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Disentangling defense: the function of spiny
lobster sounds
E.R. Staaterman,T. Claverie & S.N. Patek1)
(Department of Integrative Biology, University of California, Berkeley, CA 94720, USA)
(Accepted: 20 August 2009)
Summary
The function of anti-predator signalling is a complex, and often-overlooked, area of animal
communication. The goal of this study was to examine the behavioural function of an anti-
predator acoustic signal in the ocean. We observed the acoustic and defensive behaviours
of California spiny lobsters (Palinuridae: Panulirus interruptus) to a model predator, model
conspecific and blank pole, both in the tank and in the field. We found that P. interruptus make
a ‘rasp’ sound once physically contacted by an aggressor, rather than during the approach.
The model predator and conspecific elicited no discernable changes in defensive behaviour,
but the responses by the lobsters to aggressors in the tank versus field were distinct. Our
results indicate that the spiny lobster’s rasp is used as a startle or aposematic signal, which
may be coupled with visual aposematism of their spines. Alternatively, the rasp may function
as a vibratory escape mechanism or as an acoustic analogue to eye-spots. This study offers
insights into the role of acoustic signalling in the marine environment and demonstrates a
central role for sound production in spiny lobster ecology.
Keywords: anti-predator signals, aposematism, warning, startle, Palinuridae.
Introduction
“As a general rule it is better to mate tomorrow than be a meal today”
(Bailey, 1991).
Approximately 125 million years ago, spiny lobsters evolved a sound-
producing apparatus at the base of their spiny antennae (Palero et al., 2009).
1) Corresponding author’s current address: Department of Biology, 221 Morrill South,
University of Massachusetts, Amherst, MA 01003, USA, e-mail: patek@bio.umass.edu
©Koninklijke Brill NV, Leiden, 2010 Behaviour 147, 235-258
DOI:10.1163/000579509X12523919243428 Also available online - www.brill.nl/beh
236 Staaterman, Claverie, & Patek
Lacking claws, palinurid lobsters rely on their long and powerful antennae
to defend themselves against intruders (Kanciruk, 1980; Spanier & Zimmer-
Faust, 1988; Kelly et al., 1999; Herrnkind et al., 2001; Barshaw et al., 2003;
Briones-Fourzán et al., 2006). With the origin of the sound-producing ap-
paratus in one group of spiny lobsters (the ‘Stridentes’) (George & Main,
1967), the antennae became both mechanical and acoustic weaponry (Patek
& Oakley, 2003). Indeed, since its origin, the sound-producing apparatus
has diversified into a fantastic array of sizes, shapes and colors (George &
Main, 1967; Patek & Oakley, 2003). Given that the acoustic structures are
indistinguishable between males and females (Patek, 2002; Patek & Oakley,
2003; Patek & Baio, 2007; Patek et al., 2009), and that the spiny lobsters
produce the sounds when interacting with potential predators, the function
of the sound is assumed to deter predators (Lindberg, 1955; Moulton, 1957;
Moulton, 1958; Smale, 1974; Meyer-Rochow & Penrose, 1976; Mulligan &
Fischer, 1977; Bouwma & Herrnkind, 2009). Remarkably, over the millennia
of documentation of these sounds in the literature (Athenaeus, 3rd century;
Parker, 1878, 1883), not until recently has the anti-predator function of these
signals been experimentally tested (Bouwma & Herrnkind, 2009). Even with
this foundational study of function, how the spiny lobsters’ sounds deter
predators (Edmunds, 1974; Bradbury & Vehrencamp, 1998; Caro, 2005) re-
mains unknown in this system.
Most spiny lobster taxa exhibit forms of gregarious behaviour that offer
defense against predators (Butler IV et al., 1999; Kelly et al., 1999; Her-
rnkind et al., 2001; Barshaw et al., 2003; Childress, 2007; Briones-Fourzán
& Lozano-Álvarez, 2008). For example, many species share dens (Childress
& Hernkind, 1997; Childress & Herrnkind, 2001), aggregate when presented
with predators (Kelly et al., 1999; Herrnkind et al., 2001), migrate in for-
mation (Bill & Herrnkind, 1976) and sense conspecific olfactory alarm sig-
nals (Shabani et al., 2008). The spiny lobster’s acoustic signal, the ‘rasp’, is
used in both solitary and gregarious settings when interacting with potential
predators (S.N.P., pers. observ.). Three behavioural studies have suggested
the possibility of intraspecific communication with sound as acoustic warn-
ing signals to conspecifics (Lindberg, 1955; Berrill, 1976; Meyer-Rochow et
al., 1982), but strong experimental evidence is lacking and it is not presently
known whether spiny lobsters can hear beyond the near-field region (approx.
1 wavelength from the source =4 m: Patek et al., 2009) (reviewed in Budel-
mann, 1992; Popper et al., 2001).
