This study investigated the effect of anthropogenic noise on shoaling cohesion in three-spined sticklebacks. The researcher exposed stickleback shoals to white noise playback and found that during noise exposure, the distance between fish in the shoal decreased significantly compared to silent control trials. This suggests that anthropogenic noise causes sticklebacks to group closer together, mirroring their anti-predatory response when threatened by a predator. The findings demonstrate that anthropogenic noise has the potential to influence anti-predatory behavior and vigilance in shoaling fish.

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The effect of anthropogenic noise on shoaling cohesion in three-
spined sticklebacks (Gasterosteus aculeatus)
A report submitted in part fulfilment of the examination requirements for the award of a B.Sc.
(Hons) Animal Behaviour and Welfare awarded by the University of Lincoln, June 2014,
supervised by Tom Pike.
Thomas Trew
12357944

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CERTIFICATE OF ORIGINALITY
This is to certify that I am responsible for the work submitted in this thesis, that the original
work is my own, except as specified in the acknowledgements and in references, and that
neither the thesis nor the original work contained therein has been previously submitted to any
institution for a degree.
Signature:
Name:
Date:
CERTIFICATE OF COMPLIANCE
This is to certify that this project has been carried out in accordance with University principles
regarding ethics and health and safety. Forms are available to view on request.
Signature:
Name:
Date:

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Abstract
Noise pollution in both terrestrial and aquatic habitats has considerably increased over the
last few decades, and there is growing evidence that anthropogenic noise can affect
behaviour in a variety of species. There are increasing concerns that this may affect the
fitness of many animals. A majority of fish species spend a part of their life in shoals,
which are important for both predator protection and group foraging. Therefore the aim of
this study was to assess the effect on anthropogenic noise on shoaling cohesion. To do this,
three-spined sticklebacks (Gasterosteus aculeatus) were used in a tank based playback
experiment. Results showed that during exposure to anthropogenic noise, sticklebacks
would group closer together, essentially mirroring behaviour seen in shoals when
threatened by a predator. The findings of this study suggested anthropogenic noise has the
potential to influence anti-predatory behaviour and vigilance of shoals. Future research is
required for more in depth analyses of the impact anthropogenic noise has on direct fitness.
Keywords
Anthropogenic, noise, pollution, Three-spined stickleback, Gasterosteus aculeatus, shoal,
cohesion, behaviour.
Word count
3464.

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Introduction
The human population is ever growing, and so is its impact on wildlife (Chan et al., 2010).
One factor being the amount of noise pollution we produce, from activities such as urban
development, expansion of transport networks and resource extraction (Wale et al., 2013).
Past studies have shown increasing evidence that anthropogenic (man made) noise can
affect the behaviour of a wide and diverse range of animals (Normandeau Associates, Inc,
2012; Morely et al., 2014; Slabbekoorn and Ripmeester, 2008; Barber et al., 2010).
Anthropogenic noise, especially when loud, persistent, unexpected or novel, has the
potential to cause stress (Wysocki et al., 2006; Wright et al., 2007), to distract (Chan et al.,
2010) and to mask important sounds (Wale et al., 2013; Siemers and Schaub, 2011; Lowry
et al., 2012).
For example, Habib et al. (2007) conducted a study on male ovenbirds (Seiurus
aurocapilla); their results showed that males on louder territories were less likely to attract
a mate than those based at quieter locations. They hypothesized that noise pollution was
interfering with male ovenbirds songs, which could reduce the distance to which females
can hear the songs, or give the perception the male is of lower quality due to distortions of
song characteristics. If female ovenbirds were then to base mate choice on noise conditions
of the males’ territory over size, age and body condition of the male ovenbird; then male
mate pairing success may be negatively affected by anthropogenic noise.
Another example of animal communication being affected by increasing noise pollution
can be seen in the Sun and Narins (2005) study on frogs. They observed that certain
species of pond-dwelling frogs, which were particularly acoustically active, would reduce
their call rate when exposed to playbacks of traffic noise. These results suggest that the
frogs changed their calling behaviour to avoid auditory masking.
Anti-predator vigilance may also be increased by animals when exposed to loud noises.
Rabin et al. (2006) observed that in California ground squirrels (Spermophilus beecheyi)
the individuals located in areas around loud wind turbines exhibited higher rates of
vigilance when hearing alarm calls of conspecifics than those in quieter areas.
It has also been suggested that anti-predator behaviour may be affected by anthropogenic
noise (Chan et al., 2010; Karp and Root, 2009; Wale et al., 2013). Predator avoidance is
crucial for animals survivability and reproduction success (Caro, 2005); and yet there are
few studies that have investigated the potential effect of anthropogenic noise on anti-
predatory behaviour (Voellmy et al., 2014). Chan et al. (2010) observed that whilst

