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Developmental experience with anthropogenic


noise hinders adult mate location in an
acoustically signalling invertebrate

Article in Biology letters · February 2018


DOI: 10.1098/rsbl.2017.0714

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Gabrielle Gurule-Small Robin M Tinghitella


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Animal behaviour

Developmental experience with


rsbl.royalsocietypublishing.org anthropogenic noise hinders adult
mate location in an acoustically
signalling invertebrate
Research
Cite this article: Gurule-Small GA, Tinghitella Gabrielle A. Gurule-Small and Robin M. Tinghitella
RM. 2018 Developmental experience with Department of Biological Sciences, University of Denver, Denver, CO 80210, USA
anthropogenic noise hinders adult
RMT, 0000-0002-0049-5539
mate location in an acoustically
signalling invertebrate. Biol. Lett. 14: Phenotypic plasticity facilitates survival and reproduction in rapidly changing
20170714. and novel environments. Traffic noise spectrally overlaps with (i.e. masks) the
http://dx.doi.org/10.1098/rsbl.2017.0714 sounds used by many acoustically signalling organisms to locate and secure
mates. To determine if pre-reproductive exposure to noise improves adult
performance in noisy environments, we reared field crickets (Teleogryllus
oceanicus) in one of three noise environments: masking traffic noise, traffic
Received: 18 November 2017 noise from which frequencies that spectrally overlap with the crickets’ song
Accepted: 5 February 2018 were removed (non-masking), or silence. At reproductive maturity, we
tested female mate location ability under one of the same three acoustic
conditions. We found that exposure to noise during rearing hindered female
location of mates, regardless of the acoustic environment at testing. Females
reared in masking noise took 80% longer than females reared in silence to
Subject Areas: locate a simulated singing male who was less than 1 m away. Impaired mate
behaviour location ability can be added to a growing list of fitness costs associated
with anthropogenic noise, alongside reductions in pairing success, nesting
Keywords: success and offspring survival.
anthropogenic noise, behaviour,
developmental plasticity, mate location,
Orthoptera 1. Introduction
Adult traits, including behaviour, are shaped by ecological and social environ-
ments experienced during development and beyond [1], when adaptive,
Author for correspondence: behavioural plasticity can reduce negative impacts of environmental change on
Robin M. Tinghitella individual fitness and enhance population persistence. Mating preferences and
decisions are particularly plastic, varying, for instance, with risk encountered
e-mail: robin.tinghitella@du.edu
[2] and social experience [3]. Developmental experience alters adult mating
behaviour in ways that likely reshape evolutionary trajectories (e.g. [4–5]). Here
we ask how developmental experience with anthropogenic noise impacts repro-
ductive components of fitness at adulthood [6], because noise transforms the
mating environment [7].
Anthropogenic noise is a major and expanding human-induced global pollu-
tant that can have dramatic physiological (reviewed in [8–10]) and behavioural
(reviewed in [7,8,10,11]) impacts on animals. Noise could influence reproductive
success through effects on signals and signalling strategies (e.g. [6,12]), contest be-
haviour, location of mates and mate preferences (e.g. [13]), nesting or pairing
success (e.g. [14,15]) and parental investment (e.g. [16]). Much research has
focused on whether signallers can improve detection in noisy environments
(reviewed in [17]), but less attention has been paid to effects of noise on receivers
Electronic supplementary material is available [18–20]. Anthropogenic noise may impede receivers’ ability to locate signallers if
it impacts hearing development, distracts mate searchers, masks acoustic cues or
online at https://dx.doi.org/10.6084/m9.
induces stress responses. Given this, we might expect receiver behaviour to
figshare.c.4007593. depend on, and perhaps compensate for, experience with anthropogenic noise.

