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First published online January 31, 2007
Journal of Experimental Biology 210, 614-619 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.001362
Flexible information sampling in vibrational assessment of predation risk by red-eyed treefrog embryos
1 Department of Biology, Boston University, Boston, MA 02215, USA
2 Smithsonian Tropical Research Institute, Apartado 2072, Balboa, Panama
3 Department of Aerospace and Mechanical Engineering, Boston University, Boston,
MA 02215, USA
* Author for correspondence (e-mail: kwarken{at}bu.edu)
Accepted 5 December 2006
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Summary |
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Key words: hatching, predator detection, playback, prey uncertainty, seismic, vibration, Leptophis ahaetulla, Leptodeira annulata, Agalychnis callidryas
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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; Warkentin,
1995), fishes (Kusch and
Chivers, 2004; Wedekind,
2002), reptiles (Moreira and
Barata, 2005)] and have probably evolved multiple times. Some
embryos respond to chemical cues (e.g.
Chivers et al., 2001;
Johnson et al., 2003) and
others to vibrational cues from predators
(Warkentin, 2005). These
responses provide a natural context in which to examine the sensory and
information-processing capacity of embryos. We examined information sampling
by frog embryos that use substrate-borne vibrations to cue behaviorally
mediated premature hatching.
Risk assessment is critical for inducible defenses
(Tollrian and Harvell, 1999)
and requires that animals distinguish predator cues from benign-source stimuli
(noise). This is fundamentally a signal detection problem
(Bradbury and Vehrencamp, 1998;
Macmillan and Creelman, 2005).
For any cue property that an animal could assess, overlap is likely between
the value of that property in predator cues and noise. Such overlap occurs in
communication signals selected to be conspicuous
(Endler, 1992) and is likely
greater for cues from predators or prey selected for crypsis
(Getty and Krebs, 1985;
Wilcox et al., 1996). Thus,
any criterion used to distinguish predator cues will result in errors,
including false alarms (unnecessary defense) and/or missed cues (failure to
defend). The criterion may be adjusted depending on the cost of each error
type, but there is a trade-off. For instance, the criterion may be relaxed to
minimize fatalities from missed cues; however, this increases the incidence of
false alarms. Strong selection against both missed cues and false alarms
should favor sampling strategies that accept additional costs in order to
improve accuracy of risk assessment. Prey could use more information to
ameliorate the trade-off in two ways. (1) They could assess multiple,
independent properties of predator cues simultaneously. Overlap with noise
should decrease with each property added, but the required neural processing
likely increases as well. (2) They could base their response on a larger
sample of the cue property. Increased sampling improves the precision of
estimates, potentially reducing overlap. However, if a hunting predator is the
source of cues, increased sampling before defense increases risk.
We examined information sampling by frog embryos that use substrate-borne
vibrations to assess predation risk. Vibrational sensitivity is evolutionarily
ancient and phylogenetically widespread
(Hill, 2001), and a diverse
range of prey use vibrations to cue antipredator behavior
(Tautz and Markl, 1978;
Bacher et al., 1997;
Burger, 1998;
Warkentin, 2005;
Castellanos and Barbosa, 2006).
Some show immediate defensive responses to vibrations, and the behaviors
involved, such as ceasing to call (Lewis
and Narins, 1985; Narins,
1990), freezing (Burger,
1998) or changing posture
(Gnatzy and Kämper,
1990), appear low cost. In these cases, response criteria may have
been relaxed to reduce missed cues and, if so, we expect high false alarm
rates, i.e. defensive responses to non-predator vibrations. There may also be
a selective premium on response speed, if risk increases steeply with sampling
time prior to defense. If so, the cue properties used should be amenable to
rapid assessment, e.g. frequency or amplitude. Assessing larger-scale temporal
properties requires more time and, in the case of predator vibrations, more
risk, although temporal properties of vibrations appear more robust to
degradation than frequency properties and more important in intraspecific
communication (Michelsen et al.,
1982; Randall,
1995; Hill, 2001;
Virant-Doberlet and Cokl,
2004).
