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Available online at www.sciencedirect.com
The less amorous Gammarus: predation risk affects mating
decisions in Gammarus duebeni (Amphipoda)
AL ISON M. DUN N* , J AI MI E T . A . DIC K† & MEL ANIE J. HAT CHER‡
*Faculty of Biological Sciences, University of Leeds
ySchool of Biological Sciences, Queen’s University Belfast
zSchool of Biological Sciences, University of Bristol
(Received 27 February 2008; initial acceptance 28 April 2008;
final acceptance 10 June 2008; published online - - -; MS. number: D-08-00121)
We examined the trade-off between the behaviours associated with predator avoidance and mate acquisition in the mate-guarding amphipod crustacean Gammarus duebeni. We used laboratory experiments to investigate the impact of olfactory predator cues on activity, mate choice and mate-guarding behaviour of
males and females. Pair formation declined under perceived risk of predation, reflecting reduced activity
of both males and females and hence a reduced likelihood of encountering a mate. We also observed a reduction in the choosiness of both males and females. Under increased perceived predation risk, assessment
of the female by the male was more likely to be followed by pair formation, and males showed a nonsignificant trend towards reduced discrimination in favour of large females and were less tenacious in their
pair bond when they paired during exposure to predator cues. Females also showed less resistance behaviour, suggesting that both males and females trade off the costs of maximizing current reproductive success
against the benefits of predator avoidance for survival and reproduction in the future. We discuss the implications of such context-dependent mating behaviours for ecological interactions between species and
suggest that predators, via the effects of perceived predation risk on mate choice and mate guarding in
the prey species, induce trait-mediated indirect effects with the potential to influence population dynamics and community structure.
Ó 2008 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Keywords: amphipod; flexible strategy; Gammarus duebeni; mate choice; mate guarding; precopula; predation risk; time
budget; trade-off; trait-mediated interaction
How animals budget their time is of fundamental importance in behavioural ecology. A conflict over time allocation arises when different activities contributing to fitness
cannot be performed concurrently (Sih 1980; Lima 1998),
and in such situations animals are predicted to optimize
fitness payoffs by trading off the benefits of performing
one act against the costs of not performing the other
(Houston & McNamara 1999). We examined the tradeoff between the behaviours associated with predator
avoidance and mate acquisition in the mate-guarding amphipod crustacean Gammarus duebeni.
Correspondence: M. J. Hatcher, School of Biological Sciences, University
of Bristol, Woodland Road, Bristol BS8 1UG, U.K. (email: mel.
[email protected]). A. M. Dunn is at the Institute of Integrative
and Comparative Biology, University of Leeds, Leeds L52 9JT, U.K.
J. T. A. Dick is at the School of Biological Sciences, Queen’s University
Belfast, Belfast BT9 7BL, U.K.
0003e 3472/08/$34.00/0
Aquatic invertebrates show a range of behavioural responses to both visual and chemical predator cues (eg. Moses & Sih 1998; Lass & Spaak 2003). For example, the virile
crayfish, Orconectes virilis, shows a trade-off between predator avoidance and feeding (Hazlett 1999). Food odours
lead to increased locomotion and decreased burrowing
activity; however, the locomotory response to food odours
is greatly reduced when the animals are simultaneously exposed to predator olfactory cues (Hazlett 1999). Trade-offs
between predator avoidance and mate-searching behaviour have also been observed in this crayfish; males were
more active and showed lower antipredator responses
when exposed to female pheromones than when exposed
to both pheromone and predator cues (Pecor 2006). Gammarus spp. (Crustacea, Amphipoda) have been found to
avoid olfactory cues of fish predators (Dahl et al. 1998;
Baumgartner et al. 2002), and to use refuges more (Baumgartner et al. 2003; Abjornsson et al. 2004) and decrease
1
Ó 2008 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Please cite this article in press as: Dunn, A.M., et al., The less amorous Gammarus: predation risk affects mating decisions in Gammarus duebeni (Amphipoda), Anim.
