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Turbidity increases risk perception but constrains collective behaviour during foraging by fish shoals

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Turbidity reduces the distance that animals can detect food, predators and conspecifics. How turbidity affects decision making in social contexts has rarely been investigated; moreover, it is unknown whether decreased shoaling in turbid water is due to visual constraints (a mechanistic explanation) or a reduced perception of predation risk (an adaptive explanation). Using a V-shaped decision-making arena, we investigated the effect of turbidity on foraging in groups of three-spined sticklebacks, Gasterosteus aculeatus. In turbid conditions, fish took longer to leave a refuge and locate the food in one of the arms and consumed less food once it was found. This increase in risk-averse behaviour was further supported by improved accuracy over repeated trials and a speed–accuracy trade-off only being observed in turbid conditions. Despite evidence of a higher perception of risk in turbid water, the first fish to choose an arm of the maze was more likely to be alone in turbid water; thus, this individual lost the antipredator and decision-making benefits of collective behaviour. This suggests that turbidity acts mechanistically as a visual constraint, shifting decisions away from being made collectively to being made by individuals separated from the group, which could have potential impacts for wild prey populations.
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Turbidity increases risk perception but constrains collective behaviour
during foraging by sh shoals
Alice C. Chamberlain, Christos C. Ioannou
*
School of Biological Sciences, University of Bristol, Bristol, U.K.
article info
Article history:
Received 2 March 2019
Initial acceptance 18 April 2019
Final acceptance 17 July 2019
MS. number: 19-00154
Keywords:
antipredator behaviour
collective behaviour
foraging
group decision making
refuge
stickleback
Turbidity reduces the distance that animals can detect food, predators and conspecics. How turbidity
affects decision making in social contexts has rarely been investigated; moreover, it is unknown whether
decreased shoaling in turbid water is due to visual constraints (a mechanistic explanation) or a reduced
perception of predation risk (an adaptive explanation). Using a V-shaped decision-making arena, we
investigated the effect of turbidity on foraging in groups of three-spined sticklebacks, Gasterosteus
aculeatus. In turbid conditions, sh took longer to leave a refuge and locate the food in one of the arms
and consumed less food once it was found. This increase in risk-averse behaviour was further supported
by improved accuracy over repeated trials and a speedeaccuracy trade-off only being observed in turbid
conditions. Despite evidence of a higher perception of risk in turbid water, the rst sh to choose an arm
of the maze was more likely to be alone in turbid water; thus, this individual lost the antipredator and
decision-making benets of collective behaviour. This suggests that turbidity acts mechanistically as a
visual constraint, shifting decisions away from being made collectively to being made by individuals
separated from the group, which could have potential impacts for wild prey populations.
©2019 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Turbidity is caused by suspended particles in water that atten-
uate and increase the scattering of light (Utne &Utne-Palm, 2002).
The subsequent decrease in visibility reduces the availability and
reliability of visual cues for aquatic animals, limiting the private and
social information available for decision making. In addition to
some habitats being naturally highly turbid, anthropogenic activity
is driving an increase in turbidity via eutrophication and sedi-
mentation from intensied agriculture, deforestation and urbani-
zation (Davies-Colley &Smith, 2001). Accordingly, there is much
research interest in quantifying and predicting behavioural re-
sponses to increased turbidity as behaviour can mediate the impact
of turbidity on wild animal populations and their distributions
(Abrahams &Kattenfeld, 1997; Tuomainen &Candolin, 2011; Utne
&Utne-Palm, 2002).
Previous research exploring the effect of turbidity on behaviour
has focused on predatoreprey interactions, including foraging
behaviour by predators and antipredator behaviour in prey. In
turbid water, detection of prey has been shown to be impaired
(Pekcan-Hekim &Lappalainen, 2006; Quesenberry, Allen, &Cech,
2007; Utne, 1997), which can account for decreased encounter
rates between predators and prey (Turesson &Br
onmark, 2007)
and reduced selectivity regarding prey choice (Abrahams &
Kattenfeld, 1997; Kimbell &Morrell, 2016; Sohel, Mattila, &
Lindstr
om, 2017). A reduced predation rate in turbid water has
been used to explain a decrease in risk-averse behaviours in prey
(Lehtiniemi, Engstr
om-
Ost, &Viitasalo, 2005). Examples include
shifts in habitat choice by fathead minnows, Pimephales promelas,
where the use of more risky areas increases (Abrahams &
Kattenfeld, 1997), and in three-spined sticklebacks, Gasterosteus
aculeatus, responding to the sudden appearance of a predator, the
use of shelters decreases and fewer individuals show escape re-
sponses (Sohel &Lindstr
om, 2015). Other studies, however, have
found an increase in antipredator behaviours, possibly due to the
reduced visibility in detecting predators increasing the perception
of risk. Three-spined sticklebacks in turbid water were shown to
increase refuge use and reduce activity (Ajemian, Sohel, &Mattila,
2015); a reduction in activity in turbid water has also been found in
guppies, Poecilia reticulata (Borner et al., 2015) and zebrash, Danio
rerio (Suriyampola, Cac
eres, &Martins, 2018). Turbidity has also
been shown to increase the rate of freezing by guppies in response
to detecting a predator (Kimbell &Morrell, 2015) and reduce
foraging in spiny damselsh, Acanthochromis polyacanthus (Leahy,
McCormick, Mitchell, &Ferrari, 2011). These mixed results may
be explained by differences in predator hunting modes and the
*Correspondence: C. C. Ioannou, School of Biological Sciences, University of
Bristol, Life Sciences Building, 24 Tyndall Avenue, Bristol, BS8 1TQ, U.K.
E-mail address: c.c.ioannou@bristol.ac.uk (C. C. Ioannou).
Contents lists available at ScienceDirect
Animal Behaviour
journal homepage: www.elsevier.com/locate/anbehav
https://doi.org/10.1016/j.anbehav.2019.08.012
0003-3472/©2019 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Animal Behaviour 156 (2019) 129e138
relative visibility of predators and prey in clear and turbid water;
they all indicate, however, that turbidity affects both predation and
antipredator behaviour.
A handful of recent studies have shown shoaling tendencies in
sh are reduced in turbid water (Borner et al., 2015; Fischer &
Frommen, 2013; Kimbell &Morrell, 2015). Because shoaling is a
key antipredator behaviour in many sh species (Rieucau, Fern
o,
Ioannou, &Handegard, 2015), this reduction in shoaling in turbid
water could represent a lower perception of risk. In contrast,
turbidity could act as a visual constraint, reducing the ability of sh
to form and maintain groups as vision is a widely used and
important sensory modality in shoaling (Ioannou, Couzin, James,
Croft, &Krause, 2011). Despite extensive work on collective de-
cisions in animal groups (Conradt &List, 2009; Ioannou, 2017b), it
is unknown how decision making in social contexts is impacted by
turbid conditions. Decisions in groups can be made collectively,
where a large proportion of the group contribute to a group deci-
sion, or be led by one or a few individuals, or groups can split with
different decisions made by different subsets, or even individuals,
from the group (Ioannou, Ramnarine, &Torney, 2017). Although in
this latter case individuals are not constrained by maintaining
group cohesion after they have separated from the group (Ioannou,
Singh, &Couzin, 2015), they lose antipredator benets of grouping.
As with shoaling in general, groups may split during decision
making in turbid water because of a mechanistic constraint in vi-
sual information or this may be an adaptive change in behaviour if
the perception of risk is reduced.
Three-spined sticklebacks are facultatively group living and
widely distributed across a range of habitats, including in clear
and turbid water, making them an ideal system for studying the
effect of turbidity on decision making in a social context
(Quesenberry et al., 2007). In this study we used a V-shaped
decision-making arena, where the sh started in a refuge at the
base of the V and had to choose between two arms, only one of
which contained food. Shoals were tested in either clear or turbid
water, and given multiple trials per day, to test how turbidity af-
fects foraging and social interactions. In addition to exploring how
foraging decisions in a social context are affected by turbidity, we
also measured the social cohesion of the individual that rst
entered an arm of the maze, that is, the deciding, or initiator,
individual (Bevan, Gosetto, Jenkins, Barnes, &Ioannou, 2018).
Whether turbidity is predicted to have a positive or negative effect
on the speed of decision making, the accuracy of choosing and
cohesion between individuals in the group will depend on
whether turbidity increased or decreased the perception of pre-
dation risk. By investigating group cohesion in parallel with
foraging, we can also infer whether changes in social cohesion are
due to altered perception of risk in turbid water (as revealed by
the response in foraging) or are more likely to be due to altered
visibility of other individuals. Repeated testing within a day
allowed us to test how the cumulative effect of habituation,
training in the presence and location of food, and satiation
(McDonald, Rands, Hill, Elder, &Ioannou, 2016) differs in clear
versus turbid environments. We predicted that due to the reduced
spatial information in turbid water, for example from landmarks
(Odling-Smee &Braithwaite, 2003), decision making would
improve more slowly in turbid water over repeated trials. We also
varied shoal size to test whether the effect of turbidity was sen-
sitive to the number of individuals in the group, which can have
multiple effects on decision making such as reducing the
perception of risk in individuals, increasing the likelihood that
bolder or more cognitively able individuals are included in the
group, and allowing for information transfer and feedback be-
tween individuals which results in swarm intelligence (Ioannou,
2017a).
