HomeMy WebLinkAboutSubmittal-Ronald Hoenig-Letter to Commissioners and Impact Study ReportUNIVERSITY OF MIAMI
ROSENSTIEL
SCHOOL of MARINE &
ATMOSPHERIC SCIENCE
Li
November 13, 2018
Dear City of Miami Mayor and Commissioners,
Submitted into thepub
record f r neins) , y__.,
on
Office of the Dean City Clerk
Science and Administrative Building 107
4600 Rickenbacker Causeway
Miami, FL 33149-1031
Phone: 1 305 421-4000
Fax: 1 305 421-4711
Web Site: http://www.rsmas.miami.edu
I am writing to express our concern regarding the impact the ULTRA concert will have on our aquaculture fish and research
at the University of Miami Rosenstiel School Experimental Hatchery (UMEH).
Of paramount concern for the ongoing research at UMEH is the well documented cases of noise -induced disruptions to
the reproductive success in captive fish. Such disruptions are directly related to the interaction of stress hormones, such
as cortisol, on the reproductive and immune systems of fish.
The time of year when the proposed ULTRA event will occur is during the prime reproductive ("spawning") season for the
valuable fish species maintained at the UMEH facility. For many of these species, environmental conditioning to prepare
them for spawning has been underway for years. The damage associated with even short-term acute noise events during
this critical time would disrupt this conditioning and would set our research efforts back for years.
Such setbacks would lead to an inability to complete research projects that have invested millions of dollars to get to this
point.
Grants and Private contracts to be impacted include:
Gulf of Mexico Research Initiative - $3,000,000+
NOAA SeaGrant Award - $950,000
Open Blue Sea Farms Service Contract - $250,000
There are numerous scientific studies identifying the negative impacts of man-made noise on fish (see attached review
paper). The University of Miami Experimental Hatchery's close proximity to the proposed 2019 ULTRA Music Festival will
likely subject highly valuable research animals (many of which are the only captive breeding groups in the United States)
to these consequences. The 110 dB threshold (per the Miami Herald article), in many cases, exceeds levels shown to
negatively impact fish. When reading these studies one must add roughly 62 dBs to calculate for the difference in the
sound level in air versus water (i.e. 110 dB in air is 172 dB in water). The immediate concern would be the fish experiencing
a startle reaction at the onset of loud music reaching our holding tanks. This has a high probability of resulting in the death
of some animals due to striking the tank walls or jumping out of the tank to escape the noise. Prolonged exposure to loud
noise will likely have non -lethal impacts that are equally as damaging to our research. Noise induced stress can result in
reduced disease resistance, growth, reproductive success, and survival at all life stages.
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The UMEH is a unique facility that is dependent on this location on Virginia Key to provide access to seawater in an
environment that is hospitable to the breeding and rearing of all types of marine life. The creation of a major concert
venue immediately adjacent to this site will severely degrade this facility and its ability to carry out its mission to study
marine animals to better understand the factors threatening these species in the wild and to train the next generation of
marine scientists.
We respectfully request that this information be taken into account before voting on the resolution.
Warm regards,
Roni Avissar, Dean
Rosenstiel School of Marine & Atmospheric Science
University of Miami
cc: City of Miami Office of the Clerk
Encl: The Impact of Ocean Noise Pollution on Fish and Invertebrates by Ocean Care and Dalhousie University
THE IMPACT OF OCEAN NOISE POLLUTION
ON FISH AND INVERTEBRATES
LINDY WEILGART, PH.D.
OCEANCARE & DALHOUSIE UNIVERSITY
1 MAY 2018
THE IMPACT.OF OCEAN NOISE POLLUTION
ON FISH AND INVERTEBRATES
LINDY WEILGART, PH.D.
OCEANCARE & DALHOUSIE UNIVERSITY
1 MAY 2018
ocean cIt
are
Submitted into the pub1�'e
record fo Iiter�(s Y�t�_
on // City Clerk
DALHOUSIE
UNIVERSITY
Inspiring Minds
The Impact of Ocean Noise Pollution on Fish and Invertebrates
Submitted into the pubic
record fbf ite (s)
Table of Contents on _1City Clerk
The importance of context
............................................................................................................................._..._.................................
16
Introduction -: .5
......................................... t..........................................................................................................................................
Development...................................................................................................................................................................
............................ ................7
Anat......................................................................................................................................................................................................................._...9
Foraging and feeding ........................
I?hysiology.. (Stress)...............................................................................................................................................................................................11
Attention
Important concepts for interpreting noise impact.studies.................................................................................................1.4
S5 ftgq ing,behav„ior
Behavior.,...._...............................................................................................................................................................................................................15
Ecosystem consequences _
..............................................................................................................................._.....................
The importance of context
............................................................................................................................._..._.................................
16
Reproduction
17
Antipredator behavior
......... 1,7
Foraging and feeding ........................
18
Attention
19
S5 ftgq ing,behav„ior
19
Ecosystem consequences _
..............................................................................................................................._.....................
21
.
Seabed vibration
21
Masking.......................................................................................................................................................................................................................21.
Catch rates.. abundances and distribution..........................................................................................................................................22
.......................... ..............
Interactions between stressors including.synergistic impacts....................................................................................... 24
................................................................................................
Reviewsof noise impact literature ..........................................................................................................................................................25
Scientificgaps and studies............................................................................................................................................................26
..................ic ................ s
Management,and mitigation recommendations........................................................................................................................ 27
......... ..... ...............
References ... 28
The Imnar t of Ocean Noi-e lollution on Fish and Invertebrates
Submitted into the public
Abstract record flr it m(s)
on City Clerk
Most fish and invertebrates use sound for vital life functions. This review of 115 primary studies
encompasses various human -produced underwater noise sources, 66 species of fish and 36 species of
invertebrates. Noise impacts on development include body malformations, higher egg or immature
mortality, developmental delays, delays in metamorphosing and settling, and slower growth rates.
Zooplankton suffered high mortality in the presence of noise. Anatomical impacts from noise involve
massive internal injuries, cellular damage to statocysts and neurons, causing disorientation and even death,
and hearing loss. Damage to hearing structures can worsen over time even after the noise has ceased,
sometimes becoming most pronounced after 96 hrs. post -noise exposure. Even temporary hearing loss
can last months. Stress impacts from noise are not uncommon, including higher levels of stress hormones,
greater metabolic rate, oxygen uptake, cardiac output, parasites, irritation, distress, and mortality rate,
sometimes due to disease and cannibalism; and worse body condition, lower growth, weight, food
consumption, immune response, and reproductive rates. DNA integrity was also compromised, as was
overall physiology. Behaviorally, animals showed alarm responses, increased aggression, hiding, and flight
reactions; and decreased anti -predator defense, nest digging, nest care, courtship calls, spawning, egg
clutches, and feeding. Noise caused more distraction, producing more food -handling errors, decreased
foraging efficiency, greater vulnerability to predation, and less feeding. Schooling became uncoordinated,
unaggregated, and unstructured due to noise. Masking reduced communication distance and could cause
misleading information to be relayed. Some commercial catches dropped by up to 80% due to noise, with
larger fish leaving the area. Bycatch rates also could increase, while abundance generally decreased with
noise. Ecological services performed by invertebrates such as water filtration, mixing sediment layers, and
bioirrigation, which are key to nutrient cycling on the seabed, were negatively affected by noise. Once the
population biology and ecology are impacted, it is clear fisheries and even food security for humans are
also affected. Turtles, sharks, and rays were especially underrepresented in noise impact studies. Research
on an individual's ability to survive and reproduce, and ultimately on population viability and ecosystem
community function, is most vital. More long-term, realistic field studies also considering cumulative and
synergistic effects, along with stress indicators, are needed.
Introduction
The World Health Organization (2011) notes that human -caused (anthropogenic) noise is recognized
as a global pollutant; indeed, it is one of the most harmful forms. Human -caused noise is pervasive
both in terrestrial and aquatic ecosystems. There are about 170,000 known species of multi -cellular
marine invertebrates and 20,000 species of marine fish. All fish studied to date are able to hear sounds
(Slabbekoorn etaL 2010), and more and more invertebrates have been found to be able to detect sound
and/or vibration and to respond to acoustic cues (e.g. Simpson etaL 2011 b). Fish are very acoustic
animals, in general, using sound to perceive their environment, for mating, communication, and
predator avoidance (Popper 2003). Noise can affect an individual's behavior, physiology, anatomy, and
development. For instance, Kunc etaL (2016) show how noise impacts on behavior such as compromised
communication, orientation, feeding, parental care, and prey detection, and increased aggression, can
lead to less group cohesion, avoidance of important habitat, fewer offspring, and higher death rates.
Similarly, noise impacts on physiology can cause poor growth rates, decreased immunity, and low
reproductive rates. Anatomical impacts from noise can include abnormal development or malformations,
hearing loss, or injured vital organs, which can result in strandings, disorientation, and death. While
some animals may recover from behavioral or physiological impacts, others, such as changing the DNA,
or genetic material, or injury to vital organs, are irreversible (Kight & Swaddle 2011). Kunc etaL (2016)
depict how all of these impacts, reversible or not, can, in turn, have broad ramifications on the ecosystem,
changing the population biology (how healthy and resilient populations of various species are) and
ecology (how different species interact and remain in balance). Once the population biology and ecology
are impacted, it is clear fisheries and even food security for humans are also affected.
For this review, the following noise sources were used in the studies: ship and boat noise, airguns,
pile driving, aquaculture noise, low -frequency playbacks, tones, sweeps, and white noise. The animals
The Impact of Ocean Noise Polluticn on Fish and Invertebrates Submitted into the pu
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observed in the studies were 36 species of invertebrates (European squid (Loligo vulgaris), southern
shortfin squid (1/lexcoin detii), southern reef squid (Sepioteuthis australis), giant squid (Architeuthis dux),
common Mediterranean cuttlefish (Sepia officinalis), common octopus (Octopus vulgaris), commercial
scallop (Pecten fumatus), sea hare (Aplysia californica), sea squirt (Ciona intestinalis), fried egg jellyfish
(Cotylorhiza tuberculate), barrel jellyfish (Rhizostoma pulmo), zooplankton, water flea (Daphnia magna)
lined seahorse (Hippocampus erectus), common prawn (Pa/aemon serratus), Southern white shrimp
(Litopenaeus schmitti), Southern brown shrimp (Crangon crangon), Atlantic seabob (Xiphopenaeus
kroyeri), brown bryozoan (Bugula neritina), barnacle (Balanus amphirite), southern rock lobster (Jasus
edwardsii), Norway lobster (Nephrops norvegicus), American lobster (Homarus americanus), European
spiny lobster (Palinurus elephas), New Zealand green -lipped mussel (Perna canaliculus), blue mussel
(Mytilus edulis), Pacific oyster (Maga/lana gigas), Manila clam (Venerupis philippinarum), razor clam
(Sinonovacula constricts), brittle star (Ophiuroidea), tunneling mud crab (Austrohelice crasso), hairy -
handed crab (Hemigrapsus crenulatus), shore crab (Carcinus maenas), Caribbean hermit crab (Coenobita
clypeatus), common hermit crab (Pagurus bernhardus), Dungeness crab (Cancermagister), snow crab
(Chionoecetes opilio)) and 66 species of fish (Atlantic herring (Clupea harengus), Pacific herring (Clupea
harengus pallasi), blue whiting (Micromesistius poutassou), mesopelagic fish, pollock/saithe (Pollachius
virens) Greenland halibut (Reinhardtius hippoglossoides), bluefin tuna (Thunnus thynnus), sprat (Sprattus
sprattus), dab (Limanda limanda), golden redfish (Sebastes norvegicus), ling (Molva molva), lesser sandeel
(Ammodytes marinus), European eel (Anguilla anguilla), Atlantic cod (Godus morhua L.), sole (Solea solea),
haddock (Me/anogrommus aeglefinus), thicklip mullet (Chelon labrosus), pout (Zoarces americanus), pink
snapper (Pagrus auratus), horse mackerel (Trachurus trachurus), Atlantic mackerel (Scomberscombrus),
roach (Rutilus rutilus), European perch (Perca fluviatilis), European sea bass (Dicentrarchus labrox),
gilthead sea bream (Sparus ourata L.), black sea bream (Spondyliosoma contharus), trevally (Pseudocaranx
dentex), European plaice (P/euronectes p/atesso), giant kelpfish (Heterostichus rostratus), wild mulloway
Argyrosomus japonicas), greenspotted rockfish (Sebastes chlorostictus), chilipepper (Sebastes goodie),
bocaccio (Sebastes paucispinis), olive rockfish (Acanthoclinus fuscus), black rockfish (Sebastes melanops),
blue rockfish (Sebastes mystinus), vermilion rockfish (Sebastes miniatus), two -spotted goby (Gobiusculus
flavescens), painted goby (Pomatoschistus pictus), Lusitanian toadfish (Holobatrachus didactylus), oyster
toadfish (Opsanus tau), cardinalfish (Pterapogon kauderni), orange clownfish (Amphiprion percula), ambon
damselfish (Pomacentrus amboinensis), charcoal damselfish (Pomacentrus brachialis), lemon damselfish
(Pomacentrus moluccensis), Nagasaki damselfish (Pomacentrus nagasakiensis), Mediterranean damselfish
(Chromis chromis), Ward's damselfish (Pomacentrus wardi), spiny chromis damselfish (Acanthochromis
polyacanthus), brown meagre (Sciaena umbra), red -mouthed goby (Gobius cruentatus), oscar (Astronotus
ocellatus), goldfish (Carassius auratus), catfish (Pimelodus pictus), common carp (Cyprinus carpio), gudgeon
(Gobio gobio), three-spined sticklebacks (Gasterosteus aculeatus), largemouth bass (Micropterus salmoides),
fathead minnow (Pimephales promelas), sheepshead minnow (Cyprinodon variegatus variegatus),
European minnow (Phoxinus phoxinus), longnose killifish (Fundulus similis), rainbow trout (Oncorhynchus
mykiss), daffodil cichlid (Neolamprologus pu/cher), convict cichlid (Amatitlania nigrofasciato), zebrafish
(Danio rerio)).
