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Early interactions with adults mediate the
development of predator defenses in guppies
Article in Behavioral Ecology · January 2008
DOI: 10.1093/beheco/arm111 · Source: RePEc
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Behavioral Ecology
doi:10.1093/beheco/arm111
Advance Access publication 15 November 2007
Early interactions with adults mediate the
development of predator defenses in guppies
Ben B. Chapman, Lesley J. Morrell, Tim G. Benton, and Jens Krause
Institute of Integrative and Comparative Biology, University of Leeds, Leeds LS2 9JT, United Kingdom
P
redation is a powerful selective force, contributing significantly to mortality in many ecological systems. This means
that the development of effective antipredator defenses can
be of huge importance to individual fitness. Antipredator
defenses have been shown to have a strong genetic basis
across a wide range of taxa (damselflies: Stoks et al. 2003; fish:
Huntingford and Wright 1993; birds: Veen et al. 2000; amphibians: Gallie et al. 2001). However, the development of
defenses can be costly (Tollrian and Harvell 1999), and so
when predation risk varies temporally or spatially it may be
adaptive for prey organisms to phenotypically respond to
changes in the environment to avoid incurring such costs where
unnecessary. This is known as phenotypic plasticity (Pigliucci
2001). Phenotypic plasticity can take a variety of forms, including morphological (Olsson et al. 2007), life historical (Evans
et al. 2007), and behavioral (e.g., learning: Svanback and
Bolnick 2007).
Learning is an important component in the acquisition of
antipredator defenses. Exposing coho salmon fry Oncorhynchus kisutch to a predator early in life led to a 75% survival
rate in the subsequent encounter, compared with a 46% survival rate for naive fry (Patten 1977), highlighting the importance of early experience in successfully evading predators.
More recent work supports the importance of learning across
a range of taxa (e.g., birds: Maloney and Maclean 1995, fish:
Kelley and Magurran 2003, mammals: Mineka et al. 1984).
Inducible morphological defenses have been documented
across a variety of both vertebrate and invertebrate taxa
(Tollrian and Harvell 1999). For example, experience of predator cues induces morphological defenses in Daphnia
(Laforsch et al. 2004) and crucian carp Carrasius carrasius
(Bronmark and Miner 1992). Carp exposed to piscivorous
pike Esox lucius develop deeper bodies, which lead to in-
Address correspondence to B.B. Chapman. E-mail: bgy4b2c@leeds.
ac.uk.
Received 4 July 2007; revised 30 August 2007; accepted 28
September 2007.
The Author 2007. Published by Oxford University Press on behalf of
the International Society for Behavioral Ecology. All rights reserved.
For permissions, please e-mail: journals.permissions@oxfordjournals.org
creased handling times for pike and a higher probability of
escape for prey. Such individuals also constitute a less desirable prey phenotype than more fusiform carp (Nilsson et al.
1995).
Early experience is therefore profoundly important in the
development of antipredator defenses, but the mechanism for
this is unclear as when faced with highly effective predators,
naive juveniles may have little opportunity to hone their responses to predator attacks. Some evidence suggests that
adult/juvenile interactions may constitute a proximate mechanism by which juveniles can develop antipredator defenses
prior to direct experience with a predator (Goodey and Liley
1986; Tulley and Huntingford 1987). In sticklebacks (Gasterosteus aculeatus), fry from high-predation populations raised
with parental care showed a significant improvement in their
antipredator responses compared with fry raised with no care
(Tulley and Huntingford 1987).
The Trinidadian guppy has no such system of parental care,
and neonates respond to conspecific adults by displaying a variety of antipredator behaviors (Magurran and Seghers 1990).