METHODS
Study Subjects and Husbandry
Three-spined sticklebacks were caught from the River Cary,
Somerset, U.K. (ST 469 303) in September 2014. The collection site
is surrounded by arable land and turbidity varies frequently
throughout the year due to variation in agricultural activity and in
the weather. Fish were transported to the University of Bristol by
car where they were placed in glass stock tanks (40 x 70 cm and
34 cm deep) in a temperature-controlled room (water tempera-
ture: 15e16
C; photoperiod: 12:12 h). The tanks housed 60e90
sh and were enriched with plastic plants and dark plastic tubing
the sh could use as refuges. Fish were not sexed as the water
temperature and light cycle prevented breeding. They were fed
defrosted bloodworms and tropical ake food daily. At the time of
testing, the sh in the study had a mean standard body length of
42.3 mm (SD 3.9 mm).
Trials were carried out in January to March 2016. The day before
they were tested, up to three groups consisting of two, four or eight
individuals were formed by transferring randomly chosen in-
dividuals to three separate breeding nets (16.5 x 12.7 cm and
12.7 cm deep) within a glass stock tank, so that up to three groups
were tested each day. Fish within each group came from the same
stock tank so were familiar with one another and were held over-
night in the breeding nets and between trials on the test day that
followed. Each group was tested in only one water treatment and
individual sh were not tested in more than one group; 132 in-
dividuals were exposed to the turbid treatment (groups of two,
N¼20; groups of four, N¼9; groups of eight, N¼7) and 116 in-
dividuals to the clear treatment (groups of two, N¼20; groups of
four, N¼7; groups of eight, N¼6). At the start of testing, sh had
not been fed since the previous day to standardize hunger before
the start of trials.
Experimental Apparatus and Protocol
Experiments took place in a V-shaped maze constructed from
white Perspex (Ioannou &Dall, 2016), ca.130 cm in length (Fig. 1).
Each day, one arm of the maze (left: 130 trials; right: 133 trials) was
randomly chosen to contain a bloodworm reward inside a Petri dish
(two bloodworms per sh per trial). The arm containing blood-
worms was kept constant throughout that day of testing. Opaque
white plastic covered the front half of the petri dishes to prevent
sh seeing the reward prior to swimming into the arm of the maze.
Without this visual barrier, the food would have been visible from a
greater distance in clear versus turbid water; once past the visual
barrier, the bloodworms were visible to the sh even in the turbid
water treatment. Trials were recorded with a Panasonic SD800
camera at a resolution of 1920 1080 pixels, mounted 1 m above
the maze on a tripod.
The maze was lled with aged water to a depth of 8 cm (42 litres
in total). On the morning of turbid treatment days, 4.5 g (0.11 g/
litre) of kaolin clay (Trustleaf, Cambridge, U.K.) was added to the
maze water and mixed thoroughly, producing a measurement of
30.98 ±2.24 NTU (mean ±SD) in line with previous studies (Leahy
et al., 2011; Meager &Batty, 2007). Suspended clay particles are
frequently a large component of turbidity in natural aquatic habi-
tats (Horppila, Eloranta, Liljendahl-Nurminen, Niemist
o, &Pekcan-
Hekim, 2009; Rhoton &Bigham, 1997), so is an ecologically relevant
method for manipulating turbidity. Clear water was measured at
0.36 ±0.21 NTU (Appendix Fig. A1).
For each trial, the sh were transferred to the refuge (an area
covered with 5 mm black plastic mesh; Fig. 1) and acclimatized for
2 min; the door was then raised remotely using shing line,
A. C. Chamberlain, C. C. Ioannou / Animal Behaviour 156 (2019) 129e138130
allowing the sh to enter the maze. Trials ended when all blood-
worms had been consumed or after 20 min if the bloodworms were
not all eaten. The group was then returned to their breeding net.
After each trial, the water was thoroughly mixed in both water
treatments to maintain turbidity. Up to three groups were tested
per day in up to 10 trials per group; no further trials for a group
were conducted if no bloodworms were eaten within 20 min for
two sequential trials. This was to avoid testing groups that were
already satiated, and hence unlikely to be motivated to nd food. At
the end of each day all sh were returned to stock tanks and not
reused. The water in the maze was replaced with aged water at the
end of each day and ltered overnight using an external Eheim
2213 lter pump, which was turned off during trials.
Trials were conducted over 23 days (turbid, N¼12; clear, N¼11
days). Water treatment (clear or turbid) was randomized between
days. On each day, each group received its rst trial, then all groups
received their second trial, then their third, etc. The mean time
between consecutive trials starting was 24.64 min (SD 18.46 min).
Typically, three groups were tested each day, consistingof one large
group of four or eight individuals and two groups of two in-
dividuals. More trials of smaller groups were conducted as these
were expected to be more variable than larger groups (as they are
less likely to contain a representative sample of the overall
population).
Video Analysis
Data were extracted from video recordings per trial rather than
per individual sh because tracking individual identities in turbid
water was too unreliable (Kimbell &Morrell, 2015). The time taken
to leave a refuge is a commonly used method of assessing risk-
taking behaviour (Webster, Atton, Ward, &Hart, 2007) and was
measured as the latency from when the refuge door was raised
until the whole body of the rst sh to leave was past the door. The
time taken to make the rst decision was the time that elapsed
between the rst sh leaving the refuge and the rst sh to touch
19 cm
20 cm
128 cm
48 cm
13 cm
48 cm
Figure 1. The experimental V-maze used to determine the effects of turbidity on decision making in three-spined sticklebacks. The shaded box represents the refuge where the
sticklebacks were released by raising a door on a pulley at the right-hand side of the refuge. The dashed line is the point that determined when a decision had been made (the
decision boundary). The circles at the ends of both arms represent the petri dishes where food was placed prior to each trial, and the red line represents the opaque plastic used to
cover the front half of the dishes to prevent sh seeing the contents of the arm. To minimize disturbance and prevent light reection on the water surface, a white curtain screened
the maze during trials. The camera was connected to a monitor beside the maze to allow sh behaviour to be observed remotely without causing disturbance.
0
0.2
0.4
0.6
0.8
1
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0
0.2
0.4
0.6
0.8
1
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Decision-making accuracy
Trial number
(a) (b)
Figure 2. The relationship between water treatment and trial number on decision-making accuracy. (a) Turbid and (b) clear water. Accuracy is measured as whether the arm
containing food is chosen rst. The line for each treatment represents the tted values calculated from the GLMM coefcients, while controlling for group size at its mean value. The
dotted lines around each line of best t shows 2 predicted standard error of each line. Jitter has been added to the raw data to allow overlapping points to be visualized.
A. C. Chamberlain, C. C. Ioannou / Animal Behaviour 156 (2019) 129e138 131
the decision boundaryof either arm with its snout (Fig. 1). This
determined the point in the trial at which a sh rst decided which
arm to enter, and this sh was considered the deciding sh by being
the rst to initiate a movement into an arm. Accuracy of decision
making was determined by whether this arm contained the food
reward. The time to locate food was measured as the time taken
from rst crossing a decision boundary to when the rst blood-
worm was consumed, and foraging success was the proportion of
bloodworms consumed within 20 min of the trial starting.
The spatial distribution of sh was measured to quantify the
social cohesion of the rst sh to make a decision (Ioannou et al.,
2015). Coordinates were manually recorded from the centre of
every sh using ImageJ (Rasband, 2012) at the time of the rst
decision to enter an arm in each trial. Any sh in the refuge were
given the same coordinate, xed at the centre of the refuge area, as
their exact position was unknown. Position coordinates were used
to calculate the distance between the rst sh that made a decision
and its nearest neighbour (Ioannou et al., 2015). The proportion of
individuals outside the refuge was measured from the number of
individuals inside and outside the refuge when the rst decision
was made.