Behav. (2008), doi:10.1016/j.anbehav.2008.06.013
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ANIMAL BEHAVIOUR, --, -
activity (Williams & Moore 1985; Holomuzki & Hoyle
1990; Wudkevich et al. 1997) in response to these cues.
However, few studies have considered the impact of predator cues on the complex mating behaviour of Gammarus
(Strong 1973; Mathis & Hoback 1997). Since predator
avoidance is associated with reduced activity and changes
in habitat use (Lima 1998), it conflicts with mate acquisition which, in Gammarus, entails active encounter between males and females, inspection of potential mates,
resistance behaviours by the female, and manouvring
and holding the female by the male (Birkhead & Clarkson
1980; Elwood et al. 1987; Kelly et al. 2001a).
Many amphipod species show precopula guarding; the
male guards a potential mate by carrying her beneath his
ventral surface, thus increasing his chances of mating
with the female during the short time interval when she
moults and lays her eggs (reviewed in Conlan 1991; Jormalainen 1998). In Gammarus species, mating is size assortative (Elwood et al. 1987): males prefer large, fecund
females and the size of female that a male guards is determined by the constraints of mechanical load (Adams et al.
1989; Hatcher & Dunn 1997) and by maleemale competition (Elwood et al. 1987). Males will guard large females
for longer than small females (Ward 1988; Elwood &
Dick 1990) and prefer to guard females that are close to
their moult (e.g. Birkhead & Clarkson 1980; Dunham
et al. 1986). Females also show evidence of mate choice
by resisting pairing attempts (fleeing from contact with
the male and kicking during attempts at pair formation;
Hatcher & Dunn 1997); female resistance may contribute
to size-assortative pairing and ensures that larger females
obtain larger males as mates.
There are a number of costs associated with mate guarding in amphipods, including the loss of time available for
searching for other females (Parker 1974), the energetic cost
of carrying a potential mate (Elwood & Dick 1990; Plaistow
et al. 2003), the loss of feeding ability by guarding males
(Robinson & Doyle 1985) and a reduced ability to swim
against the current in comparison with singletons (Adams
& Greenwood 1987). Precopula guarding may also carry
an increased risk of predation, particularly by active, sizeselective predators such as fish (Ward 1986; Cothran
2004) as pairs are more visible and swim more slowly than
single animals (Strong 1973; Verrell 1985; Adams et al.
1989). Cothran (2004) has recently shown that precopula
pairs of the amphipod Hyallela azteca are more likely than
singletons to be consumed by fish predators.
We investigated possible trade-offs between mate guarding and predator avoidance in G. duebeni by measuring the
impact of olfactory predator cues on its activity, mate
choice and mate-guarding behaviour. We tested the hypotheses that G. duebeni should show less pair formation
and be less choosy when exposed to olfactory cues from
a fish predator.
METHODS
Animal Collection and Husbandry
In JanuaryeApril 2005 and 2006, we collected G. duebeni from Budle Bay, Northumberland, U.K., using a fine
mesh net. They were maintained in stock tanks in aerated
brackish water (6.5 ppt) at 12 C. Rotting sycamore leaves
and green algae (Enteromorpha sp.) provided food and shelter. After the experiments, the animals were returned to
stock tanks for teaching use. Predator cue water was obtained from sticklebacks, Gasterosteus aculeatus (three fish
in 5 litres of aerated tap water at 12 C) collected from
the same site and fed on fish food pellets and G. duebeni.
The fish were kept in the tank for 5 days before the water
was used for the experiments. This was designed to give
a realistic mimic of a predatory threat, that is, a combination of fish odour and ‘alarm cues’ from (consumed) conspecifics, as these two cues in combination have been
shown to elicit distinct antipredator behaviour in other
species (e.g. Dalesman et al. 2006). The fish were returned
to the field 2 days after the experiments.