Adults behave agonistically to juveniles and have been shown
to prey on fry (Magurran 2005), suggesting that adults may
behave as proxy predators in this system and provide juveniles
with their first opportunity to develop antipredator skills. In
support of this idea, Goodey and Liley (1986) demonstrated
that juveniles with early experience of encounters with adults
had a significantly improved escape ability later in life. How
this enhanced escape ability develops is unknown. Here, we
investigate the nature of the defenses induced by adults in fry
by rearing guppies in the presence and absence of adults. We
predict that juveniles with early experience of adults will modify their shoaling behavior (a common antipredatory strategy
in fish; Krause and Ruxton 2002) and respond more quickly
to a fright stimulus. We also examine the impact of early experience on morphological development. Previous work has
shown that olfactory cues are sufficient to trigger the development of morphological defenses in a number of species
(Tollrian and Harvell 1999). We investigate the type of
cues that ‘‘activate’’ plasticity in this system by rearing fry in
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Antipredator defenses in many species have been shown to exhibit phenotypic plasticity in response to variable predation risk.
Some evidence suggests that in certain species adults act as proxy predators, triggering the development of adaptive defenses in
juveniles where interaction with a predator is unlikely to occur. However, almost nothing is known about how adult/juvenile
interactions mediate plasticity. Here, we examine the nature of the antipredator defenses that develop in Trinidadian guppies as
a function of early social experience and investigate the importance of different types of cue (physical, visual, and olfactory) by
rearing juveniles under 3 different social conditions. In the first, only juveniles are present; in the second, only visual and
olfactory interaction occurs between adults and juveniles; and in the third, adults physically interact with juveniles. Our analyses
show that juveniles reared in the physical presence of adults spend significantly less time shoaling with adults than fish from
other treatments in an adult versus juvenile shoal-choice trial. Further, we show that juveniles with experience of adult aggression have a decreased response latency to a simulated avian predation attempt and travel a greater distance in the first 5
frames of movement after the simulated strike. Finally, juveniles reared with physical experience of adults developed relatively
deeper bodies and were significantly shorter in standard length than guppies reared without physical experience of adults. Key
words: development, inducible defenses, phenotypic plasticity, rearing experience, social environment. [Behav Ecol 19:87–93 (2008)]
Behavioral Ecology
88
3 different treatments: with physical experience of adults, with
visual and olfactory adult cues but no physical mixing, and in
the absence of adults.
METHODS
Study population and maintenance
Rearing conditions
We captured juveniles of 10-mm size (mean 6 standard deviation [SD]: 8.09 6 0.09) using a dip net and assigned them
randomly into one of 3 different rearing conditions. This
meant that fry were unlikely to be from the same brood, ruling
out the importance of any maternal effects. In the first treatment, 4 of these juveniles were reared in the presence of 2
adult males. In this ‘‘mixed’’ treatment, adults and juveniles
were free to interact physically. Previous work has shown that
agonistic and competitive encounters between adults and juveniles when allowed to interact physically were commonplace
(Goodey and Liley 1986); our observations confirmed this. In
the second treatment (to be referred to as ‘‘v and o’’), we were
interested in isolating the impact of visual and olfactory interactions and reared 4 neonate fry separated from 2 adult males
by a transparent perforated screen. To ensure the transmission of olfactory cues, water was pumped from the adult compartment to the juvenile compartment. This occurred in all
treatments to control for flow patterns. In the third, control
treatment, 4 neonate fry were reared in the absence of adults
(to be referred to as the ‘‘all juvenile’’ treatment). Although
density differed among treatments, the size of the tanks rendered any variation negligible.
Each rearing tank was of the same design: tanks were 50 3
20 3 20 cm, had a gravel substrate, and had opaque sides to
minimize disturbance and to mimic natural conditions. Water
depth was kept constant at 12 cm deep. Tanks were divided
into 2 compartments by a transparent, perforated plastic
screen (see Figure 1). In each tank, the larger compartment
(30 3 20 3 20 cm) contained a free-floating circular plastic
feeding ring (diameter ¼ 8 cm) with 2 square polystyrene
floats (2 3 2 3 1 cm) opposite to one another, which floated
on the surface of the water. In addition, a strip of green plastic
mesh (3 3 25 cm) was tied loosely into a knot and placed on
the substrate to provide a refuge for the juvenile guppies. The
larger compartment contained 4 fry in each rearing treatment
and 2 additional adult males in the mixed treatment. In the
mixed and all juvenile treatments, the smaller compartment
was unoccupied; in the v and o treatment the smaller compartment contained 2 adult males. A foam filter was fixed to
the side of the smaller compartment with silicon sealant.