Spiny lobster sounds 237
The sound-producing mechanism itself may relate to its anti-predator
function. Spiny lobsters produce sound by rubbing a soft-tissue extension
(the ‘plectrum’) at the base of each antenna over an oblong, macroscopically
smooth ‘file’ under each eye; rasp sounds are generated using stick-slip fric-
tion between the two surfaces (Patek, 2001, 2002; Patek & Baio, 2007). Patek
(2001) proposed that the use of non-rigid surfaces to produce these stick-slip
sounds allowed the animals to generate sound throughout their moult cy-
cles when the exoskeleton is softened, thereby providing an acoustic defence
when their other physical defences are compromised. Latha et al. (2005)
confirmed that recently moulted lobsters can effectively generate loud rasps.
The first published performance tests of the spiny lobster’s anti-predator
rasp examined how silencing Caribbean spiny lobsters (Panulirus argus) af-
fected their nocturnal interactions with predatory octopus (Octopus briareus)
in experimental tanks (Bouwma & Herrnkind, 2009). The authors found that
stridulating lobsters were better able to escape octopus attacks and resist at-
tacks for a longer duration than silenced lobsters. While the first approach
of the octopus did not yield an acoustic response until physical contact with
the lobster, in subsequent approaches, the spiny lobsters initiated tail flip es-
cape responses (not necessarily with sound) before contact. Once caught,
the lobsters stridulated for an extended time (average 90 s). Even though
the stridulating lobsters fared better than the silenced lobsters, the octopuses
showed no obvious response to the rasp signal, leading the authors to sug-
gest that perhaps the rasp does not function to startle the octopus and instead
the vibrations make it more difficult to grasp the rasping lobster. While this
study offers a number of keen insights into the acoustic function of the rasp,
it is important to note that there was no control for the surgery that removed
the sound-producing apparatus in silenced lobsters. Given that the plectrum
is an integral part of the antennal joint (Patek, 2002), it is possible that the
differences in performance could be due to the experimental removal of this
joint articulation, rather than the absence of sound production. In an unpub-
lished dissertation (Bouwma, 2006), similar performance results were found
in daytime face-offs between triggerfish and tethered silenced and stridulat-
ing spiny lobsters.
Ideally, in order to determine the behavioural function of the rasp, one
would observe naturally occurring predator–prey interactions in the field
with freely-moving individuals (e.g., Cocroft, 1999). However, spiny lob-
sters pose particular challenges to this experimental approach. First, spiny
lobsters are nocturnal foragers, often going on excursions far from their
238 Staaterman, Claverie, & Patek
daytime rocky and coral crevices, thus making visualization of behaviours
and tracking difficult. Nonetheless, illumination at night with red lights is
minimally disruptive to spiny lobsters, although the lights can attract small
fish (Weiss et al., 2006). Second, and more critically, spiny lobsters gener-
ate these rasp sounds in water. Sound travels approximately five times more
quickly in water than in air, making localization of sounds nearly impossible
without an array of hydrophones or only while in very close range of the
sound source. Furthermore, the ambient background noise in their habitats
can be high enough that rasps may not be reliably recorded from distances
beyond approx. 1 m from the source (Patek et al., 2009). Tethering lobsters is
one solution, but it affects the ability of the lobsters to escape, and, therefore,
the dynamics of the predator–prey interactions and the type of predators that
approach (Zimmer-Faust et al., 1994) as well as possibly the acoustic behav-
iour of the lobsters (Bouwma & Herrnkind, 2009).
Given these limitations, one approach is to conduct the experiments in
the field with freely-moving spiny lobsters, record the rasps in close range
and use model predators rather than real predators. Numerous studies have
documented the importance of olfactory cues during predatory interactions
(e.g., Sih et al., 1998; Dicke & Grostal, 2001; Lima, 2002). Clawed lobsters
(Nephropidae) (Wahle, 1992) and spiny lobsters (Berger & Butler IV, 2001)
are able to detect predators using chemical cues. In addition to chemore-
ception, crustaceans use their antennae as mechanosensory structures and
can detect the low-frequency signatures of locomoting animals (Tautz &
Sandeman, 1980; Tautz, 1990; Derby & Steullet, 2001). Thus, models would
lack both the olfactory cues of predators and the finer-tuned vibratory cues
of swimming predators. However, the models would generate the low-
frequency waves produced by any approaching object in a fluid environment,
thus giving them advanced warning of an approaching model predator. Vi-
sual cues, however, can be sufficient to alert arthropods to predators; in a
study of spider responses to a range of predator signals, spiders were able to
appropriately respond solely on the basis of visual cues (Lohrey et al., 2009).
In addition, the study by Bouwma and Herrnkind (2009) on octopus preda-
tors suggest that the visual and physical contact experience may supersede
ambient olfactory cues in the Caribbean spiny lobster.
