The effect of substrate on the efficacy of seismic courtship signal transmission in the jumping spider Habronattus dossenus (Araneae: Salticidae)
1 Department of Neurobiology and Behavior, Cornell University, Seeley G.
Mudd Hall, Ithaca, NY 14853 USA
2 Integrative Behaviour and Neuroscience, Department of Life Sciences,
University of Toronto at Scarborough, 1265 Military Trail, Toronto, ONT M16
1A4, Canada
* Author for correspondence (e-mail: doe2{at}cornell.edu)
Accepted 24 August 2004
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Summary |
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Key words: vibration, jumping spider courtship, seismic communication, multimodal, signal design, signal evolution
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Introduction |
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The seismic channel has special relevance to spiders as vibrations are the
predominant modality in most sensory-guided behaviours (Barth,
1998,
2002
;
Foelix, 1996
;
Uetz and Stratton, 1982
).
Spiders are found in virtually all terrestrial (and some aquatic) habitats
and, thus, potentially signal on a diversity of substrates with drastically
different physical properties, especially highly mobile cursorial species.
Given communication via seismic signals, how are signals affected by
substrate heterogeneity, and how do senders and receivers of seismic signals
deal with the effects that the channel imposes on them?
Males of the jumping spider, Habronattus dossenus
(Griswold, 1987), court
females using a complex multimodal display consisting of multiple visual and
seismic signals (Elias et al.,
2003
). Previous work has shown that seismic components in
courtship are crucial in mate choice (Elias
et al., in press
). Like many jumping spiders, H. dossenus
are cursorial and highly ambulatory. They are found predominantly on small
rocks, sand and leaf litter in the Sonoran desert. To investigate the seismic
channel and the constraints it imposes on H. dossenus communication,
we characterized the vibrational properties of these natural substrates using
laser vibrometry and combined this with behavioural trials that quantified
courtship behaviour on the same substrates. We found that the three natural
substrates (rocks, sand and leaves) had different filtering properties. In the
lab, males reliably courted on all substrates, but females mated more often
with males courting on leaves and rejected males on other substrates. These
results indicate a potentially large effect of the communication channel on
mating success and signal evolution.
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Materials and methods |
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Properties of natural substrates
Vibrations were generated using an adjustable phonograph tone-arm (Dual
1019 turntable) with a piezoelectric actuator (Type 350/025/0.60 Strip
Actuator; APC International, Mackeyville, PA, USA) attached at the end. The
actuator was mounted at a shallow angle with its narrow edge (2.5 mm width)
contacting the substrate. As loading the substrate affects its vibrational
properties, the adjustable tone-arm allowed us to vary the load placed on the
substrate to match the mass of a male spider (9.0±1.3 mg, mean ±
S.D., N=44). The load was calibrated by resting the
tone-arm-mounted transducer on a balance (Ohaus E10640; Ohaus, Pine Brook, NJ,
USA). The actuator was calibrated using a laser Doppler vibrometer (LDV,
Polytec OFV 3001 controller, OFV 511 sensor head; Polytec, Waldbronn,
Germany). Test stimuli were synthesized frequency sweeps (System 3;
TuckerDavis Technologies, Alachua, FL, USA) (12500 Hz for rocks
and sand, 11500 Hz for leaf litter). We recorded propagated substrate
vibrations with the LDV sensor head attached to a translation stage (Newport
Model 421; Newport, Irvine, CA, USA) allowing precise movement of the
recording point. The LDV was positioned perpendicular to the substrate
surface. Rocks (N=8) were partially embedded in a dish of desert sand
approximating conditions in the field. Sand recordings were conducted in a
large container (21x26x10 cm) and sand was replaced between
experiments (mass: 7300 g, N=4). For leaf litter, individual leaves
(N=10) were recorded in a dish containing desert sand. Recordings
were taken at 5 mm intervals starting just beyond the actuator tip, five
sweeps at each position. Reflective tape (3M, 0.5 mm2; Scotchlite,
Neuss, Germany) was attached to rocks and leaves as measurement points for the
LDV. Sand was reflective enough to measure without reflective material. The
vibration actuator was applied to a randomly selected position on each sample,
with the provision that for smaller samples the point of stimulation was near
one end to allow sufficient distance for measurements.
We calculated transfer functions for each sample, averaging sweeps at each position using Matlab (The Mathworks, Natick, MA, USA) and present gain curves for vibration velocity (dB relative to input signal). Variance between sweeps at each position was low (mean standard deviation: rock 0.0003 dB, N=20; sand 0.0032 dB, N=6; leaf litter 0.0168 dB, N=18). We show average attenuation with distance by calculating the average gain curves at each distance for the same substrate. We also present attenuation by calculating the total attenuation as change in dB per doubling of distance at different frequencies. This was calculated by averaging the change in intensity for each frequency at 5 vs 10 mm and 10 vs 20 mm.