A length of hosing (34 cm) was attached to the outlet pipe
of the filter with silicon sealant and placed so that the open
Figure 1
Experimental set up. Four juvenile guppies are reared in
compartment 1, separated by a transparent perforated screen (TS)
from compartment 2. A pump (P) in compartment 2 pumps water
to compartment 1 through a length of hosing, ensuring the
transmission of olfactory cues. Food in the compartment 1 is
aggregated in a floating feeding ring (FR), and fry are provided with
a mesh refuge (R). The 3 treatments differ in the following way: 1)
mixed has 2 adults in compartment 1; 2) visual and olfactory has 2
adults in compartment 2; and 3) all juvenile has no adults in the
tank.
end was below the water surface in the larger compartment.
This pumped water from the small compartment to the larger
one and ensured that olfactory cues were transmitted from
the adults to the juveniles in the v and o treatment.
We reared 14 replicates of the mixed and all juvenile treatments and 11 replicates of the visual and olfactory treatment
for a total of 47 days each between April and December 2006.
Replicates had staggered start dates, with one replicate of each
of the 3 treatments beginning at a given time to control for
any effect of start date. On the start date of a set of replicates,
12 fry and 4 adult males were captured from the source population and randomly assigned to rearing treatments. Individuals’ body lengths were measured and recorded. Adult males
only were used: in high-predation populations, guppies segregate by sex, with more males tending to occupy the shallower
waters. Juveniles are hence more likely to have a higher frequency of encounter with males than with females (Croft et al.
2006). In each rearing regime, fish were fed daily ad libitum
with dried flake food. Food was sprinkled into the feeding
ring located on the water surface in the larger compartment
in all treatments. This aggregated the food resource spatially,
encouraging competitive and agonistic interactions to occur
between adults and juveniles in the mixed treatment. After
47 days of rearing, we recorded the final tank density.
Experimental assays
After 42 days, we carried out 2 behavioral assays. The first was
a binary shoal-choice test that took place on day 42; the second examined individual escape responses to a simulated
avian predation attempt (day 47). Finally, individuals’ body
lengths were measured and recorded. A subset of the fish were
photographed for morphometric analysis (see below), and all
were returned to a stock tank.
Shoaling tendency
To investigate shoaling behavior, focal fish were allowed to
swim freely in a tank containing 2 choice chambers; one
contained 2 adult males and the other 2 juvenile stimulus
fish. All stimulus fish were taken from the original stock
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All fish used in this experiment were the descendents of
wild-caught guppies sourced from the Tacarigua River in the
northern mountain range of Trinidad in 2005 (Trinidad national grid reference: PS 787 804; coordinates: 1040.736#N
06119.168W). This site is characterized as a high-predation
locale (Croft et al. 2006) due to the presence of a variety
of aquatic piscivore predators, particularly the pike cichlid
Crenicichla alta.
Stockfish were reared at the University of Leeds in a 100 3
100 3 25 cm tank with gravel substrate and clumps of moss to
provide refuge for fry. Controlled temperature (28 C) and
lighting conditions were maintained (18 W overhead fluorescent strips set on a 12-h light/dark cycle). Water depth was
kept constant at 13 cm. All fish were fed daily ad libitum with
dried flake food.
Chapman et al.
•
Early experience and predator defenses
Response to a simulated threat
Escape response trials took place in a 20 3 20 3 20 cm tank
with opaque sides. Water depth was kept at 2 cm to minimize
vertical movement in escape responses, a depth within the
range of which juveniles would be likely to experience in
the wild. Focal individuals were introduced into the arena
and allowed 5 min to acclimatize. After this, a plastic stick
(diameter ¼ 0.8 cm, length ¼ 50 cm with Bluetak attached
to the tip) was dropped vertically from 18 cm above the water
surface within 5 cm of the focal fish to mimic an avian predation attempt and elicit an escape response (Ward et al.