Thus, in this study, we present the first published field and laboratory ex-
periments to examine the behavioural function of rasps produced by freely-
moving California spiny lobsters (Panulirus interruptus) interacting with a
model predator, a model conspecific and a blank pole. Panulirus interruptus
Spiny lobster sounds 239
Figure 1. The California spiny lobster (Panulirus interruptus) hides in rocky crevices dur-
ing the day (A) and often the only visible parts of the body are the extended antennae and
eye-spots (B). The sound-producing apparatus is located at the base of each antenna, beneath
the eyes. The characteristic eye-spots are located adjacent to the sound-producing apparatus,
immediately below the eyes. This figure is published in colour in the online version of this
journal, which can be accessed via http://www.brill.nl/beh
are gregarious (although coordinated anti-predator behaviours have yet been
described in this species), nocturnal spiny lobsters with brightly coloured
‘eye-spots’ adjacent to their sound-producing apparatus (Figure 1). Like
240 Staaterman, Claverie, & Patek
other sound-producing spiny lobsters, this species also generates stick-slip
‘rasp’ sounds when interacting with potential predators (Patek & Baio, 2007;
Patek et al., 2009). We addressed three central questions. First, based on the
timing and context of sound production, which type of anti-predator signal is
being used? Second, do spiny lobsters respond differently to a model preda-
tor than to a control model (conspecific) or a blank pole? Lastly, given that
most previous studies of anti-predator signaling have taken place in the lab-
oratory or confined conditions, how does defensive behaviour vary between
field and tank environments?
Materials and methods
Lindberg (1955) found that sheepshead (Pimelometopon pulchra) preyed
most heavily on P. interruptus; thus, one of our models approximated the
size and morphology of a sheepshead fish. A second model represented a
spiny lobster as a generally non-predatory aggressor. We cast a frozen fish
(33 cm body length) and a frozen spiny lobster (8 cm carapace length) with
a commercial mold material, and then made the models with a commercial
silicone material and spray paint (alginate mold and Silicone RTV SR-1610,
Douglas and Sturgess, Richmond, CA, USA). We also used a blank pole
(without an attached model) as a control.
During all of the experiments, we simultaneously recorded the lobsters’
behavioural and acoustic responses using two separate audio–video systems,
one attached to the aggressor pole and one attached to the observer pole (Fig-
ures 2 and 3). By using two systems, we could verify the timing of acoustic
response from two vantage points during the experiments. The first system,
which we call the ‘aggressor pole’, was used to approach the lobsters with the
model aggressor. This pole was equipped with a hydrophone (20–25 000 Hz;
HTI-96-Min hydrophone, High Tech, Gulfport, MS, USA), a low-light cam-
era (Submersible Under-Water CCD 480TVL Bullet Color Camera, Sony,
New York, NY, USA) and a small, dimmed, white dive light. Depending
on the particular experiment, the aggressor pole also had the fish or lob-
ster model attached to it. The second system, termed the ‘observer pole’,
recorded the sound of the focal lobster before and during the approach of
the aggressor pole. The observer pole was equipped with the same type of
hydrophone as the aggressor pole. The video and audio data were recorded
Spiny lobster sounds 241
Figure 2. Field experiments were conducted with an aggressor pole and observer pole
focused on a freely-moving live spiny lobster. A hydrophone, camera and small flashlight
were attached to the aggressor pole. Only a hydrophone was attached to the observer pole.
Both poles had cables leading to recording devices on the surface. For each experiment, one
person held the observer pole above the lobster, while the other person approached the lobster
with the aggressor pole equipped with either a model fish, model lobster, or blank pole.
Figure 3. Tank experiments utilized an aggressor and observer pole setup similar to the
field experiments. A camera, hydrophone and small dimmed dive-light were attached to the
aggressor pole. The observer hydrophone was positioned above the lobster, and the observer
camera was positioned at a right-angle to the aggressor pole to capture the lobster’s behaviour
during the approach. We approached lobsters with the aggressor pole, equipped with either
the model fish, model lobster, or a blank pole.
242 Staaterman, Claverie, & Patek
for both poles using the same equipment (Sony GV-A500 Hi8 Video Walk-
man, Sony; digital audio recorder, 48 kHz sample rate, maximum 20 kHz
frequency response (−0.5 dB), PMD670, Marantz, Mahwah, NJ, USA).
Experiment 1: response to nocturnal approaches in the field
The goal of this experiment was to measure the defensive acoustic and be-
havioural responses of spiny lobsters during nocturnal foraging. Spiny lob-
sters hide deep in rocky crevices during the day and emerge to forage at
night. As a result, they were inaccessible to our equipment during the day
and we only conducted experiments at night. During these nocturnal exper-
iments, one person held the observer pole above the lobster while a second
person approached the lobster with the aggressor pole (both scientists were
equipped with snorkelling equipment). The observer pole was used to record
the acoustic response during the approach of the aggressor pole, and after the
pole made contact with the lobster (Figure 2).