Behavioural trials
Spiders were randomly assigned to one of three treatments: (1) rock, (2)
sand or (3) leaf litter. Males were randomly paired with a female, and each
individual was only used once.
For rock trials, a large rock (granite, 23x20x7 cm) was used as the behavioural arena to provide sufficient area while limiting courtship to the rock surface. While H. dossenus was not found on this particular rock, its transmission properties are similar to rocks on which the animal was found (Fig. 1, red). An acetate cylinder (12.5 cm diameter, 13.5 cm height) was glued to this rock. For sand and leaf litter trials, a similar sized plastic cylinder was used as the courting arena with either sand (7 cm in depth) or leaf litter atop a small amount of sand (2 cm in depth). An opaque paper cylinder around each setup prevented visual distractions. Surfaces were cleaned with ethanol and the sand stirred between trials to remove chemical cues.
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Females were placed into the arena first. Trials lasted 30 min and were
only included if males courted. Habronattus dossenus courtship
comprises four phases identifiable by stereotyped postures and movements
(Elias et al., 2003). Phase 1
includes only visual signals (Elias et al.,
2003
). Multimodal courtship (phases 24) begins when males
are within approximately one body length of the female, and includes multiple
bouts of prolonged seismic and visual signalling. Three different seismic
signals are identified: narrow-band buzzes (65 Hz + harmonics); broadband
thumps (2001200 Hz); and scrapes (200550 Hz)
(Elias et al., 2003
). We
obtained several measures of courtship (1) copulation success, (2) phase 1
duration and (3) multimodal duration. Results were analyzed with ANOVA
(analysis of variance) and Bonferonni-corrected Tukey post hoc tests,
using Systat (SSI, Richmond, CA, USA).
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Results |
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Average transfer functions were calculated at different distances for each substrate to determine their attenuation characteristics (Fig. 2). On rocks, we sometimes observed an amplification of very low frequencies (>50 Hz), potentially an artefact caused by the rocking of the entire substrate (Fig. 2A,D). Attenuation was frequency dependent with overall attenuation increasing at higher frequencies for all substratum types (Fig. 2). Attenuation was similar for all types at low frequencies (>700 Hz). For rocks and leaf litter, the overall form of the gain curves did not change with distance (Fig. 2A,C) although there was a moderate increase in attenuation with frequency in leaf litter (Fig. 2D). Attenuation in sand was strongly frequency dependent and increased with frequency (Fig. 2B,D).
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Courtship on natural substrates
The proportion of pairs that mated was significantly higher on leaf litter
(N=15) compared with either rocks (N=14) or sand
(N=14) (F2,41=5.945, P=0.005; Tukey
post hoc, leaf litter vs rock, P=0.025; leaf litter
vs sand, P=0.009; Fig.
3). The proportion of males copulating with females was not
statistically different between rocks and sand (P=1;
Fig. 3).
|
Courtship duration did not differ between treatments for either phase 1 (visual only; F2,41=1.640, P=0.206; Fig. 4) or multimodal (phases 24; F2,41=2.866, P=0.068; Fig. 4) courtship. Males did not change their signalling behaviour according to substrate, although there was a non-significant tendency to court less on sand.
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Discussion |
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At distances where courtship naturally occurs, the filtering
characteristics of each substrate were different. Rocks passed low frequencies
but because rocks are inelastic, little energy was transferred from the
stimulator to rocks. The intensity of our stimulator approximated courting
males hence initial attenuation approximates natural conditions. Sand had band
pass properties, attenuating relevant frequencies (especially buzz signals).
Aicher and Tautz (1990)
reported similar characteristics for sand but with a different pass band. This
difference may result from differences in stimulation methods or sand
characteristics particle size and sand composition differ between
beach and Sonoran desert habitats. Leaf litter had a flat frequency response,
although there was considerable variation. Some of this variability may have
been due to heterogeneities in the structure of the leaf, such as veins
(Magal et al., 2000
). We did
not systematically test such effects, but they are likely to be less
pronounced in our system as desert leaf litter is thoroughly desiccated and
leaves were uniformly stiff. In general, previous studies of vibrations in
leaves on plants show similar all-pass filtering properties
(Barth, 2002
;
Magal et al., 2000
;
Michelsen et al., 1982
).
Environmental filtering has important effects on signal design
(Endler, 1992;
Larsen and Michelsen, 1983
;
Romer, 2001
). Considering the
animal's signal bandwidth, rocks (albeit with low amplitude) and leaf litter
are best suited to transmit frequency information while signals on sand would
be transmitted with significant distortion. Therefore, if frequency
information is important, males should signal (and females accept males) on
leaf litter or rocks.