2004). This was repeated for each of the 4 fish in each of
the rearing treatments. Trials were recorded at 25 frames/s
using a Sony DSR-PD100AP video camera suspended 32 cm
above the top of the tank. Variables measured were an individual’s latency to respond (frames), the distance traveled in
the first 5 frames of movement (millimeters), and the maximum speed achieved in the first 10 frames (millimeters per
frame). Video was transferred to .avi using vdub freeware
(http://www.virtualdub.org/) and analyzed frame by frame
using ImageJ (also available free at http://rsb.info.nih.gov/
ij/). Each fish was subjected to this stimulus only once.
Morphological measurements
After the behavioral assays, we measured the body length of
the fish and placed it in an individual container for morphometric analysis. To investigate whether early experience of
adults triggered the development of differential morpholo-
Figure 2
Juvenile guppy with standard length and caudal base depth shown.
gies in juvenile guppies, we calculated the relative body depth
of test fish after 47 days.
An image of each fish was captured using a JVC TK1280E
color video camera using the program Imagedok 2.0 (Kinetic
Imaging Ltd, Liverpool, United Kingdom). The relative caudal base depth of each fish was calculated by dividing caudal
base depth by standard length (Figure 2). The standard
length is the distance between the fish’s snout and the point
at which the spine meets the base of the caudal fin. We defined ‘‘depth’’ as the distance from the anus to a point on the
dorsal edge that could be located by drawing a line perpendicular to the line of standard length through the anus and
the dorsal edge. Distances were calculated using tpsDIG (available free at http://life.bio.sunysb.edu/morph/).
Statistical analysis
All data were checked for deviations from normality and homoscedasticity. Only individual response latency data failed to
conform to parametric model assumptions; when tank means
were calculated, the necessary assumptions were met. In this
case, we used a general linear model to investigate the effects
of final tank density, mean body length, and treatment on
mean response latency. All other statistical analysis utilized
mixed-effects models with ‘‘tank’’ as a random factor to avoid
pseudoreplication of the data and to control for any tank
effect, with details of specific fixed effects below. In multiple
comparisons of parametric data, the false discovery rate post
hoc test was carried out to investigate pairwise differences
(Verhoeven et al. 2005). All statistical analysis was carried
out using R (freeware available at www.r-project.org/) and
SPSS 11.0. Where mortality had occurred during the 47-day
rearing period, this was either controlled for statistically by
including tank as a random factor where data fulfilled parametric assumptions or by including density as a fixed factor
where tank means were used. Nonsignificant interactions were
dropped, and then the analysis was rerun. Differences in sample sizes between experiments are indicative of technical
issues related to video and image capture or exclusion from
trials based on the specific criteria detailed.
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population. The choice arena was a rectangular tank of dimensions 32 3 20 3 20 cm, of 7-cm water depth with gravel
substrate. A transparent perforated cylindrical plastic choice
chamber (diameter ¼ 8 cm) was placed 2 cm from the side of
the tank at each side along the midline, with 12 cm separating
the 2 choice chambers. A shoaling zone of 2 body lengths
width (approximately 3 cm) surrounded each chamber, with
a neutral zone in the center of the tank (of approximately 6
cm at the narrowest point). To minimize disturbance, the
sides of the tank were opaque; focal individuals were observed
with the use of a mirror angled at 45 above the tank. In the
trial, 2 adult male stimulus fish were placed in one of
the choice chambers and 2 juvenile fish placed in the other
chamber to investigate individual shoaling preferences.
At the beginning of each trial, a focal fish was placed in
a transparent plastic cylinder in the neutral zone. Once all
stimulus fish had resumed movement, this holding chamber
was removed. To ensure the fish had recovered from any disturbance this may have caused, the trial began once the focal
fish began to move after the removal of the holding chamber.
Fish that took .30 s to resume movement were excluded from
the trial (4 out of 144 individuals). The focal individual’s
shoaling behavior was then monitored for a 5-min period.
When the focal fish was within 2 body lengths from the edge
of a choice chamber (in practice within 4 body lengths from
the center of a choice chamber), it was considered as actively
shoaling with the individuals within that chamber (4 body
lengths is the interindividual distance most commonly documented as occurring in shoals of wild fish in nature; Pitcher
and Parrish 1993). The time spent shoaling with the fish in
each chamber was recorded and the total time spent shoaling
(overall shoaling tendency) calculated. Each juvenile from the
3 treatments was assayed. The position of the chambers was
alternated between trials, as was the order in which individuals
from the 3 treatments were tested. Stimulus fish were changed
after a focal fish from each treatment had been assayed. Once
tested, fish were kept in holding aquaria before being returned to their original rearing tanks after the trial.