Data were collected in three distinct regions of the subtidal zone; each
region was sampled twice, over a two-month interval in the spring of 2008
(Big Fisherman’s Cove, University of Southern California, Wrigley Institute
for Environmental Studies, Santa Catalina Island, CA, USA). The data from
one region were eliminated from the first sampling session due to technical
problems. Water temperature ranged from 16–20◦C. We approached differ-
ent individuals for each trial; however, there are thousands of lobsters living
in this marine sanctuary, so there is a small chance that the same lobsters
were measured twice across the two-month interval.
Experiment 2: response to nocturnal and diurnal approaches in tanks
In the spring of 2008, spiny lobsters were collected at Santa Catalina Island
in baited lobster traps or by hand (CA Department of Fish and Game permit
No. SC-5751). The lobsters were maintained in a large rectangular tank with
a continuous supply of seawater (14–16◦C) and were fed frozen squid every
two days. Twenty-eight females (carapace length range: 68–104 mm) and 15
males (carapace length range 64–111 mm) were used for this study. Lobsters
were transferred individually to cylindrical experimental tanks (152 cm dia-
meter, 81 cm deep); each tank had a burrow made of rocks. Lobsters were
given 15–30 min to acclimate before the trial began. After each trial, we
determined the animal’s sex and measured its carapace length to the nearest
Spiny lobster sounds 243
0.01 mm (Absolute Coolant Proof Digital Calipers IP67, Mitutoyo, Hacienda
Heights, CA, USA).
We used the same aggressor pole setup as in the field experiments. The
‘observer pole’ from the field experiments was separated into an ‘observer
hydrophone’ and an ‘observer camera’ to capture lobster behaviour from a
distance and record the acoustic response before and during the entire trial
(Figure 3). We performed tank trials both at night (2200–0400 h) and during
the day (0900–1800 h). All tank experiments were performed during the first
field session.
Experimental design
As we approached lobsters in both the tank and the field, we presented the
fish, lobster, or blank pole at random. In the tank trials, we randomized the
aggression level of the aggressor pole, and made physical contact with the
lobsters in about half of the trials. In the field, randomization of physical con-
tact was attempted but not always possible due to logistical constraints. For
the field experiments, we approached 98 lobsters. For the tank experiments,
14 lobsters were first sampled during the day, then at night, and the other 29
lobsters were sampled first at night, then during the day.
Analysis of lobster behaviour and sound production
In order to independently analyze the acoustic and behavioural responses of
the lobsters, we digitally separated the video and audio recordings from each
trial (iMovie 4.0.1, Apple, Cupertino, CA, USA; Raven 1.3, Cornell Lab of
Ornithology, Ithaca, NY, USA). Audio recordings were scanned visually and
acoustically for the stereotypical ‘rasp’ spectrogram (settings: Hanning win-
dow, 512 sample window size; 3 dB filter bandwidth at 135 Hz resolution)
(Figure 4) and waveform. Each video trial was watched several times and
the movements of the lobsters were described and quantified (Table 1). Any
trials in which we could not see at least the anterior end of the lobster were
omitted from analysis.
χ2tests were used to determine whether aggressor type, exposure, or
direction of approach relative to antennal position affected lobster behaviour
or rasping during the approach (cf. Table 1 for details). We noted whether the
lobsters made sound during the approach (before physical contact) or during
the attack (once physical contact was made), because this information can be
244 Staaterman, Claverie, & Patek
Figure 4. A typical rasp spectrogram from a field recording. One rasp is indicated between
the dotted vertical lines. The rasp is composed of a series of broadband pulses.
Table 1. The definitions and states of the variables used in the behavioural
analyses.
Variable Definition
Exposure Not exposed =lobster hidden in burrow
Partially exposed =lobster near shelter (<approx. 1 m)
Exposed =lobster distant from any shelter (>approx. 1 m)
Direction of ap-
proach relative
to antennal
position
Match =anterior approach with forward antennae; lateral approach
with antennae pointing out; posterior approach with posteriorly-
pointing antennae
Non-match =anything that is not a match (dorsal approach is always a
non-match)
Behavioural re-
sponse of
lobster
Behaviour 1 =no movement of antennae or other body parts
Behaviour 2 =movement of antennae/antennules towards camera but
minimal leg movement
Behaviour 3 =movement of antennae/antennules and use of legs to
move away from camera
Behaviour 4 =tail flip
Physical contact Contact =model or pole touches the lobster
No contact =nothing touches the lobster
Rasp Present =lobster makes at least one identifiable rasp
Absent =no rasps detected
Spiny lobster sounds 245
used to determine which signal type the lobsters are using (see Discussion).
We also compared the lobsters’ response between the tank and field using
the first field session only. To compare the lobsters’ rasping and behaviour
during the day and at night in the tanks, we performed paired McNemar
tests.
