Evidence that ship noise increases
stress in right whales
Rosalind M. Rolland1,*, Susan E. Parks2,†, Kathleen E. Hunt1
,
Manuel Castellote3, Peter J. Corkeron4,‡, Douglas P. Nowacek5
,
Samuel K. Wasser6 and Scott D. Kraus1
1
Research Department, New England Aquarium, Boston, MA 02110, USA 2
Applied Research Laboratory, The Pennsylvania State University, State College, PA 16804, USA 3
Alaska Fisheries Science Center, NOAA National Marine Mammal Laboratory, Seattle, WA 98115, USA 4
Bioacoustics Research Program, Cornell Lab of Ornithology, Ithaca, NY 14850, USA 5
Nicholas School of the Environment and Pratt School of Engineering, Duke University Marine Laboratory,
Beaufort, NC 28516, USA 6
Center for Conservation Biology, Department of Biology, University of Washington, Seattle, WA 98195, USA
Baleen whales (Mysticeti) communicate using low-frequency acoustic signals. These long-wavelength
sounds can be detected over hundreds of kilometres, potentially allowing contact over large distances.
Low-frequency noise from large ships (20–200 Hz) overlaps acoustic signals used by baleen whales,
and increased levels of underwater noise have been documented in areas with high shipping traffic.
Reported responses of whales to increased noise include: habitat displacement, behavioural changes
and alterations in the intensity, frequency and intervals of calls. However, it has been unclear whether
exposure to noise results in physiological responses that may lead to significant consequences for individuals or populations. Here, we show that reduced ship traffic in the Bay of Fundy, Canada, following the
events of 11 September 2001, resulted in a 6 dB decrease in underwater noise with a significant reduction
below 150 Hz. This noise reduction was associated with decreased baseline levels of stress-related faecal
hormone metabolites (glucocorticoids) in North Atlantic right whales (Eubalaena glacialis). This is the
first evidence that exposure to low-frequency ship noise may be associated with chronic stress in
whales, and has implications for all baleen whales in heavy ship traffic areas, and for recovery of this
endangered right whale population.
Keywords: right whales; glucocorticoids; stress; underwater noise; ship traffic
- INTRODUCTION
Underwater ocean noise from anthropogenic sources
has increased over the past 50 years [1,2]. This acoustic
pollution is a by-product of a rising tide of human
maritime activities including seismic exploration by the oil
and gas industries, military and commercial use of sonar,
recreational boating and shipping traffic. In many ocean
areas, the dominant source of human-generated lowfrequency noise (20–200 Hz) is from the propellers and
engines of commercial shipping vessels, and noise levels
have been increasing [2–4]. These sound frequencies can
propagate efficiently over long distances in the deep-water
marine environment. Studies monitoring trends of underwater noise in the Northeast Pacific found that since the
1960s, low-frequency ambient noise (less than 80 Hz) has
increased by 10–12 decibels (dB), coinciding with a doubling of the global shipping fleet [5,6]. This rising level of
noise has raised concerns about effects on marine mammals
that rely on acoustic signalling [7–9]. In particular, shipping
noise directly overlaps the frequency band of acoustic
communication signals used by the largest of cetaceans,
the baleen whales (Mysticeti) [10,11].
Living in an environment where sound propagates
far better than light, many marine animals, particularly
cetaceans, evolved to rely primarily upon acoustic signalling to communicate, locate prey and navigate [12].
The acoustic repertoire of baleen whales consists of
low-frequency, long-wavelength sounds that propagate
efficiently underwater, potentially allowing communication
over large distances in the open ocean [10–12]. For
example, data from the U. S. Navy’s SOund SUrveillance
System (SOSUS) has shown that blue whale (Balaenoptera
musculus) calls can be detected offshore at ranges of hundreds of kilometres [13]. However, the range at which
baleen whales actually communicate with each other
remains unknown. Elevated low-frequency underwater
noise levels near busy shipping routes and ports have the
potential to interfere significantly with whale calls used to
maintain contact, aggregate to feed and locate potential
mates (‘acoustic masking’), potentially affecting critical
life-history events [1,7–11]. Reported whale responses to
increases in background noise have included: habitat
displacement, behavioural changes and alterations in vocalization patterns such as shifting the frequency band or
energy level of calls, making signals longer or more repetitive, or waiting to signal until the noise is reduced [8,9].
