 2005; Takahashi et al., 2013). Chemical control of ticks has been widely implemented, and potential biological control agents have been listed and tested (Samish and Rehacek, 1999; Samish et al., 2001, 2004; Willadsen, 2006). Because chemical controls are not necessarily effective in reducing tick-borne diseases, and public concerns about environmental pollution by these agents have been raised, there is a high demand for biological agents to control tick populations, in combination with chemical controls (Samish et al., 2004). Pseudoscorpions (Arachnida, Pseudoscorpiones), which include more than 3,200 species, are known to live under soil around the litter layer, under the bark of dead trees, or near vertebrates, e.g., on guano in caves or in rodent nests (Weygoldt, 1969; Harvey, 1992; Murienne et al., 2008). All pseudoscorpions are predators of small arthropods; they can ambush approaching prey, often at their nest entrance, but sometimes actively approach prey alone or in cooperation with conspecifics (Weygoldt, 1969; Del-Claro and Tizo-Pedroso, 2009). The predatory behaviors of some species are relatively well described: they use palpal chelae on the pedipalpi to sense and prey on living arthropods and suck their body fluid (Weygoldt, 1969); however, behaviors of some species remain unknown. Some pseudoscorpions, including most Megachernes (Chernetidae) species are unique in that they maintain close relationships with small rodents by inhabiting their nests and exploiting them for migration (phoresy) (Hoff and Clawson, 1952; Francke and Vallegas-Guzmán, 2006; Harvey et al., 2012). Megachernes ryugadensis was first collected on bat guano in a cave in Kochi, Japan, and was later recorded in bumblebee nests or body surfaces of the brown rat, Rattus norvegicus and Japanese mole, Mogera wogura during phoresy in Japan except for the Nansei Islands (Morikawa, 1954, 1960; Sato and Sakayori, 2015). Although Morikawa (1954 and 1960) suggested that the species fed on ticks in guano, no evidence was provided. In a preliminary study, we found that M. ryugadensis was commonly phoretic on forest mice in Morioka, Japan. In this study, we focused on tick predation by this species. To assess the performance of M. ryugadensis as a natural enemy of ticks, parasitizing wild animals including small rodents, we observed predatory behavior of M. ryugadensis on ticks. Because we were not able to observe their behavior under natural conditions, we supplied common ticks (Haemaphysalis megaspinosa) at different developmental stages to M. ryugadensis pseudoscorpions in a laboratory and observed interactions between these species. Small rodents Tick predation by Megachernes ryugadensis 3 host a wide range of immature ixodids (Oliver, 1989); therefore, we estimated the potential performance of M. ryugadensis as a natural enemy of ticks based on our laboratory experiments.

