165A.N. Popper and A. Hawkins (eds.), The Effects of Noise on Aquatic Life, Advances in Experimental Medicine and Biology 730, DOI 10.1007/978-1-4419-7311-5_37,© Springer Science+Business Media, LLC 2012

E. R. Staaterman (�) • T. Claverie • S. N. Patek Biology Department , University of Massachusetts Amherst , Amherst , MA 01003 , USA e-mail: e.staaterman@gmail.com

C. W. Clark Bioacoustics Research Program , Cornell Laboratory of Ornithology , Ithaca , NY 14850 , USA

A. J. Gallagher Marine Science Center , Northeastern University , Nahant 01908 , MA , USA

M. S. de Vries Department of Integrative Biology , University of California, Berkeley , Berkeley , CA 94720 , USA

1 Introduction

Acoustic communication plays a major role in the behavioral ecology of various marine organisms (Busnel 1963 ) , especially marine mammals and fish. However, little attention has been given to acoustic communication in marine crustaceans (Popper et al. 2001 ) . Furthermore, the interplay between anthropogenic noise and the acoustic ecology of marine crustaceans remains virtually unexplored. In this study, we investigated the acoustic environment of a benthic stomatopod crusta-cean, the California mantis shrimp ( Hemisquilla californiensis , Crustacea, Stomatopoda).

California mantis shrimp produce a “rumble” sound that has been anecdotally observed in the field (Haderlie et al. 1980 ) and first documented in the scientific literature in 2006 (Patek and Caldwell 2006 ) . Patek and Caldwell’s recordings were obtained in tanks and sounds were recorded when the animals were physically handled or approached by a stick. Fifty percent of the adult males produced rumbles, whereas none of the adult females produced sound. The rumbles were produced by vibrations of a pair of muscles that attach to the edge of the carapace. Rumbles lasted less than 2 s and the mean dominant frequency was 45 ± 10 (SD) Hz ( n = 53 rumbles). The general function of this sound and whether or not females are capable of generating it remains unknown.

Although the laboratory-based recordings of rumbles provide a starting point for identifying the source of the sound, field recordings are essential for interpreting the rumble’s function and role in the ecology of mantis shrimp. However, to our knowledge, no field recordings have been published for any stomatopod crustacean. The three primary goals of this study were to 1) characterize the sounds of H. californiensis in its natural habitat, 2) describe diel patterns of behavior and sound production, and 3) examine the presence of anthropogenic noise in the acoustic habitat of the California mantis shrimp. We employed several tools and techniques to accomplish these goals, including a coupled audio-video system and a passive acoustic device.

Acoustic Ecology of the California Mantis Shrimp (Hemisquilla californiensis)

Erica R. Staaterman, Christopher W. Clark, Austin J. Gallagher, Thomas Claverie, Maya S. de Vries, and Sheila N. Patek

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2 Recording Methods and Results

Recordings were obtained in the naturally occurring communities of H. californiensis off the coast of Santa Catalina Island, CA, in March 2009. A coupled audio-video system was placed in front of several animals’ burrows by a SCUBA diver, and the resulting footage was later imported into digi-tal audio files for analysis. These recordings (48 kHz, 16-bit sampling rate) were used to describe general characteristics of the rumbles (Fig. 1 ). The average rumble had a dominant frequency of 167 ± 40.9 (SD) Hz and lasted 0.2 ± 0.08 (SD) s ( n = 3,858 rumbles from an undetermined number of individuals). We found that the rumbles were typically produced in groups of twos, threes, and fours, which we now refer to as “rumble bouts.” The leading rumble of each bout was louder by an average of 4.8 ± 0.185 dB and longer in duration by an average of 0.093 ± 0.005 s than the second rumble in the bout ( n = 304 rumbles from ~17 individuals). Despite these general similarities, recordings from various individuals’ burrows yielded rumbles that differed in dominant frequency and temporal patterning.

An autonomous recording unit (see Clark and Clapham 2004 ) was deployed ~9 km from the first site in a different mantis shrimp population and was run continuously (32 kHz, 16-bit sampling rate) for an 8-day period. We scanned this recording’s spectrogram both visually and aurally and found distinct trends across the 8 days. During crepuscular periods, loud rhythmic rumbles were audible. At night, the mantis shrimp were acoustically active, but their rumbles were quieter and lower in frequency than during the day. We observed few rumbles during hours of peak sunlight.

We found that at the site of the 8-day recorder, boat activity was substantially higher during the day and during weekdays than during nights and weekends (Fig. 2 ). When averaging the acoustic energy across 1-h periods, we saw that midday energy values in the 100- to 500-Hz range, e.g., were, on average, 15.6 ± 0.7 dB louder than midnight energy values (Fig. 3 ; matched-pairs t -test; n = 8; t -ratio = 23.08; P < 0.0001).

Rumbles produced amid boat noise were compared with rumbles produced during normal ambient noise conditions. When the rumbles were not completely obscured by boat noise, rumble dominant frequencies decreased when boats were present (difference = 37 ± 1.3 [SD] Hz, t -test; degrees of freedom [DF] = 3893.01; P < 0.0001).