Because the shape and mass of solids affects vibrational properties, we estimated the predictability of seismic transmission as an animal encounters different rocks, leaves or patches of sand. Vibration characteristics were more consistent on sand and leaf litter than rocks. Therefore, these substrates should allow more consistent signal characteristics from one location to the next and, if predictable signal quality is important, sand or leaf litter should be preferred.
Attenuation determines the range of signal transmission. Attenuation in rocks was steep at all frequencies; was more complex in sand, with a steep increase in the overall attenuation with higher frequencies; and was moderate with some increase at higher frequencies in leaf litter. Attenuation was similar at low frequencies for all substratum types. Rocks, however, showed the least overall attenuation with distance but were initially highly attenuated, especially compared with leaves. Therefore, if signal range is important, leaf litter should be preferred.
Successful mating was three times more likely on leaf litter. This is
consistent with our observations that leaf litter transmits signals most
effectively, reliably and extensively. No significant differences were
observed in male courtship effort on different substrates. As males were
confined to a particular substrate in these experiments, however, they do not
address the question of whether males in the field may adopt strategies
favouring courtship opportunities on particular substrates. Alternatively, the
fact that males produce seismic signals only at short distances
(Elias et al., 2003) may itself
be a strategy to compensate for substrate heterogeneity and attenuation.
Future work will address this possibility.
Based on the physical properties of rocks, sand and leaf litter, and the behaviour of spiders on these substrates, we can make inferences as to the salient properties of courtship signals. Frequency content, especially of buzz components, may be particularly important. Broad-band signals (thumps and scrapes) occur at greater distances than do narrow-band signals (buzzes), suggesting that a clear assessment of buzzes is important in mate choice. Furthermore, we can infer from the predictability of transmission properties and female mate-choice behaviour on leaf litter that the reliability (consistency) of the frequency components in signals is important.
Natural selection should optimize signal transmission and reception, and
both signalling behaviour and the receivers' sensory systems should evolve to
match the characteristics of the environment (Endler,
1992,
1993
). Habitat-specific
effects on signal evolution have been studied predominantly in visual signals
in fish (Boughman, 2001
;
Endler, 1991
,
1992
;
Seehausen et al., 1997
) and
birds (Marchetti, 1993
), and
in the acoustic (air-borne) signals in insects
(Larsen and Michelsen, 1983
;
Romer, 1998
), birds
(Richards and Wiley, 1980
;
Ryan and Brenowitz, 1985
;
Wiley, 1991
), and frogs
(Ryan et al., 1990
;
Ryan and Wilczynski, 1991
).
Signals in most modalities, such as visual and auditory, are adapted to a
single medium (e.g. air or water). While signalling conditions may be highly
complex in these modalities, the overall characteristics of the transmission
medium are relatively homogeneous. Animals using seismic signals may regularly
traverse substrates with widely varying physical properties (e.g. rock and
vegetation) each of which could be a potential signalling channel. Seismic
signal evolution may thus be constrained by such low predictability of the
signalling environment. Several strategies are possible. Generalist signals
could be designed to function in all available channels. This `lowest common
denominator' strategy would limit both reliability and information content. A
second strategy would be to specialize in a subset of available channels
increasing signal reliability at the cost of signalling opportunity.
Our data suggest that H. dossenus signals are well-suited to the leaf
litter microhabitat and that males should prefer to signal on leaves. We
detected no pattern in the locations of males and females in the field, but we
cannot control for differences in detectability of animals (to humans) on
different substrates.
Substrate variability and consequent signal specialization may account for
the diversity of seismic signalling behaviour in different
Habronattus species (Elias et al.,
2003, 2004;
Maddison and Stratton, 1988
).
Members of the agilis species group, often found on beaches, signal
with higher intensity and larger bandwidth than H. dossenus
(Maddison and Stratton 1988
;
D.O.E., A.C.M., W. Maddison and R.R.H., manuscript in preparation)
characteristics that are better matched to sand environments particularly if
the temporal properties of signals are important
(Aicher and Tautz, 1990
;
present study). Several Habronattus species can be found in the same
location and each may use signalling channel `resources' differently. This
could explain the large diversity observed in seismic signals and signalling
mechanisms. Such `signalling microhabitat' partitioning could also be a
mechanism underlying the intense speciation observed in the
Habronattus genus (Griswold,
1987
; Maddison and Hedin,
2003
; Masta and Maddison,
2002
). In addition, because courtship in these animals is
multimodal and there is a high degree of coordination between visual and
seismic signals (Elias et al.,
2003
), the interaction between signal components in different
modalities may be important in microhabitat use and signal design. Optimal
habitats for these two signal modalities may not be identical. Future work
will examine the possibility that substrate effects on signal use are modified
by interactions between visual and seismic modalities.
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Acknowledgments |
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