Results
Experiment 1: response to nocturnal approaches in the field
The aggressor type, exposure and direction of approach relative to anten-
nal position did not affect lobster behaviour or rasping during the approach
(Table 2). We did, however, find a difference in lobster behaviour once the
aggressor made physical contact with the lobster (χ2=47.1;df =3;
p < 0.001). After contact was made, lobsters exhibited a tail-flip escape
response 95% of the time (Table 2), whereas when no contact was made,
Table 2. Statistical results of the aggressor experiments across field and tank
trials.
Trial Variable Behaviour Rasp
df χ2df χ2
Field Aggressor type 6 11.79 2 0.35
Exposure 6 7.41 2 0.20
Direction of approach relative to antennal position 3 0.33 1 0.85
Contact 3 47.05∗∗ 1 10.81∗∗
Daytime Aggressor type 6 9.39 2 3.56
tank Exposure 6 2.30 2 1.08
Direction of approach relative to antennal position 3 6.99 1 0.23
Contact 3 4.17 1 1.97
Nighttime Aggressor type 6 2.89 2 0.05
tank Exposure 6 16.35∗2 5.06
Direction of approach relative to antennal position 3 6.61 1 0
Contact 3 5.62 1 1.05
Chi-square analyses were used to test the correlation between the behavioural response and
aggressor variables, as well as the presence or absence of a rasp in response to the aggressor
variables (Table 1). Results are shown as degrees of freedom andchi-square value. ∗p < 0.05,
∗∗p < 0.01.
246 Staaterman, Claverie, & Patek
Figure 5. Defensive behaviour of lobsters depending the presence or absence of physical
contact with an aggressor. The total number of trials is indicated for each bar; data from the
first field session are represented by the hatched portion of the bar and data from the second
field session are represented by the solid portion of the bar. While antennal and leg movement
(dark grey) and tailflips (black) were observed in both treatments, antennal movement only
(light gray) and no movement (white) were only observed in trials with no contact. In both
field sessions, more tail-flips occurred after physical contact with an aggressor.
lobsters tail-flipped only 17% of the time (Figure 5). We also observed a
difference in lobster rasping depending on contact (χ2=10.8;df =2;
p=0.001);lobsters rasped in 56% of the trials when touched, but only
rasped in 18% of the trials when not touched (Figure 6).
Given that the two field sessions were conducted over an interval of two
months, we independently analyzed the data from each session. In the first
session alone, both lobster behaviour (χ2=4.414;df =1; p=0.035)and
lobster rasping (χ2=3.556;df =1; p=0.059)were affected by physical
contact, although the effect on rasping was not significant (Figures 5 and 6).
The second session, however, yielded fewer trials in which we made physi-
cal contact with the lobster, which resulted in insufficient data for analysis.
Regardless of the aggressor type, exposure, and direction of approach rela-
tive to antennal position, we saw a difference in defensive behaviour prior
to physical contact between the two field sessions (χ2=9.18;df =3;
p=0.027), but there was no difference in the acoustic response prior to
physical contact (χ2=0.21;df =1; p=0.645). Lobsters were more
physically active in the second field session (when water temperatures were
warmer).
Spiny lobster sounds 247
Figure 6. Number of trials with a rasp (black) and without a rasp (white), depending on
physical contact by the aggressor (predator, conspecific and blank pole combined). Each bar
indicates the total number of trials; within each bar the non-hatched region includes trials
from the second field session and the hatched region indicates data from the first field session.
There was a significantly higher number of rasps after contact in both experimental datasets.
Experiment 2: response to nocturnal and diurnal approaches in tanks
The aggressor type, exposure (during the day), and direction of approach
relative to antennal position had no significant effect on lobster rasping or
behaviour during the approach (Table 2). The only significant factor influenc-
ing lobster behaviour was the exposure level at night (χ2=16.35;df =6;
p=0.01). Exposed lobsters at night were more physically and acoustically
active than sheltered lobsters at night or during the day. There was no effect
of physical contact on lobster behaviour or rasping in tanks, during the day
or at night (Table 2).
Lobsters in tanks responded more actively to intrusion during the day
compared to the night (McNemar’s test: χ2=20.40, df =6, p < 0.005),
but their rasping behaviour did not change depending on time of day (Mc-
Nemar’s test: χ2=1.5, df =1, p=0.221). During the day, in 51% of
the trials, lobsters pointed their antennae toward the aggressor and retreated
more deeply into their shelters. At night, however, lobsters were less active;
in 59% of the trials, lobsters did not move their legs or antenna.
Comparison of nocturnal behaviour in the tank versus field
Lobsters exhibited a more physically active behavioural response in the field
compared to the tank, both during the approach (χ2=31.3;df =3; p <
248 Staaterman, Claverie, & Patek
0.001)and after physical contact (χ2=22.1;df =3; p < 0.001). We
did not, however, find differences between the acoustic response in the tank
versus the field, during the approach (χ2=0.14;df =1; p=0.70)or after
contact (χ2=2.2;df =1; p=0.14).