Experiment 1: General Activity
Precopula pairs of G. duebeni were separated by placement
on dry tissue paper and allowed to recover in brackish water
for 1 h. For each sex separately, single animals (N ¼ 30 each
sex) were put into 200 ml of brackish water in a cylindrical
pot to which we added either (1) 10 ml of predator cue water
or (2) 10 ml tap water which had been left to stand overnight (control). We counted the times each animal crossed
a line drawn across the diameter of the pot each minute over
5 min. Mean numbers of crosses were examined in a threefactor repeated measures ANOVA with respect to ‘treatment’ (predator cue/control water), ‘sex’ (male/female)
and ‘time’ (1e5 min; repeated measure) using StatView.
SAS Institute Inc., Cary, NC, U.S.A.
Experiment 2: Precopula Pair Formation
Individual females from pairs were placed in either (1)
predator cue (N ¼ 51) or (2) control water (N ¼ 49) as
above and a male (from a different pair) was added
5 min later (size ratio male: female approximately 1.3).
We recorded the number of replicates where pairs formed
within 30 min. For the subset of 42 replicates where pairs
formed (20 predator cue, 22 control), we recorded the time
to pair formation and the number of male/female contacts
before pairs formed. We also looked in detail at the outcome of each male assessment behaviour (antennal touching bouts) for 51 replicates (26 predator cue, 25 control),
recording the number of assessments that led to pair
formation and that resulted in female resistance.
We used chi-square tests to compare the frequency of
pair formation in the two treatments. To analyse the data
for contact frequency and outcomes of assessment, we
used the generalized linear modelling package GLIM
(Numerical Algorithms, Group, Oxford, U.K.). The significance of factors was assessed by their deletion from the
maximal model, and the change in deviance compared
with F tables or chi-square tables as appropriate. Data for
the number of contacts were square-root transformed.
The number of assessments that led to pair formation or
female resistance were proportion data and were analysed
specifying a binomial error structure. We corrected for
Please cite this article in press as: Dunn, A.M., et al., The less amorous Gammarus: predation risk affects mating decisions in Gammarus duebeni (Amphipoda), Anim.
Behav. (2008), doi:10.1016/j.anbehav.2008.06.013
ARTICLE IN PRESS
DUNN ET AL.: PREDATION RISK AND MATING IN AN AMPHIPOD
overdispersion with a heterogeneity factor (Hf ¼ Pearson’s
c2/df; Crawley 1993).
16
14
(a)
Control
Predator cue
12
10
Experiment 3: Mate Choice: One Male,
Two Females
6
No. of line crosses
We repeated experiment 2 above but with males
presented with two females, one large and one small (by
visual inspection, with the ratio male: large female
approximately 1.3) in either (1) predator cue (N ¼ 39) or
(2) control water (N ¼ 43) and recorded whether the
male took the smaller or larger female into precopula.
Again, we used chi-square tests for analysis of frequencies.
8
4
2
0
14
12
(b)
10
Experiment 4: Mate Choice: Multiple
Males and Females
8
We added 20 males and 20 females, obtained as for
experiment 1, to tanks containing 2 litres of brackish
water at 12 C with either (1) 100 ml of predator cue water
added immediately preceding animal introductions
(N ¼ 7) or (2) 100 ml of control water (as above; N ¼ 6).
We recorded the number of pairs formed at each minute
for the first 5 min and then at 5 min intervals for a
further 25 min. Mean numbers of precopula pairs formed
were examined in a two-factor repeated measures ANOVA
with respect to ‘treatment’ (predator cue/control) and
‘time’ (0.5e30 min; repeated measure) using StatView.
4
Experiment 5: Tenacity of Precopula Pairs
Males and females from split precopula pairs as for
experiment 1 were allowed to pair in either (1) predator
cue (N ¼ 21) or (2) control water (N ¼ 12) in 200 ml pots.