MATERIAL AND METHODS

Collection of materials We collected the pseudoscorpion M. ryugadensis (Fig. 1) in phoresis on the large Japanese wood mouse Apodemus speciosus and the small Japanese wood mouse A. argenteus (Rodentia: Muridae), which were trapped using Sherman traps in a deciduous forest located within the Takizawa research forest of Iwate University, Morioka, Iwate, Japan (39°47’N, 141°09’E, approximately 200 m a.s.l.). Adult and tritonymphal M. ryugadensis were removed from rodents with forceps during rodent sampling in the field and maintained in the laboratory in a plastic cup (diameter at top: 5 cm, height: 3.5 cm) with wet wood pieces at the bottom (thickness: ca. 1 cm) and covered by a lid with small holes for ventilation. Once per week, approximately 30 acarid mites (mostly adults), which had probably originated from a wild lucanid beetle (Dorcus rectus) and been reared on dry yeast, were released into the cup as food. We collected ticks at all stages using the flagging method (Fujimoto et al., 1986) in forests in Nikko, Tochigi, in October 2017 and some unfed adult ticks and fed nymphal and adult ticks from dead sika deer in November 2017. Living ticks were identified in a laboratory to stages and at the species (nymphal and adult ticks) or genus level (larvae) using published identification keys (Fujita and Takada, 2007; Yamauchi and Takada, 2015). As H. megaspinosa was abundant, we used this species in pseudoscorpion predation experiments. We maintained living ticks, for 1 week at most, on moistened flannel in a plastic bag at 15 ± 2℃ or in a plastic bottle in a refrigerator at around 5℃. Predation experiment We used adult and tritonymphal pseudoscorpions collected within the previous 4 months (August–November 2017) and 6 months (June–November 2017), respectively. About 24 h prior to the experiments, we confined each M. ryugadensis in a small plastic Petri dish (diameter: 3.7 cm, height: 1.1 cm) with a small amount of wet peat moss in the middle of the dish to maintain moisture and provide a hiding place for the pseudoscorpion. In our preliminary experiments, pseudoscorpions survived for at least 5 days without food under these conditions. We released tick(s) into the Petri dish as prey using a fine paintbrush. We transferred five larval ticks, one nymphal tick, or one adult tick to a Petri dish containing a pseudoscorpion. We conducted eight and five replicates for each sex of adult pseudoscorpion to examine the predation of larval ticks and of the other stages, respectively (Table 1). Due to limited sample sizes, we conducted four and two replicates of tritonymphal pseudoscorpion introduction for larval and nymphal ticks, respectively (Table 1). For the same reason, we did not provide adult ticks as prey. We used a different pseudoscorpion in each replicate to avoid any influence of previous feeding experience. Petri dishes containing a pseudoscorpion and tick(s) were sealed with plastic paraffin film (Parafilm) and maintained in a thermostatic chamber (25 ± 2°C, 60 ± 10% relative humidity, and 12 h light:12 h dark). We checked M. ryugadensis survival and the number of ticks consumed daily by opening the 4 Kimiko OKABE et al. lid (also providing ventilation) until all ticks within a dish were dead. If ticks, particularly larvae, were found in the tiny space between the lid and bottom of the dish, we transferred them back to the bottom of the dish. When body contents of the dead ticks were lost (Fig. 2) or when we found a pseudoscorpion preying on a tick, we considered the ticks to be consumed by the pseudoscorpion. Still and moving images of pseudoscorpions and ticks were recorded ad libitum under a stereomicroscope (Leica, S8APO) equipped with a photo system (Leica, MC170HD). To determine whether pseudoscorpions also prey on fed ticks, we provided an adult male pseudoscorpion with a tick that had been sucking blood to an extent (two adult females but one was larger than the other because of feeding; two nymphs); however, we did not perform any statistical analyses due to the limited sample size. To determine whether the pseudoscorpions showed interest in dead ticks as prey, we also provided three larval and one nymphal tick that were killed by freezing at about –30℃ for 3.5 h before the experiment to five adult male pseudoscorpions. Statistical analyses We used data from five individual pseudoscorpions of each sex that had survived the experiments for statistical analysis. We excluded (but recorded) pseudoscorpions that were dead before predation from the analysis. We compared the numbers of larval ticks consumed on the first day and the total number of days to consume provided tick(s) between adult female and male pseudoscorpions using a t-test after homogeneity of variance was examined using an F-test. We used the R statistical package (R Core Team, 2017) for statistical analyses. Due to small sample numbers (fewer than five replicates), we did not calculate the average and standard deviation for the nymphal pseudoscorpion predation experiments.

RESULTS

The idiosomas of larval and nymphal ticks became transparent, except for the scutum, after being fed upon by pseudoscorpions (Fig. 2A, B). In adult ticks, the dorsal idiosomal color was maintained, but body contents seen through the outer skin displayed a specific pattern in H. megaspinosa (pale and dark brown with occasional white patterns), which was lost (Fig. 2C). Of the 20 dead adult ticks, 17 more or less lost body fluid and/or had a bite mark on the ventral idiosoma near the coxal base (Fig. 2D). This mark was probably caused by exudation of the dark body contents; a small amount of liquid material similar in color to body contents was usually found in Petri dishes containing dead ticks. Two female and one male adult ticks maintained their body contents; however, video recordings showed pseudoscorpions exhibiting feeding behavior on two of these, and the third had a bite mark on the ventral idiosoma near coxa I. All pseudoscorpions consumed living ticks, except for two adult females: one adult female died after 3 weeks without preying on an adult female tick, and the other died the day that an adult male tick was provided (Table 1). Numbers of larval ticks preyed on by adult female and male pseudoscorpions on the first day were not significantly different (F-test, df = 7, p = 0.8796; Student’s t-test, df = 14, p = 0.7522). The longest periods required for an adult female pseudoscorpion to consume five larvae, one nymph, one adult female, and one adult male tick were 11, 1, 13, and 6 days, respectively. The equivalent periods for an adult male pseudoscorpion Tick predation by Megachernes ryugadensis 5