While most species mentioned in this review are marine, there are some fresh -water ones included,
as they share an aquatic environment, are sometimes related, and share many characteristics, such as
how they sense and react to noise. The research areas included: Italy, Spain, Portugal, Norway, Sweden,
the Netherlands, Germany, England, Scotland, Ireland, New Zealand, Australia, French Polynesia, Brazil,
Canada, USA, and the U.S. Virgin Islands. Clearly, there is a preponderance of European and U.S. studies.
Asia and Africa are very underrepresented, as is South America. Of the 144 references used, 135 were
from peer-reviewed journals, 4 from reports, 3 from book chapters, one Ph.D. thesis, and one abstract. A
total of 115 primary studies were described, which do not include reviews.
Underwater sound is made up of both particle motion and acoustic pressure, but particle motion is
more dominant in the low frequencies of a few hundred Hertz (Kunc eta/. 2016). Particle motion is also
considered to be more relevant over short distances, where it is not proportional to pressure, but may
also be important over longer distances (Normandeau Associates, Inc. 2012). All fish and invertebrates
can detect particle motion, though many can detect pressure as well. Particle motion is especially
Submitted' he pub
The Imoact of Ocean Wise'ollution on Fish and Invertebrates
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on W I � M • City Clerk
important to animals for locating sound sources through directional hearing (Hawkins & Popper 2017).
Mammals mainly only detect acoustic pressure (Nedelec etaL 2016). Taking into account particle motion
is relevant if levels of particle motion at close distances are enough to cause physical injury even when
pressure levels may not be very high.
Development
When survival or the ability to reproduce is diminished in early life, there are serious consequences to
the population's resilience, potentially leading to overall weakened ecosystem community structure
and function. Early development stages of marine life, such as eggs, embryos (fertilized eggs), larvae,
or fry (juvenile fish), may be more or less sensitive to noise effects than the adult stages. This may have
something to do with when in their development they are able to detect sound (Kunc etal. 2016), or
when their body changes affect the transmission of sound through them, such as the development of
shells (Aguilar de Soto etaL 2013). Scallop larvae in tanks subjected to recordings of seismic airgun pulses
exhibited significant developmental delays and 46% developed body malformations compared with
controls (Aguilar de Soto etal. 2013). No malformations were found in the 4,881 control larvae examined.
Seismic shots were recorded tens of kilometers away from a seismic survey (SEL pulse 163 dB,,, re
1 pPa2-s, at 3-4 ms -Z), and the total duration of exposure was 90 h of pulses every 3 s. The unequivocal
damage in the experiment was likely due to particle motion, but acoustic pressure could also contribute
at greater distances, affecting potentially tens to hundreds of square kilometers, and thus, survival of the
young until adulthood in the wild, harming the scallop stock (Aguilar de Soto etaL 2013). Development
was also impaired in the sea hare, a slug -like marine invertebrate, after recordings of boat noise were
played back to embryos and recently hatched larvae in the field. The successful development of these
embryos was reduced by 21 % and the larvae suffered increased mortality of 22%, when compared with
those exposed to natural, background noise playbacks (Nedelec etaL 2014). These effects might have
occurred due to tissue damage, disrupted tissue formation, or even from a change in how genes were
expressed (Nedelec etaL 2014). Though repeated boat -noise playbacks significantly increased larval
mortality and the chances of developmental failure in embryos, the rate of embryo development did not
appear to be affected (Nedelec etaL 2014). Sea hares are ecologically and socio -economically important,
as they keep corals and algae in balance, and specialize on grazing on toxic bacteria (Nedelec etaL 2014).
Larval Atlantic cod were exposed in the laboratory to two days of both regular and random ship noise
(Nedelec etaL 2015). Fish exposed to regular noise had lower body width -length ratios, an indicator of
condition. These larvae were also easier to catch in a predator -avoidance experiment, affecting survival.
Even subtle effects at this early life -history stage could have population consequences (Nedelec etaL
2015). Contrary to expectation, regular noise was more disturbing to the larvae than random noise,
perhaps because the regular noise events, occurring every 45 mins., did not allow for sufficient energetic
recovery from the disruption of foraging, leading to a cumulative stress response. Longer recovery time
intervals during random noise disturbance might have allowed for more compensation or habituation
(Nedelec etaL 2015).
In the presence of around 20 hrs. of low -frequency (30 Hz) sound, barnacle larvae were inhibited from
metamorphosing and settling (Branscomb & Rittschof 1984). Especially the very young larvae (0 days
old) were affected, as less than I% settled during sound exposure. As larvae age, they become less
discriminating about where to settle, yet, even at 13 days old, the percentage metamorphosing and
settling was lower in the noise condition (Branscomb & Rittschof 1984). In contrast, mussel larvae in
the presence of ship noise (126 and 100 dB re 1 pPa,R,,) settled 40% faster compared to a silent control
(Wilkens et al. 2012). The more intense the ship noise, the faster the settlement time (Wilkens et al. 2012).
Jolivet etaL (2016) also found that a planktonic food cue together with playbacks of low -frequency ship
noise (source level 130 dB re 1 p Pa between 100 and 10,000 Hz) in the laboratory drastically increased
blue mussel settlement by a factor of 4 compared to the control. Settlement levels approached 70% in
67 hrs, compared to more typical settlement success of 20%. While underwater noise increases mussel
settlement (causing more biofouling on ships), it also decreases the size of the settler with "potential
cascading ecological impacts"(Jolivet etaL 2016). Stanley etal. (2014) conducted a field study on
The Impact of Ocean Noise Pollution on Fish and Invertebrates
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biofouling and found that playbacks of noise emitted through a vessel's hull in port (128 dB 1 NParm,,
30-10,000 Hz) enhanced the settlement and growth of biofouling organisms within four weeks of the
clean surfaces being placed in the sea. More than twice as many bryozoans, oysters, calcareous tube
worms, and barnacles settled in the presence of noise vs. without. Individuals from four species also grew
significantly larger in size in the presence of vessel noise (Stanley etal. 2014).
McDonald etal. (2014) also investigated biofouling and ship noise, as vessel hull fouling can be
responsible for at least 75% of the invasive species brought in by ships. They found increased rates of
settlement, metamorphosis, and survival of sea squirt larvae when exposed to vessel generator noise
(127.5-140.6 dB re 1 µPar,=, 30-100 Hz) in the laboratory. About half of the surviving larvae exposed to
generator noise had settled just 6 hrs. after the experiment began, with the rest settling by 18 hrs. In
marked contrast, for the control, it took 15 hrs. for half of the surviving larvae to settle and 26 hrs. for
the remaining ones (McDonald etal. 2014). Metamorphosis occurred in 60% of the larvae exposed to
noise vs. 20% in the control over a 12 hr period. Biofouling on the four fishing vessels examined was
highest nearest the generator, which was also the area of highest intensity of noise, and lowest on the
bow. Larvae under the loudest noise conditions, near the generator, had a 100% survival rate vs. 66% for
the control (McDonald et al. 2014). Calculated from the levels of noise used in this experiment, a clean
vessel entering a port infected with invasive species and running a generator could be attracting pest
species from a ca. 500 m radius. As such, shore -based power rather than the use of generators should be
encouraged both to avoid invasive species and to reduce biofouling, something which costs the U.S. Navy
US$1 billion every year and US$56 million for a single vessel class of the Navy (McDonald etal. 2014).
Larval coral reef fish orient towards natural shrimp or fish sounds when returning from the open ocean
to find a suitable place to settle and live out their adult lives (Simpson etal. 2005). Settlement -stage
coral larvae (Vermeij et al. 2010) and many free-swimming crustacean development stages or species
(Simpson et al. 2011 b) also use sound as an orientation cue. When four species of 3 -week old larval
damselfish were conditioned on 12 hours of artificial tone noise, however, they were subsequently
attracted to it (Simpson et al. 2010). Those larvae that were conditioned on reef noise, in contrast,
avoided the artificial tone noise. These results indicate that anthropogenic noise could cause confusion
and disrupt orientation behavior at a critical life stage (Simpson etal. 2010). This could, in turn,
affect population welfare and weaken the connectivity between populations, thus diminishing the
replenishment of fished species. Holies et al. (2013) also determined that the settlement of coral reef
fish larvae was disrupted by boat noise as only 56% of larvae swam towards boat noise mixed together
with reef sounds, whereas 69% of fish swam towards the reef sounds alone. In terms of aversion, 44% of
fish larvae moved away from the boat noise mixed together with reef sounds, compared with only 8%
from the reef -sounds -only playback. Holies et al. (2013) explained this response by fish being confused
by the addition of boat noise, with some attracted while others are repelled. If noise disrupts the
crucial settlement process, larvae could spend longer times swimming before settling, suffering greater
predation and energetic costs, altering population dynamics (Holies etal. 2013).
Banner & Hyatt (1973) raised eggs and larvae of sheepshead minnows and longnose killifish in tanks with
high water -pump noise (118 dB re 1 µPa) and in quieter control tanks (103 dB re 1 pPa). Sheepshead
minnows suffered a greater mortality of eggs and fry in the noisy tanks, and both species showed slower
growth rates of fry in the noisy tanks. Caiger et al. (2012) compared the hearing abilities of juvenile
snapper in comparatively low -intensity noisy (120 dB re 1 µPa) aquaculture tanks to those in quiet ones
(107 dB re 1 NPa). After only 2 weeks of exposure, the fish displayed significant hearing losses of 10 d6.