Pairs were allowed 30 min in the treatment water and
then removed by pouring the water through a tea strainer
and carefully placing the pair onto dry tissue paper. The
time to pair separation was recorded and compared using
a Student’s t test.
6
2
0
1
2
3
Time (min)
4
5
Figure 1. Activity (measured as mean SE number of line crosses/
min) of individual Gammarus duebeni in predator cue and control
water treatments. (a) Males (N ¼ 30); (b) females (N ¼ 30).
P < 0.05). Time to pair formation was significantly shorter
in predator cue (X SE ¼ 108:5 120 s) than in control
water (454.1 86.1 s; ANOVA: F1,40 [ 7.7, P < 0.05). This
reflects the significantly fewer contacts between males
and females before pairs formed in predator cue than
control water (0.61 0.10 versus 1.74 0.37; ANOVA:
F1,40 ¼ 9.46, P < 0.01). The percentage of male assessments
leading to pair formation was significantly higher in predator cue than in control water (48.8 19.5 versus 24.4 9.0;
ANOVA: F1,49 ¼ 4.69, P < 0.05; data corrected for overdispersion, Hf ¼ 1.59) and the percentage of assessments leading to female resistance was significantly lower (33.4 17.0
versus 67.9 7.6; F1,49 ¼ 6.52, P < 0.05; data corrected for
overdispersion, Hf ¼ 1.69).
RESULTS
Experiment 1: General Activity
Individuals were less active with predator cue than
control water (ANOVA: F1,56 ¼ 11.7, P < 0.002; Fig. 1).
There was no sex difference in activity (F1,56 ¼ 0.3,
P > 0.05). Overall, activity decreased with time
(F4,224 ¼ 7.7, P < 0.001; Fig. 1); the significant ‘time*treatment’ interaction effect (F4,224 ¼ 11.7, P < 0.05) reflects
the more pronounced reduction in activity over time
with predator cue than control water. There were no other
significant interaction effects.
Experiment 2: Precopula Pair Formation
Significantly fewer pairs formed in predator cue (29/
51 ¼ 56%) than in control water (39/49 ¼ 79%; c21 ¼ 5.93,
Experiment 3: Mate Choice: One Male,
Two Females
There was a nonsignificant trend for random pairings
in predator cue water (larger female chosen in 21/
39 ¼ 54% of trials) and male selection of the larger female
in control water (larger female chosen in 30/43 ¼ 70% of
trials; c21 ¼ 2.2, P ¼ 0.14; Fig. 2).
Experiment 4: Mate Choice: Multiple
Males and Females
Significantly fewer precopula pairs formed with predator cue than control water (ANOVA: F1,110 ¼ 5.7, P < 0.05;
Fig. 3). More pairs formed over time in both treatments
(F10,110 ¼ 49.3, P < 0.001; Fig. 3), but there was no
Please cite this article in press as: Dunn, A.M., et al., The less amorous Gammarus: predation risk affects mating decisions in Gammarus duebeni (Amphipoda), Anim.
Behav. (2008), doi:10.1016/j.anbehav.2008.06.013
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ANIMAL BEHAVIOUR, --, -
35
Large female chosen
Small female chosen
Frequency
30
25
20
15
10
5
0
Predator cue
Control
Treatment
Figure 2. Mate choice by individual Gammarus duebeni males for
large versus small females in predator cue (N ¼ 39) and control
(N ¼ 43) water treatments.
significant ‘treatment*time’
P > 0.05; Fig. 3).
interaction
(F1,110 ¼ 1.5,
Experiment 5: Tenacity of Precopula Pairs
Pairs that formed in predator cue water took significantly less time to separate than those in control water
(169.3 254.0 s versus 484.7 112.7 s: Student’s t test:
t32 ¼ 2.2, P < 0.05).
DISCUSSION
This study suggests that G. duebeni has a flexible strategy
for mate acquisition, moderating levels of searching,
mate assessment/resistance and precopula guarding in relation to the perceived threat from predators in a manner
consistent with adaptive explanations (Crowley et al.
