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Sound production in the coconut crab, the largest terrestrial crustacean
Zoology 137 (2019) 125710
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Sound production in the coconut crab, the largest terrestrial crustacean Shin-ichiro Oka ⁎, Nozomi Kobayashi , Taku Sato , Keiichi Ueda , Maki Yamagishi a,
a
b
a
T
c
a
Okinawa Churashima Foundation, 888 Ishikawa, Motobu-cho, Okinawa, 905-0206, Japan Research Center for Marine Invertebrates, National Research Institute of Fisheries and Environment of Inland Sea, Japan Fisheries Research and Education Agency, Momoshima, Onomichi, Hiroshima, 722-0061, Japan c Conservation & Animal Welfare Trust Okinawa, 308-7 Maehara, Uruma-shi, Okinawa, 904-2235, Japan b
A R T I C LE I N FO
A B S T R A C T
Keywords: robber crab acoustic communication scaphognathite tapping sound
Sound production in terrestrial crustaceans, including the coconut crab, Birgus latro, is not fully understood. Here, we present the first description of the acoustic features and sound production mechanisms of coconut crabs. The sound production system was determined based on X-ray videography and anatomical observations. The results indicated that the crabs produced a tapping sound by beating the scaphognathite, which is also used for ventilation, in the efferent branchial channel. The frequencies of the produced sounds were diverse, and the sound interval also varied within the same individual. From observations under captivity, differences in the sounds were confirmed at each mating phase. Although the relationship between the sounds and actions was not clarified in this study, it is probable that the crabs deliberately produce various types of sounds for different occasions. The coconut crab is known to use visual and chemical communication mechanisms, but these results suggest that a diverse set of sounds is an additional communication pathway during agonistic and mating interactions.
1. Introduction Sound production has been reported in several aquatic crustaceans, which have evolved various sound production mechanisms, including stridulation (Salmon, 1967; Boon et al., 2009), carapace vibrations (Henninger and Watson, 2005; Patek and Caldwell, 2006), stick and slip friction (Patek, 2001; Patek and Baio, 2007; Patek et al., 2009), snaps (Knowlton and Moulton, 1963), and bubble emissions (Crane, 1966). Acoustic signals may be produced in a variety of contexts such as defense against predators (Patek, 2001; Patek and Baio, 2007; Patek et al., 2009), courtship (Salmon, 1965; Crane, 1966; Takeshita and Murai, 2016), and agonistic encounters (Patek and Caldwell, 2006; Boon et al., 2009). In addition to the aforementioned acoustic behaviors of aquatic crustaceans, there is some evidence of acoustic signals in terrestrial crustaceans. Some intertidal crabs are known to use sound communication associated with breeding behaviors (Davie et al., 2015; Takeshita and Murai, 2016), but little is known about sound communication in crustaceans in inland areas other than in the intertidal zone. Some terrestrial hermit crabs are known to produce sounds, but the sound production mechanism has only been determined in Coenobita purpureus (Imafuku and Ikeda, 1990). This species produces sound by tapping or rubbing the uropod against the inner surface of the shell, but the function of this sound, which is not related to mating behavior,
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remains unclear (Imafuku and Ikeda, 1990). Since sound transmission differs between aquatic and terrestrial environments, the significance and function of sound production in terrestrial crustaceans may differ from that of aquatic crustaceans. As mentioned above, only a few studies have examined sound production in terrestrial crustaceans, and additional studies are needed to determine the significance and function of acoustic communication in terrestrial crustaceans. The coconut crab, Birgus latro, is the largest terrestrial crustacean, and it is widely distributed in the tropical Indo-Pacific area (Drew et al., 2010). Abundant ecological data have been collected to develop appropriate management strategies designed to protect this endangered species. Coconut crabs can weigh up to 4 kg, and the lifespan is up to 60 years (Drew et al., 2010). The larger size of males compared to females is important for their breeding success (Sato and Yoseda, 2010; Sato et al., 2010). Coconut crabs are thought to communicate with each other using visual and chemical substances for agonistic and aggregating behaviors (Helfman, 1977a; Hansson et al., 2011). However, details regarding intra-specific communication in the species have not been reported. Through our previous experiments in the field and with captive coconut crabs, in which we examined life history characteristics (e.g., Sato and Yoseda, 2010; Oka et al., 2015), we found that coconut crabs generate tapping-like sounds. Therefore, we hypothesized that coconut crabs may use these sounds for communication between
Corresponding author. E-mail address: [email protected] (S.-i. Oka).
https://doi.org/10.1016/j.zool.2019.125710 Received 4 February 2019; Received in revised form 13 August 2019; Accepted 12 September 2019 Available online 18 September 2019 0944-2006/ © 2019 Elsevier GmbH. All rights reserved.
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individuals. As a first step to test this hypothesis, in the present study, we aimed to determine how coconut crabs generate sound.
sound element (duration); pulse rate per second (sound frequency); silence in the interval before sound production (interval); frequency at maximum amplitude (peak frequency); first harmonic of a sound element (fundamental frequency); lowest frequency, where the amplitude is first detected below the threshold (minimum frequency); and the highest frequency, where the amplitude is first detected below the threshold (maximum frequency).