Fig. 1. Morphological terms of the pseudoscorpion Megachernes ryugadensis. Scale = 1 mm. were 5, 14, 8, and 3 days, respectively. The number of days required to consume all larval ticks was also not significantly different between sexes (F-test, df = 7, p = 0.01969; Welch’s t-test, df = 8.9515, p = 0.5195). The number of days required to consume a nymphal tick did not differ significantly between sexes, although one male took 14 days to feed on a nymph (F-test, df = 4, p = 0.003367; Welch’s t-test, df = 4.1956, p = 0.404). The number of days required to consume an adult female tick differed significantly between pseudoscorpion sexes (F-test, df = 4, p = 0.468; Student’s t-test, df = 8, p = 0.03895), whereas the time required to consume an adult male tick did not (F-test, df = 4, p = 0.676; Student’s t-test, df = 8, p = 0.8798). Tritonymphal pseudoscorpions also consumed larval and nymphal ticks within a few days after ticks were transferred to the Petri dish, although the sample sizes were small (Table 1). Although we did not observe predation directly, one dead nymphal tick had lost its entire body contents within 24 h of being transferred to a Petri dish with a male pseudoscorpion. One dead nymphal and three dead larval ticks that had initially been placed on the bottom of the Petri dish 6 Kimiko OKABE et al.

Fig. 2. Dead ticks consumed or not consumed by M. ryugadensis. A: Tick larva (Haemophysalis sp.) without body contents after predation by an adult female pseudoscorpion on the left, without predation on the right; B: tick nymph (H. megaspinosa) without body contents after predation by an adult female pseudoscorpion on the left, without predation on the right; C: adult male tick (H. megaspinosa) without body contents after predation by an adult male pseudoscorpion on the left, without predation on the right; D: injury sites on the ventral side of an adult tick idiosoma (H. megaspinosa). Dark areas indicated by arrowheads are injury sites. Scale = 1 mm. were moved to the dish wall within 24 h by pseudoscorpions; however, their body contents remained. Therefore, it was unclear whether these four ticks had been preyed upon by the pseudoscorpions. Adult male pseudoscorpions also caught and fed on nymphal ticks with deer blood soon after the ticks were transferred, and probably preyed on female ticks containing deer blood within 24 h. In some cases, we observed that males attacked a smaller female tick but not others. However, because a female containing deer blood that had been walking around energetically in the dish was found lying dead on its back within 24 h, we judged that the pseudoscorpion had killed it. The sizes of ticks fed deer blood were not significantly reduced. and no deer blood appeared around the dead ticks after feeding by pseudoscorpions. The predation behavior of M. ryugadensis was very similar to that of Chelifer species (Cheliferidae) as described by Weygoldt (1969). The pseudoscorpions typically stayed under a piece of wet peat moss in the Petri dish until a tick larva was caught using the palpal chela, by extending a pedipalpus toward the prey (Supplementary Material (SM) 1). We observed predatory activities several times under the stereomicroscope. One adult female caught a larval tick by a palpal chela, brought it closer to the chelicera using either or both pedipalpi, held the tick for some time, and then started to feed, probably by vigorous movement of the upper and lower lips (SM 1). On another occasion, a male pseudoscorpion held an adult male tick and appeared to look for a biting site. Approximately 5 min after catching the tick, the Tick predation by Megachernes ryugadensis 7

pseudoscorpion stuck the fixed finger of the chelicerae into the tick and then sucked out the body ) fluid of the tick, perhaps mixed with secreted digestive juices (SM 2). It took 43 min for the adult female pseudoscorpion to catch, feed on, and release a tick larva, and about 2 min to begin searching for a biting site after catching it. The tick moved its legs for at least 30 min after the feeding started. Within