Most aquaculture tanks are much noisier than the "noisy"tank used in this experiment (Caiger et al. 2012).
With this amount of hearing damage, aquaculture -raised snapper would be predicted to hear reef sounds
at half the distance (18 km) that wild fish could (36 km), based on modelling (Caiger etal. 2012).
McCauley et al. (2017) found that even small or microscopic zooplankton, especially immatures, can be
killed by shots from a single seismic airgun. Phytoplankton, the "grass" of the ocean, are at the base of the
food web, but zooplankton, the grazers or the"grasshoppers"of the seas, are just above them, providing
not only an essential food source for whales but also upon which the whole ocean ecosystem, from fish
Submitted into the
The Impact of Ocean Noise "ollution on Fish and Invertebrates
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to larger invertebrates (oysters, clams, crabs, shrimp) to seabirds, depends. A large kill -zone or"hole"
in zooplankton abundance formed after the single airgun passed, where their numbers were cut more
than in half in most of the species (McCauley etaL 2017). All immature krill (shrimp -like zooplankton)
were killed. One-third of the zooplankton species even showed decreases in numbers of over 95%. The
seismic airgun caused a 2 -3 -fold increase in dead zooplankton overall, compared with controls. These
impacts extended out to at least 1.2 km, which was the maximum range studied. The zooplankton "hole"
could be detected via sonar 15 mins. after the airgun passed and was observed to continue to expand
until about 1.5 hrs. It should be remembered that most seismic surveys consist of 18-48 airguns with
total air volumes of 3,000-8,000 cu. in. versus the single airgun of only 150 cu. in. used in this experiment.
McCauley etaL (2017) conclude that their results have "enormous ramifications for ... ocean health..."
given the long time and spatial scale of seismic surveys.
Eggs or immature stages of at least some fish and invertebrates, in contrast, are apparently relatively
resilient to noise. Recordings of small motor boat noise played back to early life stages of freshwater
cichlid fish in tanks did not seem to affect hatching success, fry survival, growth, or size (Bruintjes &
Radford 2014). There was no evidence of harm from these four weeks of playbacks of chronic, though
moderate, noise. Wysocki et aL (2007) also did not find that rainbow trout suffered significant negative
impacts from noise levels typical in recirculating aquaculture systems. There were no detectible effects
on hearing sensitivity, growth, survival, stress, and disease susceptibility (Wysocki et al. 2007), but trout
are known to be relatively insensitive to sound (not a hearing specialist). Pearson etaL (1994) exposed
the larval forms of Dungeness crabs to single shots from a 840 cu. in. seismic array (maximum exposure
231 dB re 1 NPa) in the field. Pearson et al. (1994) found minimal impacts on survival (<7-12% reduction)
and time to molt (one day shorter for the exposed larvae), but the background sound measured during
the control periods of the experiment was unusually high (156 to 168 dB re 1 µPa) because the airgun
compressors were operating despite the airguns not shooting. Day etaL (2016) discovered that southern
rock lobster embryos were not harmed by airgun exposure, as they could find no differences in the
quantity or quality of hatched larvae compared with controls. At the time of exposure to airguns in the
field, the eggs were at an early embryonic developmental stage, just after being laid and before eye
development, so were just composed of soft tissue with no large internal density differences. This may
have protected them from acoustic impacts, and results may be different if older embryos or larvae are
exposed to airguns (Day etaL 2016).
Anatomy
Hearing damage or damage to sensory systems may represent a combination of impacts to an animal's
anatomy and physiology. Noise can damage single cells or whole organs. Invertebrates use organs
called statocysts for balance, orientation, and body positional information. These can be harmed by
noise (Andre etaL 2011) as well as the ears or swim bladders in fish, causing loss of buoyancy control,
disorientation, and stranding. Andre etaL (2011) found that experimental exposure to low sound
frequencies of two species of squid, one species of cuttlefish, and one species of octopus resulted in
"...massive acoustic trauma, not compatible with life,..." The noise produced substantial, permanent,
cellular damage to the statocysts and neurons. A total of 87 individuals in tanks were exposed for only
2 hrs. to received levels of 157 dB re 1 µPa (peak levels up to 175 dB re 1 µPa); particle motion was not
measured. The injuries appeared immediately and worsened over time, becoming most pronounced
after 96 hrs., the maximum time studied. All individuals showed the same injuries and the same
incremental effects over time (Andre etaL 2011) . These may be the result of particle motion, acoustic
pressure, or both. Further studies using additional individuals and controls confirmed these results,
where the massive damage affected a broad range of statocyst inner areas (Sole etaL 2013a, Sole etaL
2013b). Both mechanical and metabolically -caused injuries were observed. To remove the possible
artifact of tank walls on particle motion, Sole etaL (2017) conducted offshore noise controlled exposure
experiments on cuttlefish, using three different depths and distances from the source. As before, injuries
to the statocysts were apparent using a scanning electron microscope, and the severity of the injuries was
greater, the closer the distance to the sound source (139-142 dB re 1 NPaz at 1/3 octave bands centred
at 315 Hz and 400 Hz). Damage increased with time after sound exposure (Sole etaL 2017). Cuttlefish
Submitted into the Publi�
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are therefore shown to be sensitive to noise in their natural habitat, affecting them at physiological and
pathological levels, and likely altering their sound perception mechanisms which compromises their
survival in the wild (Sole etaL 2017).
In 2001, five giant squid mass stranded in one localized area off northern Spain (Guerra etaL 2004). Two
years later, four more giant squid mass stranded or were found floating in the same area. All of these
nine strandings, some of them live, occurred together with geophysical seismic surveys using air guns
(Guerra etaL 2004). Even though externally, they showed no obvious cause of death, the squid all had
massive internal injuries. Two of the squid suffered "...extensive damage to internal muscle fibres, their
stomachs were ripped open and their digestive tracts were mangled.' (Guerra etal. 2011). Some also
showed substantial damage to their statocysts, leaving them effectively disoriented. As a result, these
normally deep -water animals might have floated to warmer surface waters, where, because of their blood
chemistry, they lost oxygen, potentially causing their death (Guerra etaL 2004).
Sole etaL (2016) exposed two species of jellyfish (fried egg jellyfish and barrel jellyfish) to a sweep of
low frequency sounds (received levels 157 ± 5 dB re 1 p Pa with peak levels up to 175 dB re 1 µ Pa SPL)
for two hrs. in the laboratory. Scanning electron microscopy revealed ultrastructural changes that took
place following damage to the jellyfish statocyst sensory epithelium of both species after noise exposure,
compared to controls (Sole et al. 2016). These injuries are similar to the massive acoustic trauma observed
in other species. Damaged hair cells were extruded or missing or with bent, flaccid or missing structures.
The severity of the acoustic damage also increased over time (Sole etaL 2016). Such injuries could
prevent or hinder orientation, even in these species that are not hearing specialists.
In terms of hearing impairment in fish, Hastings etal. (1996) showed hearing damage in the ear hair
cells of the oscar after one hour of continuous exposure to a 300 Hz pure tone at 180 dB re 1 µPa, but
interestingly, the damage was only visible four days after sound exposure, so there appears to be a
delayed response. Scholik & Yan (2001) found that the fathead minnow, a hearing specialist, showed
significant decreased hearing sensitivity in three out of the four frequencies tested, after just one hour
of white noise exposure, at much lower levels than above (142 dB re 1 µPa). After 2 hours of noise
playback, hearing sensitivity was worse in all four frequencies, and even as bad as with 24 hours of
playback. Recovery ranged from one day to over 2 weeks (the maximum tested), depending ori the
frequency measured. Recovery also depended on the duration of exposure, with 2 hrs. of exposure
showing recovery after 6 days, but 24 hrs. of exposure not showing recovery even after 2 weeks (Scholik
& Yan 2001). When goldfish, hearing specialists, were reared under either quiet (110-125 dB re 1 µPa) or
noisy (white noise, 160-170 dB re µPa) conditions, they exhibited a significant loss of hearing sensitivity
after just 10 mins. (Smith et al. 2004). This hearing loss worsened linearly up to 24 hrs. of exposure. Even
though there was recovery after playbacks, hearing sensitivity for the 24 -hr exposed fish didn't fully
return to pre -exposure levels even after 18 days. Smith etal. (2004) suggest that it may take 28-35 days
to fully repair any temporary threshold shifts (temporary loss of hearing sensitivity). Noise from an idling,
single 55 -horsepower outboard motorboat was played back to fathead minnows for 2 hours at 142 dB re
1 µPa (Scholik & Yan 2002). A significant loss of hearing sensitivity resulted from this short, relatively mild
exposure, especially over the fishes' most sensitive hearing range. More boats and travelling at speed,
rather than idling, would presumably be much louder and cause more hearing loss (Scholik & Yan 2002).
Amoser & Ladich (2003) played back white noise at 158 dB re 1 µPa at 12 and 24 hrs. duration to goldfish
and catfish, both hearing specialists. Both species, but especially the catfish, showed a significant loss of
hearing sensitivity, particularly in their most sensitive frequencies. Recovery took 3 days for the goldfish,
but the catfish needed 2 weeks, and even then, hearing at one frequency didn't recover (Amoser & Ladich
2003). These differences may reflect differences in habitat. Species that are less impacted could live in
a naturally noisier habitat and not communicate using sound (Aguilar de Soto & Kight 2016). Amoser
& Ladich (2003) note that this large degree of hearing impairment, even if temporary, could change
the outcomes of fights between males, which could reduce the quality of offspring. Hearing damage
would also decrease the distances over which individuals could communicate and limit the detection
of predators and prey, both potentially affecting the survival and reproduction of individuals (Amoser &
Ladich 2003).
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The Impact of Ocean Noise Pollution on Fish and Invertebrates
A single seismic air gun (source level 222.6 dB �,.P re 1 µPa) extensively damaged caged pink snapper
ears in the field at distances of from 5-15 m (closest approach) to 400-800 m (McCauley et at 2003). The
equivalent highest levels (at closest approach) for a large seismic array would be experienced within
500 m (McCauley etaL 2003). Since it was not known whether the fish were more injured from the few
close exposures or the many more moderate ones (McCauley etaL 2003), the equivalent distance for a
large seismic array could extend to several kilometers. No recovery was apparent in the fish even 58 days
after exposure (McCauley etaL 2003), though fish hair cells can regenerate after noise exposure (Smith
etaL 2006). The snapper ear is apparently typical of many commercial species such as tuna, cod, and
haddock (Popper 1977). Song et at (2008), however, found no damage to the ears of 3 freshwater fish
species exposed to 5-20 shots from a very small (730 cu. in.) seismic airgun array at received levels of 205-
209 dB peak re 1 µPa. Since they were only able to examine fish no later than 24 hours after exposure, they
might have missed some injuries, however, given the delayed response some effects show. Physiological
responses to reduce swelling in the inner structures of the ear or statocysts after noise exposure may
be one reason why delayed damage has been observed in terrestrial mammals, cephalopods (squid
and octopus), and fish (Aguilar de Soto & Kight 2016). Another mechanism that can cause delayed
damage from noise is sensorineural hearing loss due to delayed nerve cell death (Aguilar de Soto &
Kight 2016), which, at least in terrestrial mammals, can appear months after exposure and worsen over
years (Kujawa & Liberman 2009). Such damage first appears in the ability to hear in noisy conditions and
complex acoustic environments (Aguilar de Soto & Kight 2016). Typical measures of hearing loss, i.e. TTS
(temporary threshold shift) and PTS (permanent threshold shift), however, do not detect such injuries,
as these measurements are carried out in quiet settings (Aguilar de Soto & Kight 2016). Sensorineural
hearing loss can be present even if there is no TTS or damage to the usual structures that identify hearing
effects. Thus, TTS may not be so temporary after all (Kujawa & Liberman 2009).