2. Materials and Methods 2.1. Determining the sound production system To detect moving organs during sound production, we attempted to nondestructively observe the internal structure of two living coconut crabs. The thoracic lengths (ThL) of the two crabs were 30.7 mm and 59.1 mm in the female and male, respectively. The lateral side of the crab was held by hand while the crab was photographed using an X-ray fluoroscopy system (Rotanode DRX-61A, Toshiba Corporation) with a digital movie recorder. Although the noise created by the X-ray fluoroscopy device made it impossible to record sounds with a movie recording, it had been confirmed by observation that the coconut crab had been making tapping sounds throughout the recording. The X-ray movie (720 p, 59 fps) was filmed for a total of 13 min (male: 10.5 min; female: 2.5 min); from this, a total of 5 min (male: 4 min; female: 1 min) in which moving organs during sound production were clearly detected was used for the analysis. Tapping sound frequency (taps/ second) made by the scaphognathite, which was the only organ with internal movement, were calculated from the duration of 10 tappings of the scaphognathite observed from the X-ray movies. The scaphognathite is a thin leaflike appendage of the second maxilla of decapod crustaceans. It usually serves as a pumping organ to draw water and air though the gill cavity, which is also its function in coconut crabs (Cameron and Mecklenburg, 2010). Tapping sound frequency measurements were made using 70 randomly chosen scenes from the recorded movies. Two registered and preserved (10% formalin) specimens that were deposited in the Okinawa Churashima Foundation (OCF-Cr00052, 33.6 mm ThL, male; OCF-Cr00053, 30.5 mm ThL, female) were dissected. The lateral side of cephalothorax was determined to be the anatomical observation area, based on the results of the X-ray movie analysis.
2.3. Consideration of animal welfare Although the Guide for Care and Use of Laboratory Animals of Okinawa Churashima Foundation outlines procedures for animal experiments, they are waived for crustaceans. Therefore, we considered crab welfare and maintained the specimens as described below. All living crabs used in the present study were captured at the Ocean Expo Park (26°41′N, 127°52′E), and were returned to their original areas immediately after the conclusion of the experiments. We also confirmed that released crabs (even those under captive conditions for several years) exhibited normal growth based on data from our previous studies (Oka et al., 2013, 2015). A previous study examined crayfish and found that the anatomical method of sound producing organ removal effectively identified the sound production mechanism (Favaro et al., 2011). However, the coconut crab is an endangered species that requires decades of individual growth, so this experiment was avoided to protect living crabs. 3. Results 3.1. Observations of X-ray movies and analysis of anatomy data X-ray movie analysis and anatomical observation were performed for one crab per sex. X-ray movie analysis indicated that the right and left scaphognathites were only tapped vertically in the efferent branchial channel (EBC) during sound production (Movie S1 in the supplementary online Appendix); this movement was clear in a lateral view, although it was unclear in a dorsal view. The tapping frequency was 1.8–6.2 taps/s, but there was no significant difference in the tapping frequency between females (n = 18) and males (n = 52) (Mann Whitney U-test, z = 1.44, p = 0.15). The results of the anatomical observations confirmed the results of the X-ray analysis in that scaphognathites were found in the EBC (Fig. 1A). Although the scaphognathite was flat and soft, the hard and slender plate was only found on the dorsal side of the scaphognathite (Fig. 1B). In addition, the scaphognathite was confirmed to move only vertically from the center of the base (Fig. 1A). The hard organ consisted of three hard panel units (HPU), which were found on the dorsal edge of the EBC (Fig. 1C). The hard plate on the dorsal side of the scaphognathite contacted the HPU when the scaphognathite was moved. The study of one specimen per sex did not reveal any obvious differences between male and female specimens.
2.2. Sound recording and analysis Recordings of coconut crab sounds were made using a digital audio recording device (linear PCM recorder; SONY PCM-D100) with a builtin microphone, which had a flat frequency response from 100 to 1400 Hz, under the following two conditions: Exp 1: Recordings of coconut crab sounds were conducted while the crabs were secured by their legs, holding the crab at a position approximately 100 mm apart from the fixed recording device in a room; Exp 2: Recordings of coconut crab sounds were conducted during mating of one pair of crabs (52.5 mm ThL, male; 33.7 mm ThL, female) in a soundproof box (0.9 m × 0.6 m × 0.6 m) where the floor was covered with a rubber mat for absorbing the sound of crab legs tapping as it moves. In Exp 1, two males and four females were recorded for approximately 180 s each. In Exp 2, the recording device was installed on top of the soundproof box, and sound recordings were continuously collected inside the box overnight. Furthermore, time lapse photographs (every 5 s) of the crabs in the box were taken using a digital camera (GoPro HERO 3+). The time series of the recorded sounds and the time lapse photography data were synchronized based on the logged time for both the sounds produced and mating behaviors. Mating success was confirmed using time lapse photographs and from adhesion of a spermatophore mass to the abdomen of the female. The sampling rate for all recordings was 44.1 kHz, 16 bit, and background noises were filtered out using the Noise Reject application function Audacity version 2.2.2 for sound analysis. Data were analyzed using the sound analysis software AvisoftSAS Lab Pro version 5.2.10, and the following parameters were measured for each coconut crab sound using the Automatic Parameter Measurements application function of the software: the duration of a
3.2. Acoustic analysis In Exp 1, we recorded the sounds from two males and four females, and we confirmed tapping sounds from every individual (Table 1, Fig. 2, Movie S2). One of the sounds is indicated in Fig. 2A-C. Fig. 2A represents a sonogram of tapping sounds and Fig. 2B, oscillogram, is coincided with the sonogram in which the short pulses with large amplitude vibration are synchronized with the tapping sounds in the sonogram (Fig. 2A, B). The six parameters (duration, intervals, peak frequency, fundamental frequency, minimum frequency, and maximum frequency) and standard deviations for the mean values of each sound parameter varied between different individuals and within the same individuals at different times (Table 1, Figs. 2–4). For example, the sound durations for the six individuals ranged between 5–40 ms, and the tapping frequency was 5–14 taps/s. The sounds were structured 2
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Fig. 1. Anatomical photographs of the coconut crab airway system (specimen number: OCF-Cr00052). A: Left side view of the partially dissected specimen. B: (1) Dorsal and (2) ventral side view of the excised left scaphognathite. C: Ventral side view of the efferent branchial channel (EBC). Solid and white dashed lines indicate the hard plate on the dorsal side of the scaphognathite and the outline of the scaphognathite, respectively. Green arrow indicates the direction of the movement of the scaphognathite. HPU: hard plate unit in EBC.
was recorded in the same condition. In Exp 2, the mating behavior was recognized only once, as follows. Phase 1: the crabs faced each other for approximately 17 min. Phase 2: the male held the female’s claws, and then pushed the female in the male’s direction; the male climbed onto the female, and both abdomens were in contact for 2 min. Phase 3: the male released the female, and
with sound elements that were lower than 18 kHz, and it ranged from 450 Hz to 17140 Hz. The fundamental frequency was distributed between 860–9560 Hz, and sound intervals varied within the same individual (Fig. 3, Movie S2). Although there were potential effects of reverberation on the sounds recorded in Exp 1, there were differences confirmed within the sound features emitted by each individual which
Table 1 Data and results of sound analyses for the six experimental individuals in Exp 1. Parameters with asterisks are the mean value and the standard deviation ( ± ) for a total of 30 sound samples for each individual. No.