Megachernes ryugadensis about 10 min, the tick idiosoma became transparent, except for the scutum, probably because the body contents had been removed. In another case, a female pseudoscorpion likely sucked body fluid from a larval tick for about 15 min and then moved away, leaving the tick with its body contents still remaining. However, because the tick was transparent within 24 h, we concluded that the pseudoscorpion had returned to feed on the tick. The predatory behavior of the pseudoscorpions varied from case to case. Some caught a larval tick with the palpal chela soon after it was placed nearby (within 1 min) and begun sucking its body fluid immediately after the capture, but some did not in others) by tritonympal and adult pseudoscorpions ( move their palpal chelae even when ticks approached. Feeding behavior was very similar among adult female, male, and nymphal pseudoscorpions. We directly observed the H. megaspinosa predatory activities of an adult female pseudoscorpion toward a nymphal tick only once, and it was almost identical to that of the larval tick. However, an adult female tick resisted an attack by

spp. in larvae and a female pseudoscorpion for longer than observed in other cases, probably due its larger body size, suggesting that the pseudoscorpion may not be capable of preying on a more powerful adult tick in

Haemaphysalis a single attack (SM 3). Ticks did not avoid encounters with pseudoscorpions in the dish. We sometimes observed a tick walking on the surface of a

Feeding of ticks ( pseudoscorpion, but the pseudoscorpion did not react by preying on the tick, perhaps due to the limits of pedipalpal locomotion. However, when a

Table 1. Table pseudoscorpion sensed a tick nearby as prey, it 8 Kimiko OKABE et al. usually caught it immediately (SM 1). Although a larval tick did not appear to confront the pseudoscorpion, except for moving its appendages during predation, an adult female tick behaved differently: the tick straddled the bottom of the Petri dish with its appendages, and then tried to escape capture by the palpal chelae of the adult pseudoscorpion, mainly through intense movement of the idiosoma and appendages (SM 2). Larval ticks never successfully escaped predation. Adult female ticks sometimes escaped; however, most of these were eventually killed by the predators (Table 1).