Statistical Analysis
Time taken response variables (latencies for the rst sh to leave
the refuge, the rst decision to enter an arm and the rst time food
was consumed) and nearest-neighbour distance (the NND of the
rst individual to choose an arm, i.e. the deciding sh) were each
analysed using a negative binomial generalized linear mixed model
(GLMM; the analyses did not meet the assumptions of normal
(Gaussian) or Poisson linear models). Decision-making accuracy,
the proportion of sh outside the refuge when the decision was
made, whether at least one other sh was out of the refuge when
the decision was made and the proportion of bloodworms
consumed were each analysed using a binomial GLMM. However,
due to convergence warnings in the models with the proportion of
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Incorrect Correct
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10
100
1000
Incorrect Correct
Accurac
y
Time taken to make first decision (s)
(a) (b)
Figure 3. The relationship between speed and accuracy of decision making in (a) turbid and (b) clear water treatments. Speed is measured as the time taken to make the rst
decision. Medians are illustrated by thick black lines, the interquartile range (IQR) is shown within the boxes and the whiskers represent data points within 1.5 x IQR. The open
circles represent data points outside of the whiskers. The y-axes show natural log transformed time taken to make the rst decision for visual clarity in plotting.
10
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Nearest-neighbour distance (pixels)
Trial number
(a) (b) (c)
Figure 4. The effect of group size and trial number on the nearest-neighbour distance of the sh making the rst decision at the time the rst decision is made in clear (dash line,
lled circles) and turbid (solid line, crosses) water treatments. (a) Two, (b) four and (c) eight sh. Lines are the predicted trends calculated from GLMM coefcients. The y-axes show
natural log transformed nearest-neighbour distance for visual clarity in plotting.
A. C. Chamberlain, C. C. Ioannou / Animal Behaviour 156 (2019) 129e138132
bloodworms consumed as the response variable, whether at least
50% of the bloodworms were eaten in each trial was analysed as an
alternative measure of food consumed. In 79% of trials (271 of 343),
all or none of the bloodworms were consumed, suggesting that
much of the variation in the proportion of bloodworms consumed
was captured by a simple threshold of whether 50% were
consumed. To analyse the speedeaccuracy trade-off (i.e. the rela-
tionship between the decision-making time and whether the
rewarding arm was chosen rst), the time taken to make the rst
decision (i.e. cross the arena) was used as the response variable and
decision-making accuracy was included as an additional explana-
tory variable in a negative binomial GLMM.
The initial model for each response variable included all two-
way interactions between the water treatment (clear or turbid),
the number of sh in the group (a continuous variable: 2, 4 or 8)
and trial number (also a continuous variable: 1st to the 10th) terms.
Using a stepwise backward elimination approach, models were
simplied to remove nonsignicant interactions (P>0.05) and the
nal models always included all main effects. Group identity was
also always included as a random factor. The dispersion parameter
for each statistical model was checked to be approximatelyequal to
one using an equivalent generalized linear model without a
random term. Statistical analyses were carried out using R version
3.14.2 (The R Foundation for Statistical Computing, Vienna, Austria,
http://www.r-project.org).
Ethical note
All procedures were approved by the University of Bristol
Ethical Review Group (UIN UB/11/042 and UB/14/045). Manipu-
lating turbidity using dissolved clay powder is a common
method in laboratory experiments (Ferrari, Lysak, &Chivers,
2010), and has been used in previous behavioural studies of
sh with no observed ill effects (Vollset &Bailey, 2011). Turbidity
less than 40 NTU was used which is within ecologically realistic
limits in the habitats of sticklebacks where turbidity can change
rapidly due to increased precipitation and runoff from sur-
rounding land. A number of studies have shown the use of clay
powder to induce turbidity has no signicant effect on water pH
(Johannesen, Dunn, &Morrell, 2012; Leahy et al., 2011). After use
in the laboratory, sh were rehomed in a pond unconnected to
other water bodies, in accordance with the U.K.s Environment
Agency regulations.
RESULTS
Latency to Leave the Refuge
The latency of the rst sh to leave the refuge was signicantly
longer in turbid water and increased over repeated trials (negative
binomial GLMM: turbidity:
c
21
¼4.93, P¼0.026; trial number:
c
21
¼44.62, P<0.0001; Appendix Fig. A2). As expected, the latency
to leave the refuge decreased with increasing group size
(
c
21
¼28.22, P<0.0001).
Time Taken to Make First Decision
The time taken to make the rst decision, that is, the time taken
from a sh rst leaving the refuge to a sh rst crossing one of the
decision lines into an arm, depended upon a signicant interaction
between group size and trial number, where repeated exposure
over sucessive trials had no effect on groups of two but groups of
four and eight became slower over repeated trials (negative bino-
mial GLMM: group size*trial number:
c
21
¼9.26, P¼0.002;
Appendix Fig. A3). Independent of this effect, the time taken to
make the rst decision was higher in turbid water (
c
21
¼27.60,
P<0.0001; Appendix Fig. A3).
Decision-Making Accuracy
Conrming that the food was adequately concealed from the
sh when they rst chose an arm, the tted probability of choosing
the rewarding arm at the start of testing was approximately 0.5
(Fig. 2). The probability of the rewarding arm being chosen rst
increased over successive trials in the turbid treatment but
remained close to chance levels (0.5) in clear water (binomial
GLMM: water treatment*trial number:
c
21
¼7.60, P¼0.006; Fig. 2).
Group size had no signicant effect on decision-making accuracy
(
c
21
¼0.80, P¼0.37).
We then assessed whether the time taken to make the rst
decision was related to accuracy (choosing the rewarding arm or
not), to determine whether the sh showed a speedeaccuracy
trade-off during decision making. The time taken to make the
rst decision (the response variable) depended signicantly upon
the interaction between water clarity and accuracy of decision
making (negative binomial GLMM:
c
21
¼4.80, P¼0.029; Fig. 3). In
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Trial number
Probability 50% bloodworms consumed
(a) (b) (c)
Figure 5. The effect of group size and trial number on whether 50% of the bloodworms were eaten in clear (dash line, lled circles) and turbid (solid line, crosses) water treatments.
(a) Two, (b) four and (c) eight sh. The lines are the predicted values calculated from GLMM coefcients. Jitter has been added to the raw data to allow overlapping points to be
visualized.
A. C. Chamberlain, C. C. Ioannou / Animal Behaviour 156 (2019) 129e138 13 3
turbid water, decisions took longer to make if they were accurate
(Fig. 3a) whereas in clear water, the time taken to make the rst
decision was not associated with decision accuracy (Fig. 3b). In
contrast to the statistical model where accuracy was not included
as a main effect, group size and trial number had nonsignicant
effects on time taken to make the rst decision (group size:
c
21
¼2.07, P¼0.15; trial number:
c
21
¼3.14, P¼0.77).
Social Cohesion of the First Fish to Choose an Arm
The NND of the rst individual to make a decision regarding
which arm to choose (the deciding sh) depended signicantly on
water turbidity, group size and trial number (Fig. 4), although there
were no signicant interaction terms. The NNDs increased as the
trials progressed (negative binomial GLMM:
c
21
¼24.43,
P<0.0001) and, as expected, were lower in larger groups
(
c
21
¼27.23, P<0.0001). They were signicantly greater in the
turbid water treatment (
c
21
¼5.06, P¼0.025), that is, the rst sh
to make a decision was further from its nearest neighbour in turbid
water.
In the turbid water treatment, there was a signicantly smaller
proportion of the group out of the refuge when the rst decision
was made compared to the clear water treatment (binomial GLMM:
water treatment:
c
21
¼19.25, P<0.0001; Appendix Fig. A4). With
increasing group size and trials, the proportion of sh out of the
refuge also decreased (group size:
c
21
¼14.90, P<0.0005; trial
number:
c
21
¼52.20, P<0.0001). Although the proportion of sh
per group declined with group size, the probability that at least one
other sh was out of the refuge increased with group size, as ex-
pected (
c
21
¼11.98, P¼0.001). There was no effect of trial number
(
c
21
¼2.98, P¼0.084). Reecting the trend of the proportion of the
group out of the refuge, the probability that another sh was out of
the refuge when the rst decision was made was lower in turbid
water (
c
21
¼4.77, P¼0.029).
These results demonstrate the increased isolation of the sh
making a decision in turbid water, controlling for the number of sh
in each trial. To explore these trends further, we repeated the
analysis of the deciding sh's NND but only including cases when at
least one other sh was out of the refuge (285 trials remained in
this analysis, compared to 331 trials in the initial analysis of NND).
While the NND still decreased when larger groups were tested
(negative binomial GLMM:
c
21
¼14.89, P<0.0005) and increased
as trials progressed (
c
21
¼27.56, P<0.0001), the effect of water
turbidity became nonsignicant (
c
21
¼1.13 , P¼0.29). This suggests
that the effect of water turbidity on NND was mainly driven by
whether or not there were any other sh out of the refuge, and
when two or more sh were out, the deciding sh could maintain a
similar NND in both clear and turbid water.
Time to Locate Food and Proportion of Bloodworms Eaten
The time taken to locate food, that is, the latency between rst
entering an arm and initiating feeding, was signicantly longer in
turbid water (negative binomial GLMM: water treatment:
c
21
¼11.42, P¼0.001; Appendix Fig. A5a). This included latencies
from the incorrect arm being chosen rst, although this cannot
explain the longer times taken in turbid water as choosing the
incorrect arm rst was not more frequent in the turbid treatment
(Fig. 2). The time taken to locate food also increased signicantly
with trial number (trial number:
c
21
¼8.35, P¼0.004; Appendix
Fig. A5b). Group size had no signicant effect (group size:
c
21
¼0.026, P¼0.87).