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exposed to anthropogenic noise, simulated predators could get significantly closer to the
Caribbean hermit crabs (Coenobita clypeatus) before they retreated into their shells, in
comparison to the silent trials. They proposed the ‘Distracted prey hypothesis’, which
states that any stimulus an animal can perceive is capable of distracting it by reallocating
part of its finite attention and thus preventing it from responding accordingly to an
approaching threat. Attention is the process by which an individual filters out several
stimuli from the surrounding environment, letting in only as much as it can process
(Bushnell, 1998). Chan et al. (2010) then went on to suggest that anthropogenic noise
could be a distracting stimulus, and could reduce an animal’s fitness by increased
vulnerability to predators.
Another theory as to how anthropogenic noise may affect anti-predatory behaviour is that
the additional noise could mask important acoustic cues produced by predators, or warning
calls from conspecifics (Wale et al., 2013). Prey are often alerted to the presence of
predators by auditory cues, from acts such as intraspecific communication or the
inadvertent sound produced from movement (Barrera et al., 2011; Siemers and Schaub,
2011). Furthermore, alarm calls have evolved into a wide range of animals to warn others
of imminent danger (Hollen and Radford, 2009); other vocalizations can be used to
provide information on the level of risk (Hollen et al., 2008; Bell et al., 2009). Masking
can either be described as ‘energetic’, whereby the masking is complete and the signal is
not detected at all, or ‘informational’, where the signal can be detected by the listener,
however the content is hard to understand (Wale et al., 2013). Either way, there is likely
consequences to foraging and anti-predator behaviour from a reduced ability to detect
valuable auditory information (Brumm and Slabbekoorn, 2005; Siemers and Schaub, 2011;
Lowry et al., 2012).
Fish populations have been negatively impacted by human population growth for a number
of well known reasons (Slabbekoorn et al., 2010) such as fisheries (Jackson et al., 2001),
habitat degradation (Munday, 2004) and chemical pollution (Van Der Oost et al., 2003).
Underwater anthropogenic noise pollution could potentially be another big threat to fish
populations (McDonald et al., 2006). The amount of fresh water and marine noise
pollution produced by humans has been increasing significantly over the last few decades
(Codarin et al., 2009), not just around coastal areas, but also in the open ocean (Andrew et
al., 2002; Tyack, 2008). Sound travels approximately 5 times faster in water than it does in
air (around 1500m/s in water – 300m/s in air), meaning that sound wavelengths are also

6. ~ 6 ~
about 5 times longer in water than they are in air (e.g. 100Hz signal = 15m in water - 3m in
air). This results in sound traveling greater distances and at higher amplitude levels in
water, enabling long distance communication, but also resulting in long distance noise
pollution (Slabbekoorn et al., 2010). For example, anthropogenic noise produced during
pile-driving for wind turbines can be detected over background underwater noise levels
from as far as 70km away (Bailey et al., 2010). This increase of sound amplitude and area
of effect makes underwater anthropogenic noise pollution a real cause for concern
(Slabbekoorn et al., 2010). To this date there’s only one study I am aware of that assesses
the impact of underwater anthropogenic noise on anti-predatory behaviour in fish.
Voellmy et al. (2014) used both European minnow (Phoxinus phoxinus) and three-spined
sticklebacks (Gasterosteus aculeatus) in their study. They observed increased vigilance in
sticklebacks and faster response rates to a simulated predator when exposed to
anthropogenic noise; whereas minnows did not significantly differ in response rate
depending on noise exposure. However, both three-spined sticklebacks and European
minnow are shoaling fish (Huntingford and Ruiz-Gomez, 2009; Ward and Krause, 2001).
Voellmy et al. (2014) only tested the effect of anthropogenic noise on individual anti-
predatory behaviour, even though both species of fish spend a large proportion of their
lives as part of a shoal.
A majority of fish species spend some part of their lives in groups (Shaw, 1978); these
groups of fish are commonly termed as ‘shoals’ (Miller and Gerlai, 2012; Kenedy and
Pitcher, 1975). Predators and food have been said to be the two fundamental keys of
understanding fish shoals (Pitcher, 1993). In order to survive and reproduce successfully,
animals must minimize the risk of starvation and predation (Wale et al., 2013). Living in
shoals is very important for defence against predation; synchronized co-operation confuses
predators and reduces the threat of a successful attack (Pitcher, 1993). Past research has
already shown that anthropogenic noise can have a negative impact on shoaling fish’s
foraging efficiency (Purser and Radford, 2011); however no research that I am aware of
has been done on the effect it has on shoal anti-predatory behaviour. Once a predator is
detected, predator defence takes precedence over food (Pitcher, 1993); suggesting the
results of Purser and Radford’s (2011) study with three-spined sticklebacks was due to the
fish choosing predator defence over food. In the presence of a predator, shoal cohesion
increases (distance between each fish reduces) (Ryer and Olla, 1998); which is why in this
study, I aim to test the effects on anthropogenic noise on shoaling cohesion using three-

