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Sound production in the aquatic isopod Cymodoce japonica (Crustacea: Peracarida).

Abstract. A vast variety of acoustic behaviors and mechanisms occur in arthropods. Sound production, in particular, in insects and decapod crustaceans has been well documented. However, except for a brief, anecdotal statement, there has been no report on the acoustic behavior of aquatic isopods. We present the first empirical evidence in aquatic Isopoda that males of Cymodoce japonica produce sound by stridulation, or the rubbing together of body parts. Sound production was associated with tail-lifting behavior, suggesting that stridulation occurs on thoracic and/or abdominal somites. Acoustic analysis revealed that syllable length was similar throughout the stridulation, at a mode of 2500-3000 Hz. With a scanning electron microscope, we identified file-like structures on the inner surface of the dorsal exoskeleton. Each file consisted of 188 [+ or -] 11.1 ridges at about 0.5 [micro]m intervals; the theoretical frequency (number of ridges per syllable length) was estimated to be 2208-3646 Hz. This finding suggests that the stridulation sounds arose from these structures. Laboratory observations show that stridulation may play a role in the threatening of other males in the context of territorial and/or reproductive competitions.

Introduction

Arthropods have evolved a vast variety of acoustic behaviors and mechanisms as communication tools (Dumortier, 1963; Alexander, 1967). Vibrational communication has been observed in many arthropods, especially in terrestrial and semi-terrestrial species such as insects, spiders, and decapod crustaceans (Dumortier, 1963; Alexander, 1967; Popper et al., 2001; Virant-Doberlet and Cokl, 2004). The species of 16 orders of insects produce sound or substratum-borne vibration (Dumortier, 1963; Alexander, 1967; Virant-Doberlet and Cokl, 2004).

In arthropods, various sound-producing methods have been developed. Tremulation (whole-body vibration (Virant-Doberlet and Cokl, 2004)) and stridulation (the rubbing together of body parts) are frequently used by insects (Dumortier, 1963; Walker and Carlysle, 1975; Carisio et al., 2004; Virant-Doberlet and Cokl, 2004; Nakano et al., 2008), spiders (Stratton and Uetz, 1983), and decapod crustaceans (Dumortier, 1963; Hazlett, 1966; Abele et al., 1973; Meyer-Rochow and Penrose, 1976; Sandeman and Wilkens, 1982; Popper et al., 2001; Bouwma and Herrnkind, 2009). Percussion by substrate(s) beating (Dumortier, 1963; Horch, 1975; Popper et al., 2001 ; Virant-Doberlet and Cokl, 2004), tymbal (or tymbal-like) systems (Dumortier, 1963), vibration of appendages or wings (Dumortier, 1963; Popper et al., 2001; Jonsson et al., 2011), passage of fluid such as gas or foam (Abele et al., 1973; Fraser and Nelson, 1982), and cavitation bubble collapse in snapping shrimp (Versluis et al., 2000) are also well known.

In terrestrial species, acoustic sound can be the most powerful, useful, and economical signal, delivering information to conspecific individuals and/or other species. Insects use both airborne and solid-borne sound to transmit species-specific signals, which sometimes differ in sex and situation, such as encounters with enemies, competitors, or mating partners. In contrast, acoustic communication by aquatic invertebrates is less common; research on this subject has been limited to particular species. Moreover, underwater environmental noise can disturb signal transmission. Thus, little attention has been paid to acoustic and vibrational signal production by aquatic crustaceans. In fact, some sound detection studies in crayfishes and lobsters showed that these animals could detect particle motion of water-borne, vibrational stimuli occurring only within about 0.9 cm (Popper et al., 2001). Nevertheless, it is well known that a great number of aquatic arthropods exhibit sophisticated social behaviors, suggesting that hitherto unknown communications, regardless of signal type, play a role in social networking in these species. Among the aquatic crustaceans, decapods have been studied most often with regard to acoustic communications. In this order, a large number of species use acoustic communications for aposematism. In spiny lobsters such as Panulirus argus, stridulation occurs during the struggle to escape octopus predation (Bouwma and Herrnkind, 2009). In sponge-dwelling snapping shrimps, such as Synalpheus regalis, which exhibit eusocial structures, acoustic activity (snapping) occurs while they defend their colony from intruders (Duffy, 1996). Sound production is also used for intraspecific communications. An acoustical warning signal directed to conspecific individuals was reported in the Murray River crayfish Euastacus armatus (Sandeman and Wilkens, 1982). Furthermore, at least two genera of semi-terrestrial crabs, Uca and Ocypode, use species-specific acoustical signals for courtship (Popper et al., 2001).