- Author for correspondence (rrolland@neaq.org).
† Present address: Department of Biology, Syracuse University,
Syracuse, NY 13244, USA.
‡ Present address: NOAA Northeast Fisheries Science Center,
Woods Hole, MA 02543, USA.
Proc. R. Soc. B (2012) 279, 2363–2368
doi:10.1098/rspb.2011.2429
Published online 8 February 2012
Received 18 November 2011
Accepted 18 January 2012 2363 This journal is q 2012 The Royal Society
Owing to the challenges of studying free-swimming large
whales, it is unknown whether these responses to background noise translate into biologically significant effects
that may have long-term consequences for individuals or
populations [7].
The tragic events of 11 September 2001 (9/11 hereafter) resulted in an unplanned experiment on the
effects of underwater noise on western North Atlantic
right whales (Eubalaena glacialis). These baleen whales
congregate during late summer in the Bay of Fundy,
Canada, to feed and nurse their calves. Since 1980, the
New England Aquarium (Boston, MA, USA) has conducted longitudinal population surveys annually in this
critical right whale habitat. In the immediate aftermath
of 9/11, we noted a marked decrease in ship traffic in
the Bay of Fundy, Canada, and acoustic recordings
revealed a noticeable decrease in low-frequency background noise levels. A study of stress-related faecal
hormone metabolites was also underway throughout the
2001 field season and over the four subsequent years.
We analysed acoustic recordings and ship traffic data
along with faecal glucocorticoid (fGC) measures of physiological stress before and after 9/11. Here, we show that a
post-9/11 decrease in background underwater noise from
reduced large ship traffic corresponded to a decrease in
stress-related fGC hormone levels in right whales.
- MATERIAL AND METHODS
(a) Acoustic data
Acoustic data were collected in the Bay of Fundy in August and
September 2001 for a project related to right whale social behaviour. Data were collected with a single factory-calibrated
HTI-94-SSQ hydrophone with a built-in preamplifier recorded
into a Sony TCD-D8 Digital Audio Tape (DAT) recorder with
constant recording gain setting (system frequency response
50 Hz–20 kHz+1 dB). The hydrophone was deployed from
the side of a small vessel (with the engine shut off ) using a
spar buoy to minimize vertical displacement.
We analysed 93 min of recordings collected from 2 days
before 9/11 (25 and 29 August 2001) and 90 min of recordings
from 2 days immediately following 9/11 (12 and 13 September
2001) all with the same sea-state conditions (Beaufort 1-2).
Recordings collected during several individual recording sessions from each day were compiled and converted to .wav
files with a sampling rate of 48 kHz. The records were then
bandpass filtered to 50 Hz–20 kHz. Extraneous noises (e.g.
splashing sounds and whale calls) were removed to select the
quietest section of background noise in each recording. The
DAT recorder gain was measured in the laboratory by recording known voltage signals directly into the recorder. The sound
pressure level (SPL) at the hydrophone was calculated using
the known sensitivity of the hydrophone, the hydrophone preamplification gain and the measured gain from the recorder
to obtain the overall gain for the system. A custom MATLAB program was used to calculate SPL in dBRMS re 1 mPa for the full
band (50 Hz–20 kHz) and power spectrum density level (PSL)
in mPa2 Hz21 for the range 50–500 Hz.
(b) Ship traffic data
The Bay of Fundy (BOF) has a Traffic Separation
Scheme (i.e. shipping lanes) that is mandatory for all vessels
of or over 20 m in length, and vessel-tracking radar data are
collected. Ship traffic data on the same days as the acoustic
recordings were extracted from the Kongsberg Norcontrol IT
Vessel Traffic Management and Information System computerized log-files stored with the Marine Communication and
Traffic Services, Saint John, New Brunswick, Canada [14].
Figure 1 shows the Grand Manan Basin Right Whale Conservation Area in the Bay of Fundy where the study was
conducted, and the location of the shipping lanes (in 2001).