Sex
Thoracic length (mm)
Duration* (ms)
Interval* (ms)
Sound Freq.* (Hz)
Peak Freq.* (Hz)
Fundamental Freq.* (Hz)
Minimum Freq.* (Hz)
Maximum Freq.* (Hz)
1 2 3 4 5 6
male male female female female female
63.3 46.5 33.7 27.8 24.1 23.8
8 ± 5 6 ± 3 9 ± 7 7 ± 5 6 ± 3 10 ± 8
115 ± 38 183 ± 90 184 ± 47 135 ± 85 80 ± 31 81 ± 46
9.3 ± 0.5 5.5 ± 0.8 5.5 ± 0.5 9.0 ± 0.6 14.3 ± 1.0 12.2 ± 1.5
1986 1799 5711 3226 2621 3041
1959 1801 5740 3051 2590 3128
619 ± 123 766 ± 135 2482 ± 485 1386 ± 406 1219 ± 199 745 ± 138
8989 ± 2403 5483 ± 1946 10827 ± 2199 6962 ± 3452 6504 ± 2774 11512 ± 2160
3
± ± ± ± ± ±
379 259 2214 368 620 280
± ± ± ± ± ±
341 258 2524 588 655 255
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Fig. 4. Figures A, B, and C are examples of sounds recorded in Exp 2. A: The sound was recorded when the male and female stopped to face each other while 10 cm apart. B: The sound was recorded when the male climbed on the female for mating. C: The sound was recorded when the female separated and moved away from the male after mating. We were unable to distinguish which individuals emitted sounds during Exp 2.
Fig. 2. Example of the tapping sounds of coconut crabs. Figure shows the sounds of a female coconut crab (Individual #5 in Table 1) recorded in Exp 1 (A: sonogram, B: oscillogram, C: power spectrum). The square in A indicates the sound of the coconut crab, and the arrow indicates a sound interval.
fundamental frequency and sound intervals were 3718 (SD = 1541) Hz and 89 (SD = 25) ms, respectively. Sound C (Fig. 4C, Movie S2 in the supplementary online Appendix) was observed after mating behavior was observed when the female separated and moved away from the male (Phase 3). Mean values for the fundamental frequency and the sound intervals were 2549 (SD = 257) Hz and 182 (SD = 43) ms, respectively. Although we were unable to distinguish which individual emitted Sounds A, B, and C, we can affirm that both crabs did not simultaneously emit sounds. 4. Discussion In this study, although X-ray video analysis and anatomical observation were performed for only one crab per sex, we were able to obtain some evidence about the sound production system of the coconut crab. Only the scaphognathite moved during sound production, and no other movements were confirmed that could have produced the sounds. Moreover, the range of beating movement frequencies was confirmed in the X-ray movies, and the tapping sound obtained in the actual sound recording overlapped with that of the organ movements recorded in the X-ray movies. Therefore, the tapping sound was generated by striking the hard plate of the scaphognathite against the hard panel unit (HPU) on the roof of EBC, thus providing a mechanism by which a soft scaphognathite could efficiently generate sound. The soft scaphognathite may also serve as a cushion to prevent an excessive abrasion of the two hard plates. Coconut crab lungs are ventilated by the scaphognathite, which draws air forward through the lung (Cameron and Mecklenburg, 1973; Greenaway et al., 1988), and ventilation could reach over 1 L/min by increasing the frequency of scaphognathite beating (Cameron and Mecklenburg, 1973). The highest estimated scaphognathite beating rate associated with ventilation reached about 5.8–6.7 cycles/s based on a study of coconut crab air ventilation (Cameron and Mecklenburg, 1973). These ranges overlapped with both the frequency observed during the X-ray and tapping sound recordings, thus indicating that scaphognathite beating is associated with sound production. Therefore, it is possible that the
Fig. 3. Example of tapping sounds performed by a male (Individual #2 in Table 1) that was observed in Exp 1. A: Pulse rate was 11 taps in 3 s; the mean interval value was 299 (SD = 73) ms; and values for points a, b, and c were 412, 220, and 272 ms, respectively. B: Pulse rate was 17 taps in 3 s; the mean interval value was 176 (SD = 22) ms; and values for points d, e, and f were 162, 142, and 179 ms, respectively.
the crabs went in opposite directions. After that, the crabs did not have any other contact until the end of the experiment. Several tapping sound patterns were observed during Exp 2 (Fig. 4, Movie S2 in the supplementary online Appendix). Sound A (Fig. 4A, Movie S2 in the supplementary online Appendix) was observed when the experimental individuals (a male and a female) faced each other approximately 10 cm apart in an experimental box before the mating behavior was observed (Phase 1). Mean values for the fundamental frequency and the sound intervals were 2357 (SD = 139) Hz and 104 (SD = 37) ms, respectively. Sound B (Fig. 4B, Movie S2 in the supplementary online Appendix) was observed when the male climbed on the female when exhibiting mating behavior (Phase 2). Mean values for the 4
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Okinawa Churaumi Aquarium.