Until our study, the only report on this topic in aquatic isopods was a brief anecdotal statement on sphaeromids (Stridulating crustaceans, 1878). In terrestrial oniscoid isopods, presumable stridulatory apparatus has been reported. Practical stridulatory apparatus and sound production were documented in Armadillo officinalis (Caruso and Costa, 1976). The isopod genus Cymodoce is marine and cosmopolitan in its distribution, and is found in a wide range of habitats, from shallow waters to deep sea. Cymodoce japonica Richardson, 1906 (Richardson, 1906), live in colonies in natural or artificial, narrow-opening cavities such as barnacle shells or slits in plastic containers. Similar habitats with small openings were also reported in other sphaeromatid isopods, including various sponges, the palliai groove of chitones, barnacle shells, and tunnels bored into mangrove roots (Shen, 1929; Glynn, 1968; Thiel, 1999). When we collected C. japonica from shore and stored the animals in a bucket, we heard "creaking" sounds emanating from the bucket. Interestingly, the sound was rapidly repeated and sufficiently audible through water.

We present the first empirical evidence of sound production in the aquatic isopod. On the exoskeletal surface of these animals, we found file-like structures that are most probably the acoustic organs. Our results strongly suggest that males of C. japonica produce sound by stridulation. The social and physiological roles of sound production are also discussed.

Materials and Methods

Animals

Specimens of Cymodoce japonica were collected from the shells of dead barnacles and hanging fishery baskets sunken under the pier near the Oki Marine Biological Station, Dogo (one of the Oki Islands), on the Sea of Japan (36[degrees]10'40" N, 133[degrees]16'38" E). Animals were stored in aquaria with running seawater and were fed with pet crayfish food ("Zarigani-no-esa," Kyorin, Hyogo, Japan). To avoid conspecific predation, empty barnacle shells were placed on the bottoms of the aquaria for shelter. Gender was determined by morphology of the posterior edge of the pleotelson. The pleotelson of the male of C. japonica has two deep slits with three small processes, many tubercles, and setae; the female pleoteleson, in contrast, has shallow slits but no processes or tubercles.

Sound recording and analysis

An electric condenser microphone (ME-15; Olympus, Tokyo, Japan) was embedded in a shell of the barnacle Megabaianus rosa (Pilsbry, 1916) with fluoroplastic waterproof tape and silicone resin bond. The microphone was then placed on the bottom of a 24-cm, round-bottomed plastic container filled with filtered seawater (~10 cm deep). For each experiment, 31 males were placed in this container. The containers held only males. The recordings were conducted at night (approximately 2100-0100) at room temperature (about 13-18 [degrees]C; data provided by the Japan Meteorological Agency) under fluorescent light. Sound was recorded by a Linear PCM recorder (LS-11 ; Olympus) and analyzed with Sonority software (Olympus). The sampling rate of the recorder was 44.1 kHz. A total of 130 syllables and 400 impulses were measured from oscillograms with 0.1 ms and 0.01 ms scales, respectively. The sound-producing behavior was recorded with a video camera (HDRCX630, Sony Corp., Tokyo, Japan) and analyzed with Final Cut Pro V. 5.1.4 software (Apple, Inc., Cupertino, CA).

Scanning electron microscopy

Isopods were euthanized by freezing (4 [degrees]C) and desiccated by refrigeration. Each specimen was treated with 0.1% actinase-E (Kaken Pharmaceutical Co., Tokyo, Japan) in digestion medium (50 mmol [l.sup.-1] NaHC[0.sup.3], pH 9.0) for 22 d at 37 [degrees]C. The remaining undigested specimens (mostly exoskeletons) were rinsed with distilled water, and all pereiopods were removed using forceps. Dissection of samples produced 10 parts each: a cephalon, seven free thoraxes, an abdomen, and a pleotelson; each part was stored separately in 70% ethanol. Specimens were washed with 30 mmol [1.sup.-l] N-2-Hydroxyethylpiperazine-N'-2-ethanesulfonic acid (HEPES; pH 7.0) and fixed with 1% Os[O.sub.4] in 40 mmol [l.sup.-1] HEPES (pH 7.0). Specimens were dehydrated by immersion in a series of ethanol solutions (60%-100%) and 100% tert-Butyl alcohol, placed in a freezer, and desiccated under vacuum. Finally, samples were coated with platinum/palladium for 2 min and analyzed by scanning electron microscopy (Hitachi S-4800, Tokyo, Japan) at 5.0 kV.