Study system
Red-eyed treefrogs, Agalychnis callidryas Cope 1862, lay eggs on
vegetation over ponds and swamps, and tadpoles fall into the water upon
hatching. Embryos hatch as much as 30% prematurely – both earlier and
less developed – to escape from egg-eating snakes, wasps and other
dangers (Warkentin, 1995;
Warkentin, 2000;
Warkentin et al., 2001;
Warkentin, 2002). Although in
many animals hatching is a slower and largely enzymatic process
(Carroll and Hedrick, 1974;
Yamagami, 1981;
De Vries and Forward, 1991), in
A. callidryas, as in some other frogs and fishes
(Brown and Iskandar, 2000;
Griem and Martin, 2000),
hatching is a rapid behavioral process. Hatching is also an irreversible
life-stage transition that exposes hatchlings to a new suite of aquatic
predators. Premature hatchlings are substantially more vulnerable than
full-term hatchlings to aquatic predators
(Warkentin, 1995;
Warkentin, 1999a). Thus, the
cost of false alarms is high and, as with missed cues, exacted as increased
mortality.
Escape hatching can be induced by vibrations recorded from snake attacks
(Warkentin, 2005), and two
temporal properties, vibration duration and interval or spacing, affect the
hatching response (Warkentin et al.,
2006b). Since assessing temporal properties requires time and
entails risk, we asked two questions: (1) how much time do A.
callidryas devote to sampling vibrational cues before hatching and (2) do
they use a fixed or flexible sampling strategy? Information from duration and
interval properties accrues with cycles of vibration and silence. Thus, a
given time sample contains more of such information if cycles are short rather
than long. By contrast, risk appears to accrue with time, not vibration
cycles, as snakes consume eggs (K.M.W. and A.T.D., manuscript in preparation).
Embryos might use a fixed sampling rule, for instance based on a time period,
number of vibrations or simply amount of stimulation. Alternatively, they
might balance the potential cost of sampling with the value of information,
adjusting sampling period with the rate at which information accrues. To
assess sampling, we compared the time course of hatching for eggs exposed to
vibrational stimuli that elicit similar levels of hatching
(Warkentin et al., 2006b) but
differ in cycle length, i.e. the rate at which temporal pattern information
accrues. We also examined videotapes of snake attacks on egg clutches to
assess the latency of hatching and duration of attacks.
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Materials and methods |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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), but
differ across an order of magnitude in cycle length (= vibration duration +
interval), while holding duty cycle (= vibration duration/cycle length) and
total energy constant. Vibrations had approximately rectangular amplitude
envelopes and were matched for peak acceleration. Stimuli were played to egg
clutches for 5 min, during which we counted the number of hatched embryos
every 10 s. Following stimulation, we counted hatchlings every 10 s for 1 min,
then every 60 s for an additional 4 min.
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). We
used A. callidryas egg clutches collected from Ocelot Pond and tested
in an open-air laboratory in Gamboa. Clutches were mounted on plastic cards
for support, maintained over water in plastic cups and misted several times
daily to prevent desiccation. We returned all hatchlings to their pond after
experiments. This research was conducted under permits from the Panamanian
Autoridad Nacional del Ambiente, and approved by the Smithsonian Tropical
Research Institute and by the Institutional Animal Care and Use Committee of
Boston University.
Vibrations were generated by an electrodynamic minishaker (Model 4810;
Bruel and Kjær, Nærum, Denmark) controlled by Canary (v. 1.2.4,
Cornell Laboratory of Ornithology, Ithaca, NY, USA) on a Macintosh G4 laptop
computer, via an external sound card (MSE-U33HB; Onkyo, Osaka, Japan)
and a custom-made amplifier designed to have a flat frequency response from DC
to 5 kHz (E. Hazen, Boston University Electronic Design Facility). Vibrations
were transferred to the eggs via a minishaker-clutch interface (MCI)
of stainless steel tines inserted into the clutch between eggs. Eggs were
vibrated vertically, and hatchlings fell into a tray of aged tapwater. Minimum
initial clutch size was 20 eggs, and all clutches fit within the MCI tine
field. After MCI insertion and any hatching induced by that procedure, we
allowed five hatching-free minutes before the start of a playback. We used
each clutch in only one trial, and if 
25% of a clutch hatched during
set-up we did not use it. To limit variation in hatching response due to egg
development and diel cycle, all playbacks were conducted from
20:30–05:30 h using clutches that were 5 days old at the start of the
playback session, i.e. laid six nights before the playback night. Development
is highly synchronous within and among clutches laid at the same time and
developing together at a site (Warkentin,
1995; Warkentin,
1999b).