1991; Lima 1998; Morrell 2004). We found that exposure
of G. duebeni to olfactory predator cues led to a decrease in
pair formation (Fig. 3). This reduction in pair formation
16
14
12
Number of pairs
4
10
8
6
4
Control
2
Predator cue
0
0
5
10
15
20
25
30
Time (min)
Figure 3. Precopula pair formation by Gammarus duebeni (20 males
and 20 females) in tanks with predator cue (N ¼ 7) and control
(N ¼ 6) water treatments. Mean SE number of precopula pairs
observed over 30 min.
reflects the reduction in activity in both males and females
(Fig. 1) in accord with previous studies (Williams & Moore
1985; Holomuzki & Hoyle 1990; Wudkevich et al. 1997),
which will, in turn, lead to a reduction in the time spent
searching for mates and the likelihood of encountering
a mate. A reduction in activity including mating activity
in response to increased predation risk has also been
recorded in water striders (Gerris marginatus and Gerris
remigis: Sih et al. 1990; Moses & Sih 1998).
Although the frequency of precopula pair formation
was reduced, for those animals that formed pairs the time
to pair formation was shorter for the predator cue
treatment (108 s) than in the control (454 s). This observation is in accord with a study of Gammarus pseudolimnaeus
in which latency to pair formation was reduced in predator cue water (Mathis & Hoback 1997). The reduced time
to pair formation reflects the observation that, once
a male encountered a female, he was, in fact, more likely
to pair with her in the predator cue water than in control
conditions. The increased likelihood of pairing following
assessment (49% versus 24% in control water) and the
trend towards reduced preference for large females
(Fig. 2) suggest that males become less choosy under
higher predation risk. Similarly, male pipefish, Syngnathus
typhle, showed reduced courtship and copulation frequency (Fuller & Berglund 1996) and a reduced preference
for large females (Berglund 1993) in the presence of a fish
predator, and male Panamanian bishop fish, Brachyrhaphis
episcopi, from populations with fish predators showed
a reduced preference for unfamiliar females (Simcox
et al. 2005).
Females also showed reduced choosiness; they were less
likely to resist pair formation under enhanced predation
threat. A similar response has been reported in female
guppies, Poecilia reticulata, with reduced avoidance of copulation under the risk of predation (Kelly & Godin 2001).
Our observations are in accord with theoretical predictions that female choosiness should decrease as predation
risk increases (Crowley et al. 1991). A consequence of reduced activity under the threat of predation is that
maleefemale encounter rates decrease and the costs of
sampling increase; again this is theoretically predicted to
select for reduced choosiness (e.g. Fawcett & Johnstone
2003). The presence of fish predators also reduces preference for large and colourful males by female sand gobies,
Pomatoschistus minutus (Forsgren 1992) and for bright
males in guppies (Godin & Briggs 1996), while female
green swordtails, Xiphophorus helleri, show a reversal in
mate choice, preferring long-tailed males in control conditions, but tail-less males after exposure to a video recording of predation of a long-tailed male (Johnson & Basolo
2003).
The reduction in choosiness observed in our study
suggests that male and female G. duebeni adjust the time
allocated to conflicting behaviours in a trade-off between
predator avoidance and the benefits of choosiness. Mate
searching incurs a greater risk of predation for a number
of species through increased conspicuousness and activity
(Magnhagen 1991; Cothran 2004). For the G. duebeni
male, the decision to guard a particular female will depend
on whether he should expect a higher benefit from
Please cite this article in press as: Dunn, A.M., et al., The less amorous Gammarus: predation risk affects mating decisions in Gammarus duebeni (Amphipoda), Anim.