89
Behavioral Ecology
90
RESULTS
Mortality
Levels of mortality did not differ between rearing treatments
(Kruskal–Wallis: v2 ¼ 0.196, degrees of freedom ¼ 2, P ¼
0.907); 4 out of 56 fry died over the 70-day rearing period
in the mixed and all juvenile treatments and 4 out of 44 fry
in the visual and olfactory treatment.
Shoaling behavior
Response to a simulated avian predation attempt
Our analysis of variables relating to escape performance in
juvenile guppies uncovered evidence of differences related
to both early social environment and body length. Juveniles
with experience of adults reacted significantly faster than juveniles lacking physical experience of adults (general linear
model (LM): F2,26 ¼ 12.58, P , 0.001; Figure 4a). Mean individual body length and final tank density had no significant
effect on mean response latency (LM: F1,26 ¼ 0.18, P ¼ 0.67;
F1,26 ¼ 2.65, P ¼ 0.12, respectively). For this analysis, data from
the single treatment with a density of 2 were excluded as all
other treatments had a final density of 3 or 4 (mean 6 SD ¼
3.76 6 0.43) and tank density was explicitly included in the
model as a fixed factor. Individuals that initially froze before
taking evasive action (fish with latencies of 10 frames, n ¼ 7
out of 132 individuals) were also excluded from this analysis.
Juveniles with experience of adults reacted significantly faster
Figure 4
(a) Mean (62 standard error [SE]) of tank mean response latency
to a simulated avian predation attempt (frames) (b) Mean (62 SE)
distance traveled in the first 5 frames of movement after a simulated
avian predation attempt (millimeters). n ¼ 132. Note: *P , 0.05,
**P , 0.01, ***P , 0.001.
than juveniles lacking physical experience of adults. Both individual body length and early social environment influenced
the distance traveled in the first 5 frames of movement after
a fright stimulus, with larger fish traveling farther (REML:
body length F1,54 ¼ 7.04, P ¼ 0.01; treatment F2,26 ¼ 3.81, P ¼
0.035; Figure 4b). No relationship between an individual’s
relative caudal depth and the distance traveled in 5 frames
was found (F1,54 ¼ 2.30, P . 0.05). Fish with physical experience of adults traveled farther in the first 5 frames of movement than fish lacking actual physical experience of adults.
Our analysis of the greatest distance a juvenile traveled in
a single frame (in the first 10 frames), that is, the maximum
velocity achieved (millimeters per frame) suggested that only
body length influenced maximum speed achieved (REML:
body length F1,54 ¼ 6.63, P ¼ 0.01). Neither early rearing
experience nor relative caudal depth impacted on maximum
speed achieved (treatment: F2,26 ¼ 1.86, P . 0.05; caudal
depth: F1,54 ¼ 1.91, P . 0.05).
Morphometric analysis: size and shape
There were no differences in initial body length of fish between treatments (analysis of variance: F2,153 ¼ 0.225, P ¼
0.799). After 47 days of differential rearing experience, however, differences in mean standard length were evident
(REML: F2,33 ¼ 5.16, P ¼ 0.011; Figure 5a) Fish reared in
the physical presence of adults were, on average, significantly
shorter than fish reared without experience of such interactions with adults.
Finally, our analyses revealed a treatment effect on relative
body depth of fish (REML: F2,34 ¼ 7.914, P , 0.001, Figure 5b).
Fish with experience of adults had relatively deeper bodies than
fish reared in the absence of any form of interaction with
adults.
Figure 3
Mean (62 standard error) time focal fish spent shoaling with
juvenile stimulus fish (seconds) in an adult/juvenile–choice trial.
n ¼ 140. Note: *P , 0.05, **P , 0.01, ***P , 0.001.