(c) Faecal sample collection and hormone analysis
In a second study (conducted from 2001–2005), we collected faecal samples from right whales and measured
metabolites of steroid reproductive hormones (oestrogens,
androgens and progestins) and adrenal glucocorticoids
(GCs) [15,16]. Circulating steroid hormones are metabolized in the liver and excreted in bile (and urine), and the
resulting metabolites are measurable in faeces [17,18]. The
pattern of faecal metabolites reflects the average level of circulating parent hormone with a lag time of hours to days,
depending on hormone turnover rates and gastrointestinal
passage time for the species [18,19]. Based on data from
other species, the lag time for right whales was estimated as
1 day for this study [20]. Previous work has demonstrated
that concentrations of fGCs reflect adrenal activation and
relative physiological stress levels in a wide variety of animals
[19], including North Atlantic right whales [15].
Faecal samples were collected near right whales in the Bay
of Fundy from late July to early October. Samples were found
opportunistically and using detection dogs trained to find
right whale faeces [21]. Floating faeces were scooped from
the water using a 300 mm dipnet (Sea-Gear Corp., Melbourne, FL, USA), temporarily stored at 2208C, and
shipped overnight on dry ice to the laboratory. Species of
origin was confirmed photographically and by amplification
of mitochondrial control region DNA [21].
Samples were lyophilized (2208C) to remove variation
owing to water content and diet, then sifted and mixed to homogenize hormone metabolites. Steroid metabolites were
extracted from weighed faecal powder with a methanol
vortex method [19]. Radioimmunoassays for faecal
0 10 20 40
N
km
Bay of
Fundy
Right Whale
Conservation
Area
shipping lanes
Canada
United
States Atlantic
Ocean
Figure 1. The study site in the Bay of Fundy, Canada. The
Canadian Right Whale Conservation Area and the location
of the designated shipping lanes (in 2001) are shown.
2364 R. M. Rolland et al. Ship noise and stress in right whales
Proc. R. Soc. B (2012)
oestrogens, progestins, androgens and GCs have been previously validated for right whales, and detailed methods have
been described [15,16]. Briefly, faecal extracts were diluted in
the appropriate amount of assay buffer, and GC and oestrogen
metabolites were assayed using double-antibody 125I radioimmunoassay kits (MP Biomedicals, Costa Mesa, CA, USA)
and counted with a Packard Crystal II gamma counter. Progestin and androgen assays were in-house 3
H radioimmunoassays
counted with a Beckman LS6500 liquid scintillation counter.
All samples were assayed in duplicate, with a full standard
curve and two controls (low and high) in every assay.
Any samples with percent-bound outside of the standard
curve, or with greater than 10 per cent coefficient of variation
between duplicates, were re-assayed. Results are expressed as
nanograms of immunoreactive hormone metabolites per
gram of freeze-dried faeces (abbreviated as ng g21
).
(d) Statistical methods
We compared levels of fGC metabolites before (and including) 11 September and after 11 September for the years
2001–2005 using a two-way, unbalanced Kruskall–Wallis
test. The main effects were year (2001–2005) and period
(before and after 11 September for all years). The null
hypothesis was no effect of period, year or interaction
between period and year. We were interested in assessing
whether there was a pre-9/11 versus post-9/11 effect on
fGCs in 2001 that differed from other years. Samples with
faecal metabolites of testosterone greater than 5000 ng g21
and progesterone greater than 6000 ng g21 were removed
from the analyses to control for physiologically normal
elevations of fGC levels in adult males (mean androgens+
standard error of the mean ¼ 10 192+986 ng g21
) and pregnant females (mean progestins ¼ 201 240+27 025 ng g21
)
[15,16]. The hormone cut-off values were derived from conditional inference trees used to classify identified whales with
known reproductive states based on faecal hormone levels
(P. J. Corkeron, unpublished data). - RESULTS
The acoustic analyses showed a 6 dB decrease in the overall
background noise (50 Hz–20 kHz) in recordings made
after 9/11. More importantly, the noise spectrum changed
dramatically, with a significant reduction of noise below
150 Hz (figure 2). Records from the ship traffic monitoring
programme in the Bay of Fundy (Fundy Traffic) confirmed
a decrease in large vessel traffic following 9/11. Ship traffic
(within 16 km of the Right Whale Conservation Area,
figure 1) on the same dates in 2001 as the acoustic recordings, decreased from nine large ships on 25 and 29
August (five and four ships, respectively) to three ships on
12 and 13 September (one and two ships, respectively).