Discussion
Interpreting the function of anti-predator signals is rarely straightforward,
given that many are multi-functional, multi-modal and not mutually exclu-
sive. Nonetheless, we can draw conclusions about the function of the spiny
lobster’s rasp from our experiments, both by using existing frameworks for
understanding anti-predator signal function and by examining the use of
these signals in the aquatic environment.
Useful for examining the rasp’s function, Bradbury & Vehrencamp (1998)
offers an organizational framework for the function of what they term ‘en-
vironmental signals’ (Table 3). Environmental signals contain information
about external factors, such as available resources or potential predators, and
can be directed at either conspecifics or heterospecifics. A starting point for
understanding the function of the rasp is to determine whether it is directed
at the potential predator or toward conspecifics.
Environmental signals directed toward conspecifics include: (1) recruit-
ment of conspecifics to food resources, (2) low-risk warnings to conspecifics
that danger is nearby, possibly including information about the type and loca-
tion of predator, (3) high risk warnings to conspecifics during attack that put
the sender at risk, but the risk is offset by a direct benefit to the sender (May-
nard Smith, 1965; Charnov & Krebs, 1975) and (4) distress calls in which
conspecifics are recruited to help during attack (Maynard Smith, 1965; Ro-
hwer et al., 1976).
Although not directly related to anti-predator signalling, spiny lobsters
regularly recruit conspecifics to feeding sites (a feature used by fishermen
who put lobsters in traps to attract more lobsters; Hunt et al., 1986), indicat-
ing a gregarious approach to feeding, and, by association, a potential use for
gregarious anti-predator behaviours. However, our field observations did not
yield any obvious coordinated response to predators – one rasping lobster did
not apparently influence nearby lobsters (which typically continued to forage
during our simulated attacks), thus suggesting that low-risk warnings are un-
likely, although it is possible that the threshold for response was decreased
Spiny lobster sounds 249
Table 3. A number of inter- and intra-specific environmental signals are used
during interactions with predators (Bradbury & Vehrencamp, 1998).
Signal type Modality Sender Receiver Timing Purpose
Inter-specific acoustic kangaroo snake before attack inform predator that
warning rat1(predator) it has been detected
Intra-specific acoustic squirrel squirrel pups before or warn offspring of
warning adults3during attack danger
Inter-specific acoustic starling raptors before or attract second
distress birds4(predators) during attack predator to interfere
with first predator’s
attack
Intra-specific acoustic marmot marmot before or elicit help from
distress pups2parents during attack parents
Inter-specific acoustic insects5mice, spiders during attack startle predator,
startle (predators) induce hesitation
Inter-specific acoustic tiger bats during attack warn of toxicity
aposematic moths6(predators)
visual bivalves, variety of before or highlight weaponry
insects, predators during attack (i.e., spines)
crustaceans7
Examples of inter- and intra-specific warning, distress, startle and aposematic signals, partic-
ularly in the acoustic realm, and their timing relative to predator detection and attack are pro-
vided. References: 1, Randall & Stevens (1987); 2, Blumstein et al. (2008); 3, Davis (1984);
4, Hogstedt (1983); 5, Masters (1979); 6, Hristov & Conner (2005); 7, Inbar & Lev-Yadun
(2005).
(which we did not assess in this study). Furthermore, there was no indication
that the lobsters responded differentially to the predator model and controls
and, thus, were unlikely to be providing information about predator type and
location to conspecifics. Alternatively, when lobsters congregate in burrows
during the day, it is possible that they make use of low-risk warning effects,
such as diluting the probability of attack, influencing group movements to
decrease success of attack or generating chaos to confuse the predator (Caro,
2005), that we did not observe in these experiments. However, we observed
that lobsters in crevices during the day typically retreat further back into the
burrow and brace their bodies against the crevice walls rather than chaoti-
cally or synchronously swimming out and away.
250 Staaterman, Claverie, & Patek
High risk warnings to conspecifics also seem unlikely given that there
are no obvious benefits to helping conspecifics in this system (Maynard
Smith, 1965; Rohwer et al., 1976); spiny lobster larvae cycle through the
ocean for 6–9 months before settling on the substrate and it is unlikely
that co-denning lobsters are kin (Lindberg, 1955; Childress & Hernkind,
1997; Phillips et al., 2006). Lastly, there have been no reports of, and we
have never observed, conspecifics offering assistance during attack, making
distress signals unlikely. Thus, beyond gregarious feeding, using the rasp as
an environmental signal to conspecifics is improbable in this system.