scaphognathite has two functions: ventilation and sound production. Our results, however, did not clearly refute the possibility of the sounds being produced with the changes in the ventilation frequency or strength in the situation of breeding and/or of facing an enemy, so additional studies and analyses are essential to clarify the nature of the tapping sound. A similar sound-producing mechanism using scaphognathite beating was reported in aquatic crayfish (Procambarus clarkii) via an anatomical approach (Favaro et al., 2011). The present study is the second to experimentally demonstrate the role of scaphognathite movement in crustacean sound production, and it represents the first reported case in terrestrial crustaceans. The results of the present study suggest that both male and female coconut crabs can produce various sounds (Figs. 3 and 4, Table 1), and this was also supported by the movement of scaphognathites at various speeds based on X-ray movies. Why do the crabs need to produce various sounds? Although the acoustic signals of aquatic crustaceans were thought to be used for defense against predators, courtship, and agonistic encounters (Salmon, 1965; Crane, 1966; Patek, 2001; Patek and Caldwell, 2006; Patek and Baio, 2007; Boon et al., 2009; Patek et al., 2009), the significance of sound production in terrestrial crustaceans was not clarified, with the exception of some intertidal crabs that produced vibration signals to induce mating (Davie et al., 2015; Takeshita and Murai, 2016). In the present study, the various sounds were confirmed at a fixed state and during mating (Figs. 2 and 3, Table 1). The mating behavior observed in Exp 2 was considered to be normal, because the sequence of behaviors was similar to that observed in a previous study (Helfman, 1977b, Hicks et al., 1990). Regarding sound production during mating, although both crabs did not simultaneously produce sounds, it was not possible to distinguish which crab (male or female) made each sound. However, we found that the fundamental frequency and sound intervals changed during each mating phase (Fig. 4, Movie S2 in the supplementary online Appendix), which suggests the existence of communication using sound during their mating behavior. To clarify the significance and effects of these sounds, additional experiments (e.g., sound analyses under different conditions) are needed, especially those aiming at the identification of specific male and female sounds. The results of this study suggest that coconut crabs may communicate using sound. However, it is undeniable that sound production using the ventilation system may be related to other functions. Crustaceans are known to have various chemical communications for mating, aggregation, and agonistic actions (Sato and Goshima, 2007; Breithhaupt, 2011). In aquatic lobsters and crayfish, urine is diffused for chemical communication using the ventilation system (Aggio and Derby, 2011; Breithhaupt, 2011). As an adaptation to a terrestrial habitat, coconut crabs have acquired excellent olfactory senses (Stensmyr et al., 2005; Hansson et al., 2011), thus strongly suggesting that they communicate using chemical substances (Hansson et al., 2011). Further studies of the interactions between acoustic signals and chemical communication are also needed as these investigations would improve our understanding of inter-individual communication in coconut crabs.
Appendix A. Supplementary data Supplementary material related to this article can be found, in the online version, at doi:https://doi.org/10.1016/j.zool.2019.125710. References Aggio, J., Derby, C.D., 2011. Chemical communication in lobsters. In: Breithaupt, T., Thiel, M. (Eds.), Chemical Communication in Crustaceans. Springer, New York, pp. 239–256. Boon, P.Y., Yeo, D.C.J., Todd, P.A., 2009. Sound production and reception in mangrove crabs Perisesarma spp. (Brachyura: Sesarmidae). Aquat. Biol. 5, 107–116. Breithhaupt, T., 2011. Chemical communication in crayfish. In: Breithaupt, T., Thiel, M. (Eds.), Chemical Communication in Crustaceans. Springer, New York, pp. 257–276. Cameron, J.N., Mecklenburg, T.A., 1973. Aerial gas exchange in the coconut crab Birgus latro with some notes on Gecarcoidea lalandii. Respirat. Physiol. 19, 245–261. Crane, J., 1966. Combat, display, and ritualization in fiddler crabs (Oxypodidae, genus Uca). Phil. Trans. Roy. Soc. B 251, 459–472. Davie, P.J.F., Guinot, D., Ng, P.K.L., 2015. Anatomy and functional morphology of Brachyura. In: Castro, P., Davie, P.J.F., Guinot, D., Schram, F., Von Vaupel Klein, C. (Eds.), Treatise on Zoology-Anatomy, Taxonomy, Biology. The Crustacea, Volume 9 Part C. Brill, Leiden, pp. 11–163. Drew, M.M., Harzsch, S., Stensmyr, M., Erland, S., Hansson, B.S., 2010. A review of the biology and ecology of the robber crab, Birgus latro (Linnaeus, 1767) (Anomura: Coenobitidae). Zool. Anz. 249, 45–67. Favaro, L., Tirelli, T., Gamba, M., Pessani, D., 2011. Sound production in the red swamp crayfish Procambarus clarkia (Decapoda: Cambaridae). Zool. Anz. 250, 143–150. Greenaway, P., Morris, S., McMahon, B.R., 1988. Adaptation to a terrestrial existence by the robber crab Birgus latro, II. In vivo respiratory gas exchange and transport. J. Exper. Biol. 140, 493–509. Hansson, B.S., Harzsch, S., Knaden, M., Stensmyr, M., 2011. The neural and behavioral basis of chemical communication in terrestrial crustaceans. In: Breithaupt, T., Thiel, M. (Eds.), Chemical Communication in Crustaceans. Springer, New