Analysis of hatching response to playbacks
The total proportion of embryos hatched was not significantly different
across the four stimuli (Kruskal-Wallis test: H3=0.672,
P=0.88; mean ± s.e.m., proportions hatched were
0.48±0.09, 0.49±0.07, 0.48±0.07 and 0.40±0.08 for
1.1 through 11 s cycles, respectively). Because we were interested in the
timing of hatching, not the proportion hatched, we restricted subsequent
analysis to only embryos that hatched during the experiments. We used two Cox
regression models to test for an effect of cycle length on the amount of time
and the number of cycles prior to each embryo hatching using the PHREG
procedure in SAS v. 8.00 (Allison,
1995; SAS Institute,
1999). We included clutch in the model, as siblings in an egg mass
are not independent. However, the survival analysis did not allow nesting
clutch within cycle length. This is conservative with respect to the test for
a cycle length effect, as some of its variance may be attributed to clutch. We
also compared two points of interest in the hatching response using
Kruskal-Wallis tests. (1) We compared latency from the start of the vibration
playback until the first embryo hatched from each clutch as a measure of the
minimum stimulus time, and cycles of vibration, necessary to elicit hatching.
This is the value most directly comparable to hatching latency in snake
attacks. (2) We compared the point of peak or modal hatching (i.e. maximum
hatching rate) as a central estimate of the requirements to elicit hatching.
The hatching peak is near the point at which 50% of embryos that would hatch
had hatched, and 25–55 s before the mean hatching time. Mean hatching
time may, however, be overestimated because we counted hatchlings only every
60 s in the last 4 min.
Hatching latency in snake attacks
As part of another study (K.M.W. and A.T.D., manuscript in preparation), we
videotaped 22 attacks on 5-day-old A. callidryas egg clutches by two
species of snakes (11 attacks per species, by five individual Leptophis
ahaetulla L. and six individual Leptodeira annulata L.). Snakes
were collected from ponds near Gamboa, housed in an ambient temperature and
humidity laboratory in Gamboa (Warkentin,
2005) and offered egg clutches hung over trays of water in their
home cages. Videotapes were recorded under infrared illumination with Digital
8 cameras (DCR-TRV120 and TRV350; Sony, Tokyo, Japan). For each attack we used
the time code recorded on the videotape to measure latency of embryos to begin
hatching. We considered tongue, snout or mouth contact of the snake with the
clutch that was followed by biting to be part of an attack and assessed
latency as the time from the first such contact until the first tadpole
hatched. For 19 attacks (nine by L. annulata, 10 by L.
ahaetulla) we recorded the duration from first contact until all embryos
had hatched or been eaten. In three attacks the snake stopped feeding while a
few eggs remained on the clutch, unhatched; we do not include these attack
durations. We also calculated escape hatching success of 5-day-old clutches in
11 L. ahaetulla and 15 L. annulata attacks as the proportion
of attacked embryos that were found as tadpoles in the water after the attack;
not all of these attacks were videotaped. Other data on snake behavior will be
reported elsewhere (K.M.W. and A.T.D., manuscript in preparation).