Popper et al. (2007) exposed rainbow trout, a nonhearing specialist, to low -frequency active sonar
to a maximum received level of 193 dBrms re 1 µPaz for 324 or 648 s. They found temporary hearing
impairment at one frequency but no other impacts. There were differences between different groups of
the same species of trout obtained from the same supplier (Popper etaL 2007).
Physiology (Stress)
Much research has focused on noise effects on hearing, however current scientific knowledge shows that
the non -hearing effects of noise on marine animals, such as stress, may be as, or more, severe than hearing
effects (Aguilar de Soto 2016). Even temporary exposures to stressors in early life stages can have health
and reproductive consequences later on (Kight & Swaddle 2011). Aguilar de Soto & Kight (2016) argue that
'bottom-up'(genetic, cellular, and physiological) processes allow us to make broad predictions about the
mechanisms of noise effects. There are many similarities between species in the basic biochemical and
physiological pathways of noise effects. For example, the stress response is largely conserved and shared
across many species, enabling us to predict immunosuppression as one effect of stress for a wide variety of
species. In contrast,'top-down'(driven by environment, behavior, and ecology) mechanisms illuminate the
complexity of responses to noise between species (Aguilar de Soto & Kight 2016).
Just because fish may remain in noisy areas, it does not mean that they are not affected by the noise. Fish
may need to "put up"with the noise if the habitat is sufficiently valuable for other reasons, such as feeding,
mating, or if the area is part of their familiar home territory, containing their nest. Remaining in a noisy
area does not mean the fish are unscathed, as "...adverse effects are not necessarily overt and obvious..."
(Slabbekoorn et at 2010). In fact, some of the most serious impacts, such as stress, can be largely invisible.
Noise -induced stress could compromise reproduction, health, and immunity (Wright et at 2007).
One measure of stress used are the levels of stress hormones such as cortisol. Cortisol can negatively
affect growth, sexual maturation, reproduction, immunity, and survival. Wysocki et al. (2006) played back
underwater ship noise at realistic levels (153 dB re 1 µPa) for 30 min. to one hearing generalist (European
perch) and two hearing specialists (common carp, gudgeon). Another experiment used white noise
played back at 156 dB re 1 µPa. On average, cortisol increased 99% over control values in the perch, 81 %
The Impact of Ocean Noise Pollution on Fish and Invertebrates
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in the carp, and 120% in the gudgeon for the shipping noise playback, though white noise didn't cause a
significant change compared to the controls (Wysocki etaL 2006). Wysocki etaL (2006) theorized that this
may be due to the greater unpredictability (changes in frequency and level) of shipping noise compared
to the continuous white noise. There were no differences in cortisol levels relative to fish hearing ability,
i.e. between generalists and specialists (Wysocki etaL 2006). In goldfish, mean levels of plasma cortisol
tripled after the first 10 mins. of white noise (160-170 dB re µPa) was played back, relative to controls
(110-125 dB re 1 µPa), but dropped to control levels after one hour of noise exposure (Smith etaL 2004).
This may be due to acclimation or, because there was already a measured loss in hearing sensitivity after
10 mins. of noise exposure, the goldfish didn't perceive the noise as being as loud, so experienced less
stress (Smith etaL 2004).
When boat noise (regular intermittent, random intermittent, or continuous) was played back to juvenile
giant kelpfish in tanks, they exhibited acute stress responses (Nichols etaL 2015). Intermittent noise
at high SPL (136.9 dBrms and 141.9 dBrms re 1 µPa) caused the greatest response, elevating cortisol
concentrations. Continuous noise did not show an acute stress response even though fish in continuous
noise conditions were exposed to more than twice the duration of intermittent noise during each trial
(Nichols etaL 2015). Fish subjected to a random pattern of noise responded with significantly higher
cortisol levels compared with continuous noise or natural sounds. Thus, predictability in the timing of
noise events may matter, with lower predictability causing more stress (Nichols et aL 2015). A biochemical
stress response was exhibited in caged European sea bass when a seismic survey (2,500 cu. in.) passed
by at distances from 180 m to 6,500 m (Santulli etaL 1999). Cortisol in the plasma, muscle, and liver all
increased significantly after exposure to seismic airgun noise. Other biochemical measures (glucose,
lactate, etc.) also showed a primary (e.g. plasma cortisol) and secondary (e.g. blood glucose and other
blood measures) stress response even at distances of 2 km from the seismic survey. Most biochemical
values returned to pre -exposure levels after 72 hrs. Fish already showed behavioral responses to the
seismic noise at distances of 2,500 m (Santulli et aL 1999). Buscaino et aL (2010) exposed European sea
bass and gilthead sea bream to a sweep of frequencies that are produced by vessel traffic, at a level of 150
dBrms re 1 µPa for 10 mins. The amount of movement of both species was significantly higher compared
to controls. Changes in blood measures (glucose and lactate) showed intense metabolic activity during
exposure, which could cut into the fishes' energy budget, leaving less energy for feeding, migration, and
reproduction (Buscaino et aL 2010). Anderson etaL (2011) housed lined seahorses in noisy (123-137 dBrms
re 1 µPa) and quiet (110-119 dBrms re 1 µPa) tanks for one month. Seahorses responded both behaviorally
and physiologically, displaying a chronic stress response. Animals in loud tanks showed more irritation
behavior, pathological and distress behavior, lower weight, worse body condition, higher plasma cortisol
and other blood measures indicative of stress, and more parasites in their kidneys. In addition to the
primary and secondary stress indices in the blood and plasma, seahorses exhibited tertiary ones (e.g.
growth, behavior, and mortality) as well (Anderson et aL 2011).
Cardiac output is also a sensitive indicator of fish stress. Largemouth bass were subjected to three noise
disturbances: canoe paddling, trolling motor, and 9.9 horsepower combustion engine for 60 s (Graham &
Cooke 2008). While all three noise types produced higher cardiac output (dramatically higher heart rate),
the paddling caused the least response in the fish and the engine, the most. Recovery from the paddling
also took the least time 05 mins.) and from the engine, the longest time --40 mins. (Graham & Cooke
2008). Celi etaL (2016) found that 10 days of vessel noise playbacks (123-136 dBrms re 1 µPa) to gilthead sea
bream produced significant biochemical changes in the blood or plasma (cortisol, ACTH, glucose, lactate,
hematocrit, etc.) showing clear primary and secondary stress response to maritime vessel traffic. Wale et
aL (2013a) played back ship noise (received levels: 148-155 dBrms re 1 µPa) to a marine invertebrate, the
shore crab. Playbacks lasted 15 mins. and mimicked two successive ship passes. Crabs subjected to the
ship noise used 67% more oxygen than those exposed to ambient noise (received levels: 108-111 dBrms re
1 µPa), with heavier crabs showing a more pronounced response (Wale et aL 2013a). The increased oxygen
consumption of the ship -noise -exposed crabs was not due to greater crab movement but to a higher
metabolic rate, which in turn, can indicate higher cardiovascular activity from stress (Wale etaL 2013a). The
size -dependent response may indicate that larger individuals in noisy conditions are less likely to survive,
whereas the remaining smaller ones may be less likely to reproduce (Wale etaL 2013a).
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Brown shrimp reared in loud (128 dB re 1 NPa) tanks exhibited decreased growth, food consumption,
lower reproductive rates (50% vs. 80%), fewer egg -bearing females (70% vs. 92%), and increased mortality
because of a higher incidence of disease and cannibalism, compared with controls in quiet (88 dB re 1
µPa) tanks (Lagardere 1982). Lagardere (1982) took these as indicators of stress. Regnault & Lagardere
(1983), using the same species, also found increased metabolism, as indicated by increased oxygen
consumption and ammonia excretion, in loud tanks (105 dB re 1 µPa). These increases in metabolic
rate appeared within hours, without evidence of habituation over the 5 -day experiment (Regnault &
Lagardere 1983). Sierra -Flores et al. (2015) played back a linear sweep (100-1000 Hz) to cod in tanks at
levels typical of land-based aquaculture facilities. They discovered a mild, transient elevation in cortisol
levels, with higher intensity noise inducing higher levels of the stress hormone, but returning to baseline
levels in under an hour. However, when broodstock were exposed to noise in a 9 -week-long experiment,
higher cortisol content in the resulting eggs significantly suppressed the fertilization rate. The addition
of noise reduced fertilization rates by 40%, which decreased viable egg productivity by over 50%. This
translates to a loss of about 300,000 weaned juvenile cod in a hatchery situation (Sierra -Flores et a/. 2015).
The long-term sound stressor on the broodstock could have elevated cortisol levels in the females and
subsequently transferred the cortisol to the eggs, or produced lower sperm quality in the males, either or
both causing the reduction in fertilization success observed. Sierra -Flores eta/. (2015) thus found noise to
negatively impact cod spawning performance.
Spiga et al. (2016) used a semi -open field experiment to examine the effect of impact pile driving on
clearance rates in blue mussels. Clearance rate, the rate at which filter -feeders sift out suspended
particles from the water, is a reliable indicator of feeding activity in mussels. Increased clearance rates
may be a sign of mussels trying to cope with stress and the attendant higher metabolic demand this
requires (Spiga etal. 2016). Mussels had significantly higher clearance rates during pile driving (SEL,
158.47 dB re 1 pPa2•s; 45.58 dB re (1 nm/s)2•s), meaning they were perhaps physiologically changing from
a maintenance state to active metabolism due to noise stress (Spiga et al. 2016). The effect of pile driving
noise on the oxygen uptake, a secondary stress response, of black seabream and European plaice was
also investigated (Bruintjes eta/. 2017). Fish were exposed to 30 mins. of pile driving at 184.41 dB re 1
NPa2 SEL,,,m compared with 30 mins. of ambient conditions (159.33 dB re 1 NPa2 SEL.m). Seabream, but
not plaice, increased their oxygen uptake, implying higher stress levels (Bruintjes et a/. 2017).
Using a mechanistic, integrative approach as suggested by Kight & Swaddle (2011), Wale et a/. (2016)
demonstrated that up to 6 hours of ship noise playbacks affected the blue mussel. There were
significantly higher breaks in the DNA of cells of noise -exposed mussels. Algal clearance rates were also
lower and oxygen -consumption rates higher, indicating stress (Wale et a/. 2016). This is the first study to
show noise affecting DNA integrity in a marine animal, as well as to use oxidative stress as an indicator of
noise impacts. These impacts can cause reduced growth, reproduction, and immune response. The lower
algal clearance rates imply that the mussels could not perform an important ecological service in terms of
water filtration (Wale et a/. 2016). In contrast to Spiga et al. (2016), see above, where clearance rates in the
same species increased with pile -driving noise, ship noise caused the opposite reaction.
An extensive field study by Day etal. (2017) on scallops off Tasmania used either a 45 or 150 cu. in. airgun,
simulating the passage of large air gun array operating in 30-100 m water depth passing within 114-875
m (depending on the number of passes, ranging from one to four) of the test animals. There was also a
high amplitude "shaking"of the seabed lasting for about 70 ms, with an acceleration maximum of 68 ms -2,
but over short ranges; 3-20 ms -2 for the single air gun within 100 m range. The cumulative number of
mortalities and the probability of mortality were very significantly higher the more airgun passes the
scallops experienced, after a maximum of 120 days post -exposure studied (Day etal. 2017). Mortalities
were up to 20% in scallops subjected to four passes of the airgun, compared with a 4-5% mortality rate in
the control scallops. Seismic noise substantially disrupted behavioral patterns and reflex responses, and
the altered reflex responses persisted to at least 120 days after exposure (Day et a/. 2017). Such abnormal
reflexes may indicate damage to mechanosensory organs, which could severely compromise scallops,
with ecological ramifications (Day etal. 2017). Scallops were also immunocompromised, a major cause of
mortality in bivalves, over chronic (months) time scales. Exposure to air guns chronically disrupted their
The Impact of Ocean Noise Pollution on Fish and Invertebrates Submitted Into the
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physiology and biochemistry, causing imbalances in their electrolytes which can affect a range of cellular
functions (Day etaL 2017). Overall, the seismic surveys impacted scallops both behaviorally and
physiologically, less able to cope with additional stressors such as dredging, warm water, or predation
stress. The impacts were likely due to large vibrations and particle acceleration in the seabed from the
airgun signal (Day etaL 2017). Bivalves such as scallops improve water quality through biofiltration,
increasing the light available for underwater plants, and decrease eutrophication, while helping to feed
other benthic organisms through deposition of organic matter from the water column. As such, impacts
on their welfare can compromise ecosystem services.