DISCUSSION
Our principal findings clearly show for the first time that
early experience of adult/juvenile interactions impact on the
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We found no evidence to suggest that experience of adult/
juvenile interactions affected overall shoaling tendency (i.e.,
total time spend shoaling with adults or juveniles [seconds];
restricted maximum likelihood [REML]: F2,36 ¼ 0.478, P ¼
0.62). However, when we examined how individuals with differing early social environments spent their time, differences
became clear. Rearing treatment influenced the time fish
spent shoaling with juveniles (REML: F2,36 ¼ 12.7041, P ,
0.001; Figure 3). Juveniles reared with physical experience
of adults spent significantly more time shoaling with juveniles
than fry reared in other treatments.
Chapman et al.
•
Early experience and predator defenses
91
Evasive response
behavioral and morphological development of Trinidadian
guppies. We found that this experience affected shoaling behavior, response to a simulated avian predation attempt, and
morphological development. Furthermore, we investigated
the importance of different cues, finding that physical experience of adults was of primary importance in the acquisition
of heightened evasive responses, morphological development,
and mediating shoal-choice behavior. How might this behavioral and morphological plasticity translate into actual fitness
benefits in the wild? We argue that the plasticity evident in
these traits may confer enhanced defenses in a predator situation in real life.
Grouping behavior
We found evidence of differences in shoal-choice behavior as
a function of early social environment. Juveniles reared with
physical experience of adults spent significantly more time
shoaling with other juveniles than either guppies reared with
only the visual and olfactory cues of adults or guppies reared
in the absence of adults. This means that juveniles from the
mixed treatment spent significantly more time in phenotypically homogenous (i.e., size matched) shoals. Both the dilution effect and the confusion effect rely for their maximum
effect on shoals being homogenous (Krause and Ruxton
2002); should individuals join shoals with phenotypically different fish, their probability of being attacked will be greater
than if they had joined shoals containing similar individuals.
This is known as the oddity effect (Landeau and Terborgh
1986) and has been experimentally shown to be important
in increasing predator preference and attack success for
‘‘odd’’ prey (Krause and Ruxton 2002). Hence, juveniles
reared without experience of physical interactions with aggressive adults may suffer greater predation risk due to their
more readily forming mixed size shoals. Two hypotheses may
explain this pattern: firstly, experience of adult aggression and
competition may lead to avoidance and the passive formation
of homogenous shoals. Secondly, the process may be active—
adult/juveniles interactions may adaptively mediate the
phenotypic structure of shoals through modifying the shoalchoice preferences of juveniles.
Size and shape
Guppies with physical experience of agonistic and competitive
encounters with conspecific adults were shorter in standard
length but had deeper caudal peduncles than individuals
reared in the absence of adults. This variation in body shape
matches variation between high- and low-predation sites in the
wild, with guppies from high-predation rivers (and the mixed
treatment) being smaller (Reznick and Endler 1982) and having deeper caudal peduncles (males only—Hendry et al.
2006) than fish from low-predation rivers (and the all juvenile
treatment). Furthermore, Langerhans and Dewitt (2004)
found consistent patterns of morphological divergence in
a cross-population comparison of 3 species of livebearing fish.
They reported that individuals from high-predation rivers had
relatively larger caudal peduncle regions than fish from lowpredation rivers, suggesting that these morphological features
may have adaptive antipredatory significance. In support of
this, Langerhans et al. (2004) showed that caudal size was
positively related to enhanced locomotor performance in
mosquito fish Gambusia affinis.
Conversely, relative caudal depth was not statistically related
to any of the components of escape response measured in our
study. It is possible that at this stage in the guppy’s ontogeny
differences in escape response are related to differences in
risk perception (potentially via experience of adult aggression) rather than physiological differences (i.e., differences
in caudal size). It would be interesting to examine the impact
of adult/juvenile interactions in the juvenile stage on the
morphology and escape responses of adult guppies to further
investigate whether this early morphological divergence has
implications for escape response later in life.