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Results |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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2=49.38, P<0.0001; clutch effect,
2=4.36, P=0.037). Considering hatching as a function
of cycles of vibration, there was an even stronger effect of cycle length
(Fig. 1B) (cycle length,
2=344.9, P<0.0001; clutch, 2=3.66,
P=0.056). Embryos sampled fewer cycles of long-cycle stimuli before
hatching, and the entire hatching curve was shifted to occur over
progressively more cycles as those cycles became shorter. The minimum
requirements for induced hatching in playbacks, measured by hatching latency
as in attacks, varied with cycle length. Embryos sampled more time
(vibrational stimulation) but fewer cycles (information) as cycles increased
in length (Fig. 2A)
(Kruskal-Wallis tests: time, H3=8.473, P=0.037;
cycles, H3=17.604, P=0.0005). Similarly, the
modal hatching point varied; embryos sampled 240% more time but 76% fewer
cycles as cycles increased an order of magnitude in length
(Fig. 2B) (time,
H3=19.442, P=0.0002; cycles,
H3=26.640, P=0.0001).
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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;
Warkentin, 2005). The
vibrations are caused by the snake directly moving eggs, mostly by biting
them; thus they indicate imminent high risk of being eaten. Despite this,
embryos rarely hatch instantly in snake attacks. On average hatching began at
16 s, and in one videotaped clutch, embryos waited over a minute before
beginning to hatch. Some waited longer, as snakes continued to feed, so that
all eggs were not gone from the clutch until, on average, almost 5 min after
the snake began its attack. The hatching response of A. callidryas to
synthetic vibrational stimuli was similarly measured, with many embryos taking
minutes to hatch. Moreover, both the time course of hatching and the number of
vibrational cycles sampled before hatching varied with cycle length, revealing
that the embryos employ a flexible strategy when sampling vibrations to assess
risk.
Why do attacked embryos not hatch immediately?
Attacked embryos clearly do not hatch as rapidly as they are able. Embryos
hatch by performing specific movements and exit the egg in under a second
(K.M.W. and M.S.C., personal observation); in two of our videotaped attacks,
the first embryo hatched in 0.17 and 0.97 s. In both attacks and vibration
playback trials, embryos remained basically inactive until just before
hatching, then rapidly pushed out of their capsules. Thus, they experienced
many seconds to minutes of stimulation before initiating hatching
behavior.
In attacked clutches, the risk is highest and stimulation may be most intense close to the predator, but the risk is somewhat less immediate and stimulation may be weaker at the far side of the clutch. This might contribute to the distribution of hatching times in attacks, with embryos hatching only as the predator approaches them closely. Spatial heterogeneity in risk and/or cues cannot, however, explain the delay before the first egg – potentially the egg receiving the strongest or clearest cues – hatches. Furthermore, our vibration playback apparatus was designed to deliver vibrations uniformly across the clutch. Thus, the latency to hatch and distribution of hatching times in playback trials reflects behavioral decisions of embryos under spatially homogeneous stimulus conditions.
We suggest that the relatively long delay before attacked A.
callidryas initiate hatching represents a period of information sampling.
This is consistent with strong selection against both false alarms and missed
cues (Warkentin, 1995;
Warkentin, 1999a;
Warkentin, 2000), which puts a
premium on correct decisions. It is also consistent with both the cue
properties that red-eyed treefrog embryos use to assess risk and the variation
in vibrations caused by their predators
(Warkentin, 2005).
Frequencies, particularly high frequencies, can be assessed rapidly, but
larger-scale temporal properties, such as the duration and spacing of
vibrations used by A. callidryas
(Warkentin et al., 2006b),
require more time to assess. Moreover, the variation in temporal properties of
vibrations in attacks and their overlap with those in rain storms mean that
information about multiple duration and interval values is required for good
discrimination (Warkentin,
2005). Long sampling times may be an inevitable cost of reasonable
accuracy with such cues.
The vibration sampling strategy of A. callidryas embryos
As with absolute hatching time, the variation in hatching timing across
stimuli is not consistent with embryos simply hatching as fast as possible
after some minimum required stimulation. Stimuli were matched for frequency,
amplitude and total energy to provide a consistent amount of stimulation. They
were also matched for duty cycle (ratio of vibration duration to cycle length)
and the longest cycle length was shorter than the shortest mean latency to
hatching (11 vs 25±4 s). Thus, differences in hatching timing
do not reflect differential buildup of stimulation within cycles. Finally, all
stimuli elicited similar levels of hatching and hatching peaked well before
playbacks ended. Thus, the variation in embryo behavior is not due to
differences in either the amount of simulation provided or the overall
salience of the stimuli.