& 2018 The Author(s) Published by the Royal Society. All rights reserved.
Downloaded from http://rsbl.royalsocietypublishing.org/ on March 1, 2018

Table 1. ANCOVAs testing effects of rearing and phonotaxis noise environments on female location of mates. Significant p-values are indicated in italics. 2

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outcome variable effect F d.f. p

time to first movement rearing environment 3.38 2,126 0.038


phonotaxis environment 0.52 2,126 0.596
rearing  phonotaxis 0.61 4,120 0.658
pronotum width 5.30 1,128 0.023
time to contact speaker rearing environment 3.18 2,126 0.045
phonotaxis environment 1.42 2,126 0.247

Biol. Lett. 14: 20170714


rearing  phonotaxis 1.12 4,120 0.353
pronotum width 0.60 1,128 0.808
search time rearing environment 1.50 2,126 0.226
phonotaxis environment 0.81 2,126 0.445
rearing  phonotaxis 1.12 4,120 0.351
pronotum width 3.21 1,128 0.076
no. grids crossed (search path) rearing environment 2.49 2,126 0.087
phonotaxis environment 1.22 2,126 0.299
rearing  phonotaxis 0.60 4,120 0.662
pronotum width 4.26 1,128 0.041

The taxonomic focus on vertebrate study systems in noise of the five locations into a single continuous 5 min track
research [11,17,21] limits our understanding of the effects (electronic supplementary material, figure S1A). We produced
of anthropogenic noise on reproductive success (but see a non-masking traffic noise by filtering out frequencies from
[14 –16,18]); this is likely because of logistical difficulties 3 to 6 kHz using the ‘filter’ command in RavenPro14 (electronic
supplementary material, figure S1B).
measuring their fitness. Yet, mating behaviour is key to the
We pulled females from our laboratory stock (established in
evolution of male signals, and to fitness more generally.
2014 from Mo’orea, French Polynesia) when sex could be reliably
Switching the focus to invertebrates offers advantages: invert-
identified and the hearing organs were apparent, and randomly
ebrates compose most of the biodiversity on earth, are often assigned them to one of three acoustic rearing environments:
small, have short generations, and can be laboratory- masking (n ¼ 44), non-masking (n ¼ 43) or silence (n ¼ 42). We
maintained under experimental conditions [11]. We use a broadcast the masking or non-masking noise inside the incubators
field cricket study system to ask (i) does pre-reproductive (Percival I36VLC8) crickets were reared in for 14 h a day (1 h pre-
exposure to anthropogenic noise impact adults’ ability to dawn to 1 h post-dusk, mimicking traffic patterns) from EcoXBT
locate mates, and, if so, (ii) does developing in noise improve wireless speakers. We rotated treatments among incubators
performance in noisy environments? every two weeks and rotated container positions within incubators
Teleogryllus oceanicus lives in habitats ranging from urban during cleanings. Because incubators produce background noise
(76–92 dBA), we kept them off during the entire experiment, but
lots in Australia to undisturbed fields on sparsely populated
maintained a photo-reversed 12 h light–dark cycle. The tempera-
Pacific Islands. Traffic noise overlaps with the frequency of
ture fluctuated between light and dark phases (21.28C230.58C at
the calling and courtship songs males use to attract mates
the light source) but did not exceed those experienced in nature.
from afar and to entice them to mate once in close proximity We reared females in 64 oz Tupperware containers until sexual
(4–6 kHz). Females are locomotory and search for stationary maturity with rabbit food ad libitum egg carton shelters and
calling males less than 1 m to more than 20 m away in a fresh water [3]. Females spent 15.5 + 0.7 days in their rearing
matrix of grass and rocks. We manipulated pre-reproductive treatment prior to eclosion, regardless of treatment (F2,126 ¼ 2.58,
experience with traffic noise, rearing female T. oceanicus p ¼ 0.08, electronic supplementary material, figure S2).
under masking noise (traffic noise that overlaps spectrally We conducted phonotaxis (mate location) trials in a ran-
and temporally with male calling song; electronic supplemen- domly assigned acoustic environment (masking, non-masking
tary material, figure S1), non-masking noise (traffic noise that or silent) when females were 7 days post-eclosion. Phonotaxis
trials took place inside of a square arena 1.45 m2 in size, with a
does not overlap spectrally with male calling song), or silence,
10 cm grid on its floor, located within a 2.3  2 m room with
and then tested adult female location of mates under the same
acoustic foam-lined walls. We conducted phonotaxis trials
three acoustic environments in a fully factorial design.
0 – 7.5 h post-dusk (mean ¼ 2.9 + 0.2 h). Time of testing did not
differ among rearing (F2,126 ¼ 1.81, p ¼ 0.17) or phonotaxis
environments (F2,126 ¼ 1.50, p ¼ 0.23). In each trial we placed
the focal female at the centre of the arena under an inverted plas-
2. Material and methods tic cup for 2 min, after which we simultaneously released the
To produce masking and non-masking traffic noises, we female and projected (i) a strongly preferred T. oceanicus calling
recorded traffic noise at five Denver, CO, USA locations using song (electronic supplementary material, figure S3) from a
a Marantz (PMD620MKII) digital recorder and Shure SM58 speaker in one randomly assigned corner and (ii) the noise treat-
microphone. Locations captured varied vehicular types, volumes ment from a speaker suspended 141 cm above the arena. Both the
and speeds. We compiled two representative 30 s clips from each song and noise treatment were broadcast at realistic volumes
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(70 dBA from the female’s starting point) using EcoXBT wireless (a) 3
speakers. We measured the time to first movement, whether or 125
A
not a female contacted the speaker broadcasting song, contact