Whether at least half of the bloodworms were eaten in each trial
was signicantly affected by an interaction between group size and
trial number (binomial GLMM:
c
21
¼12.45, P<0.0005) and an
interaction between the water treatment and trial number (GLMM:
c
21
¼4.020, P¼0.045). Fewer bloodworms were eaten as trials
progressed, as expected if the sh became satiated over repeated
trials. In earlier trials per group, larger groups were more likely to
eat at least 50% of the food compared to smaller groups, although
this probability declined to close to zero for all group sizes as trials
progressed (Fig. 5). Similarly, sh tended to consume fewer
bloodworms in earlier trials in turbid versus clear water, but the
difference also declined as the trials progressed.
DISCUSSION
Our results demonstrate effects of water turbidity at multiple
stages of foraging in a social context. The latencies of the rst sh to
leave the refuge, make the rst decision and consume the food after
choosing an arm were all slower in turbid water, with these effects
being independent of group size and trial order (i.e. there were no
interactions with these variables and the turbidity treatment). The
higher latencies are consistent with reduced activity in turbid
water. This suggests that the perception of predation risk was
higher in turbid water in our experiment; the latency to leave a
refuge in particular is commonly used to assay perception of risk in
sh (Ajemian et al., 2015; Bevan et al., 2018). The higher perception
of risk in the turbid treatment could be a consequence of turbidity
being a more novel environment, rather than turbidity being
perceived as a higher risk habitat per se. However, we found no
evidence that the water treatment affected how the latencies
changed over repeated trials, suggesting novelty of a turbid envi-
ronment, which would decrease with more experience, was not
driving the effects on perceived risk. The sh may have reduced
their activity to acquire adequate information in the visually con-
strained turbid water, but this would not explain why fewer of the
available bloodworms were eaten in the turbid water treatment,
which also supports the interpretation that the turbid treatment
condition was perceived as riskier.
Olfactory cues from the bloodworms did not appear to inuence
the rst decision made; the probability of choosing the rewarding
arm would be expected to be greater than 0.5 if nonvisual cues
were being used. Evidence of improved decision making over time,
possibly due to learning, came from the sh increasing their
probability of choosing the correct (i.e. rewarding) arm as trials
progressed, but only in the turbid water treatment. Fish in the clear
water treatment tended to choose arms randomly throughout
testing. This is particularly surprising because sticklebacks are
known to use landmarks during spatial learning (Odling-Smee &
Braithwaite, 2003), and the ability to detect landmarks would be
constrained in more turbid water (Utne &Utne-Palm, 2002).
Together with the apparent increased perception of risk in the
turbid water treatment, this result suggests that improved decision
making over time occurred only in the turbid water treatment due
to the increased cost of making a wrong decision. An increased cost
could arise from moving over a greater area than is necessary,
which would increase the chance of encountering a predator the
sh are unable to detect from a distance in turbid water. This would
also explain the reduced activity in turbid water (Ajemian et al.,
2015), and could be studied further by measuring the movement
of the sh under the different conditions (Ioannou, Ruxton, &
Krause, 2008). The cost of making an inaccurate decision is
further supported by there being a speedeaccuracy trade-off only
in turbid water, where choosing the rewarding arm took longer
than choosing the incorrect arm. When the risk of making an
inaccurate decision is high, speed is typically reduced to maximize
accuracy (Chittka, Skorupski, &Raine, 2009). Thus, our results
suggest the sh made more careful (i.e. risk-averse) decisions that
showed patterns typical of other decision-making studies (e.g. a
A. C. Chamberlain, C. C. Ioannou / Animal Behaviour 156 (2019) 129e138134
speedeaccuracy trade-off) when perceived risk was high from
being in a turbid environment.
Despite these multiple lines of evidence that turbid water con-
ditions were perceived as higher risk, the analysis of the spatial
distribution of sh at the point when a sh rst chose an arm of the
maze shows that a reduced proportion of the group was outside the
refuge in turbid water and the deciding sh was more likely to be
alone, and this drove an increased NND for the deciding sh.
Increased shoaling after exposure to predation risk has been
demonstrated previously (Hoare, Couzin, Godin, &Krause, 2004);
thus, the increased perception of risk in turbid water should result
in greater cohesion with groupmates. One possibility is that
grouping may be a less benecial antipredator strategy for in-
dividuals in turbid environments, a key issue often ignored in
studies comparing antipredator behaviour in turbid versus clear
water conditions. Of the common antipredator grouping mecha-
nisms (Ioannou, 2017a, 2017b), the confusion effect is less likely to
be effective in turbid conditions as predators targeting one of
multiple prey from a group should be less confused when nearby
prey are less visible. However, the increased uncertainty regarding
the presence of a predator should increase reliance on group
(rather than individual) vigilance, and hence make groups safer
than solitary individuals in turbid water. The effect of turbidity is
distance dependent, having a greater effect when objects are
further away. Thus, larger groups will not be as conspicuous as they
are in clear water, and encounter rates between predator and prey
will instead be more important. As aggregation in prey reduces
encounter rates with predators (Ioannou, Bartumeus, Krause, &
Ruxton, 2011), turbid water should thus favour larger groups.
A more likely explanation for reduced shoaling is that the
reduced visibility in turbid water acted as a constraint to social
interactions. Vision is a key sensory modality used in the formation
and maintenance of shoals in many sh species (Ioannou, Couzin,
James, Croft, &Krause, 2011), and the optical effects of turbidity
mean that while individuals in close proximity are visible to one
another, visual contact is quickly lost once interindividual distances
increase. This optical property of turbidity is consistent with the
results from the NND analysis: with at least one other sh out of the
refuge, the rst sh to make a decision was able to maintain visual
contact with another sh and maintain similar NNDs as in clear
water. Although sticklebacks can shift reliance from visual to ol-
factory cues (Suriyampola et al., 2018; Webster et al., 2007), our
results suggest that they are not able to fully compensate for
reduced visual cues in turbid water during shoaling. Previous
studies have shown reduced shoaling in turbid conditions (Borner
et al., 2015; Fischer &Frommen, 2013; Kimbell &Morrell, 2015);
by examining effects of turbidity on other behaviours such as refuge
use and foraging in parallel with the social cohesion of the deciding
sh, our study provides evidence that turbidity constrains shoaling
behaviour, rather than the reduced tendency to shoal being an in-
direct response to lower perceived risk in turbid environments.
We have demonstrated the impact of turbidity on foraging
behaviour via increased perception of risk which inuences deci-
sion making, but that turbidity also constrains greater shoal cohe-
sion in response to increased risk. The multiple potential
mechanisms underlying our results demonstrate the complexity of
understanding behaviour in environments where sensory systems
are limited, as both proximate (the reduced ability to detect other
group members) and adaptive (the effects of reduced ability to
detect, and be detected by, predators) factors operate simulta-
neously. Improving our understanding of the social responses to
turbidity and other changes driven by anthropogenic activity, such
as ocean acidication (Duteil et al., 2016) and increasing noise
(Herbert-Read, Kremer, Bruintjes, Radford, &Ioannou, 2017; Tidau
&Briffa, 2019), is essential in implementing appropriate mitigation
strategies for natural populations, given the predicted increase in
anthropogenic disturbance in aquatic habitats and potential
widespread implication for individual tness and population
viability (Nel et al., 2009). Our study suggests that sticklebacks can
respond plastically to increased turbidity by slowing their foraging
and making more accurate decisions, which may minimize short-
term negative impacts.
Acknowledgments
We thank Sean A. Rands, Amy S.I. Wade and two anonymous
referees for comments. This work was supported by a Natural
Environment Research Council Independent Research Fellowship
(NE/K009370/1) and responsive mode standard grant (NE/
P012639/1) awarded to C.C.I. The authors declare they have no
competing interests.
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Appendix
0
5
10
15
20
25
30
5101520
Mean turbidity (NTU)
Da
y
Figure A1. Turbidity levels in the experimental V-maze remained stable between the front (open circles) and back (crosses) of the arena, across each day in both the turbid (high
NTU values) and clear (low NTU values) treatments. Water samples were taken from both ends of the maze at the start and end of each day to monitor turbidity, which was
determined using a calibrated spectrophotometer. Turbidity did not vary signicantly within each treatment at different locations or at the start or end of the test days (two-way
ANOVA for each turbid and clear treatments: start or end of day: turbid: F
1,45
¼1.8, P¼0.18; clear: F
1,40
¼0.25, P¼0.62; position in maze: turbid: F
1,45
¼0.001, P¼0.98; clear:
F
1,40
¼0.14, P¼0.72).