Using similar methods to the above, with estimated mean exposures equivalent to the passage of a large
commercial air gun array (2000-4000 cu. in.) within a 500 m range, field experiments were conducted
on southern rock lobsters (Fitzgibbon etaL 2017). Seismic airgun noise consistently decreased total
hemocyte count (THC) 23-60% in a prolonged way for up to 120 days post -exposure, suggesting a
chronic reduction of immune competency. In contrast, after 365 days post -exposure, THC levels more
than doubled which could signify an immune response to infection (Fitzgibbon etaL 2017). There were
also signs of chronic impairment of nutritional condition 120 days post -exposure. Survival was not
affected perhaps because lobsters had access to plentiful and nutritional food sources in the experiment,
and experiments were conducted in favorable environmental conditions, but, in the wild, an impairment
in immunological capacity and nutritional condition could have much greater consequences to their
survival and reproduction (Fitzgibbon etaL 2017).
Exposure of European spiny lobsters to boat noise in tanks led to significantly increased locomotor
activities and biochemical indicators of stress (Filiciotto etaL 2014). Filiciotto etaL (2014) found twice the
levels of protein in the hemolymph in individuals subjected to noise vs. controls. Total hemocyte counts
were reduced, indicating the possibility of immune depletion and an increased risk of infection. Lobsters
also abandoned their group formation, a common reaction to imminent threat, suggesting that noise
represents a danger and source of stress (Filiciotto etal. 2014). Filiciotto etal. (2016) also played back boat
noise in tanks to the common prawn, showing significant changes in locomotor patterns and more time
spent outside their shelter, where sound pressure levels were lower, and more time resting. Changes in
total protein concentrations in the hemolymph and brain, and DNA fragmentation were all indications of
noise stress (Filiciotto et al. 2016).
Important concepts for interpreting noise impact studies
Aguilar de Soto (2016) laid out some key concepts to keep in mind when using results from impact
studies to design effective noise mitigation:
1) Animals may not be able to escape. It should not be automatically assumed that fish will leave a
noisy area and thus avoid harmful exposures. As mentioned above, some species are territorial
and are guarding their nest. Others cannot move quickly enough to escape the noise. In
addition, a typical "fright" response is to freeze in place (Popper 2003), something that has been
observed in fish experiencing noise. Animals may respond to noise as to a predator by becoming
immobile. This may be to avoid giving away their position through hydrodynamic cues. They
also may not be able to escape because they are too disoriented from the noise effects on their
sensory systems (Aguilar de Soto 2016).
2) Conclusions must not go beyond what the study was designed for and what the results show. If
fisheries'catch rates increase after noise exposure, individuals could still have suffered acoustic
damage or have been behaviorally impacted by becoming immobile, and thus easier caught.
Therefore, noise impacts on catch rates don't allow for conclusions about noise impacts on
individuals or populations (Aguilar de Soto 2016). Similarly, if no acoustic damage is detected in
one part of the body, one cannot conclude there is no injury anywhere else in the body (Aguilar
de Soto 2016). For instance, though the rest of noise -exposed bodies of cephalopods (squid,
octopus, and cuttlefish) appeared healthy and normal, Andre etaL (2011) and Sole et aL (2013b)
nevertheless found massive acoustic injuries in their statocysts, so severe as to be life-threatening.
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The imp,�rt of n(ein Nn se 'ollution on Fish and invertebrates
3) Survival in the laboratory, where animals are sheltered from predation, fed, and in clean, filtered
water is not the same as survival in the wild (Aguilar de Soto 2016). Even temporarily injured
animals (e.g. through temporary hearing damage TTS), will suffer a greater predation risk and
compromised feeding and breeding in the wild, reducing their survival rate. Disoriented or weak
animals make for easy prey, compromised feeding abilities restrict the energy they need for
recovery, and they may be more susceptible to disease and infection from noise -induced stress,
depressing their immune system (Aguilar de Soto & Kight 2016).
Also, habituation should be treated with caution, as it can'masquerade'as hearing loss. Unless there are
other sounds, e.g. of similar frequency and intensity, that still produce reactions, it cannot be assumed
that an animal has habituated and not gone deaf.
In considering the implications on the population of some noise effects, it is important to note that if
more experienced, and therefore usually productive, males leave noisy territories, the productivity of the
habitat has suffered and not just because there are simply fewer males (Slabbekoorn et al. 2010). This is
especially relevant for fish and invertebrates, as many species are territorial and older, larger individuals
often produce more offspring. Moreover, the populations in noisy areas may not just be affected by fewer
or lower -quality individuals, but may also suffer lower reproductive efficiency (Slabbekoorn et al. 2010).
In other words, "...the mere presence of fish in noisy waters does not necessarily mean that they are part
of a reproductively active population:' Other signs of population health (reproductive rate, survival rate,
growth rate) need to be measured.
Behavior
The octopus, cuttlefish, and two species of squid which exhibited such massive damage to their
statocysts, did not show a dramatic reaction during the sound exposure (Sole etaL 2013b). Some
individuals startled mildly, with some firing their ink sacs at the onset of the sound, but then stayed at the
bottom of the tank, motionless, during the remaining 2 hours of playback. After the sound stopped, the
animals remained motionless in the middle of the water column or near the surface, breathing regularly,
but did not eat, mate or lay eggs until they were sacrificed 96 hours later (Sold etaL 2013b). Samson et
al. (2014) played back pure -tone pips (85-188 dB re 1 pPa,m, ; 0-17.1 ms -Z) to cuttlefish and found that the
highest sound levels produced the greatest intensity responses, such as inking and jetting. Behavioral
responses, such as body pattern changes and fin movements, occurred down to the lowest sound levels
used (85 d6; 10-1 ms -z), however (Samson etaL 2014). Off Western Australia, one small airgun (20 cu. in.)
was towed toward and away (at 5-800 m distance) from caged southern reef squid, trevally, and pink
snapper (Fewtrell & McCauley 2012). Squid responded to received noise levels (168-173 dB re 1 µPa
mean peak) with alarm responses, ejecting ink, aggregating in parts of the cage furthest from the airgun,
showing aggression, and changing color. At the highest noise levels, squid displayed jetting and flash
expansion of the group, and then became stationary near the surface, where noise levels were 12 dB
lower (Fewtrell & McCauley 2012). The two fish species showed fast, burst swimming, in tighter groups,
near the bottom of the cage even though noise levels were higher here. For both fish and squid, as noise
levels increased, the number of alarm responses increased exponentially (Fewtrell & McCauley 2012).
Pearson etaL (1992) conducted a field experiment using a 100 cu. in. single airgun on 4 species of captive
rockfish. They determined that 180 dB dB re 1 µPa was the general threshold for alarm responses, but
that subtle behavioral changes could occur for exposures as low as 161 dB re 1 µPa. Larvae of the brown
bryozoan, an invertebrate, decreased swimming activity when exposed to boat noise vs. recordings
from a natural reef, showing they could distinguish between these sounds (Stocks etaL 2012). Peng
et al. (2016) determined that sound playbacks induced an avoidance response in razor clams, causing
more active digging in the laboratory. Digging depth increased with sound intensity. Changes in
metabolic activity were found as the individual retreated deeper into the mud. In addition to variations in
metabolism, altered expressions of metabolic genes were discovered in response to noise exposure, most
likely due to particle motion (Peng etaL 2016).
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Wardle etaL (2001) exposed reef fish and invertebrates to 3 airguns (total volume 460 cu. in.) with
received peak levels of 195-218 dB re 1 µPa. Two tagged pollack always showed involuntary reactions
(C -starts, a flexion of the body in a C -like shape followed by a sudden jerk), but neither fish nor
invertebrate species moved away from the reef. Wardle etaL (2001) suggest that this was because the
reef is their familiar home territory and because the airguns were not approaching, with attendant
changes in intensity, giving animals directions in which they could escape. Also, fish populations
associated with underwater structures are more apt to be stationary and are less likely to disperse in the
presence of airgun noise than fish on featureless banks (Wardle etaL 2001).
Holmes etaL (2017) played back boat noise from a 30 hp 2 -stroke engine travelling 30-80 m away (70-110
dB re 1 pPa2/Hz) tojuvenile Ambon damselfish in the field. They found there was an immediate decrease
in boldness and distance moved due to the noise, but that behavior returned to a pre -exposure manner
after 20 mins. of continuous boat noise. However, since these were newly -settled juvenile fish, their
hearing sensitivity will improve markedly with development (Kenyon 1996). Also, these noise levels were
quite low, unlikely to cause even temporary hearing damage. Even a transient decrease in boldness can
cause a greater susceptibility to predators (predation pressure is extreme, with around 60% mortality
rates at this stage), and fish that are bolder immediately after settlement experience higher survival rates
(McCormick & Meekan 2010).
The importance of contex
Kastelein et al. (2008) exposed 8 captive marine fish species to tones to determine behavioral startle
response thresholds. They discovered that the reaction thresholds did not run parallel to the hearing
curves, showing that hearing sensitivity is different from behavioral reactivity to sound. Moreover, there
is much variability in how various fish species react to sound, making generalizations between species
difficult. Responses likely depend on contextual variables such as location, temperature, physiological
state, age, body size, and school size (Kastelein etaL 2008). Underlining the importance of context,
Bruintjes & Radford (2013) observed that responses of the daffodil cichlid to the noise of a passing boat
(127 dBrm, re 1 µPa) depended on sex, on whether the fish had eggs in their nest or not, and whether
fish were dominant or subordinate. Compared to ambient noise playbacks, boat noise reduced nest
digging which is vital to maintaining hiding and breeding shelters, decreased defense against predators
of eggs and fry, and increased the amount of aggression received and amount of submission displayed
by subordinates (Bruintjes & Radford 2013). Both aggression and submission are metabolically costly.
In this species, anti -predator defense is key to the survival of the young and thus to the fishes' lifetime
reproductive success, so the addition of noise would be expected to have population consequences
(Bruintjes & Radford 2013).
Purser et aL (2016) show that noise effects can be dependent on the individual's body condition.
Only juvenile European eels in poor shape breathed faster and startled less to a looming predator
stimulus under the addition of ship noise, while those in good condition did not respond differently
to playbacks of ambient coastal noise (control) vs. coastal noise with passing ships. In fact, eels in the
poorest condition displayed about double the change in respiration rate (a secondary indictor of stress)
compared to those in the best condition (Purser et al. 2016). A decrease in the startle reaction makes eels
more vulnerable to predation. These variations in reaction to noise within the population have critical
implications for population dynamics and the introduction of management and mitigation measures
(Purser et al. 2016).