7. ~ 7 ~
spined sticklebacks, a small, robust and common fish species which acts as an excellent
model for the scientific study of behaviour and acclimates well to laboratory conditions
(Purse and Radford, 2011; Huntingford and Ruiz-Gomez, 2009). If Purse and Radford’s
(2011) results were, as I suggested, due to the fish displaying anti-predator behaviour; then
I would expect to see that the exposure of anthropogenic noise will result in increase shoal
cohesion.
Methods
Thirty adult three-spined sticklebacks were used as subjects in this study. The Fish used
were sourced from a local drainage ditch off the river Till (grid reference: -53.309418, -
0.651873) in October 2014 and housed in University of Lincolns Minster House aquatics
laboratory, in an 8+/-1°C chilled room; the light timer for this room was set to match the
natural daylight times at the river from which the fish were caught. Prior to the study all
fish were housed in the same 64-L tank, fitted with an Eheim water filter, filled with 45L
of filtered, aerated and chilled tap water and containing artificial plastic plants for shelter.
They were fed on a frozen bloodworm (Chironomid larvae) diet till satiation daily. Testing
shoals consisted of 3 fish; each fish was tested only once, allowing for 10 tests, all with
unique shoals. Three fish would be randomly selected and transferred, using a net, into a
circular (31cm diameter) grey testing tub, filled with 7cm of water. Once in the testing tub,
the fish were left for a 30 minute habituation period. After habituation, the testing period
began, which lasted 1 hour and 30 minutes; consisting of a 30 minute ‘silent’ control trial,
followed by a 30 minute noise exposure trial and ending with another 30 minute ‘silent’
control trail. The silent control trials gave a baseline measure of distance between fish in
ambient conditions (Purser and Radford, 2011; Chan et al., 2010). During the noise
exposure trial the fish were exposed to a playback of white noise for the full 30 minutes;
played through two 10 watt Mila 2.0 speakers, placed opposite each other facing towards
the centre of the testing tub; bandwidth was limited between 100 and 1000 HZ, presenting
frequencies falling under the sticklebacks likely hearing range (Purser and Radford, 2011).
The volume was consistent across all trials and was, to my hearing, set to a level that was
not completely biologically unrealistic to be heard around shorelines with boat activity.
Throughout the whole testing period a Microsoft 2.0 megapixel camera mounted 55cm
directly over the grey testing tub was being used to manually take pictures (via a Dell
latitude x300 notebook) approximately every 60 seconds, giving an aerial view of the fish

8. ~ 8 ~
and their individual locations in the tub. This resulted in 90 images for each shoal, and 900
images in total. After each test, the 3 fish used were moved to another 64-L tank so as to
ensure the same fish were not used more than once; the testing tub would then be emptied
and refilled with fresh water, in preparation for the next shoal.
All 900 images taken during the 10 tests were analysed on Windows 7 Microsoft Paint,
allowing each fish to be allocated coordinates on each picture. The coordinates used were
manually worked out and based at the tip of each individual fish snout. The distance (D)
between two individual fish from each other could be calculated in every image using the
following formula:
where x1 and y1 stands for the X and Y axis coordinates of one fish, x2 and y2 represents
the X and Y axis coordinates for the second fish of which you calculate the distance
between. The average distance between all 3 individuals during the first control, noise
exposure, and second control trials were calculated for each shoal, resulting in 10 averages
of distance between fish for each trial. If my prediction that anthropogenic noise effects
shoaling cohesion is correct, we would expect to see a significant difference in distance
between individuals during the sound trial, when compared to the two control trials. To
examine this I conducted a general linear model with the average distance between fish as
the dependent variable, trial type (pre control, noise exposure and post control) as a fixed
factor, whilst controlling for non independence between the 10 shoals by including shoal
identity as a random effect. I also conducted a post-hoc Tukey test to examine pairwise
differences between trial types.