A. C. Chamberlain, C. C. Ioannou / Animal Behaviour 156 (2019) 129e138136
0
1
2
3
4
5
6
0
1
2
3
4
5
6
Clear Turbid
Water treatment
Latency to leave refuge (In(s))
13579
Trial number
(a) (b)
Figure A2. The latency to leave the refuge (a) in the clear and turbid water treatments and (b) across trials. Medians are illustrated by thick black lines, the interquartile range (IQR)
is shown within the boxes and the whiskers represent data points within 1.5 x IQR. The circles represent data points outside the whiskers. The y-axes show natural log transformed
latency to leave the refuge for visual clarity in plotting.
1
2
3
4
5
6
7
8
13579
1
2
3
4
5
6
7
8
13579
1
2
3
4
5
6
7
8
13579
Time taken to make first decision (In(s))
Trial number
(a) (b) (c)
Figure A3. The effect of group size and trial number on the time taken to make the rst decision from the rst sh leaving the refuge for both clear (dash line, lled circles) and
turbid (solid line, crosses) water. (a) Two, (b) four and (c) eight sh. The tted lines are calculated from the coefcients of the GLMM. The y-axes show natural log transformed
latency to cross the arena for visual clarity in plotting.
A. C. Chamberlain, C. C. Ioannou / Animal Behaviour 156 (2019) 129e138 137
0
0.2
0.4
0.6
0.8
1
13579
0
0.2
0.4
0.6
0.8
1
13579
0
0.2
0.4
0.6
0.8
1
13579
Trial number
Proportion of fish out of refuge
(a) (b) (c)
Figure A4. The effect of group size and trial number on the proportion of sh outside the refuge at the moment th e rst decision was made, across clear (dash line, lled circles) and
turbid (solid line, crosses) water treatments. (a) Two, (b) four and (c) eight sh. The tted lines are calculated from the coefcients of the GLMM.
2
3
4
5
6
7
2
3
4
5
6
7
Clear Turbid 1357
Water treatment Trial number
Time taken to find food (In(s))
(a) (b)
Figure A5. The effect of (a) water treatment and (b) trial number on the time taken to nd food after an arm of the maze was chosen for the rst time. Medians are illustrated by
thick black lines, the interquartile range (IQR) is shown within the boxes and the whiskers represent data points within 1.5 x IQR. The circles represent data points outside the
whiskers. The y-axes show natural log transformed latency to leave the refuge for visual clarity in plotting.
A. C. Chamberlain, C. C. Ioannou / Animal Behaviour 156 (2019) 129e138138
... In particular, we found that in D. rerio, not only the range of the attraction and alignment interactions was much shorter but also the perception was strongly reduced in front of a fish, both features contributing to a much weaker coordination of motion in pairs of fish in this species in comparison with H. rhodostomus. Certain characteristics of the natural environment in which fish swim, such as water turbidity [46][47][48] or light intensity [49], can also affect the perception of individuals and, consequently, the social interactions. Studies have shown that, as turbidity increases, fish form and maintain groups less efficiently, inter-fish distance increases, and groups are less able to coordinate their collective behavior [46][47][48]. ...
... Certain characteristics of the natural environment in which fish swim, such as water turbidity [46][47][48] or light intensity [49], can also affect the perception of individuals and, consequently, the social interactions. Studies have shown that, as turbidity increases, fish form and maintain groups less efficiently, inter-fish distance increases, and groups are less able to coordinate their collective behavior [46][47][48]. All these results show that the sensory perception characteristics of individuals have a deep impact on their ability to coordinate their movements which in turn conditions the way information propagates within a group [50,51] and the emergence of other groups level properties such as collective sensing [52,53]. ...
... For instance, it is shown in [31] that the intensity of the alignment interaction for Kuhlia mugil is roughly proportional to the mean velocity of the school. Moreover, water turbidity [46][47][48] and/or light intensity [49] have been shown to impact the interactions between fish. For instance, the authors of [49] have shown that in darkness and under low illuminance, H. rhodostomus move with lower polarization and a large mean nearest-neighbor distance that can span many body lengths. ...
Article
Full-text available
In moving animal groups, social interactions play a key role in the ability of individuals to achieve coordinated motion. However, a large number of environmental and cognitive factors are able to modulate the expression of these interactions and the characteristics of the collective movements that result from these interactions. Here, we use a data-driven fish school model to quantitatively investigate the impact of perceptual and cognitive factors on coordination and collective swimming patterns. The model describes the interactions involved in the coordination of burst-and-coast swimming in groups of Hemigrammus rhodostomus. We perform a comprehensive investigation of the respective impacts of two interactions strategies between fish based on the selection of the most or the two most influential neighbors, of the range and intensity of social interactions, of the intensity of individual random behavioral fluctuations, and of the group size, on the ability of groups of fish to coordinate their movements. We find that fish are able to coordinate their movements when they interact with their most or two most influential neighbors, provided that a minimal level of attraction between fish exist to maintain group cohesion. A minimal level of alignment is also required to allow the formation of schooling and milling. However, increasing the strength of social interactions does not necessarily enhance group cohesion and coordination. When attraction and alignment strengths are too high, or when the heading random fluctuations are too large, schooling and milling can no longer be maintained and the school switches to a swarming phase. Increasing the interaction range between fish has a similar impact on collective dynamics as increasing the strengths of attraction and alignment. Finally, we find that coordination and schooling occurs for a wider range of attraction and alignment strength in small group sizes.
... Considering macroinvertebrate community size structure, older and larger macroinvertebrate larval stages are usually under stronger predatory pressure than younger and smaller specimens (Chamberlain and Ioannou, 2019). It is possible that in the SK, turbidity acted as a certain visual constraint for fish (cf. ...
... It is possible that in the SK, turbidity acted as a certain visual constraint for fish (cf. Chamberlain and Ioannou, 2019), reducing the predatory pressure over macrozoobenthos, and enabling their growth to larger dimensions. Furthermore, larger macroinvertebrate specimens mainly belonged to predatory (e.g., Odonata, Heteroptera) and/or elongate-bodied grazers and detritivores (e.g., Chironomidae, Oligochaeta, some Ephemeroptera). ...
Article
The littoral zone of shallow water bodies (SWB) is highly susceptible to water level fluctuations (WLF) caused by ongoing climate-related hydrologic regime changes. The present study assessed the macrozoobenthos structure in the littoral of three temperate SWB after pronounced WLF and accompanying reduction of macrophyte coverage caused by excessive precipitation. The three SWB differed in environmental conditions – S1 (transparent lake covered with submerged macrophytes dominated by Ceratophyllum demersum); S2 (turbid lake without macrophyte coverage) represented the two interconnected backwater basins of the Sutla River watershed; and SK (Škrčev kut oxbow; highly turbid lake sparsely covered by floating-leaved Nuphar lutea) located in the Krapina River watershed (Croatia). With the aim to disentangle the littoral food web structure, and interactions among environmental conditions as well as structural and functional traits of the littoral community within the three SWB, the macrozoobenthos functional traits, trophic guilds and body size were correlated with the littoral environmental conditions, and with the traits of the potential macrozoobenthos prey (zooplankton) and predators (fish). Our results suggest that the littoral macrozoobenthos assemblage responded to the water level increase mainly by the decline of macroinvertebrate diversity and abundance. Due to loss of habitat heterogeneity, in general, larger-sized macroinvertebrates dominated the littoral zone of turbid SWB, particularly with high WLF, while smaller-sized detritivores and grazers prevailed in the littoral zone of the transparent SWB covered by submerged macrophytes. The correlations between different macrozoobenthos, zooplankton and fish size classes indicated that the larger-sized predatory macroinvertebrates prey on smaller-sized zooplankters and avoid predation of mid-sized fish. On the other hand, the abundance of smaller-sized macroinvertebrate detritivores and grazers, which were significantly correlated with concentrations of suspended detritus and algae, prevailed in the SWB covered by submerged macrophytes. Within the macrophyte-covered littoral habitats, macroinvertebrates coexisted with small-sized fish and zooplankters as well as with large-sized pelagic zooplankters, likely seeking shelter from fish. We assume that the increased abundance of larger-sized specimens affected macroinvertebrates and fish within the littoral community upon water level increase. Such a pattern could be recognized as an indicative trait in the evaluation of ecosystem functioning. Furthermore, we conclude that the structural and functional traits of the SWBs’ littoral communities could help us predict the ecological consequences of the climate-induced WLF.
... Turbidity also influences behavior such as feeding rates (e.g., Stuart-Smith et al. 2004) and mating patterns (e.g., Candolin 2009). Although turbidity is known to influence predation (e.g., Gregory and Northcote 1993;Bonner and Wilde 2002), growth in fishes (e.g., Sobral and Widdows 2000), population size (e.g., Sigler et al. 1984), recognition of predators and non-predators (Chivers et al. 2013), and the selection of morphological features (e.g., Franssen 2011, 2012), little is known about its influences on the collective behavior of fishes, such as forming and traveling in groups (although see Fischer and Frommen 2013;Borner et al. 2015;Kimbell and Morrell 2015a, b;Chamberlain and Ioannou 2019). ...