Faecal GC levels from a total of 144 samples were used
in the analyses (n ¼ 114 before 11 September; n ¼ 30 after
11 September, for all years). Sample sizes before/after 11
September by year were as follows: 2001 n ¼ 14/9; 2002
n ¼ 14/3; 2003 n ¼ 37/4; 2004 n ¼ 3/9; 2005 n ¼ 46/5.
Samples were collected approximately proportionally on
weekdays and weekends, 96 per cent were evenly split
between August and September, and 4 per cent were
collected in late July and early October.
There was a significant effect of year and period on
fGC levels (Kruskall–Wallis x2 ¼ 29.6889, d.f. ¼ 4, p ¼
0.000005663; figure 3a). The only year in which there
was a significant decrease in fGCs after 11 September
was 2001 (figure 3b). While the data show annual variability in fGC levels, the dominant trend was for higher fGCs
after 11 September in three of four control (non-2001)
years (figure 3b). This trend was particularly pronounced
in 2003, a year in which 75 per cent of post-11 September
samples were collected after 20 September. This is in
contrast to all other study years in which only 19 per cent
of (post-11 September) samples were collected after 20
September. A possible explanation for higher fGC levels
in later September (as in 2003) is the observation of an
increase in whale participation in surface-active (courtship)
groups as September progresses (New England Aquarium,
unpublished data). Increased courtship activity could be a
significant social stressor elevating fGC levels. - DISCUSSION
Acoustic studies have shown that right whales alter their
vocalization behaviour in noisy habitats by increasing
both the amplitude and frequency of their stereotyped
upcalls [22,23], which are the main contact sounds used
by these whales. A comparison of three right whale habitats
along the east coast of the USA and Canada found that the
Bay of Fundy had the highest levels of background lowfrequency noise associated with heavy shipping traffic,
and that the frequencies of right whale upcalls were significantly higher in this habitat [24]. While right whales alter
their vocalizations in response to low-frequency underwater noise, it has been previously unclear whether these
responses are accompanied by quantifiable physiological
effects that could potentially lead to biologically significant
impacts on individuals or populations.
Here, we show a decrease in baseline concentrations of
fGCs in right whales in association with decreased overall
noise levels (6 dB) and significant reductions in noise at
all frequencies between 50 and 150 Hz as a consequence
of reduced large vessel traffic in the Bay of Fundy following the events of 9/11. Even with relatively small sample
sizes after 11 September in 2001, the decrease in fGCs
after 9/11 was highly significant compared with other
50 100 150 200 250 300 350 400 450 500
75
80
85
90
95
100
105 Aug 25
Sept 13
Sept 12
Aug 29
frequency (Hz)
PSL (dB re 1 µPa2 Hz–1)
Figure 2. Power spectrum density level (PSL) of background
noise in the range 50–500 Hz from 2 days before (25 and 29
August 2011) and 2 days after 11 September 2001 (12 and
13 September 2011) with identical sea-state conditions.
Overall noise levels (PSL in dB re 1 mPa2 Hz21 are lower
and the peak frequency (Hz) of the noise shifted to a
higher frequency post-9/11.
Ship noise and stress in right whales R. M. Rolland et al. 2365
Proc. R. Soc. B (2012)
years. To our knowledge, there were no other factors
affecting the population that could explain this difference
besides the decrease in ship traffic and concomitantly
reduced underwater noise disturbance after 9/11.
GCs are secreted in response to a large variety of
natural stressors, such as social aggression, predators,
starvation and drought, as well as anthropogenic disturbances [25,26]. Studies of terrestrial species have
demonstrated increases in fGCs in response to noiserelated anthropogenic stressors, such as snowmobiles
[27], tourism traffic [28] and road noise [29]. Release
of GCs from the adrenal cortex is mediated by the
hypothalamic–pituitary–adrenal axis within minutes to
an hour of experiencing (or even perceiving) a stressor
[30]. This short-term stress response is beneficial to the
individual by mobilizing energy reserves and initiating
behaviours to respond to the threat. However, chronic
elevations of GCs secondary to repeated or continuous
stressors become maladaptive, suppressing growth,
immune system function and reproduction [26,30], with
implications for individual and population fitness. For
example, circulating corticosterone levels predicted
population-level survival probability in Galapagos marine
iguanas (Amblyrhynchus cristatus) during an El Nin˜oinduced famine [31], and high fGCs were predictive of
individual mortality in ring-tailed lemurs (Lemur catta)
[32]. Definitively linking chronic stress responses to detrimental health effects in large whales is extremely difficult
because of the logistics of studying free-swimming
whales and the inability to conduct a controlled study.