Reproduction
The most serious impacts, which have population consequences, are on survival and reproduction
(fitness). Repeated motorboat noise playbacks in the field to spiny chromis fish impaired parental
behavior and offspring survival (Nedelec etaL 2017). Heightened aggression and defensive behavior was
exhibited by brood -guarding males under the boat noise conditions vs. ambient -sound playback, but
the behavior was inappropriate (e.g. chasing non -predatory fish), ineffective, and inefficient, resulting
in males spending 25% less time feeding (Nedelec et al. 2017). Male -offspring interactions (an indirect
form of provisioning) were also reduced with noise. All changes in behavior showed no sign of tolerance,
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habituation, or sensitization to motorboat noise over the 12 -day study. Most importantly, while offspring
survived at all 19 nests exposed to the ambient -sound playback, under the motorboat -noise playback, six
of the 19 nests (32%) suffered complete brood mortality, indicating a fitness consequence. Stress and/
or distraction under noise conditions could have caused the male decision-making errors leading to less
efficient and effective parental care and defense (Nedelec etaL 2017).
de Jong etaL (2018) tested the effect of low -frequency continuous noise on courtship behavior in two
marine fish species, the two -spotted goby and painted goby, using aquarium experiments. With the
addition of noise, males of both species exhibited less acoustic courtship. Additionally, painted gobies
showed less visual courtship. Female painted gobies were less likely to spawn in the noise treatment
(de Jong etaL 2018). Neither species appeared to compensate for the noise by increasing their visual
signalling. Noise could have suppressed spawning because females may need to hear male song
characteristics to assess male quality and identify the correct species. Interestingly, the increased
noise levels of 20-30 d61 comparable to shipping noise and typical of UK coastal waters, did not affect
overall activity or nest building in the painted goby, so field populations behaving apparently normally
could still have less reproductive success (de Jong etaL 2018). Noise could also change a population's
genetic make-up if females prefer different traits in males in the presence of noise. More importantly, a
suppression of reproduction is likely to impact the population.
Using field experiments and playbacks of vessel noise, Krahforst (2017) observed that toadfish males
decreased their call rates and called louder in the presence of noise. Also, oyster toadfish chose nesting
sites in areas with little or no inboard motorboat activity. Finally, male oyster toadfish at noisy sites either
had no egg clutches in their shelters or the number of embryos per clutch was significantly lower than
in the quiet areas. Underwater noise compromised reproduction in toadfish (Krahforst 2017). Picciulin
etaL (2010) conducted a field experiment, playing boat noise back to free-swimming fish in a marine
protected area. Fish were videotaped 5 mins. before and 5 mins. during the noise playback. No short-
term aversion, escape, or other reactions to noise were observed, which could lead to a conclusion of
no impact. However, a time -budget analysis revealed that fish in the presence of noise significantly
increased the time spent inside their shelters and significantly decreased the time caring for their nests
(Picciulin etaL 2010). These results underline the importance of considering overall fish behavior in noise
impact studies, rather than just the short-term responses to noise. Fish may not have escaped the noise
because such behavior would have resulted in greater predation to their eggs and more aggression from
other fish (Picciulin etaL 2010). Sebastianutto et al. (2011) discovered that in the presence of boat noise,
resident fish were more submissive and won less encounters. Noise thus affected an ecologically crucial
behavior—the ability of a resident to maintain its territory (Sebastianutto etaL 2011).
Antipredator behavior
In another field experiment in a marine protected area, La Manna etaL (2016) found that boat noise
(average levels 134-146 dB re 1 µPa; maximum levels 145-154 dB re 1 NPa) increased the duration of
fish flight reactions together with more individual fish performing them, increased the amount of
hiding, but did not change levels of fish activity nor calling (La Manna etal. 2016). Flights and hiding
behavior are usually related to predation, so these fish seemed to react to boat noise as if it were a
predator attack. Behavioral recovery was quick but could still lead to physiological and metabolic
consequences, along with population impacts (La Manna etaL 2016). Simpson etal. (2016) determined
that damselfish increased their metabolic rate and responded less often and slower to simulated
predatory attacks in the presence of boat noise. They were captured more easily by their natural
predator, the dusty dottyback, which consumed twice as many prey when motorboats were passing.
In this scenario, boat noise clearly favored the predator (Simpson et al. 2016), which could change the
community structure of the habitat. Simpson etal. (2015) determined that juvenile eels experienced
higher breathing and metabolic rates, indicators of stress, in the presence of noise from ship passages
vs. ambient noise without ships. They also performed worse on spatial tasks. Eels were 50% less likely
and 25% slower to startle to a simulated'ambush predator'and were caught more than twice as quickly
by a simulated'pursuit predator,'during playbacks of noise (Simpson etaL 2015). Compromising life -
or -death responses could affect individual and population welfare. However, subsequent research
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(Bruintjes etaL 2016) showed that juvenile eels quickly recovered their startle responses and their
delayed startling, though their breathing rate didn't recover completely in the 2 mins. after the noise
stopped. Seabass also exhibited a higher breathing rate with noise but completely recovered in the 2
mins. after noise ceased (Bruintjes etaL 2016). Still, repeated startling could compromise eel welfare in
the long-term.
Normally, when juvenile Ward's damselfish are exposed to odors from hurt individuals of the same
species, they dramatically decrease the distance they travel, the maximum distance they venture from
their shelter, and their boldness. McCormick et al. (2018), however, found that in the presence of real
two-stroke boat noise in the field, the fish did not respond to these alarm odors appropriately, but rather
increased their activity and space use and became bolder. Fish appeared to misinterpret the information,
becoming confused by the boat noise, and responded by feeding instead. This maladaptive response
could have mortal consequences (McCormick et aL 2018). Fewer fish also responded appropriately to
a looming threat while exposed to a two-stroke engine, reacting almost 40% more slowly. Noise thus
appears to impact the wayjuvenile fish assess risk, likely affecting their survival and fitness. Interestingly,
boats with two-stroke engines dramatically affected the fish while similar -sized (30 hp), quieter four-
stroke engines (10 dB lower in pressure and particle motion) had a much more negligible impact,
though still a detectable one. Four-stroke outboards tend towards greater fuel efficiency but also cost
substantially more. Two-stroke engines are "rattly" in contrast to four-stroke ones which "hum;'as more
cylinders are firing with less power per piston stroke (McCormick etaL 2018).
Wale et aL (2013b) used 7.5 mins. of ship noise (148-155 dBRMs re 1 NPa) compared with ambient noise
(103-108 dBRMs re 1 NPa) on shore crabs to test responses. They found that in the presence of ship noise,
crabs'feeding was interrupted, they were slower to return to shelter after a simulated predator attack,
and they righted themselves faster, which also might expose them to increased risks of predation, since
by remaining entirely motionless, they could avoid detection by the predator (Wale et aL 2013b). Thus, all
of these responses to noise could make starvation and predation more likely (Wale etaL 2013b). Many of
the above studies show that even if responses to noise are subtle, they could affect an animal's survival.
Moreover, they underline the importance of examining significant behavior patterns, rather than simply
describing changes in movements or simple startle reactions.
Foraging and feeding
Magnhagen etaL (2017) used an actual motorboat in the field to examine the effect of noise (SPL 150-152
dB re 1 NParm,: particle acceleration 72 and 75 dB re 1 pm s -' ,ms) on foraging behavior in roach and the
Eurasian perch. Perch made fewer feeding attempts during noise exposure compared to controls. Over
the five days of the experiment, however, they gradually increased feeding and time spent in the open
area (not covered in vegetation), both with and without noise, indicating habituation (Magnhagen etoL
2017). Roach, which hear better, were more disturbed by the noise than perch and did not habituate.
With noise, there were fewer feeding attempts, greater delays in entering the open area, and longer
time spent in the vegetation vs. controls (Magnhagen et aL 2017). Damselfish also fed less frequently
with greater boat traffic volume in a Marine Protected Area (Bracciali et al. 2012). Within the B -zone,
which allowed recreational use, the daily feeding pattern of the damselfish was highly modified during
times of greatest boat traffic. Instead of foraging during the day, when there was better light to detect
their zooplankton prey as was the pattern in the no -take A -zone, B -zone fish foraged mostly at sunset
(Bracciali et aL 2012). Boat passages induced escape responses, whereas moored boats did not. At peak
traffic times, fish had to escape 30 times per hour, not only interrupting their feeding, with the attendant
energetic costs, but also requiring energy to escape. In one of the two areas studied, the fish in worse
body condition were found in the busiest zone. Fish in the no -take A -zone escaped most of the boat
impacts on their foraging activity, except on busy days when they were only slightly buffered against the
heavy traffic disturbance from the B -zone (Bracciali et aL 2012). While noise and the approach of boats
were not separated out here, it is likely noise played a major part in the disturbance.
McLaughlin & Kunc (2015) discovered that playbacks of ferry noise (mean SPL 170 dB re 1 pParA to
convict cichlids caused an increase in sheltering at the expense of foraging, compared with controls.
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The Impact of Ocean Noise Pollution on Fish and Invertebrates
American lobster increased their feeding several weeks after being exposed to airguns in the laboratory
(Payne etaL 2008).
In a field study, Payne etaL (2014) found that boating activity can have a significant impact on the
foraging success of wild mulloway fish. Increasing boating activity, based on underwater noise trends
over the week, caused fish to reduce their activity and move to deeper water. There was a 61% decrease
in stomach content on weekends, when boating activity is greatest, compared with weekdays, along with
an altered diet composition (Payne etaL 2014). In addition to a drop in foraging success, mullowayfish
could perceive boats and boat noise as threats, causing stress and suppressing appetites. Underwater
noise levels likely played a large role in reducing foraging success as the boat noise produced is within
the hearing range of most fish species. Such a dramatic reduction in feeding intensity could incur
significant fitness costs (Payne et aL 2014).
Attention
Purser & Radford (2011) played back white noise to sticklebacks at levels that were detectable by the fish
but not enough to induce hearing damage. They found that fish in the presence of noise did not alter the
amount of food they ate, but made more food -handling errors and were less able to distinguish between
food and non-food items, suggesting a shift in attention (Purser & Radford 2011). Thus, fish decreased
their foraging efficiency, with more attacks on prey needed to eat the same number of prey items. Purser
& Radford (2011) argue that even very brief noise exposure can cause substantial impacts on function if
attention is diverted by noise. Similarly, Chan etaL (2010) found that hermit crabs assessed predator risk
differently in the presence of boat noise. In noisy conditions, a simulated predator was able to approach
the crabs more closely before they hid. Chan etaL (2010) concluded that noise can distract prey and
make them more vulnerable to predation. Walsh etaL (2017) exposed a different species of hermit
crab to noise during shell selection, which is a critical process as individuals in poor shells suffer lower
reproductive success and higher mortality. Experimental noise exposure in the laboratory shortened
the crabs'shell assessment process. Crabs approached the shell faster, spent less time investigating it,
and entered it faster (Walsh etaL 2017). The known cues (chemical, visual, tactile) used in shell selection
are not acoustic, yet still noise affected a process involving fitness --an example of a cross -modal impact.
Noise likely altered the crabs'attention, as individuals can only process a finite amount of information at
the same time (Walsh et aL 2017).
Three-spined stickleback and the European minnow ate fewer live prey and startled more during
playbacks of ship noise (Voellmy et aL 2014). However, with noise, minnows shifted from foraging
behavior to greater inactivity and more social behaviour, a more classic stress- or fear -based response,
while sticklebacks maintained foraging effort but made more mistakes, implying more of an impact on
cognition. Regardless, since both species reacted to noise by feeding less, there are potential population
and ecological consequences (Voellmy etaL 2014).