DISCUSSION

Although many predators are listed as natural enemies of ticks and mites, ticks and mites have developed defenses such as a large body size, sclerotized cuticles, and thanatosis against natural enemies during the course of evolution (Walter and Proctor, 1999). Haemaphysalis megaspinosa is a large, hard tick, but it was unable to escape from predation by M. ryugadensis. Given that the sclerotization of mites was not an effective defense against natural enemies, as suspected in oribatids (Walter and Proctor, 1999), it is likely that hard ticks cannot avoid predation by the pseudoscorpion. Adult ticks, especially females, were strong against the pseudoscorpion, defending themselves by straddling with claws on the plastic dish; this behavior sometimes facilitated escape from the predator (SM 3). However, tick larvae, which are as large as the chela of an adult M. ryugadensis, seemed to be the easiest prey to catch, but most adult H. megaspinosa were also eventually preyed upon. Thanatosis may be another defense behavior of the tick; when we disturbed ticks using a fine paintbrush, they stopped their activities and drew in their legs ventrally (Okabe et al., pers. obs.). When we found several living larvae in a Petri dish 24 h after being transferred, most had assembled and attached to the upper surface of the dish in the corner or in the tiny space between the dish bottom and the cover, and did not move at all. We presumed that M. ryugadensis could not find ticks that were standing still based on previous observations that pseudoscorpions do not actively search for prey, but attack those that approach (Weygoldt 1969; Del-Claro and Tizo-Pedroso, 2009). However, because M. ryugadensis appeared to be able to scavenge dead ticks, thanatosis appeared to be an imperfect strategy against predation. The maximum number of ticks that M. ryugadensis is able to prey on remains unknown; however, our results suggest that the pseudoscorpion is capable of controlling tick populations based on its long adult life period of 1 yr or longer, as reported in a number of pseudoscorpions (Weygoldt 1969; Okabe et al., unpublished data). Male pseudoscorpions preyed on female H. megaspinosa faster than did female pseudoscorpions, possibly because the male has massive pedipalpi and much stouter chelae and patellae than the female, as suggested by the observations reported here and those of other Megachernes species such as M. kanneliyensis (Harvey et al., 2012). However, because the longest days required for each sex to consume ticks at different developmental stages appeared to be unrelated to prey body size, more information about M. ryugadensis is required, including its life history traits, to compare the effectiveness as a natural tick predator between the sexes. Ticks appeared to be among their favored prey, as most reacted quickly during encounters with ticks at any stage including fed ticks. We did not test M. ryugadensis predation behavior in mouse nests, but suspect that it would be possible based on Tick predation by Megachernes ryugadensis 9 their capacity to prey on acarids, as observed under rearing conditions in small wood chips (Okabe et al., unpublished data). For nesting animals, small nidicolous predators such as M. ryugadensis are expected to play a beneficial role by preying on harmful or nuisance organisms, such as fleas or mites, as suspected in other pseudoscorpions (Hoff and Clawson, 1952; Francke and Vallegas-Guzmán, 2006). Rodents are common hosts, and it is therefore likely that numerous ticks, especially juveniles, inhabit mouse nests (Oliver, 1989). Most rodents rarely prey on engorged ticks, and preying on actively moving, unfed ticks is difficult for them (Samish and Rehacek, 1999). Instead, they sometimes exploit other organisms for this purpose; some rabbits are able to avoid ticks by living closer to particular ants that secrete tick-repellent body fluid (Samish and Alekseev, 2001). In our preliminary observations, A. speciosus exhibited no interest in pseudoscorpions introduced into its rearing cages (Okabe and Shimada, pers. obs.), although mice typically prey on insects and/or other invertebrates in the wild (Mizushima and Yamada, 1974; Tachibana et al., 1988). These observations, combined with our present results, may suggest that M. ryugadensis is not merely a commensal but can be a mutualist for the rodent in that it depends on the host for food (small animals inhabiting rodent nests) and migration, and benefits as a natural enemy of harmful animals, e.g., ticks. To better understand the role of pseudoscorpions as natural enemies for tick control beneficial to wild animals, further studies are necessary to determine the life history traits of both ticks and pseudoscorpions, impacts of ticks on rodents with and without pseudoscorpions, and the fauna of their potential prey including ticks in rodent nests.

ACKNOWLEDGEMENTS

This study was supported by Japan Society for the Promotion of Science (JSPS) KAKENHI grants (nos. 17H00807 and 16K07794).

REFERENCES

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摘要日本産小型哺乳類と共生するオオヤドリカニムシ（カニムシ目：ヤドリカニムシ科）によるマダニの捕食岡部貴美子・牧野俊一（森林総研）・島田卓哉（森林総研・東北）・古川拓哉・飯島勇人・ Tick predation by Megachernes ryugadensis 11

亘悠哉（森林総研）マダニ類は様々な脊椎動物の寄生者で、重要な害虫でもある吸血生物である．化学防除に対する懸念から，生物防除によるマダニ個体群およびマダニ媒介疾患拡大の制御への期待が高まっている．本研究では，実験室内でオオヤドリカニムシ（Megachernes ryugadensis）によるマダニの捕食を初めて観察した．アカネズミ類に便乗しているカニムシ成虫および第三若虫を採集し，シャーレ内で実験した．これらのカニムシはチマダニ属の幼虫，オオトゲチマダニ若虫および雌雄成虫を捕食した．カニムシは概ね，幼虫を与えられた最初の一日間に，2， 3 頭を捕食した．カニムシ成虫の雌雄間で，初日の捕食数および与えられた幼虫を食べ尽くすまでの日数には差がなかった．またマダニの若虫，雄成虫の捕食に費やす日数に差はなかったが，カニムシ雄成虫は雌成虫よりも短期間でマダニ雌成虫を捕食した．供試数は少ないが，カニムシ第三若虫もマダニ幼虫および若虫捕食において同様の傾向を示した．オオヤドリカニムシのマダニ天敵としての評価のためには，マダニとカニムシの生活史特性，小型げっ歯類および巣内の生物相への影響に関する更なる研究が必要である．