Results

Cymodoce japonica may have a polygynous mating system, based on our observations. Males cover the opening of a barnacle shell with their tubercled pleotelson. This position also has been reported as the "protective position" in other species (e.g., Hordich, 1976). The shell was inhabited by about one to seven brooding young females. Females molt inside the shell. Occasionally, we found females in these shell cavities that had laid more than 250 eggs inside their body. The embryos developed directly into juveniles (manka). In laboratory observations, the females died a few days after hatching the juveniles from their bodies, suggesting semelparity. The juveniles remained in the cavity for several days, then left it.

C. japonica exhibits remarkable sexual dimorphism in the size of its adult body and the shape of its pleotelson (Fig. la). Upon field collection of this species, animals were noted to be colonized in a nesting cavity where a single male and multiple females coexisted (Fig. lb). Such a polygynous colony can be formed in aquaria; isolated individuals were observed migrating into a barnacle shell cavity within an hour (Fig. lc), suggesting a strong, inherent ability to form nesting habitats. However, the coexistence of two adult males in the same cavity was seldom seen in the laboratory setting or in natural habitats. This finding suggests that males are territorial. When two males came into close contact around a nesting site (e.g., a barnacle shell), we often heard a series of creaking sounds (Supplemental video 1, http://www.biolbull.org/content/supplemental). Motion analysis of the time-resolved video recording revealed that high amplitude impulses were emitted when a male lifted its pleotelson slightly upwards (see Fig. 1d, 5th, 10th, and 15th arrows). Amplitude then lessened when the pleotelson was fully lifted (Fig. 1d, 6th, 12th, and 16th arrows). This action suggests that sound production occurred by rubbing the narrow posterior edges of the somite exoskeleton against the anterior edges of the other somite exoskeleton. The sound was often repeated. This sound-producing behavior was observed only in males. During our experimental periods (about 10 mo), we never heard sounds from the females of C. japonica. To confirm our observations, we forced stridulation in all study animals by bending the posterior somite to the dorsal side. Sound was produced in males but not in females, supporting our findings.

Audio analysis revealed that a single "creak" sound (defined as one syllable) was composed of approximately two dozen impulses; each impulse could be divided into several cycles (Fig. le). Statistical analysis of impulse frequency (Fig. 1f) and syllable length (Fig. lg) among sound-producing males identified a unimodal distribution with a mode of 2500-3000 Hz (frequency, n = 400) and 70 ms (syllable length, n = 130), respectively, suggesting the presence of organ(s) suitable for producing sound with a particular frequency range.

We next examined potential sound-producing organ(s) in the posterior region of the body (pereon and pleon). Each segment of the exoskeleton, devoid of connecting tissue by protease digestion, underwent scanning electron microscopy (Fig. 2a, b). We identified file-like structures (448 [+ or -] 33.6 [micro]m in diameter, n = 10) on the inner surface of each thoracic exoskeleton. These structures were distributed similarly on the seven free thoraxes in both sexes, as illustrated in Figure 2c. The width of each ridge was about 2-4 [micro]m for males and 1 [micro]m for females. The ridge interval was 0.5 [micro]m in both sexes. Each file consisted of 188 [+ or -] 11.1 ridges for males (n = 10) and 135 [+ or -] 3.0 for females (n = 14), and was always aligned perpendicularly to the anterior-posterior (A-P) axis. The theoretical frequency for males, obtained by calculation of the number of ridges divided by the average syllable length, was in the 2208-3646 Hz range, which suggests that stridulation was produced by the rubbing of these structures. The length of the file-like structure (along the A-P axis) and the number of ridges in each free thorax are shown in Table 1.

Discussion

In this study, we found that males of Cymodoce japonica stridulated. No such sound was witnessed in females of C. japonica. Sound production occurred when males lifted their telson upwards (bending toward the dorsal side). Theoretical frequency, calculated from the number of ridges and the average syllable length, was in good agreement with the actual sound produced by males. In decapod crustaceans, the frequencies of stridulation generally range from several hundreds to over ten thousand hertz (300 Hz~12 kHz (Meyer-Rochow and Penrose, 1976; Sandeman and Wilkens, 1982; Popper et al., 2001)). In C. japonica, the mode value of the frequency distribution (2600 Hz) and the average number of ridges (183) are within the ranges of other crustaceans. Frequency of stridulatory sound by "one directed" scraping motion on aligned file rides depends on the number of ridges and speed of scraping motion; that is, beating time per ridge is one cycle. In crickets, stridulation frequency depends on the number of teeth on each file and wing-closure speed (Walker and Carlysle, 1975), which provided the rationale for frequency estimation calculated from the number of ridges per file and the syllable length in C. japonica. However, our study failed to identify any scraper-like structure on the opposing surfaces of the files. To determine the counterpart of the file, careful preparation, such as microdissection without protease digestion or tomography scanning, is needed.

Furthermore, file-like areas were present in males and in females, even though females produced no sound during our experiments. These issues need to be clarified in future studies.