... Studies of shoaling fishes show a general correlation between the amounts of light reaching the eye of a fish and how close fish swim together or how long they stay together (Shaw 1961;Hunter 1968) and that shoals tend to disperse in darkness (Ryer and Olla 1998). Furthermore, Chamberlain and Ioannou (2019) concluded that while risk perception intensified in turbid waters, three-spined sticklebacks, Gasterosteus aculeatus, still showed lower group cohesion due to sensory (visual) limitation. Our findings, in addition to these, make sensory limitation more plausible. ...
Article
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Changes to the environment often affect animal behavior at the individual and group levels. For aquatic species, disturbances such as heavy rains and runoff may create a highly turbid (i.e., cloudy or visually obscured) environment, which potentially may affect individual interactions and group coordination. Surprisingly, we know little about how decreases in water clarity may influence important collective behavior, such as shoaling in fishes. We hypothesize that differences in water clarity would alter collective movement in fishes. We used an automated video tracking software to collect and process continuous, high-resolution spatial data in both clear and turbid waters. We studied two species of fishes that rely on vision for shoaling, the red shiner (Cyprinella lutrensis) and the sand shiner (Notropis stramineus). For each species, we used 20 groups of five fish each in a mixed-model design with three turbidity treatments: 0, 50–150, and 200–300 nephelometric turbidity units (NTUs). There were species-specific differences, but the patterns of response to turbidity were similar. Both species experienced decreased collective behavior in response to turbidity as indicated by significant increases in interfish distances and shoaling area as well as decreases in velocity. These findings show that turbidity may significantly influence collective behavior and group structure and are consistent with (but not conclusively so) a sensory limitation causation. We also provide basic knowledge in an area that is understudied and may be useful for conservation and management objectives, especially at a time when so many fishes are threatened due to habitat degradation and alteration. Significance statement Collective behavior, i.e., coordinated behavior of groups of animals that often increases survivorship and fitness, occurs in many animals, e.g., schooling in fishes, flocking by birds, and herding by mammals. Habitats are being altered worldwide by human activities such as construction and agriculture. Using fishes, we studied how disruptions to the environment would alter collective behavior. Natural and human disturbances cause higher sedimentation and nutrient loads in aquatic habitats, causing water to become murky, i.e., turbid. We developed and used a computer program to study swimming patterns of shoaling fishes in such conditions. We found that fishes formed and maintained groups less efficiently as water became more turbid. Studies at various levels of the organization are essential in understanding the impacts of such disturbances to habitats, and this includes how disturbances to the environment can alter the collective behavior of fishes.
... This has been shown to reduce group cohesion in a number of fish species (e.g. guppy, Poecilia reticulata: Kimbell and Morrell, 2015; three-spined stickleback, Gasterosteus aculeatus: Chamberlain and Ioannou, 2019), and could act synergistically, antagonistically or additively with sound, potentially influencing its effectiveness in guiding fish. ...
Thesis
Rising levels of anthropogenic underwater sound may have negative consequences on freshwater ecosystems. Additionally, the biological relevance of sound to fish and observed responses to human-generated noise promote the use of acoustics in behavioural guidance technologies that are deployed to control the movement of fish. For instance, acoustic stimuli may be used to prevent the spread of invasive fishes or facilitate the passage of vulnerable native species at man-made obstructions. However, a strong understanding of fish response to acoustics is needed for it to be effectively deployed as a fisheries management tool, but such information is lacking. Therefore, this thesis investigated the group behavioural responses of cyprinids to acoustic stimuli. A quantitative meta-analysis and experimental studies conducted in a small-tank or large open-channel flume were used to address key knowledge gaps that are necessary to improve the sustainability of acoustic deterrent technologies, and assist in conservation efforts to reduce the negative impacts of anthropogenic noise. Current understanding on the impact of anthropogenic noise on fishes (marine, freshwater and euryhaline species) was quantified. The impact of man-made sound is greatest for fish experiencing anatomical damage, for adult and juveniles compared to earlier life-stages, and for fish occupying freshwater environments. These findings suggest a review of the current legislation covering aquatic noise mitigation which commonly focus on marine-centric strategies, thereby undervaluing the susceptibility of freshwater fish to the rising levels of anthropogenic sound. Limitations and knowledge gaps within the literature were also identified, including: 1) group behavioural responses to sound, 2) the response of fish to different fundamental acoustic properties of sound, 3) system longevity (e.g. habituation to a repeated sound exposure), and 4) site-specific constraints. Fish movement and space use were quantified using fine-scale behavioural metrics (e.g. swimming speed, shoal distribution, cohesion, orientation, rate of tolerance and signal detection theory) and their collective response to acoustics assessed using two approaches. First, a still-water small tank set-up allowed for the careful control of confounding factors while investigating cyprinid group response to fundamental acoustic properties of sound (e.g. complexity, pulse repetition rate, signal-to-noise ratio). Second, a large open-channel flume enabled the ability of a shoal to detect and respond to acoustic signals to be quantified under different water velocities. Shoals of European minnow (Phoxinus phoxinus), common carp (Cyprinus carpio) and roach (Rutilus rutilus) altered their swimming behaviour (e.g. increased group cohesion) in response to a simple low frequency tonal stimulus. The pulse repetition rate of a signal was observed to influence the long-term behavioural recovery of minnow to an acoustic stimulus. Furthermore, signal detection theory was deployed to quantify the impact of background masking noise on the group behavioural response of carp to a tonal stimulus, and investigate how higher water velocities commonly experienced by fish in the wild may influence the response of roach to an acoustic stimulus. Fine-scale behavioural responses were observed the higher the signal-to-noise ratio, and discriminability of an acoustic signal and the efficacy at which fish were deterred from an insonified channel was greatest under higher water velocities. The information presented in this thesis significantly enhances our understanding of fish group responses to man-made underwater sound, and has direct applications in freshwater conservation, fish passage and invasive species management.<br/
... Vision directly influences collective behavior in a range of fish species including mackerel [60], tuna [61], and striped jack [62], among others. Many fish species that show robust collective behavior under normal conditions do not exhibit a complete loss of collective behavior when vision is impeded (via reduced light intensity or a physical barrier covering the eyes), but do exhibit pronounced differences in group structure, such as in saithe [63] and sticklebacks [64]. Therefore, the first point we clarified is the relationship between the loss of sight and the loss of schooling in cavefish. ...
Article
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Fish display a remarkable diversity of social behaviors, both within and between species. While social behaviors are likely critical for survival, surprisingly little is known about how they evolve in response to changing environmental pressures. With its highly social surface form and multiple populations of a largely asocial, blind, cave-dwelling form, the Mexican tetra, Astyanax mexicanus , provides a powerful model to study the evolution of social behavior. Here we use motion tracking and analysis of swimming kinematics to quantify social swimming in four Astyanax mexicanus populations. In the light, surface fish school, maintaining both close proximity and alignment with each other. In the dark, surface fish no longer form coherent schools, however, they still show evidence of an attempt to align and maintain proximity when they find themselves near another fish. In contrast, cavefish from three independently-evolved populations (Pachón, Molino, Tinaja) show little preference for proximity or alignment, instead exhibiting behaviors that suggest active avoidance of each other. Two of the three cave populations we studied also slow down when more fish are present in the tank, a behavior which is not observed in surface fish in light or the dark, suggesting divergent responses to conspecifics. Using data-driven computer simulations, we show that the observed reduction in swimming speed is sufficient to alter the way fish explore their environment: it can increase time spent exploring away from the walls. Thus, the absence of schooling in cavefish is not merely a consequence of their inability to see, but may rather be a genuine behavioral adaptation that impacts the way they explore their environment.
... Social interactions can be influenced by environmental factors such as food abundance and potential predation risk (Beauchamp, 2004;Schaerf et al., 2017), but also by many aspects of the abiotic environment, including light levels (Ginnaw et al., 2020), temperature (Bartolini et al., 2015), hypoxia (Domenici et al., 2017), turbidity (Chamberlain and Ioannou, 2019), and habitat structure (Takada and Minami, 2021), as well as by anthropogenic changes such as acoustic noise (Currie et al., 2020), and pollutants . While environmental factors can impact behavior through the masking of cues and signals (McNett et al., 2010) and shifting attention to other tasks (Chan et al., 2010), environmental conditions can also affect behavior via physiological changes. ...