9. ~ 9 ~
Results
Throughout the whole 90 minutes, the cohesiveness of the shoals differed significantly
(General linear model, F2,18 = 8.70, P = 0.002; Figure 1). Specifically, the post-hoc Tukey
tests revealed that control 1 differed from the sound treatment (T = -3.917, df = 18, P =
0.0028), control 2 differed from the sound treatment (T = -3.199, df = 18, P = 0.0131),
whereas control 1 and control 2 did not differ from each other (T = -0.718, df = 18, P =
0.7563).
Fig 1. Mean ± SE distance (mm) between fish during the three trials types.
0
20
40
60
80
100
120
140
Distance(mm)
Control 1 Sound Control 2
Trial type

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Discussion
The results of this study show that anthropogenic noise impacts shoaling cohesion of three-
spined stickleback shoals. The addition of white noise elicited the same anti-predatory
defensive behaviour (increased shoal cohesion) that is shown in shoals when in the
presence of a predator (Ryer and Olla, 1998). By using two control trials, before and after
the noise exposure trial, the results also showed that there was no difference in shoal
cohesion between the two controls; suggesting that the noise treatment had no lasting
effect on the fish.
The increase in shoal cohesion when exposed to anthropogenic noise mirrors the grouping
behaviour seen in shoals under predatory threat (Ryer and Olla, 1998). Grouping together
has several mechanisms that reduce predation risk (Ioannou et al., 2008), including the
confusion effect (Miller, 1922), the dilution effect (Foster and Treherne, 1981) and the
‘many eyes’ hypothesis (Lima, 1995). The ‘many eyes’ hypothesis states that as part of a
group, the task of scanning the environment for predators is spread out to multiple
individuals; this collaborate effort results in higher levels of vigilance (Lima, 1995). An
increase in vigilance is a result that has been seen in previous studies of noise effect on
terrestrial wildlife (Quinn et al., 2006; Rabin et al., 2006), and in individual sticklebacks
(Voellmy et al., 2014). The increase in shoal cohesion and general alertness of the fish
may be the result of a stress response caused by the noise exposure (Wright et al., 2007;
Charmandari et al., 2005). Alternatively, grouping together may be to benefit from the
‘many eyes’ hypothesis in compensation for potential masking of predator auditory cues
(such as intraspecific communication and inadvertent sound produced from movement)
(Siemers and Schaub, 2011), by relying more on visual stimulus of the environment to
detect possible threats (Rabin et al., 2006). Increased vigilance often results in faster anti-
predatory responses (Voellmy et al., 2014); a reduced latency response could be a direct
benefit to fitness (Siemers and Schuab, 2011). Krause and Godin (1996) observed this
increase in fitness in Guppies (Poecilia reticulate) when prayed upon by blue acara
cichlids (Aequidens pulcher). They found that vigilant guppies detected cichlids sooner
and initiated flight responses earlier than foraging individuals. The vigilant guppies were
more likely to escape predation, resulting in greater fitness for the individuals responding
fastest, because after all ‘an animal captured and consumed by a predator has its
cumulative fitness abruptly terminated’ Ryer and Olla (1998). However, responding faster
reduces the time spent on risk assessment, which may result in suboptimal decision