Stridulation in C. japonica may be an agonistic warning signal. Males of C. japonica often stridulate when they are pinched by human fingers, or when other individuals crawl on their back. Furthermore, our preliminary observation suggests that males, when coexisting with other males, often stridulate repeatedly in the vicinity of the nesting cavity (a barnacle shell). Some marine decapod crustaceans are known to use repeated signals as a way to advertise the quality of the sender during intraspecific contests (Briffa et al., 2003). In sphaeromatid isopods, similar repeated tail-lifting behavior was considered social behavior. For example, males of Paracerceis sculpta exhibit "telson shaking" as a consequence of courtship (Shuster, 1990).

In terrestrial isopod species, Armadillo officinalis stridulates by rubbing some epimera and pereiopods together (Caruso and Costa, 1976). The posture consists of completely or partially rolling up to the ventral side. In contrast, males of C. japonica stridulate by rubbing terga of somites while bracing themselves against the substrate and lifting their pleotelson to the dorsal side. In addition, most males of aquatic isopods engage in mate guarding, unlike many terrestrial isopods. It is likely that stridulation of male C. japonica functions as a form of threatening competitive male intruders or predators at the entrance of the narrow nesting cavity. Zimmer (2001) suggested that male precopulatory guarding in isopods has disappeared as a consequence of the evolutionary loss of the temporal-restricted female receptivity cycle, which was limited by cycle(s) of parturial molting during adaptation from aquatic to terrestrial habitats. At least, in the case of A. officinalis, it would be difficult physically to produce sound while guarding a female beneath them (ventral side). However, in C. japonica, mate guarding does not interfere with sound production. Thus, we suggest that the physiological role of sound production is related to precopulatory mate guarding in C. japonica.

For many years, there has been intensive study of the acoustical behaviors of marine vertebrates, such as whales, dolphins, and fishes (Nakazato and Takemura, 1987; Ryabov, 2011; Herman et al., 2013). Surprisingly, there have been only a few descriptions, and little discussion, of the role of acoustical behaviors in small invertebrates, such as crustaceans, that live in shallow waters.

In this study, we recorded, for the first time, acoustical behavior in aquatic isopod crustaceans. Because aquatic isopods all have a similar body plan, stridulation may be a common strategy for communication in some other species. Given that this group is highly diversified and their social behaviors remain largely unknown, cryptic acoustic behaviors in other marine isopods await discovery.

Acknowledgments

We thank Drs. Kohzoh Ohtsu, Akira Asakura, Keiichi Kakui, Noboru Nunomura, Ryuzo Yanagimachi, and Eiji Fujiwara for their technical support. This study was supported by Shimane University, which has provided research funds to two authors (IH and HN).

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TAKERU NAKAMACHI (1,2,*[dagger]), HIDEKI ISHIDA (2), AND NORITAKA HIROHASHI (1)

(1) Oki Marine Biological Station, Shimane University, 194 Kamo, Okinoshima-cho, Oki, Shimane 685-0024, Japan; and (2) Department of Biological Sciences, Shimane University, 1060 Nishikawatsu, Matsue, Shimane 690-8504, Japan

Received 21 April 2015; accepted 3 September 2015.

(*) To whom correspondence should be addressed. E-mail: nakamachi.takeru.83c@st.kyoto-u.ac.jp

([dagger]) Current address: Seto Marine Biological Laboratory, Kyoto University, 459 Shirahama, Nishimuro, Wakayama, 649-2211 Japan

Table 1

Structural indexes of file-like patches and theoretical frequencies

                      File length                  Theoretical
                      (A-P axis,                   Frequency
                      [micro]m)      Ridges (n)    (Hz)
Free
thorax  Localization  Male   Female  Male  Female  Male

1st     LC            ND     234.0   ND    123     ND
        RC            ND     229.5   ND    115     ND
2nd     LC            381.1  274.9   162   137     2314
        RC            ND     261.8   ND    137     ND
3rd     LC            399.9  273.6   170   157     2428
        RC            386.9  250.0   164   138     2349
4th     LC            ND     246.7   ND    130     ND
        RC            386.4  241.0   155   133     2208
5th     LC            388.3  248.1   194   130     2773
        RC            403.8  244.3   172   134     2452
6th     LC            410.7  240.1   175   138     2493
        RC            430.2  228.3   183   120     2612
7th     LC            638.0  269.8   255   142     3646
        RC            658.1  288.2   247   151     3525
Mean                  448    252     188   135     2680
SE                     33.6    5.0    11.1   3.0    159.1
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Author:Nakamachi, Takeru; Ishida, Hideki; Hirohashi, Noritaka
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Date:Oct 1, 2015
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