rsbl.royalsocietypublishing.org
time (the difference between start of trial and touching the AB
100

time to contact speaker (s)


speaker), search time (the difference between time to first move-
ment and contact time) and the number of grid lines females
crossed (as a measure of search path). Trials lasted 5 min. 75
Females who did not contact the speaker were assigned the B
maximum contact time.
We tested if experience with noise alters location of mates and 50
whether developing in noise prepares females for mate searching
in noisy environments using two-way analyses of covariance
(ANCOVAs) in JMP Pro 13.0. Rearing environment, phonotaxis 25

Biol. Lett. 14: 20170714


environment, and their interaction were main effects, and female
pronotum width (size) was a covariate. Size did not differ across n = 44 n = 43 n = 42
rearing environments ( p ¼ 0.76). We also considered whether 0
masking non-masking silent
females reared under noise shifted their mate searching behaviour
temporally using ANCOVAs that included rearing environment,
phonotaxis testing time (time post-dusk) and their interaction as (b) 60 A
main effects, and size as a covariate. Continuous outcome vari-
ables were natural log transformed to meet assumptions of
normality. We ran logistic regressions (size ¼ covariate) to address 50

time to first movement (s)


whether rearing or phonotaxis environments affected likelihood of
contacting the speaker because the parameter estimates in the full 40
model were unstable.