Behav. (2008), doi:10.1016/j.anbehav.2008.06.013
ARTICLE IN PRESS
DUNN ET AL.: PREDATION RISK AND MATING IN AN AMPHIPOD
guarding than from continuing to search (Grafen & Ridley
1983). Male gammarids maximize their reproductive success if they pair with larger, more fecund females (Elwood
et al. 1987; Adams et al. 1989) and with females close to
their moult (Dunham et al. 1986), thereby minimizing investment in precopula guarding. In addition, male gammarids prefer to mate with uninfected females than
those infected by acanthocephalan (Bollache et al. 2002)
or microsporidian (Kelly et al. 2001a) parasites. Any reduction in choosiness will be costly for males as parasitism
reduces female fertility (Kelly et al. 2001b; Bollache et al.
2002; Dunn et al. 2006). Our results suggest that individuals exposed to increased predation risk trade off the benefits of predator avoidance for long-term survival and
future reproduction against a reduction in immediate
reproductive success.
The predator cue-induced effects on mating behaviour
seen here can be considered as trait-mediated indirect
effects (sensu Abrams 1995; reviewed in Werner & Peacor
2003), which, in a community context, could influence
G. duebeni’s interactions with other species. Most work on
trait-mediated interactions has concentrated on predatorinduced changes in foraging activity and its knock-on
effects on resources or resource availability for competing
species (Bolker et al. 2003; Werner & Peacor 2003). For
instance, in simple food chains, the traditional population
ecology perspective suggests that predators cause a trophic
cascade by reducing prey density, thereby allowing the
prey’s resources to increase. However, the trait-mediated
trade-off between foraging activity and predator avoidance
can also drive trophic cascades (predators reduce prey foraging activity which enables resources to increase: Schmitz
et al. 2004). Recent studies suggest that many aspects of
community structure are strongly influenced by the behavioural trait-mediated effects of predators or parasites (Mouritsen & Poulin 2005; Van Veen et al. 2005; Wojdak &
Luttbeg 2005; Hatcher et al. 2006).
Predator-induced changes in mate choice and mating
frequency could have knock-on effects for populations, if
trade-offs over choosiness and mating activity affect
reproductive success. The consequences for population
dynamics are difficult to determine because they depend
ultimately on how an individual’s fitness payoffs for
a given activity are arranged, and many different patterns
are possible. For instance, fitness payoffs are unlikely to be
symmetrical (there might be no fitness benefit from
performing mate choice or guarding behaviours if predator avoidance is insufficient, but provided further opportunities for breeding exist, predator avoidance alone
provides positive fitness benefits; e.g. Morrell 2004). In addition, behavioural responses may be suboptimal if there
are behavioural correlations across different situations or
contexts (Sih et al. 2003). Suboptimal allocation strategies
may be most apparent in recently disturbed or transient
communities in which there has been insufficient evolutionary time for selection to take effect. For example,
fish predator cues cause a greater reduction in feeding
and growth in the invasive crayfish Pacifastacus leniusculus
than in the native Astacus astacus in Sweden (Nystrom
2005). In the current study system, the subspecies G. d. celticus faces competition from several invasive Gammarus
species in Northern Ireland (Dick et al. 1993; Dick & Platvoet 2000) and predator or parasite-induced trait-mediated effects could tip the balance towards invasion or
enable coexistence of natives and invaders (MacNeil
et al. 2003, 2004). As is the case for most other predatorinduced trait effects (Okuyama & Bolker 2007), the
broader long-term consequences of predator-induced
changes in mating behaviour for community structure
in our system have yet to be determined. However, given
increasing evidence for flexible context-dependent mating
behaviour in a variety of organisms and situations, we propose that the potential consequences for populations and
communities in this and other systems warrant further
attention.
Acknowledgments
We thank NERC for funding, Stephen Young and the Visitor
Programme of the NERC Centre for Population Biology,
Imperial College for helpful discussions and Natalie
Ashcroft and Rebecca Hewitt for technical assistance.
Thanks to Bob Elwood for allowing us to corrupt his title!
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