We have proposed that adults behaving as proxy predators
toward juveniles drive the development of the defenses acquired by juveniles in the mixed treatment. However, an alternative hypothesis might be that this plasticity may be a
product of competition—antagonism between adults and juveniles. Juveniles with experience of competitive interactions
may devote more time to vigilance to avoid potentially costly
competitive interactions with adults, which could have consequences for their response latency. Competitive exclusion
from access to food may also impact on the morphological
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Figure 5
(a) Mean (62 standard error [SE]) standard length (see Figure 2)
after 47 days of rearing experience (centimeters). n ¼ 144. (b) Mean
(62 SE) relative caudal base depth (caudal base depth/standard
length). n ¼ 123. Note: *P , 0.05, **P , 0.01, ***P , 0.001.
Juveniles with experience of adults responded faster to a fright
stimulus and also traveled farther in the first 5 frames of
movement after the fright stimulus. Contrary to our initial
prediction, the maximum speed achieved did not differ between juveniles reared in the different treatments. Although it
seems plausible that an increase in response latency and the
propensity to travel farther after a fright stimulus could increase survival probabilities in a predator encounter in the
wild, empirical tests of which components of the escape response are important in an actual predator attack are surprisingly rare. Fuiman et al. (2006) describe how ‘‘responsiveness’’
to a predator accounted for 86% of the variation in escape
potential in red drum larvae Sciaenops ocellatis, and Webb
(1981) found that 24–30% of anchovy larvae responded too
late to attack by clown fish. Both these studies implicate
response latency as critical in surviving a predator attack, supporting its adaptive value. Furthermore, Webb (1981) suggested that maximum speed achieved was not an important
characteristic in the evasive response as the confusion caused
by the rapid initial movement of the prey was adequate to
increase the likelihood of survival, which may explain why
we found no differences in maximum speed achieved between
treatments.
92
development of fry. Hence, enhanced antipredator skills may
be a beneficial side effect of juveniles being wary to avoid
aggressive competition for food, rather than a direct consequence of experience evading predatory conspecifics.
Furthermore, it is possible that these defenses have developed
in response to higher levels of density (and a higher frequency of interactions per se) in the mixed treatment. We
assert that although this is possible, there is no strong a priori
evidential or theoretical basis for this hypothesis. Conversely,
previous empirical work supports the hypothesis that specifically adult/juvenile interactions drive the development of
these defenses (Goodey and Liley 1986).
Conclusions
FUNDING
University of Leeds.
We thank Christos Ioannou and Ashley Ward for support in the animal house; Jon Evans, Jon Ward, Mark Botham, and attendees of the
Freshwater Biological Association Northeast Spring meeting for discussion and ideas; Christos Ioannou for comments on an earlier draft
of the paper; the Leeds Ecology R-stats team; and Anna Chapman for
endless encouragement and patience.
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Previous work has clearly elucidated the importance of natural
selection on the evolution of antipredator defenses in guppies
(Magurran et al. 1992; O’Steen et al. 2002). In this study, we
provide evidence that a number of these antipredator traits
exhibit a high degree of phenotypic plasticity. For this plasticity to be adaptive, juveniles from high-predation rivers would
have to encounter adults at a greater frequency than in lowpredation rivers in order for adult/juvenile interactions to act
as accurate cues of predation risk. This ‘‘adaptive interaction’’
hypothesis could be tested with relative ease through field
observations, comparing the spatial distribution of adults
and juveniles between environments of varying predation risk.
Also central to the notion of adaptive plasticity is that plastic
traits are costly to produce and maintain. It is likely that the
production and maintenance of deeper caudal peduncle regions are energetically expensive; individuals may trade off
burst-speed against endurance (Reidy et al. 2000). Burst swimming speed is likely to be of benefit in evading predator attacks, whereas sustained swimming may be beneficial in
foraging and mate acquisition (Domenici 2003). The tradeoffs involved in preferentially shoaling with juveniles over
adults are unclear.
In summary, we report that adult/juvenile interactions mediate the development of antipredator responses in the Trinidadian guppy. Furthermore, we elucidate the importance of
different cues, finding that physical cues—experience of agonistic/competitive interactions—are primarily important in
the acquisition of behavioral and morphological defenses.
The defenses we describe may act to enhance individual survival probability at a number of stages in the predator sequence (Fuiman and Magurran 1994). Testing whether fish
reared in differential social environments survive more effectively in the wild would provide an interesting basis for future
work in the field.
Behavioral Ecology
Chapman et al.
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Early experience and predator defenses
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