Signals directed toward predators typically (Table 3): (1) warn a predator
that the prey is aware of the predator’s presence and, thus, is more likely
to evade attack (Hasson, 1991; Caro, 1995; Blount et al., 2009), (2) star-
tle the predator, causing the predator to hesitate and providing an opportu-
nity for the prey to escape (Edmunds, 1974; Sargent, 1990; Ruxton et al.,
2004), (3) enhance predator learning and avoidance through aposematic sig-
nals (e.g., noxious chemicals, abrasive sounds, etc.), such that conspicuous
prey are more likely to be avoided (Guilford, 1990; Rowe & Guilford, 1999;
Ruxton et al., 2004), (4) inform the predator that a group of animals is cog-
nizant of its presence, typically through mobbing behaviours and (5) attract
more predators to generate confusion and perhaps interfere with the initial
predator’s attack (reviewed in Chivers et al., 1996).
For the interspecific warning function, the spiny lobsters would have to
warn the predator in advance of the attack, and we found that lobsters rarely
rasped prior to the attack of our model. Physical contact with the model ag-
gressors in our experiment and with the octopus in Bouwma & Herrnkind
(2009) was the critical stimulus for generating the rasp. Thus, we can rule
out interspecific warning signals as a function for the rasp. The mobbing
function is also unlikely, given that most lobster predators are fish that op-
erate in a 3-D environment, whereas lobsters are benthic and lack fine-tuned
locomotor control while swimming. Thus, coordinated mobbing behaviour is
unlikely and, to our knowledge, has not been observed. More commonly, but
something we did not observe with P. interruptus, some spiny lobster species
aggregate into a circular ‘spiny pincushion’ to jointly repel predatory attacks
(Kelly et al., 1999) rather than aggressively attacking the predator.
The attraction of secondary predators is possible, but also improbable.
The rasp is quickly obscured by background noise within 1 m from the
source (Patek et al., 2009). Thus, if the rasp were to function in this way,
Spiny lobster sounds 251
only nearby predators would be attracted to the scene. That being said, the
propagation of olfactory cues is effective and fast in the aquatic environment,
and it would seem more parsimonious to expect that the olfactory cues re-
leased by damaged tissue would attract secondary predators more quickly
and from a greater range. The demonstration of conspecific alarm cues in P.
argus (Shabani et al., 2008) further suggests that the olfactory channel is an
important one during predator interactions.
Thus, using the standard paradigm for anti-predator signal function, the
remaining two functions that may be operational in spiny lobster rasps are
startle and aposematism. Discerning between a startle and aposematic sig-
nal requires several lines of information; it is also important to recognize
that these functions are not necessarily mutually exclusive. To demonstrate
a startle function, it would be necessary to show that predators pause dur-
ing attack and that prey subsequently have a higher probability of escape.
This would require experiments similar to those conducted by Bouwma &
Herrnkind (2009), with the use of a surgical control for silencing the lob-
sters or an alternative mechanism for silencing that did not require surgery.
An aposematic signal requires learning by the predator, such that noxious
stimuli (e.g., coloration, noise or odor) increase the learned association with
unpalatable prey and, therefore, increase avoidance of the prey (e.g., Rowe
& Guilford, 1999; Rowe, 2002; Gamberale-Stille et al., 2009). To test this
function in spiny lobsters, it would be necessary to measure the response of
initially naïve predators over time as they approach silenced vs. stridulating
and palatable vs. unpalatable lobsters.
It is clear from the present study that tank experiments should be ap-
proached with caution, whether in the experiments testing the startle or
aposematic hypotheses. In the field, lobsters actively foraged away from
their dens whereas in the nighttime tank experiments with a short acclima-
tion time, the lobsters hid in their burrows and were minimally responsive to
the aggressor. Previous studies of tank-held lobsters suggest that nocturnal
foraging resumes after an acclimation period of several hours (S.N.P., pers.
observ.), so, at the minimum, future studies should allot more time for the
lobsters to re-establish their nocturnal behaviour patterns in a tank.
Anti-predator signaling in air versus water
It is possible that the existing framework for understanding environmental
acoustic signals does not fully encompass the realm of signalling in aquatic
252 Staaterman, Claverie, & Patek
environments (e.g., Greenstreet & Tasker, 1996). To our knowledge, there
have yet to be any studies of the function and performance of arthropod
acoustic anti-predator signals in the aquatic environment. The fundamental
difference between terrestrial acoustic signals and aquatic signals is due to
the physics of sound and vibration: wavelengths and speed of sound in water
are approximately five times greater than in air. As we mentioned above,
this leads to difficulties localizing sound sources in water, especially for
small animals (Denny, 1993). This also means that animals can sense the
vibrational component of sound (the region called the ‘near-field’; Kalmijn,
1988) over five-fold greater distances in water than in air and that even
animals that lack pressure-sensitive ears can sense most biological acoustic
signals within a meter or more of the sound source.