York, pp. 149–173. Helfman, G.S., 1977a. Agonistic behavior of the coconut crab, Birgus latro (L.). Ethology 43, 425–438. Helfman, G.S., 1977b. Copulatory behavior of the coconut or robber crab Birgus latro (L.) (Decapoda Anomura, Paguridae, Coenobitidae). Crustacena 33, 198–202. Henninger, H.P., Watson, W.H., 2005. Mechanisms underlying the production of carapace vibrations and associated waterborne sounds in the American lobster, Homarus americanus. J. Exper. Biol. 208, 3421–3429. Hicks, J., Rumpff, H., Yorkston, H., 1990. Christmas Crabs. Christmas Island Natural History Association, Christmas Island 76 p. Imafuku, M., Ikeda, H., 1990. Sound production in the land hermit crab Coenobita purpureus Stimpson, 1858 (Decapoda, Coenobitidae). Crustaceana 58, 168–174. Knowlton, R.E., Moulton, J.M., 1963. Sound production in the snapping shrimp Alpheus (Crangon) and Synalpheus. Biol. Bull. 125, 311–331. Oka, S., Matsuzaki, S., Toda, M., 2013. Identification of individual coconut crabs, Birgus latro, on the basis of the pattern of grooves on the carapace. Crust. Res. 42, 17–23. Oka, S., Miyamoto, K., Matsuzaki, S., Sato, T., 2015. Growth of the coconut crab, Birgus latro, at its northernmost range estimated from mark-recapture using individual identification based on carapace grooving patterns. Zool. Sci. 32, 260–265. Patek, S.N., 2001. Spiny lobsters stick and slip to make sound. Nature 411, 153–154. Patek, S.N., Baio, J.E., 2007. The acoustic mechanics of stick-slip friction in the California spiny lobster (Panulirus interruptus). J. Exper. Biol. 210, 3538–3546. Patek, S.N., Caldwell, R.L., 2006. The stomatopod rumble: Low frequency sound production in Hemisquilla californiensis. Mar. Freshw. Behav. Physiol. 39, 99–111. Patek, S.N., Shipp, L.E., Staaterman, E.R., 2009. The acoustics and acoustic behavior of the California spiny lobster (Panulirus interruptus). J. Acoust. Soc. Amer. 125, 3434–3443. Salmon, M., 1965. Waving display and sound production in the courtship behavior of Uca pugilator, with comparisons to U. minax and U. pugnax. Zoologica 50, 123–149. Salmon, M., 1967. Coastal distribution, display and sound production by Florida fiddler crabs (genus Uca). Anim. Behav. 15, 449–459. Sato, T., Goshima, S., 2007. Female choice in response to risk of sperm limitation by the stone crab, Hapalogaster dentata. Anim. Behav. 73, 331–338. Sato, T., Yoseda, K., 2010. Influence of size- and sex-biased harvesting on reproduction of the coconut crab Birgus latro. Mar. Ecol. Prog. Ser. 402, 171–178. Sato, T., Yoseda, K., Abe, O., Shibuno, T., 2010. Sperm limitation: Possible impacts of large male-selective harvesting on reproduction of the coconut crab Birgus latro. Aquat. Biol. 10, 23–32. Stensmyr, M.C., Erland, S., Hallberg, E., Wallen, R., Greenaway, P., Hansson, B.S., 2005. Insect-like olfactory adaptations in the terrestrial giant robber crab. Curr. Biol. 15, 116–121. Takeshita, F., Murai, M., 2016. The vibrational signals that male fiddler crabs (Uca latea) use to attract females into their burrows. Sci. Nat. 103, 49.
Acknowledgements We are grateful to Yoko Kawate (NHK Enterprise), who provided very useful information about crab acoustic communication. We thank the staff of the Okinawa Churashima Foundation for assisting us with this study, especially Taketeru Tomita and Kei Miyamoto who provided useful suggestions. Sugao Ohshiro (Conservation & Animal Welfare Trust Okinawa) supported our study. Specimen collection was conducted with the permission of the Okinawa Commemorative National Government Park Office. This study was assisted by funding from the
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Zoology journal homepage: www.elsevier.com/locate/zool
Sound production in the coconut crab, the largest terrestrial crustacean Shin-ichiro Oka ⁎, Nozomi Kobayashi , Taku Sato , Keiichi Ueda , Maki Yamagishi a,
a
b
a
T
c
a
Okinawa Churashima Foundation, 888 Ishikawa, Motobu-cho, Okinawa, 905-0206, Japan Research Center for Marine Invertebrates, National Research Institute of Fisheries and Environment of Inland Sea, Japan Fisheries Research and Education Agency, Momoshima, Onomichi, Hiroshima, 722-0061, Japan c Conservation & Animal Welfare Trust Okinawa, 308-7 Maehara, Uruma-shi, Okinawa, 904-2235, Japan b
A R T I C LE I N FO
A B S T R A C T
Keywords: robber crab acoustic communication scaphognathite tapping sound
Sound production in terrestrial crustaceans, including the coconut crab, Birgus latro, is not fully understood. Here, we present the first description of the acoustic features and sound production mechanisms of coconut crabs. The sound production system was determined based on X-ray videography and anatomical observations. The results indicated that the crabs produced a tapping sound by beating the scaphognathite, which is also used for ventilation, in the efferent branchial channel. The frequencies of the produced sounds were diverse, and the sound interval also varied within the same individual. From observations under captivity, differences in the sounds were confirmed at each mating phase. Although the relationship between the sounds and actions was not clarified in this study, it is probable that the crabs deliberately produce various types of sounds for different occasions. The coconut crab is known to use visual and chemical communication mechanisms, but these results suggest that a diverse set of sounds is an additional communication pathway during agonistic and mating interactions.