Fig. 1 An example of a rumble bout consisting of 3 rumbles. Spectrogram settings: discrete Fourier transform (DFT) = 8192; Hann window: 0.0512 s; 3-dB fi lter bandwidth at 5.62-Hz resolution

167Acoustic Ecology of the California Mantis Shrimp (Hemisquilla californiensis)

Fig. 2 A typical 24-h spectrogram from the autonomous recording unit showed substantial variation in noise levels across each day. The continuous lines at 50, 75, 125, and 160 Hz are an artifact of the recorder’s hard drive. The intense (red) bands of broadband energy, especially between ~0700–1900, are a result of vessel noise. Spectrogram settings: DFT = 819; Hann window = 0.435 s

Fig. 3 Power spectra for the 8-day period comparing the distribution of acoustic energy at midnight (0000–0100) and midday (1200–1300). Shaded regions are SE. Peaks at 125 and 160 Hz are artifacts of the recorder’s hard drive. Daytime periods were significantly louder than nighttime periods due to vessel traffic

3 Conclusions

We found an active acoustic scene in the benthos off the coast of California, an area that was previously unexplored acoustically. Furthermore, we demonstrated that the sounds produced by H. californiensis are highly variable; different individuals produce rumbles that differ in dominant frequency and number of rumbles per bout. Our recordings took place during the early part of the mating season when males are highly competitive for burrow space and actively attempt to recruit females into their burrows to mate (Basch and Engle 1993 ; J. Engle, personal communication). It is possible that the rumble plays a role in establishing territories and/or attracting potential mates.

We also observed that H. californiensis species spends a large portion of its day producing sound, which highlights the potentially important contribution of the rumble to this species’ behavioral ecology. One interesting finding was that during crepuscular periods, when H. californiensis is typi-cally found guarding its burrow entrance (Basch and Engle 1993 ) , rumbles were loud and produced in rhythmic sequences. During times when the burrow is typically closed for protection from predators

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(Basch and Engle 1993 ) , we observed very few rumbles or rumbles that were lower in frequency and relatively less intense. This may indicate that sound production continues even when the burrow is closed. This initial exploratory study reveals a system that is rich with future questions and dis-covery, including the central question: what is the function of the rumble?

The waters near Santa Catalina Island are frequented by small boats and large shipping vessels, which collectively produce a tremendous amount of acoustic energy in the communication band of H. californiensis (i.e., 100–500 Hz). During periods of intense vessel noise, we could not resolve whether mantis shrimp ceased rumbling or whether complete acoustic masking was taking place. However, given the fact that vessel noise was detectable during a large portion of the day, we suspect that acoustic masking is a frequent phenomenon in this habitat. Given the deleterious effects of acoustic masking in other taxa (e.g., Clark et al. 2009 ; Nowacek et al. 2007 ; Popper and Hastings 2009 ) , this omnipresent and acoustically overlapping vessel noise may substantially impact the acoustic ecology of the California mantis shrimp. Marine invertebrates should be included in future studies and consideration of the effects of anthropogenic noise on aquatic animals.

References

Basch LV, Engle JM (1993) Biogeography of Hemisquilla ensigera californiensis (Crustacea: Stomatopoda) with emphasis on Southern California bight populations. In Hochberg FG (ed) Third California Islands Symposium, Santa Barbara Museum of Natural History, Santa Barbara, CA, pp 211–220.

Busnel RG (1963) Acoustic behavior of animals. Elsevier Publishing Company, New York, NY. Clark CW, Clapham PJ (2004) Acoustic monitoring on a humpback whale ( Megaptera novaeangliae ) feeding ground

shows continual singing into late spring. Proc Biol Sci 271:1051–1057. Clark CW, Ellison WT, Southall BL, Hatch L, Van Parijs SM, Frankel A, Ponirakis D (2009) Acoustic masking in

marine ecosystems: Intuitions, analysis, and implication. Mar Ecol Prog Ser 395:201–222. Haderlie EC, Abbott DP, Caldwell RL (1980) Three other crustaceans: a copepod, a leptostracan, and a stomatopod.

In: Morriss RH, Abbott DP, Haderlie EC (eds) Intertidal invertebrates of California. Stanford University Press, Palo Alto, CA, pp 631–635.

Nowacek DP, Thorne LH, Johnston DW, Tyack PL (2007) Responses of cetaceans to anthropogenic noise. Mamm Rev 37:81–115.

Patek SN, Caldwell RL (2006) The stomatopod rumble: Sound production in Hemisquilla californiensis . Mar Freshw Behav Physiol 39:99–111.

Popper AN, Hastings MC (2009) The effects of human-generated sound on fish. Integr Zool 4:43–52. Popper AN, Salmon M, Horch KW (2001) Acoustic detection and communication by decapod crustaceans. J Comp

Physiol A 87:83–89.