11. ~ 11 ~
making, such as unnecessary flight response to a low/no threat situation (Voellmy et al.,
2014). In the case of fleeing individuals seeking shelter, and subsequently spending time
hiding from a stimuli of low/no threat, not only is unnecessary energy spent fleeing, but
the time wasted hiding may also lead to lost opportunities to forage or reproduce
(Ydenberg and Dill, 1986). Additionally, constant forgoing of food for unnecessary anti-
predatory behaviour will eventually result in the individual weakening, resulting in them
being more vulnerable to predation. Furthermore, in fish, predation risk is typically
negatively correlated with the size of an individual (Sogard, 1997), slow growing
individuals may be under more intense predation for a longer period of time, than those
that are well fed and therefore grow more rapidly (Houde, 1987). Attempts to compensate
for lost foraging time may also results in increased predation risk, if animals are then
forced to forage during times with increased predatory threat (Lima and Dill, 1990).
Chan et al. (2010) suggested anthropogenic noise could reallocate the attention of prey,
increasing their susceptibility to predation. The Caribbean hermit crabs (Chan et al., 2010)
and the shore crab (Carcinus maenas) (Wale et al., 2013) have exhibited this ‘distracted’
behaviour when exposed to anthropogenic noise; the noise exposure caused delayed anti-
predator response in simulated predator attacks. Krause and Godin (1996) suggested that
predators take advantage of less vigilant prey and are more likely to attack individuals that
exhibit signs of distraction. Predator bias of less vigilant prey, along with delayed response
caused by anthropogenic noise, may increase vulnerability to predation (Chan et al., 2010).
However, past studies have shown evidence that the same anthropogenic noise can have
different impacts on different species (Francis et al., 2011; Rios-Chelen et al., 2012). The
results of my study and Voellmy et al. (2014) suggest three-spined sticklebacks increase
their vigilance when exposed to anthropogenic noise. Therefore whilst the distraction
hypothesis is a valid theory for some species, sticklebacks may be one of many fish
species that this theory does not apply to. On the other hand, as anthropogenic noise
becomes more frequent, animals response to it may weaken due to habituation (Thompson
and Spencer, 1966), a common process to many animals (Chance and Wash, 2006;
Nowacek et al., 2007). If habituation was to occur in sticklebacks, then I would presume
their vigilance to noise stimuli would weaken, perhaps not only to anthropogenic noise, but
the auditory cues of predators as well, increasing their vulnerability to predation. Species
specific habituation to anthropogenic noise could be a good area for future research.

12. ~ 12 ~
Whilst the results of this study showed a significant difference in distance between fish
during the noise trial in comparison to both control trials; it is also important to note that
there was no significant difference between the pre and post controls, suggesting that there
was no lasting effect of the noise treatment. This could mean if underwater anthropogenic
noise pollution was reduced, there would be rapid changes to fish anti-predatory
behaviour. However, as mentioned before, anthropogenic noise impacts species in
different ways (Francis et al., 2011; Rios-Chelen et al., 2012), and three-spined
sticklebacks have been described as behaviourally robust, in the sense that they settle
quickly after a disturbance (Huntingford and Ruiz-Gomez, 2009); just because
sticklebacks show no lasting behavioural changes, does not mean the same can be said for
all fish species.
Although it is clear anthropogenic sound has an effect on shoaling cohesion, I can only
speculate the impact this change in shoaling behaviour has on predator vulnerability and
individual fitness. In order to gain a better understanding on how anthropogenic noise
effects anti-predator defence in shoals, further research needs to be conducted including a
simulated predator and assessing change of response latency in shoals when exposed to
noise. Additionally, care is always needed when interpreting results from a tank based
playback experiment into a real world context (Wale et al., 2013). The use of tanks is to
ensure tight control of potential confounding factors; however tank playbacks cannot
replicate natural sound fields perfectly (Okumura et al., 2002). This being said, given the
lack of studies examining the impact of anthropogenic noise on shoaling behaviours, even
preliminary evidence is potentially valuable.
Conclusion
This study has provided evidence that anthropogenic noise pollution influences shoal
cohesion in three-spined sticklebacks. The results showed that individuals grouped closer
together during noise exposure, which is similar behaviour to that seen in fish under
predatory threat. A possible implication of this may be reduced latency in flight response
to predators, at the cost of time spent assessing the level of risk, potentially resulting in
wasted energy and reduced foraging efficiency; which mirrors results seen in previous
studies assessing the effects of anthropogenic noise on sticklebacks (Voellmy et al., 2014;
Purser and Radford, 2011). However, without a simulated predator threat, this evidence
allows us to only predict how shoaling fish may react to a predator whilst exposed to

13. ~ 13 ~
anthropogenic sounds. What is clear from this study is anthropogenic noise does have an
impact on shoaling behaviour in fish and that further research is required in order to truly
quantify the direct fitness consequences. Furthermore, laboratory and tank based studies
create an artificial scenario, so care is needed when translating results into real world
context. The ideal context for future studies would be to assess potential effects of
anthropogenic noise that have direct consequences to fitness, but in the wild with real
noise sources and natural sound fields, allowing the spatial scale of impact and severity of
fitness consequences to be determined.
Acknowledgements
I’d like to thank Tom Pike for all his help and supervision as my tutor. Many warm thanks
to Helen Edwards for making the cold hours of data collection fly by. Finally, thanks to
Danielle Derrick and Matthew Hale for constant moral support and assistance with data
input.

14. ~ 14 ~
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