Sabet et aL (2015) investigated the impacts of broadband (intermittent and continuous) noise playbacks
on zebrafish preying on water fleas in the laboratory. Water flea swimming speed and depth was
unaffected by noise, but zebrafish swam faster and startled more, particularly to the intermittent noise
playbacks. These intermittent sounds caused a delay in the response to the introduction of the prey,
and all noise playbacks produced an increase in food handling errors (Sabet et aL 2015). With noise, fish
missed the prey on the first strike and had trouble handling the prey so they could swallow it. Sabet et
aL (2015) attribute this drop in performance to attention shifts, with intermittent sound causing stronger
effects than continuous sound. These consequences of noise pollution on predator -prey interactions
show impacts extend beyond single -species effects, affecting relative species abundances of both
predator and prey and likely representing changes at the community level. Noise can thus compromise
food web dynamics and stability in aquatic environments (Sabet etaL 2015).
Schooling behavior
Net -penned herring showed avoidance responses when played back sounds of large vessels approaching
at constant speed and of smaller boats but only when on accelerated approach (Schwarz & Greer 1984).
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Electronic sounds with a sudden increase in loudness produced some startle responses, but especially
alarm. Herring did not react to natural sounds nor sonars or echosounders (Schwarz & Greer 1984).
Naval sonar did not appear to affect schools of Atlantic herring either (Sivle et al. 2012). Summer
migrating fish schools neither dived nor changed their aggregation in response to the 1-2 kHz low -
frequency active sonar (received levels: 176 dB,,,,, re 1 µPa; 181 dB re 1 µPa2s) and 6-7 kHz mid -frequency
active sonar (received levels: 157 dB,m, re 1 µPa; 162 dB re 1 µPa2s) transmissions, though herring
showed a tendency to be more sensitive to stimuli, such engine sounds, in the winter (Doksaeter
et al. 2012). Nevertheless, Doksaeter et al. (2012) did not find low -frequency sonar signals elicited
a reaction in captive herring over three seasons of a year. Instead fish showed a significant diving
reaction in the presence of a two-stroke engine, despite those noise levels being much lower than
the sonar's. Doksaeter et al. (2012) explained this result by the engine noise being lower in frequency,
sudden -onset, and closer, so that particle motion might have predominated. Acoustically -tagged cod
reacted at very low levels (82-92 dB re 1 µPa/Hz) to an approaching trawler, perhaps because of the
low background noise (65 dB re 1 µPa/Hz) in the area (Eng5s et al. 1998). Blue rockfish milled tightly in
the presence of airgun shots, black rockfish collapsed to the bottom, and vermilion and olive rockfish
became motionless (Pearson et a1. 1992). Sara et al. (2007) conducted a field study using a fixed tuna
trap set near shipping routes. They observed tuna exposed to sounds from hydrofoil passenger ferries,
small boats, and large car ferries. When a car ferry approached, tuna changed swimming direction
and moved either towards the surface or bottom. The school also lost its aggregated structure and
became uncoordinated. Hydrofoils caused a similar reaction, but for shorter periods (Sari et al. 2007).
Aggressive behavior was more prominent with outboard motorboat noise. Coordinated schooling
improves tuna homing accuracy during their spawning migration, so interference in schooling can affect
the accuracy of their migration to spawning and feeding grounds (Sara et al. 2007).
Mueller-Blenkle etoL (2010) played back pile -driving noise to cod and sole held in large net pens. There
was less aggregation and more movement during noise in both species at relatively low received sound
pressure levels (sole: 144-156 dBpk re 1 µPa; cod: 140-161 dBp,.ak re 1 µPa; particle motion between
6.51 x10-3 and 8.62x10' m/s2 peak). Sole swam significantly faster in the presence of pile -driving noise.
Cod "froze"at the beginning and end of playbacks (Mueller-Blenkle etoL 2010). Both species appeared
to move away from the sound source. There was much individual variability in behavioral reactions, and
there were signs of habituation, where responses waned after multiple exposures (Mueller-Blenkle et al.
2010). Wild, free-swimming schools of sprat and mackerel were exposed to sound simulating a pile driver,
at different sound levels (Hawkins et al. 2014). The incidence of behavioral responses increased with
increasing sound level. Sprat schools were more likely to disperse and mackerel schools, to change depth.
Fish schools responded, on average, to estimated levels of 162.3 and 163.3 dB�P re 1 µPa and single
strike SELs of 135.0 and 142.0 dB re 1 pPa2 s, for sprat and mackerel, respectively, but some sprat schools
responded at levels as low as 140 dBp-p re 1 µPa, while mackerel reacted at 137 dB,,p re 1 µPa (Hawkins et
al. 2014). Sprat schools dispersing due to noise would have a metabolic cost and potentially cause stress
and reduced foraging efficiency, which could affect reproductive success. It could also expose fish to
higher levels of predation (Hawkins etaL 2014).
Neo etaL (2014) tested sounds with different temporal structure on sea bass. They observed that while
all the different playbacks caused similar behavioral changes (startle responses, faster swimming speed,
mere group cohesion and bottom diving), intermittent vs. continuous exposure produced slower
behavioral recovery. They thus concluded that intermittent sounds, like pile driving, could have a
stronger behavioral impact than continuous sounds like drilling, despite the higher total accumulated
energy from continuous noise (Neo et al. 2014). In a follow-up study, Neo etoL (2016) tested the temporal
structure of sound and'ramp up' procedures on sea bass in an outdoor floating pen. The noise treatments
consisted of: 1) continuous sound; 2) intermittent sound with a regular repetition interval; 3) irregular
repetition intervals; and 4) a regular repetition interval with amplitude'ramp-up'(gradually increasing
the level of sound). While fish swam faster, deeper, and away from the sound source, there was no
significant difference in their response and recovery related to the temporal features of the playback
(Neo etaL 2016). Fish mostly returned to their previous behavior within 30 mins. 'Ramp-ups'produced an
immediate diving response, as with the other noise treatments, but fish did not swim away from the noise
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The mnr ct of Or Pan Noir -1ollution on Fish and Invertebrates
source, as was expected. Some fish even initially approached the sound source. Thus,'ramp ups' may
actually reduce horizontal avoidance instead of deterring marine animals as intended (Neo et at 2016).
Pile -driving playbacks under controlled laboratory conditions also affected the structure and dynamics of
juvenile seabass schools in shallow water (Herbert -Read et at 2017). Ambient sound was also broadcast
to the schools and affected the coordination and spatial and directional organization, but the effect was
larger for pile -driving exposures, with a medium to strong effect size (Herbert -Read et at 2017). With
pile driving compared to ambient sound, groups became less cohesive, less correlated in speed and
directional changes, and overall were unable to coordinate their movements with one another. Thus,
social interactions were affected by noise which could compromise the benefits of group living, such as
a reduced predation risk and transmission of social information (Herbert -Read et at 2017). The response
of the group toward pile -driving noise, decreased cohesiveness, is the opposite of that toward predation.
The reaction may be mediated by noise interference with the lateral line sensory system, in effect an
example of masking (obscuring of signals of interest), or alternatively, a disruption of the ability of fish to
process sensory information because of stress or distraction (Herbert -Read et oL 2017).
Ecosystem consequences
Solan et aL (2016) showed that both impulsive and continuous broadband noise repressed burying
and bioirrigation behavior (or water circulation within lobster burrows), and reduced movement in the
Norway lobster. The Manila clam showed a stress response whereby individuals relocated less, stayed on
top of the seabed, and closed their valves. Such responses meant the clams couldn't mix the upper layers
of sediment and couldn't feed. As a result, ecosystem properties were affected (Solan etaL 2016). Some
individual clams also accumulated lactate from keeping their valves closed for an extended period of
time, a known avoidance behavior that requires the animal to breathe anaerobically. If sound exposure,
which was 7 days, had continued for much longer, these lactate levels would have been harmful (Solan
et at 2016). Noise thus changed the fluid and particle transport that invertebrates provide, which are
key to nutrient cycling on the seabed. The authors note that"... exposing coastal environments to
anthropogenic sound fields is likely to have much wider ecosystem consequences than are presently
acknowledged:' (Solan et at 2016). This study shows that responses to noise can be subtle and may take
long periods of time to become detectable at the population or ecosystem level.
Seabed vibration
Some human activities in the ocean involve direct contact with the seabed, such as construction and
pile driving, which produce radiating particle motion waves that could impact bottom -dwelling animals.
Roberts et at (2015) found clear behavioral changes to the vibration in mussels, mainly valve closure. The
thresholds of mussel response (acceleration, rms: 0.06 to 0.55 ms -2) were within the range of vibrations
measured near pile driving and blasting (Roberts et at 2015). Thus, vibration is likely to impact overall
mussel health and reproduction in both individuals and whole mussel beds, because of valve closure, which
is an energetically and otherwise costly behavior, disrupting breathing, heart rate and excretion (Roberts
et aL 2015). Even a 3- hr valve closure can halve oxygen concentrations and double carbon dioxide levels.
Growth and body condition are likely to suffer with longer valve closures and may have ecosystem and
commercial consequences (Roberts et at 2015). Seabed vibration needs to be considered along with water-
borne particle motion and acoustic pressure when looking at the effects of noise on bottom -dwellers.
Masking
Masking is the obscuring, obliterating, or"drowning out"of sounds of interest to animals. Detection,
discrimination, and recognition are all important in meaningfully hearing sounds. It is usually not
enough to detect particular calls or sounds (presence vs. absence), they must also be discriminated
(sounds distinguished from one another) and recognized (understood with the proper meaning being
communicated).
Codarin et at (2009) investigated boat noise in a marine protected area and its effect on local fish species.
Playbacks used the noise of a cabin cruiser passing at 6 kts 10 m away (132 dB re 1 µPa) which raised
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ambient noise (97 dB re 1 µPa) by about 40 dB. Codarin etaL (2009) found that such noise can reduce
the detection distance of other fish sounds by 10- to more than 100 -fold, depending on the species.
The masking effect was most pronounced in the frequency range where fish communication takes
place (Codarin etaL 2009). Alves etat (2017) examined the impact of boat noise on the communication
range of the toadfish by comparing the maximum distance a fish can perceive the advertisement signal
("boatwhistle") of another toadfish, before and after adding boat noise. Communication range before
noise was 6-13 m, depending on signal characteristics, but with noise, shrunk to about 3-8 m, respectively
(Alves etaL 2017). Boat noise can thus severely impede communication in this fish species. Since the
boatwhistle is used both to attract females and repel possible intruders, interference with this signal can
limit reproduction (e.g. finding a mate) and survival (Alves etaL 2017). Vasconcelos etal. (2007) had also
discovered that noise from ferry boats greatly masked toadfish calls, especially because this noise was in the
most sensitive hearing range of this species. If the function of an acoustic signal is to assess an opponent's
fighting ability, masking such signals could lead to misleading information and escalated contests
(Vasconcelos etaL 2007). Similarly, masking the boatwhistle signal could influence the spacing between
males and impede sexual selection (which traits females use to select males). Suboptimal pairing could, in
turn, could negatively affect individual reproductive success (Slabbekoorn etaL 2010) and result in poorly
adapted offspring, with less desirable traits for survival and reproduction, affecting whole populations.
Noise from wind and tidal turbines discouraged larval settlement and delayed metamorphosis in two
crab species (Pine etaL 2012). Pine etaL (2012) concluded that the noise masked important natural
acoustic settlement cues. Thomsen etaL (2006) concluded that pile driving (SPL:189 dBaP re 1 µPa; SEL:
166 dB re 1 µPaz s at 400 m) will be heard by cod and herring at distances possibly up to 80 km away.
Masking may also occur at these distances in some cases (Thomsen etal. 2006). Dab and salmon are
primarily sensitive to particle motion vs. pressure, so their detection threshold cannot be established
yet. Operational noise from wind turbines will be detectable up to about 4 kms for cod and herring,
and probably up to 1 km for dab and salmon. At these distances, masking of communication between
individuals is also possible (Thomsen et al. 2006).
Some ways for animals to try and overcome masking are by making their calls louder or longer, increasing
the rate of their calls, or shifting the frequency out of the range of the predominant noise. Fish are
somewhat limited in their ability to change the frequency or loudness of their calls (Amorim 2006).