30 AB
3. Results 20
B
Rearing environment was the most important predictor of
adult female mate location behaviour (table 1). Differences in
contact time (figure 1a) were due to the time it took females 10
to initially move (figure 1b), rather than the search time or
n = 44 n = 43 n = 42
search path (number of grids crossed) (table 1). Females 0
reared in masking noise took 209% longer to begin searching masking non-masking silent
(figure 1b), and 81% longer to reach the signalling male than rearing enviroment
females reared without traffic noise (figure 1a). Surprisingly, Figure 1. Adult female mate location responses by rearing environment.
the acoustic environment experienced during phonotaxis (a) Time to first movement and (b) total time to contact the speaker
never influenced mate location behaviour (table 1; electronic from the start of the trial. Non-transformed means and standard errors are
supplementary material, figure S4), and we found no inter- shown for ease of interpretation. Letters indicate statistically significant
actions between rearing environment and phonotaxis differences according to a Tukey’s test ( p , 0.05).
environment (table 1). Females who were larger were slower
to begin moving and crossed fewer grids during the search
anthropogenic noise ([21], but see [23]). While certainly valu-
(table 1; electronic supplementary material, figure S5).
able, such studies can miss effects of prior exposure altogether
Female mate location behaviour did not depend on phonotaxis
or confound previous and current experience. In general, we
testing times (time post-dusk; all p . 0.39), or on the interaction
expect masking noise to affect both signals and receiver
between rearing environment and phonotaxis testing times (all
responses [24], but organisms like singing insects that cannot
p . 0.11) (electronic supplementary material, table S1). Of the
alter their signal frequency plastically [25] or those that
129 females, 120 contacted the speaker. Whether or not females
cannot quickly leave undesired areas [26] may suffer greater
contacted the speaker did not depend on rearing environment
costs of noise, unless receiver behaviour can compensate.
(x 22 ¼ 5.77, p ¼ 0.12) or phonotaxis environment (x 22 ¼ 3.21,
Similar to our results (figure 1; see also electronic sup-
p ¼ 0.36). All data have been deposited in Dryad [22].
plementary material), noise that masks a focal signal often
elicits greater plastic and evolutionary change in signals
and signalling behaviour than non-masking noise [17,27].
4. Discussion The mechanism underlying reduced mate location ability of
Anthropogenic noise experienced prior to sexual maturity hin- females reared in masking noise is currently unknown, but
dered adult mate location behaviour, regardless of the acoustic we are testing several possibilities. There are strong effects
environment encountered at the time of searching. Females of juvenile experience with sexual signals (or lack thereof )
reared in masking noise took more than 200% as long to on adult mating decisions in this species [3], and masking
move and more than 80% longer to contact a simulated calling noise might decrease signal detection during development,
male than females reared in silence. Effects of previous and sub- limiting learning opportunities, for instance. Alternative
adult exposure to noise may be underappreciated because explanations for our results include generalized stress
studies often test for immediate behavioural responses (i.e. responses, physiological damage or impaired hearing devel-
vigilance or foraging) to projected noise or make comparisons opment stemming from juvenile experience with masking
across habitats that are regularly exposed to more or less noise [9].
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We were surprised to find no effect of phonotaxis environ- exposure, a search environment that includes males of varying 4
ment on female location of mates, though there is precedence attractiveness at more realistic (longer) search distances, and/

rsbl.royalsocietypublishing.org
for this in the literature (e.g. [25]). Nearly all females eventually or unpredictable onset and cessation of noise disturbances.
located the speaker broadcasting song, which lends support to
the hypothesis that juvenile exposure to masking noise pro- Data accessibility. Data can be accessed at https://doi.org/10.5061/
duced a more generalized effect on physiology or learning dryad.53qb3 [22].
that hindered location of mates, but that the broadcast noise Authors’ contributions. G.A.G.-S. and R.M.T. conceived of the study, and
did not completely eliminate females’ ability to localize song. contributed to experimental design, data interpretation, and writing.
With repeated adult exposure to noise, females may become G.A.G.-S. collected and analysed the data. Both authors approve the
tolerant, reducing the costs of developing in noise. However, our final content and are accountable for all aspects of the work.
experimental design minimized factors other than noise that Competing interests. We declare we have no competing interests.
might impede female mate location. Animals searched for a Funding. Research was supported by grants from Sigma Xi and the

Biol. Lett. 14: 20170714


Orthopterists’ Society to G.A.G.-S.
highly preferred simulated mate who was less than 1 m away
Acknowledgements. We thank the Tinghitella laboratory undergraduate
and experienced noise during their inactive period (daylight researchers who helped with cricket husbandry. Anna Sher, Shannon
hours) for roughly two weeks prior to sexual maturity. Costs Murphy and two reviewers provided feedback that improved
of developing in noise might be magnified by longer-term the paper.

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