1. Introduction Sound production has been reported in several aquatic crustaceans, which have evolved various sound production mechanisms, including stridulation (Salmon, 1967; Boon et al., 2009), carapace vibrations (Henninger and Watson, 2005; Patek and Caldwell, 2006), stick and slip friction (Patek, 2001; Patek and Baio, 2007; Patek et al., 2009), snaps (Knowlton and Moulton, 1963), and bubble emissions (Crane, 1966). Acoustic signals may be produced in a variety of contexts such as defense against predators (Patek, 2001; Patek and Baio, 2007; Patek et al., 2009), courtship (Salmon, 1965; Crane, 1966; Takeshita and Murai, 2016), and agonistic encounters (Patek and Caldwell, 2006; Boon et al., 2009). In addition to the aforementioned acoustic behaviors of aquatic crustaceans, there is some evidence of acoustic signals in terrestrial crustaceans. Some intertidal crabs are known to use sound communication associated with breeding behaviors (Davie et al., 2015; Takeshita and Murai, 2016), but little is known about sound communication in crustaceans in inland areas other than in the intertidal zone. Some terrestrial hermit crabs are known to produce sounds, but the sound production mechanism has only been determined in Coenobita purpureus (Imafuku and Ikeda, 1990). This species produces sound by tapping or rubbing the uropod against the inner surface of the shell, but the function of this sound, which is not related to mating behavior,
⁎
remains unclear (Imafuku and Ikeda, 1990). Since sound transmission differs between aquatic and terrestrial environments, the significance and function of sound production in terrestrial crustaceans may differ from that of aquatic crustaceans. As mentioned above, only a few studies have examined sound production in terrestrial crustaceans, and additional studies are needed to determine the significance and function of acoustic communication in terrestrial crustaceans. The coconut crab, Birgus latro, is the largest terrestrial crustacean, and it is widely distributed in the tropical Indo-Pacific area (Drew et al., 2010). Abundant ecological data have been collected to develop appropriate management strategies designed to protect this endangered species. Coconut crabs can weigh up to 4 kg, and the lifespan is up to 60 years (Drew et al., 2010). The larger size of males compared to females is important for their breeding success (Sato and Yoseda, 2010; Sato et al., 2010). Coconut crabs are thought to communicate with each other using visual and chemical substances for agonistic and aggregating behaviors (Helfman, 1977a; Hansson et al., 2011). However, details regarding intra-specific communication in the species have not been reported. Through our previous experiments in the field and with captive coconut crabs, in which we examined life history characteristics (e.g., Sato and Yoseda, 2010; Oka et al., 2015), we found that coconut crabs generate tapping-like sounds. Therefore, we hypothesized that coconut crabs may use these sounds for communication between
Corresponding author. E-mail address: [email protected] (S.-i. Oka).
https://doi.org/10.1016/j.zool.2019.125710 Received 4 February 2019; Received in revised form 13 August 2019; Accepted 12 September 2019 Available online 18 September 2019 0944-2006/ © 2019 Elsevier GmbH. All rights reserved.
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individuals. As a first step to test this hypothesis, in the present study, we aimed to determine how coconut crabs generate sound.
sound element (duration); pulse rate per second (sound frequency); silence in the interval before sound production (interval); frequency at maximum amplitude (peak frequency); first harmonic of a sound element (fundamental frequency); lowest frequency, where the amplitude is first detected below the threshold (minimum frequency); and the highest frequency, where the amplitude is first detected below the threshold (maximum frequency).
2. Materials and Methods 2.1. Determining the sound production system To detect moving organs during sound production, we attempted to nondestructively observe the internal structure of two living coconut crabs. The thoracic lengths (ThL) of the two crabs were 30.7 mm and 59.1 mm in the female and male, respectively. The lateral side of the crab was held by hand while the crab was photographed using an X-ray fluoroscopy system (Rotanode DRX-61A, Toshiba Corporation) with a digital movie recorder. Although the noise created by the X-ray fluoroscopy device made it impossible to record sounds with a movie recording, it had been confirmed by observation that the coconut crab had been making tapping sounds throughout the recording. The X-ray movie (720 p, 59 fps) was filmed for a total of 13 min (male: 10.5 min; female: 2.5 min); from this, a total of 5 min (male: 4 min; female: 1 min) in which moving organs during sound production were clearly detected was used for the analysis. Tapping sound frequency (taps/ second) made by the scaphognathite, which was the only organ with internal movement, were calculated from the duration of 10 tappings of the scaphognathite observed from the X-ray movies. The scaphognathite is a thin leaflike appendage of the second maxilla of decapod crustaceans. It usually serves as a pumping organ to draw water and air though the gill cavity, which is also its function in coconut crabs (Cameron and Mecklenburg, 2010). Tapping sound frequency measurements were made using 70 randomly chosen scenes from the recorded movies. Two registered and preserved (10% formalin) specimens that were deposited in the Okinawa Churashima Foundation (OCF-Cr00052, 33.6 mm ThL, male; OCF-Cr00053, 30.5 mm ThL, female) were dissected. The lateral side of cephalothorax was determined to be the anatomical observation area, based on the results of the X-ray movie analysis.
2.3. Consideration of animal welfare Although the Guide for Care and Use of Laboratory Animals of Okinawa Churashima Foundation outlines procedures for animal experiments, they are waived for crustaceans. Therefore, we considered crab welfare and maintained the specimens as described below. All living crabs used in the present study were captured at the Ocean Expo Park (26°41′N, 127°52′E), and were returned to their original areas immediately after the conclusion of the experiments. We also confirmed that released crabs (even those under captive conditions for several years) exhibited normal growth based on data from our previous studies (Oka et al., 2013, 2015). A previous study examined crayfish and found that the anatomical method of sound producing organ removal effectively identified the sound production mechanism (Favaro et al., 2011). However, the coconut crab is an endangered species that requires decades of individual growth, so this experiment was avoided to protect living crabs. 3. Results 3.1. Observations of X-ray movies and analysis of anatomy data X-ray movie analysis and anatomical observation were performed for one crab per sex. X-ray movie analysis indicated that the right and left scaphognathites were only tapped vertically in the efferent branchial channel (EBC) during sound production (Movie S1 in the supplementary online Appendix); this movement was clear in a lateral view, although it was unclear in a dorsal view. The tapping frequency was 1.8–6.2 taps/s, but there was no significant difference in the tapping frequency between females (n = 18) and males (n = 52) (Mann Whitney U-test, z = 1.44, p = 0.15). The results of the anatomical observations confirmed the results of the X-ray analysis in that scaphognathites were found in the EBC (Fig. 1A). Although the scaphognathite was flat and soft, the hard and slender plate was only found on the dorsal side of the scaphognathite (Fig. 1B). In addition, the scaphognathite was confirmed to move only vertically from the center of the base (Fig. 1A). The hard organ consisted of three hard panel units (HPU), which were found on the dorsal edge of the EBC (Fig. 1C). The hard plate on the dorsal side of the scaphognathite contacted the HPU when the scaphognathite was moved. The study of one specimen per sex did not reveal any obvious differences between male and female specimens.