The variation in hatching timing is consistent with a sampling period
adjusted to balance the value and cost of information
(Fig. 3). In predator attacks,
the largest cost of information is the risk of being killed, which increases
with the pre-defense delay. For A. callidryas, although risk accrues
at different rates in attacks by different types of predators [e.g. snakes and
wasps (Warkentin et al.,
2006a)], the substantial overlap in temporal properties of
vibrations across predator types (M.S.C., J.G.M. and K.M.W., unpublished)
makes it reasonable to consider risk simply a function of time, independent of
cycle length. The value of the information is the extent to which it reduces
two potentially lethal errors: missed cues that allow predators to consume
eggs, and false alarms that expose vulnerable premature hatchlings to aquatic
predators (Warkentin, 1995).
Agalychnis callidryas use vibration duration and spacing to inform
their hatching decision (Warkentin et al.,
2006b). Information from these temporal properties is expected to
accrue with cycles of vibration in some diminishing function, such that each
cycle of the same pattern carries a smaller increment of information. Under
such circumstances, information sampling prior to hatching should decline with
increasing cycle length, as each increment of information entails more risk in
longer cycles, but not to the point where sampling time remains constant. At
some point, embryos should pay higher costs in order to get sufficient
information (Fig. 3). The
hatching behavior of A. callidryas appears consistent with such a
model.
|
). That response was close to the escape success in snake
attacks, and other vibration playbacks elicit near 100% hatching (M.S.C.,
J.G.M. and K.M.W., unpublished). Despite the lower hatching response here,
latency is not much longer with our shortest-cycle stimulus than in snake
attacks (25±4 vs 16±3 s), and latencies for all but the
longest-cycle stimulus are within the range found in snake attacks. Indeed,
because we recorded hatching only every 10 s in our playback trials, we
slightly overestimate hatching latency. Moreover, with all but our
longest-cycle stimulus, the cumulative hatching curve leveled off within the 5
min playback period (Fig. 1).
This is comparable to the hatching pattern under snake predation; attacks
lasted about 5 min before all eggs had hatched or been eaten. These
similarities suggest that vibration playbacks are a reasonable abstraction of
the snake–egg predator–prey interaction with which to explore the
behavioral decisions and information processing abilities of embryos.
Red-eyed treefrog embryos adjust their hatching timing to balance a
trade-off between egg- and larval-stage risks, and similarly context-dependent
hatching timing has been shown in other taxa
(Sih and Moore, 1993;
Chivers et al., 2001;
Li, 2002;
Wedekind, 2002;
Kusch and Chivers, 2004;
Moreira and Barata, 2005).
Here we show that A. callidryas embryos also modulate the amount of
information on which their hatching decision is based depending on the amount
of time, or risk, entailed in gathering that information. This demonstrates a
second level of environmental sensitivity in the embryos' behavioral
repertoire. This may be ecologically important, given the multiple risks and
high levels of mortality faced by early life stages, and suggests that embryo
behavior may be more complex than previously recognized.
Studying risk assessment by prey
To assess risk, prey must distinguish salient cues from noise, in any
sensory modality. Elucidating the information they use, and the decision rules
they apply to it, is a fundamental problem in animal behavior. Because sounds
can be readily recorded, manipulated and played back to animals, bioacoustics
has made great contributions to our understanding of animal behavior
(Bradbury and Vehrencamp,
1998). Hunting predators, however, are often silent. Nonetheless,
if they move, they produce vibrations, and there is growing evidence that
these vibrations carry information to prey. Vibrations are amenable to
recording, manipulation and playback techniques similar to those in
bioacoustics. These techniques facilitate experiments that allow signal
detection theory and information theory to be applied to studies of risk
assessment. Vibration-cued antipredator responses offer an excellent
opportunity to explore the information processing and behavioral decision
rules that animals use in defense.
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Acknowledgments |
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