So how might these physical aspects of the aquatic environment affect
the range of possible functions for anti-predator signals? The paradigm for
acoustic anti-predator signals in the terrestrial environment is that they are
broad-band and, therefore, more difficult to localize and not tuned to parti-
cular receivers (Morton, 1977). These features are relevant in the ocean as
well as in air; however, in water, acoustic signals are inherently difficult to
localize, but, more importantly, virtually any receiver could sense a pulsatile
signal within 1 wavelength of the source, i.e., in the near-field. Furthermore,
beyond one wavelength, the near-field component would be undetectable ex-
cept to the much narrower range of receivers with pressure-sensitive ears.
Given that aquatic crustaceans are not known to have true ears (Budelmann,
1992; Popper et al., 2001) and many lobster predators rely on near-field sig-
nals, this close range region offers a highly effective channel for environ-
mental signalling that is absent beyond a few centimetres in the terrestrial
environment.
What are the implications of the aquatic environment for the function of
the rasp? First, there may not be any need for lobsters to distinguish among
predators or other intruders if all can be assumed to sense the rasp. Sec-
ond, the idea of Bouwma & Herrnkind (2009) that the vibration itself might
loosen the predator’s grip may be especially relevant in a liquid environ-
ment. Indeed, this function might be termed a ‘vibratory escape mechanism’.
Third, the rasp may function simultaneously as a seismic (through the sub-
strate or body), near-field and far-field pressure-wave signal, whereas in air,
the rasp would only be transmitted through the body vibrations and air-borne
pressure waves.
Spiny lobster sounds 253
Lastly, with sufficient agitation and physical grasping of their antennae,
spiny lobsters will automatise one or both antennae (which grow back over
subsequent molts). Visually orienting the predator toward the eye-spots that
are adjacent to the sound-producing apparatus (Figure 1) and vibrationally
orienting a predator toward the extended vibrating antennae may cause the
predator to attack the antennae which can be left behind if necessary, thereby
allowing the spiny lobsters a costly, but effective escape. In air, a rapidly
vibrating antenna would transmit a faint vibrational signal over a millimetre
to centimetre length scale which most organisms would be unable to detect.
A vibrating antenna in the aquatic environment could generate a vibrational
field from centimetres to metres, effective for nearly any aquatic animal’s
sensory capabilities. Perhaps, in the aquatic environment, such ‘acoustic eye
spots’ may be both more common and effective than presently realized.
Conclusions
Our understanding of anti-predator signals is primarily based upon exper-
imental and theoretical research in terrestrial environments, with research
on acoustic anti-predator signals largely conducted on birds and primates
(reviewed in Edmunds, 1974; Bailey, 1991; Greenfield, 2002; Ruxton et
al., 2004; Caro, 2005). While this research has produced a strong organi-
zational framework for understanding anti-predator signal functions (Ed-
munds, 1974; Caro, 2005; Bradbury & Vehrencamp, 1998), we are only be-
ginning to understand whether the same principles apply to acoustic signals
in the aquatic environment.
An additional consequence of the physics of underwater sound production
may be the disproportionate affects of anthropogenic noise on the proper
functioning of these systems. For example, anthropogenic noise has de-
creased the population density (Bayne et al., 2008) and altered acoustic be-
haviour (Slabbekoorn & den Boer-Visser, 2006) of songbirds. In the marine
environment, anthropogenic noise increased the auditory threshold and de-
creased the ability to detect conspecific signals in fish (Vasconcelos et al.,
2007). Marine mammals generated higher amplitude sounds at greater ener-
getic costs to offset high noise levels (Parks et al., 2007; Holt et al., 2009).
Studies of noise pollution in the ocean tend to focus on large vertebrates, but
the effects of anthropogenic noise on invertebrate communities should also
be taken into account when considering the impacts of noise pollution on
animal communication systems.
254 Staaterman, Claverie, & Patek
Our study offers some answers to the function of spiny lobster rasps by
narrowing the range of possibilities to interspecific startle or aposematic sig-
nals while also suggesting future experimental approaches to disentangling
the possible signal functions, including what might be termed ‘acoustic eye-
spots’ and ‘vibratory escape mechanisms’. In the millions of years since its
origin, the spiny lobsters’ acoustic mechanism still poses challenges and of-
fers insights into this untapped frontier of signalling in the sea.
Acknowledgements
We especially thank T. Zack, P. Tompkins and P. Pehl for their extensive field assistance.
Thank you to J. Bell, M. deVries, S. Nunn, M. Patek, V. Patek, D. Elias and L. Shipp for
assistance in the field and for comments on the manuscript. J. E. Baio photographed the
lobsters depicted in Figure 1. We greatly appreciate the constructive comments from two
anonymous reviewers. We also thank the staff at the Wrigley Institute for Environmental
Studies. Funding to SNP was provided by the UC Berkeley Committee on Research Junior
Faculty Research Grant and the Hellman Family Faculty Fund.
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