2.2. Sound recording and analysis Recordings of coconut crab sounds were made using a digital audio recording device (linear PCM recorder; SONY PCM-D100) with a builtin microphone, which had a flat frequency response from 100 to 1400 Hz, under the following two conditions: Exp 1: Recordings of coconut crab sounds were conducted while the crabs were secured by their legs, holding the crab at a position approximately 100 mm apart from the fixed recording device in a room; Exp 2: Recordings of coconut crab sounds were conducted during mating of one pair of crabs (52.5 mm ThL, male; 33.7 mm ThL, female) in a soundproof box (0.9 m × 0.6 m × 0.6 m) where the floor was covered with a rubber mat for absorbing the sound of crab legs tapping as it moves. In Exp 1, two males and four females were recorded for approximately 180 s each. In Exp 2, the recording device was installed on top of the soundproof box, and sound recordings were continuously collected inside the box overnight. Furthermore, time lapse photographs (every 5 s) of the crabs in the box were taken using a digital camera (GoPro HERO 3+). The time series of the recorded sounds and the time lapse photography data were synchronized based on the logged time for both the sounds produced and mating behaviors. Mating success was confirmed using time lapse photographs and from adhesion of a spermatophore mass to the abdomen of the female. The sampling rate for all recordings was 44.1 kHz, 16 bit, and background noises were filtered out using the Noise Reject application function Audacity version 2.2.2 for sound analysis. Data were analyzed using the sound analysis software AvisoftSAS Lab Pro version 5.2.10, and the following parameters were measured for each coconut crab sound using the Automatic Parameter Measurements application function of the software: the duration of a
3.2. Acoustic analysis In Exp 1, we recorded the sounds from two males and four females, and we confirmed tapping sounds from every individual (Table 1, Fig. 2, Movie S2). One of the sounds is indicated in Fig. 2A-C. Fig. 2A represents a sonogram of tapping sounds and Fig. 2B, oscillogram, is coincided with the sonogram in which the short pulses with large amplitude vibration are synchronized with the tapping sounds in the sonogram (Fig. 2A, B). The six parameters (duration, intervals, peak frequency, fundamental frequency, minimum frequency, and maximum frequency) and standard deviations for the mean values of each sound parameter varied between different individuals and within the same individuals at different times (Table 1, Figs. 2–4). For example, the sound durations for the six individuals ranged between 5–40 ms, and the tapping frequency was 5–14 taps/s. The sounds were structured 2
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Fig. 1. Anatomical photographs of the coconut crab airway system (specimen number: OCF-Cr00052). A: Left side view of the partially dissected specimen. B: (1) Dorsal and (2) ventral side view of the excised left scaphognathite. C: Ventral side view of the efferent branchial channel (EBC). Solid and white dashed lines indicate the hard plate on the dorsal side of the scaphognathite and the outline of the scaphognathite, respectively. Green arrow indicates the direction of the movement of the scaphognathite. HPU: hard plate unit in EBC.
was recorded in the same condition. In Exp 2, the mating behavior was recognized only once, as follows. Phase 1: the crabs faced each other for approximately 17 min. Phase 2: the male held the female’s claws, and then pushed the female in the male’s direction; the male climbed onto the female, and both abdomens were in contact for 2 min. Phase 3: the male released the female, and
with sound elements that were lower than 18 kHz, and it ranged from 450 Hz to 17140 Hz. The fundamental frequency was distributed between 860–9560 Hz, and sound intervals varied within the same individual (Fig. 3, Movie S2). Although there were potential effects of reverberation on the sounds recorded in Exp 1, there were differences confirmed within the sound features emitted by each individual which
Table 1 Data and results of sound analyses for the six experimental individuals in Exp 1. Parameters with asterisks are the mean value and the standard deviation ( ± ) for a total of 30 sound samples for each individual. No.
Sex
Thoracic length (mm)
Duration* (ms)
Interval* (ms)
Sound Freq.* (Hz)
Peak Freq.* (Hz)
Fundamental Freq.* (Hz)
Minimum Freq.* (Hz)
Maximum Freq.* (Hz)
1 2 3 4 5 6
male male female female female female
63.3 46.5 33.7 27.8 24.1 23.8
8 ± 5 6 ± 3 9 ± 7 7 ± 5 6 ± 3 10 ± 8
115 ± 38 183 ± 90 184 ± 47 135 ± 85 80 ± 31 81 ± 46
9.3 ± 0.5 5.5 ± 0.8 5.5 ± 0.5 9.0 ± 0.6 14.3 ± 1.0 12.2 ± 1.5
1986 1799 5711 3226 2621 3041
1959 1801 5740 3051 2590 3128
619 ± 123 766 ± 135 2482 ± 485 1386 ± 406 1219 ± 199 745 ± 138
8989 ± 2403 5483 ± 1946 10827 ± 2199 6962 ± 3452 6504 ± 2774 11512 ± 2160
3
± ± ± ± ± ±
379 259 2214 368 620 280
± ± ± ± ± ±
341 258 2524 588 655 255
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Fig. 4. Figures A, B, and C are examples of sounds recorded in Exp 2. A: The sound was recorded when the male and female stopped to face each other while 10 cm apart. B: The sound was recorded when the male climbed on the female for mating. C: The sound was recorded when the female separated and moved away from the male after mating. We were unable to distinguish which individuals emitted sounds during Exp 2.