However, a large body of literature has demonstrated
that chronic stress, assessed by persistently elevated GCs,
can lead to detrimental effects on health and reproduction
across a variety of vertebrate taxa [26,30–32].
While the results presented here provide compelling
evidence of a stress response in right whales exposed to
higher levels of low-frequency underwater noise from
ship traffic, this is a retrospective analysis based on a
non-repeatable event, with all of the inherent limitations.
Because the study was unplanned, there are no comparable acoustic recordings from the Bay of Fundy in years
other than 2001 for comparison. Additionally, sample
sizes after 11 September were relatively small in all
years because deteriorating weather conditions in later
September are much less conducive to faecal sample collection. In the absence of planned cessation of shipping
traffic, future work is needed to characterize and compare
underwater noise and fGC levels in right whales occupying habitats with varying levels of low-frequency noise
from large ships to see if an enhanced stress response to
higher noise levels is detectable given natural variability
in the hormone data.
Because of their use of near-shore habitats along eastern North America, recovery of the critically endangered
North Atlantic right whale population has been seriously
impaired by mortalities from ship collisions and fishing
gear entanglements [33]. Acoustic pollution from anthropogenic sources presents a less visible but pervasive
disturbance to these coastal-dwelling whales that may
have negative consequences for population viability.
Exposure to potentially significant underwater noise
from ships is not unique to the Bay of Fundy. For
example, data modelling and analytical approaches estimated that the acoustic communication space of calling
right whales in a second east coast habitat (Stellwagen
Bank National Marine Sanctuary) was reduced 84 per
cent by the passage of only two commercial ships
during a 13.2 h period [10]. The Stellwagen area averaged six ships per day [34], suggesting that acoustic
masking was occurring for the majority of the time that
right whales were feeding there. The communication
space of singing fin (Balaenoptera physalus) and humpback
(Megaptera novaeangliae) whales was also diminished, but
to a far lesser extent because of species-specific
120
(a) (b)
15
10
5
glucocorticoid medians: post 9/11–pre 9/11 –5
0
100
80
60
40
20
2001 2002 2003
year
2004 2005 2001 2002 2003
year
2004 2005
faecal glucocorticoids (ng g–1)
Figure 3. (a) Levels of faecal GC metabolites (ng g21
) in North Atlantic right whales before (grey boxes) and after (white
boxes.) 11 September for the years 2001–2005. Boxes show the interquartile range, the black line inside the box is the
median, whiskers represent the adjacent values (most extreme observations that are not more than 1.5 times the height of
the box), and outliers are represented by dots. (b) Yearly difference in median faecal GC levels (2001–2005) post 9/11–
before 9/11. Significantly lower faecal GC levels after 11 September were only seen in 2001, and were associated with decreased
underwater low-frequency noise resulting from a reduction in large vessel traffic.
2366 R. M. Rolland et al. Ship noise and stress in right whales
Proc. R. Soc. B (2012)
differences in acoustic signalling [10]. While increases in
low-frequency ocean noise must be considered a potential
anthropogenic stressor for all baleen whales in coastal
areas with high levels of ship traffic, depleted populations
experiencing the cumulative impact of multiple stressors
and those with particular acoustic characteristics may be
at heightened risk [7].
This work was supported by grants from the Office of Naval
Research (S.K.), NOAA Fisheries (R.R. and S.P.), and the
Northeast Consortium (R.R.). Our special thanks to the
New England Aquarium right whale team and the other
researchers who collected samples for the stress hormone
study; to Philip Hamilton for right whale data discussions;
to Jackie Ciano, Stephanie Martin and Cynthia Thomas for
assistance with acoustic recordings; to Angelia Vanderlaan
and Chris Taggert for supplying ship traffic data for the
Bay of Fundy; and to Brooke Wikgren for graphics. This
research was conducted under permits from Fisheries and
Oceans, Canada and Scientific Research Permits under the
Canadian Species at Risk Act.
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