Article
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As individual animals are exposed to varying environmental conditions, phenotypic plasticity will occur in a vast array of physiological traits. For example, shifts in factors such as temperature and oxygen availability can affect the energy demand, cardiovascular system, and neuromuscular function of animals that in turn impact individual behavior. Here, we argue that nonlinear changes in the physiological traits and performance of animals across environmental gradients—known as physiological performance curves— may have wide-ranging effects on the behavior of individual social group members and the functioning of animal social groups as a whole. Previous work has demonstrated how variation between individuals can have profound implications for socially living animals, as well as how environmental conditions affect social behavior. However, the importance of variation between individuals in how they respond to changing environmental conditions has so far been largely overlooked in the context of animal social behavior. First, we consider the broad effects that individual variation in performance curves may have on the behavior of socially living animals, including: (1) changes in the rank order of performance capacity among group mates across environments; (2) environment-dependent changes in the amount of among- and within-individual variation, and (3) differences among group members in terms of the environmental optima, the critical environmental limits, and the peak capacity and breadth of performance. We then consider the ecological implications of these effects for a range of socially mediated phenomena, including within-group conflict, within- and among group assortment, collective movement, social foraging, predator-prey interactions and disease and parasite transfer. We end by outlining the type of empirical work required to test the implications for physiological performance curves in social behavior.
... Shifts in the benefits and costs of collective behaviour can result in changes over evolutionary time [12][13][14]. Over within-generation timescales, collective behaviour can change in response to changing environmental conditions, such as cues from predators or food, or abiotic factors such as habitat structure [15][16][17][18][19][20]. Our current understanding of collective behaviour is, however, incomplete from a developmental perspective because there is limited information on the behavioural changes that occur in animal collectives over short timescales without modification to environmental conditions [21][22][23][24][25]. ...
Article
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Despite extensive interest in the dynamic interactions between individuals that drive collective motion in animal groups, the dynamics of collective motion over longer time frames are understudied. Using three-spined sticklebacks, Gasterosteus aculeatus, randomly assigned to 12 shoals of eight fish, we tested how six key traits of collective motion changed over shorter (within trials) and longer (between days) timescales under controlled laboratory conditions. Over both timescales, groups became less social with reduced cohesion, polarization, group speed and information transfer. There was consistent inter-group variation (i.e. collective personality variation) for all collective motion parameters, but groups also differed in how their collective motion changed over days in their cohesion, polarization, group speed and information transfer. This magnified differences between groups, suggesting that over time the ‘typical’ collective motion cannot be easily characterized. Future studies are needed to understand whether such between-group differences in changes over time are adaptive and represent improvements in group performance or are suboptimal but represent a compromise between individuals in their preferences for the characteristics of collective behaviour.
... These collective behaviours serve to provide the group a variety of benefits, including improved foraging, mate selection, and enhanced predator evasion (Parrish et al. 2002;Beauchamp 2013;Rieucau et al. 2015). Recent efforts have demonstrated that anthropogenically induced changes in aquatic environments can affect collective behaviours, including underwater construction noise (Herbert-Read et al. 2017), electricity-generating turbine noise (Duarte et al. 2019), crude oil exposure (Armstrong et al. 2019), and turbidity (Chamberlain and Ioannou 2019). In addition to the effects of underwater noise exposure and water quality, anthropogenically introduced habitat structures have also been shown to impact local hydrology and fish behaviour in both marine and riverine systems (Sánchez-Caballero et al. 2017;Gallo et al. 2019). ...
Article
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Animal groups are known to exhibit collective behaviours that allow for effective responses to predators and environmental factors. Habitats with high levels of structural complexity have been shown to influence the collective tendencies of these animal aggregations. However, the effect of anthropogenically induced habitat complexity on collective tendency is still unknown. We examined the effect of a water control structure (WCS), located in an estuarine salt marsh system, on the collective behaviours of free ranging juvenile Gulf menhaden (Brevoortia patronus), a schooling forage fish. Using an acoustic imaging sonar, behavioural observations prior to and during predator attacks were collected in an open marsh canal as well as in the vicinity of the WCS. We found that fish in schools responded to the WCS by swimming in a less aligned and cohesive manner, while maintaining an increased ability to transfer social information. Our results demonstrate that collective tendency in schooling fish is affected by the presence of anthropogenically introduced habitat complexity, prior to and during predator attack. Our study, thus, strengthens the idea that the complex environmental conditions induced by the presence of man-made structures may play a large role in structuring collective behaviour and trophic interactions in aquatic environments.
Article
High water turbidity, through its multifold influences on aquatic fauna, is considered a major cause of ecological concern. Here we examined the effects of elevated turbidity on the behaviour of a small cyprinid fish, the Stymphalia minnow, Pelasgus stymphalicus, using a combination of the well-established emergence, open field and predator response tests. Subjects from the two treatments differed in the way they emerged from an artificial refuge, with the turbidity-exposed fish being more hesitant. Moreover, these fish were also less active, had a lower propensity to explore and spent less time in the open centre of the test arena, compared to subjects tested in clear water. However, there was no effect of turbidity on the time fish spent immobile. Fish in both treatments responded strongly to a simulated predator attack from above. Turbidity decreased the time fish spent in the centre, the predator simulation decreased time spent immobile and both factors contributed to a decrease in activity, but without significant interaction effects. We discuss how turbidity may increase the perceived predation risk of these prey fish in our test conditions even in the absence of predator cues, as well as the implications of our findings for ecosystem management policy and conservation efforts targeting threatened freshwater fish species.
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In moving animal groups, social interactions play a key role in the ability of individuals to achieve coordinated motion. However, a large number of environmental and cognitive factors are able to modulate the expression of these interactions and the characteristics of the collective movements that result from these interactions. Here, we use a data-driven fish school model (Calovi et al. , 2018; Lei et al. , 2020) to quantitatively investigate the impact of perceptual and cognitive factors on coordination and collective swimming patterns. The model describes the interactions involved in the coordination of burst-and-coast swimming in groups of Hemigrammus rhodostomus . We perform a comprehensive investigation of the respective impacts of two interactions strategies between fish based on the selection of the most or the two most influential neighbors, of the range and intensity of social interactions, of the intensity of individual random behavioral fluctuations, and of the group size, on the ability of groups of fish to coordinate their movements. We find that fish are able to coordinate their movements when they interact with their most or two most influential neighbors, provided that a minimal level of attraction between fish exist to maintain group cohesion. A minimal level of alignment is also required to allow the formation of schooling and milling. However, increasing the strength of social interactions does not necessarily enhance group cohesion and coordination. When attraction and alignment strengths are too high, or when the heading random fluctuations are too large, schooling and milling can no longer be maintained and the school switches to a swarming phase. Increasing the interaction range between fish has a similar impact on collective dynamics as increasing the strengths of attraction and alignment. Finally, we find that coordination and schooling occurs for a wider range of attraction and alignment strength in small group sizes. Author Summary In fish schools, social interactions allow individuals to coordinate their movements and their modulation shape the emergent patterns of collective behavior. Here, we use a data-driven fish school model to investigate the impact of perceptual and cognitive factors on collective swimming patterns in the rummy-nose tetra ( H. rhodostomus ). In this species, fish only pay attention to one or two neighbors that exert the largest influence on their behavior and the interactions consist for a fish to be attracted and aligned with these neighbors. We show that there must exist a minimum level of alignment and attraction between fish to maintain group cohesion and allow the emergence of schooling and milling. Moreover, increasing the interaction range has a similar impact on collective dynamics as increasing the strength of social interactions. However, when the intensity of these interactions becomes too strong, fish can no longer coordinate their swimming and the school adopts a swarming behavior. Our results also show that a moderate level of behavioral fluctuations in fish can induce spontaneous transitions between schooling and milling. Finally, in this species that performs burst-and-coast swimming, we find that coordination occurs for a wider range of interaction strengths only in small group sizes.
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Although consistent behavioural differences between individuals (i.e. personality variation) are now well established in animals, these differences are not always expressed when individuals interact in social groups. This can be key in important social dynamics such as leadership, which is often positively related to personality traits such as boldness. Individuals consistently differ in how social they are (their sociability), so if other axes of personality variation, such as boldness, can be suppressed during social interactions, this suppression should be stronger in more sociable individuals. We measured boldness (latency to leave a refuge when alone) and sociability (time spent with a conspecific) in three-spined sticklebacks (Gasterosteus aculeatus) and tested the boldness-leadership association in pairs of these fish. Both boldness and sociability were repeatable, but were not correlated. When splitting the data between the 50% most sociable and 50% less sociable fish, boldness was more strongly associated with leadership in less rather than more sociable individuals. This is consistent with more sociable fish conforming to their partner's behaviour due to their greater social tendency. One axis of personality variation (sociability) can thus modulate the relationship between others (boldness and leadership), with potential implications for selection on personality variation in social animals.