Fig. 2. Example of the tapping sounds of coconut crabs. Figure shows the sounds of a female coconut crab (Individual #5 in Table 1) recorded in Exp 1 (A: sonogram, B: oscillogram, C: power spectrum). The square in A indicates the sound of the coconut crab, and the arrow indicates a sound interval.
fundamental frequency and sound intervals were 3718 (SD = 1541) Hz and 89 (SD = 25) ms, respectively. Sound C (Fig. 4C, Movie S2 in the supplementary online Appendix) was observed after mating behavior was observed when the female separated and moved away from the male (Phase 3). Mean values for the fundamental frequency and the sound intervals were 2549 (SD = 257) Hz and 182 (SD = 43) ms, respectively. Although we were unable to distinguish which individual emitted Sounds A, B, and C, we can affirm that both crabs did not simultaneously emit sounds. 4. Discussion In this study, although X-ray video analysis and anatomical observation were performed for only one crab per sex, we were able to obtain some evidence about the sound production system of the coconut crab. Only the scaphognathite moved during sound production, and no other movements were confirmed that could have produced the sounds. Moreover, the range of beating movement frequencies was confirmed in the X-ray movies, and the tapping sound obtained in the actual sound recording overlapped with that of the organ movements recorded in the X-ray movies. Therefore, the tapping sound was generated by striking the hard plate of the scaphognathite against the hard panel unit (HPU) on the roof of EBC, thus providing a mechanism by which a soft scaphognathite could efficiently generate sound. The soft scaphognathite may also serve as a cushion to prevent an excessive abrasion of the two hard plates. Coconut crab lungs are ventilated by the scaphognathite, which draws air forward through the lung (Cameron and Mecklenburg, 1973; Greenaway et al., 1988), and ventilation could reach over 1 L/min by increasing the frequency of scaphognathite beating (Cameron and Mecklenburg, 1973). The highest estimated scaphognathite beating rate associated with ventilation reached about 5.8–6.7 cycles/s based on a study of coconut crab air ventilation (Cameron and Mecklenburg, 1973). These ranges overlapped with both the frequency observed during the X-ray and tapping sound recordings, thus indicating that scaphognathite beating is associated with sound production. Therefore, it is possible that the
Fig. 3. Example of tapping sounds performed by a male (Individual #2 in Table 1) that was observed in Exp 1. A: Pulse rate was 11 taps in 3 s; the mean interval value was 299 (SD = 73) ms; and values for points a, b, and c were 412, 220, and 272 ms, respectively. B: Pulse rate was 17 taps in 3 s; the mean interval value was 176 (SD = 22) ms; and values for points d, e, and f were 162, 142, and 179 ms, respectively.
the crabs went in opposite directions. After that, the crabs did not have any other contact until the end of the experiment. Several tapping sound patterns were observed during Exp 2 (Fig. 4, Movie S2 in the supplementary online Appendix). Sound A (Fig. 4A, Movie S2 in the supplementary online Appendix) was observed when the experimental individuals (a male and a female) faced each other approximately 10 cm apart in an experimental box before the mating behavior was observed (Phase 1). Mean values for the fundamental frequency and the sound intervals were 2357 (SD = 139) Hz and 104 (SD = 37) ms, respectively. Sound B (Fig. 4B, Movie S2 in the supplementary online Appendix) was observed when the male climbed on the female when exhibiting mating behavior (Phase 2). Mean values for the 4
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Okinawa Churaumi Aquarium.
scaphognathite has two functions: ventilation and sound production. Our results, however, did not clearly refute the possibility of the sounds being produced with the changes in the ventilation frequency or strength in the situation of breeding and/or of facing an enemy, so additional studies and analyses are essential to clarify the nature of the tapping sound. A similar sound-producing mechanism using scaphognathite beating was reported in aquatic crayfish (Procambarus clarkii) via an anatomical approach (Favaro et al., 2011). The present study is the second to experimentally demonstrate the role of scaphognathite movement in crustacean sound production, and it represents the first reported case in terrestrial crustaceans. The results of the present study suggest that both male and female coconut crabs can produce various sounds (Figs. 3 and 4, Table 1), and this was also supported by the movement of scaphognathites at various speeds based on X-ray movies. Why do the crabs need to produce various sounds? Although the acoustic signals of aquatic crustaceans were thought to be used for defense against predators, courtship, and agonistic encounters (Salmon, 1965; Crane, 1966; Patek, 2001; Patek and Caldwell, 2006; Patek and Baio, 2007; Boon et al., 2009; Patek et al., 2009), the significance of sound production in terrestrial crustaceans was not clarified, with the exception of some intertidal crabs that produced vibration signals to induce mating (Davie et al., 2015; Takeshita and Murai, 2016). In the present study, the various sounds were confirmed at a fixed state and during mating (Figs. 2 and 3, Table 1). The mating behavior observed in Exp 2 was considered to be normal, because the sequence of behaviors was similar to that observed in a previous study (Helfman, 1977b, Hicks et al., 1990). Regarding sound production during mating, although both crabs did not simultaneously produce sounds, it was not possible to distinguish which crab (male or female) made each sound. However, we found that the fundamental frequency and sound intervals changed during each mating phase (Fig. 4, Movie S2 in the supplementary online Appendix), which suggests the existence of communication using sound during their mating behavior. To clarify the significance and effects of these sounds, additional experiments (e.g., sound analyses under different conditions) are needed, especially those aiming at the identification of specific male and female sounds. The results of this study suggest that coconut crabs may communicate using sound. However, it is undeniable that sound production using the ventilation system may be related to other functions. Crustaceans are known to have various chemical communications for mating, aggregation, and agonistic actions (Sato and Goshima, 2007; Breithhaupt, 2011). In aquatic lobsters and crayfish, urine is diffused for chemical communication using the ventilation system (Aggio and Derby, 2011; Breithhaupt, 2011). As an adaptation to a terrestrial habitat, coconut crabs have acquired excellent olfactory senses (Stensmyr et al., 2005; Hansson et al., 2011), thus strongly suggesting that they communicate using chemical substances (Hansson et al., 2011). Further studies of the interactions between acoustic signals and chemical communication are also needed as these investigations would improve our understanding of inter-individual communication in coconut crabs.
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Acknowledgements We are grateful to Yoko Kawate (NHK Enterprise), who provided very useful information about crab acoustic communication. We thank the staff of the Okinawa Churashima Foundation for assisting us with this study, especially Taketeru Tomita and Kei Miyamoto who provided useful suggestions. Sugao Ohshiro (Conservation & Animal Welfare Trust Okinawa) supported our study. Specimen collection was conducted with the permission of the Okinawa Commemorative National Government Park Office. This study was assisted by funding from the
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