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Noise produced from a variety of human activities can affect the physiology and behaviour of individual animals, but whether noise disrupts the social behaviour of animals is largely unknown. Animal groups such as flocks of birds or shoals of fish use simple interaction rules to coordinate their movements with near neighbours. In turn, this coordination allows individuals to gain the benefits of group living such as reduced predation risk and social information exchange. Noise could change how individuals interact in groups if noise is perceived as a threat, or if it masked, distracted or stressed individuals, and this could have impacts on the benefits of grouping. Here, we recorded trajectories of individual juvenile seabass (Dicentrarchus labrax) in groups under controlled laboratory conditions. Groups were exposed to playbacks of either ambient background sound recorded in their natural habitat, or playbacks of pile-driving, commonly used in marine construction. The pile-driving playback affected the structure and dynamics of the fish shoals significantly more than the ambient-sound playback. Compared to the ambient-sound playback, groups experiencing the pile-driving playback became less cohesive, less directionally ordered, and were less correlated in speed and directional changes. In effect, the additional-noise treatment disrupted the abilities of individuals to coordinate their movements with one another. Our work highlights the potential for noise pollution from pile-driving to disrupt the collective dynamics of fish shoals, which could have implications for the functional benefits of a group's collective behaviour.
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Collective decisions play a major role in the benefits that animals gain from living in groups. Although the mechanisms of how groups collectively make decisions have been extensively researched, the response of within-group dynamics to ecological conditions is virtually unknown, despite adaptation to the environment being a cornerstone in biology. We investigate how within-group interactions during exploration of a novel environment are shaped by predation, a major influence on the behavior of prey species. We tested guppies (Poecilia reticulata) from rivers varying in predation risk under controlled laboratory conditions and find the first evidence of differences in group interactions between animals adapted to different levels of predation. Fish from high-predation habitats showed the strongest negative relationship between initiating movements and following others, which resulted in less variability in the total number of movements made between individuals. This relationship between initiating movements and following others was associated with differentiation into initiators and followers, which was only observed in fish from high-predation rivers. The differentiation occurred rapidly, as trials lasted 5 min, and was related to shoal cohesion, where more diverse groups from high-predation habitats were more cohesive. Our results show that even within a single species over a small geographical range, decision-making in a social context can vary with local ecological factors.
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Ocean acidification (OA)-caused by rising concentrations of carbon dioxide (CO2)-is thought to be a major threat to marine ecosystems and has been shown to induce behavioural alterations in fish. Here we show behavioural resilience to nearfuture OA in a commercially important and migratory marine finfish, the Sea bass (Dicentrarchus labrax). Sea bass were raised from eggs at 19°C in ambient or near-future OA (1000 µatm pCO2) conditions and n=270 fish were observed 59-68 days post-hatch using automated tracking from video. Fish reared under ambient conditions, OA conditions, and fish reared in ambient conditions but tested in OA water showed statistically similar movement patterns, and reacted to their environment and interacted with each other in comparable ways. Thus our findings indicate behavioural resilience to near-future OA in juvenile sea bass. Moreover, simulated agent-based models indicate that our analysis methods are sensitive to subtle changes in fish behaviour. It is now important to determine whether the absences of any differences persist under more ecologically relevant circumstances and in contexts which have a more direct bearing on individual fitness.
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Larger groups often have a greater ability to solve cognitive tasks compared to smaller ones or lone individuals. This is well established in social insects, navigating flocks of birds, and in groups of prey collectively vigilant for predators. Research in social insects has convincingly shown that improved cognitive performance can arise from self-organised local interactions between individuals that integrates their contributions, often referred to as swarm intelligence. This emergent collective intelligence has gained in popularity and been directly applied to groups of other animals, including fish. Despite being a likely mechanism at least partially explaining group performance in vertebrates, I argue here that other possible explanations are rarely ruled out in empirical studies. Hence, evidence for self-organised collective (or ‘swarm’) intelligence in fish is not as strong as it would first appear. These other explanations, the ‘pool-of-competence’ and the greater cognitive ability of individuals when in larger groups, are also reviewed. Also discussed is why improved group performance in general may be less often observed in animals such as shoaling fish compared to social insects. This review intends to highlight the difficulties in exploring collective intelligence in animal groups, ideally leading to further empirical work to illuminate these issues.
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It is well established that living in groups helps animals avoid predation and locate resources, but maintaining a group requires collective coordination, which can be difficult when individuals differ from one another. Personality variation (consistent behavioural differences within a population) is already known to be important in group interactions. Growing evidence suggests that individuals also differ in their consistency, i.e. differing in how variable they are over time, and theoretical models predict that this consistency can be beneficial in social contexts. We used three-spined sticklebacks (Gasterosteus aculeatus) to test whether the consistency in, as well as average levels of, risk taking behaviour (i.e. boldness) when individuals were tested alone affects social interactions when fish were retested in groups of 2 and 4. Behavioural consistency, independently of average levels of risk-taking, can be advantageous: more consistent individuals showed higher rates of initiating group movements as leaders, more behavioural coordination by joining others as followers, and greater food consumption. Our results have implications for both group decision making, as groups composed of consistent individuals are more cohesive, and personality traits, as social interactions can have functional consequences for consistency in behaviour and hence the evolution of personality variation.
Article
Noise is a form of human-induced rapid environmental change, and mounting evidence suggests that it can affect the sensory environment and consequently the decision-making ability of animals. However, while the effects of anthropogenic noise on individual organisms in the context of movement patterns, foraging and predation risk have been reported, relatively little is known about how noise impacts groups and intraspecific interactions. Here we investigated the effects of anthropogenic noise on grouping preference (i.e. being with conspecifics or alone) in the European hermit crab, Pagurus bernhardus. Hermit crabs live in empty gastropod shells and frequently fight with each other to gain an optimal-fitting shell. Thus, crabs' grouping preference may depend on the optimality of their own shell and thus on their motivation to gain another. To test the effect of shell size and its interaction with noise exposure on grouping preferences, crabs were housed in either suboptimal or optimal shells before being exposed to playbacks of either ship noise or an ambient sound (control) and given the choice to group with one or five conspecifics or to remain alone in a neutral zone. Crabs occupying suboptimal shells had a longer latency to enter the zone with a single crab than crabs in optimal shells. This difference was only seen in the ambient sound treatment, disappearing completely under ship noise. Under ambient sound, crabs in optimal shells spent most of their time close to a single crab, while crabs in suboptimal shells showed no clear preference. However, exposure to ship noise reversed the effect of shell quality on grouping preference. Our results demonstrate that exposure to anthropogenic noise can alter not only individual behaviour but also social behaviour.
Article
When changing environments make the primary sensory modality less useful or reliable, animals may shift their reliance to a different sensory modality. However, such plasticity in sensory modalities may be unlikely outside of critical developmental periods or may depend on the type of behaviour associated with the sensory response. Animals' previous experience with a particular environment and its influence on the reliability of cues may also constrain the occurrence of sensory shifts. Here, we ask about the impacts of changing environments that occur during adulthood on sensory behaviour. Specifically, we housed adult zebrafish, Danio rerio, for 6 weeks either in constantly clear water, or in water that was periodically turbid. We then compared the two groups in terms of their (1) response to a reflexive optomotor stimulus, (2) choice for visual versus olfactory cues in a foraging context and (3) social behaviour. We found that fish with experiences in the turbid context responded less robustly to a reflexive visual stimulus and responded to olfactory as opposed to visual cues as the first choice, suggesting a shift in their primary sensory modality. However, other behavioural measures (e.g. shoal cohesion, charge rate, activity level) depended more on the context in which they were measured than on recent experience. Taken together, these results suggest that recent experiences in particular physical contexts may impact the use of different sensory modalities and visual physiology, but that these effects depend on the type of behaviour being considered. These compensatory shifts between sensory modalities may help animals to buffer other forms of behaviour from major changes in the environment.
Article
Fishes largely depend on visual cues to collect information from their surroundings. In many aquatic habitats, algal turbidity has become an imminent environmental concern. Algal turbidity reduces visibility and may therefore interact with prey preference by altering prey detection and foraging behaviour of predators. We investigated the effects of algal turbidity on prey choice decisions of 3-spined sticklebacks Gasterosteus aculeatus in 2 experiments manipulating turbidity levels (clear <1, 5, 10, 15 and 20 nephelometric turbidity units [NTU] in Expt 1; clear <1 and 15 NTU in Expt 2) and the proportion of prey items-large (1.8-2.0 mm) and small (0.8-1.0 mm) water fleas Daphnia magna. We found an overall negative effect of turbidity on prey consumption by stickleback. Prey selectivity was most pronounced in clear and 5 NTU water, whereas at higher turbidity levels, selectivity decreased. As the ratio of large to small prey increased, the fish became less selective. In addition, we found an interaction effect between turbidity and fish size on the total number of prey consumed. These results indicate that algal turbidity affects the prey choice decisions of sticklebacks, probably because turbidity limits their visual field. Consequently, as fish feed more randomly in turbid water, the structuring effect of fish predators on zooplankton communities will be reduced in turbid environments.