Picciulin et al. (2012) discovered that the mean pulse rate of brown meagres was higher after repeated,
though not single, boat passes. Masking was assumed, because of the high boat noise levels relative
to background noise and the fishes'calls. The increase in vocal activity could have arisen either from an
increased density of callers or from more pulses (calls) from individuals already calling (Picciulin etaL 2012),
as a form of vocal compensation for masking. Krahforst et al. (2017) conducted a field study comparing
noisy and quiet sites. They found that oyster toadfish emitted more calls in the noisy site vs. the quiet one.
Male fish appear to be using the quiet periods between vessels passing in the noisy site to call at a higher
rate. However, this would tire the sonic muscles, so cannot be sustained for long time periods. If the male
oyster toadfish cannot be heard by a mate during the passage of a vessel, and if there are many vessel
passages per day, then the males in noisy sites could reproduce less (Krahforst et al. 2017).
Catch rates, abundance, and distribution
Eng5s etaL (1996) used sonar mapping and fishing trials with trawls and longlines 7 days before, 5 days
during, and 5 days after seismic shooting to investigate whether seismic surveys (total volume: 5,000 cu.
in.) affected cod and haddock abundance or catch rates. They found seismic shooting severely affected
fish distribution, abundance, and catch rates over the entire 5,500 sq. km. study area. Trawl catches of
both fish species and longline catches of haddock dropped by 50% after shooting. Longline catches of
cod were reduced by 21 % (EngSs etaL 1996). Reductions in catch rates occurred 33 km from the seismic
shooting area but the most dramatic reductions happened within the small shooting area (103 sq. km.),
where trawl catches of both species and longline catches of haddock dropped by 70% and longline cod
catches by 45%. Abundance and catch rates didn't return to pre -survey levels during the 5 -day period
following the survey (EngSs etaL 1996).
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Lokkeborg et al. (2012) carried out a later version of the above study, also using a seismic survey (7,000
cu. in. total), with fish experiencing 140-191 dB re 1 µPa. Fishing trials started 12 days before seismic
shooting, lasted 11 weeks, and ended 25 days after shooting. Lokkeborg etal. (2012) found changes
in catch rates of all species studied, though gillnet catches for redfish and Greenland halibut increased
during seismic shooting (86% and 132% increase, respectively) whereas longline catch rates fell for
Greenland halibut and haddock (16% and 25% decrease, respectively). Fish likely responded to airguns
by descending to the bottom, which would have made them more vulnerable to bottom -set gillnets,
accounting for the higher catch rates. The closer the seismic vessel was to the longline area, the more
haddock longline catches decreased (Lokkeborg etal. 2012). Haddock and pollock length decreased
throughout the seismic survey and after, compared to the pre -exposure period, indicating larger fish were
more likely to leave the area. During seismic shooting, the stomachs of longline-caught haddock were
also emptier, even of non-mobile prey. Increasingly more gillnet-caught pollock had empty stomachs
from before to during and after shooting. Seismic surveys could have impaired feeding or the motivation
to find food in fish alarmed by the noise, accounting for the lower longline catches, which require fish to
be enticed by the baited hooks. Only pollock showed a reduction in density during and after the seismic
survey (Lokkeborg et al. 2012), with especially larger fish moving out of the seismic survey area. Because
pollock are found in shallower water than redfish and Greenland halibut, they experienced higher
sound levels, which, together with their better hearing and swimming ability, may explain why only this
species left the seismic survey area (Lokkeborg et al. 2012). Greenland halibut and redfish inhabit only
specific habitats which may be the reason why they were not displaced. Bycatches of ling increased
after shooting started, both for redfish and pollock gillnets. This may be due to fish responding to the
seismic airguns by increasing their swimming activity. Ling may have reacted more strongly and sooner
than halibut or redfish because they hear better and were in shallower depth with higher sound levels.
Lokkeborg etal. (2012)'s seismic shooting area was 1,275 sq. km. compared with Engas etal. (1996)'s 103
sq. km., thus the airgun shot rate was 19 times higher in Eng5s et al. (1996)5 study, exposing fish to louder
and more continuous noise. In Lokkeborg etal. (2012)5 study, the fish were still likely to hear airgun shots
throughout the seismic survey period regardless of how far they were from the seismic vessel.
Lokkeborg (1991) also examined the effects of a seismic survey on longline catch rates of cod. He found catch
rates dropped by 55-80% for longlines within the seismic survey area, probably because the predominant
frequencies of airguns match the most sensitive frequency band of cod (Lokkeborg & Soldal 1993). The
spatial and temporal extent of the reduced catches was over a distance of 9.5 km and over at least 24 hours
(Lokkeborg 1991). He noted that a typical seismic survey would likely have a greater impact over space and
time than the one used here, as the peak pressure of this survey was only 4-8% of a typical survey. Moreover,
the cod in this study were migrating, thus catches would not be expected to drop as much, as seismic -
exposed fish would be replaced by unexposed fish, whereas had the fish been stationary, the impact would
likely have been greater and more long-lasting (Lokkeborg 1991). Bycatches of cod in shrimp trawls dropped
by 80-85% during seismic shooting (Lokkeborg & Soldal 1993). The cod bycatch in the trawl fishery for saithe,
though, increased threefold and returned to normal right after the seismic survey ended. However, in this
case, the seismic survey was only 9 hrs. long, cut short due to poor weather (Lokkeborg & Soldal 1993).
Skalski et al. (1992) used a single 100 cu. in. airgun to expose 3 species of rockfish to peak pressures of
186 dB re 1 µPa in the field to determine the effect of seismic noise on the hook -and -line fishery. They
found an average catch -per -unit -effort decline of 52% relative to controls, translating to a 50% average
economic loss (Skalski et al. 1992). Hassel etal. (2004) showed a 2-3 week drop in landing rates of lesser
sandeel catches after a 2.5 day seismic survey. C -starts, showing the fish were scared and disturbed, also
occurred during seismic shooting but no immediately lethal effects were observed. Hirst & Rodhouse
(2000) reviewed the literature on seismic airgun impacts on fishing success. They concluded that, at that
time, the lowest airgun levels in the open ocean that produced a behavioral reaction which changed
catch rates was less than 160 dB re 1 µPa (Hirst & Rodhouse 2000).
Slotte et al. (2004) used a seismic survey (3,000 cu. in.), shooting for about 12 days, to examine fish
abundance and distribution inside the shooting area and in the surrounding waters up to 30-50 km away.
Using sonar, they found that the abundance of herring, blue whiting, and other mesopelagic (occupying
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the middle depths of the open ocean) fish was higher outside than inside the seismic shooting area,
indicating a long-term effect of the seismic survey (Slotte etal. 2004). There were also indications that
both blue whiting and mesopelagic species were found in deeper waters during shooting, suggesting
that fish were avoiding the noise vertically rather than horizontally over the short term (Slotte et at
2004). Paxton et al. (2017) analyzed fish abundance using videos of a reef near a seismic survey. The
reef probably experienced seismic noise of 181-220 dB re 1 µPa. During the seismic survey, reef fish
abundance declined by 78% in the evening when fish habitat use was highest on the previous three days
without seismic noise (Paxton et al. 2017). Thus, the pattern of heavy usage of the reefs in the evening
by the fish was disrupted. Paxton et at (2017) go beyond describing the responses of individual fish to
showing the reaction of an entire community of species to a seismic survey. If fish lose opportunities to
aggregate, their foraging, mating, and other vital functions may be impacted (Paxton et at 2017).
Andriguetto-Filho etal. (2005) found no difference in catch rates or density in a nonselective commercial
shrimp fishery of Southern white shrimp, Southern brown shrimp, and Atlantic seabob before and a day
after a small seismic survey (635 cu. in.; 196 dBp k re 1 mPa at 1 m), thus not investigating chronic impacts.
Parry & Gason (2006) examined the relationship between catches of rock lobster and 33 seismic surveys
done between 1978 and 2004 off Australia. They could find no evidence that catch rates were affected
by the surveys in the weeks or years following them (Parry & Gason 2006). However, they noted that
seismic surveys were mainly done in deep water, where the effects would be expected to be minimal. In
the one area with intensive shallow -water surveys, there were few lobsters, making the statistical analysis
insensitive. In fact, catch rates would have had to change by at least 50% in order to be detected by their
analysis (Parry & Gason 2006). Similarly, Morris etat (2018) was unable to detect any change in snow
crab catch rates due to seismic exposure off Newfoundland, Canada. Their statistical power was low, as
there was high natural spatial and temporal variation in catches. The industrial survey (4880 cu. in.) had
a horizontal zero -peak SPL of 251 dB re 1 NPa re 1 m. The exposure lasted for five days in one year, with
the closest approach of the vessel to the sound recorders being 1465 m. In the second year, the exposure
lasted 2 hrs, and the vessel passed within 100 m of the acoustic recorder (it was unclear how far the traps
were from the recorders). No increased particle motion at the seabed (i.e. ground roll) was detected
(Morris et al. 2018). This underlines the importance of authors stating the power of their statistical
analyses, for without this information, conclusions cannot be placed in proper perspective and are, more
or less, meaningless. Decision -makers should require such information as a part of all statistical analyses
regarding the impacts of noise on marine life.
Pingers (20-160 kHz; maximum source level 145 dB re 1 NPa), used to alert harbor porpoises to nets to
reduce bycatch, did not reduce herring capture success in a commercial fishery (Culik etal. 2001). A
different type of pinger (115 dB re 1 NPa, 2.7 kHz with harmonics up to 19 kHz) seemed to attract herring,
producing higher capture rates, though (Culik et al. 2001). Catch records of three trawlers built to the
same specifications showed that the noisiest boat (5-10 dB higher at frequencies >60 Hz than the other
two boats) caught significant less saithe but about the same amount of cod (EngAs & Lokkeborg 2002).
Interactions between stressors including synergistic impacts
Synergistic or multiplicative effects are those that occur when two or more stressors interact, such that
the combination effect can be more severe than the simple addition of all effects. One example is the
potential combination of ocean acidification and noise pollution. Simpson et at (2011a) found that
juvenile clown fish did not orient normally in response to reef noise when in more acidic conditions.
This could have detrimental effects on their early survival (Simpson et al. 2011 a). Day at el. (2017) found
that warm summer conditions exacerbated the effects of noise stress on lobsters from seismic airgun
exposure. Scallops that were dredged vs. collected by hand, in addition to being exposed to airgun noise,
suffered more immunosuppression (Day et at 2017).
Charifi et at (2018) studied the interaction between cargo ship noise and cadmium contamination in the
Pacific oyster, a species frequently used as a bioindicator of the state of the marine environment. Oysters
in tanks were exposed to a maximum sound pressure level of 150 dB,., re 1 µPa over a 14 day period. Tanks
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were installed on an anti -vibration bench and acceleration was measured directly. Oysters exposed to
both cadmium and ship noise accumulated 2.5 times less cadmium in their gills than controls, but their
growth rate was 2.6 times slower (Charifi et al. 2018). Noise reduced the daily activity of their valves, which
were closed more during the daytime. Gene expression in the gills changed in four genes with cadmium
contamination but without ship noise, and in seven genes with both chemical and noise pollutants. Charifi
et al. (2018) concluded that ship noise suppressed oyster activity and the volume of water flowing over
their gills. While this limited metal exposure and uptake by the gills, it also restricted food uptake, likely
explaining the slower fat metabolism and growth rate and greater oxidative stress. The slowdown in
growth constitutes "a potentially massive risk in terms of ecosystem productivity" (Charifi et al. 2018).
Reviews of noise impact literature
Carroll etaL (2017) compiled and critically reviewed a total of 70 studies which addressed the impacts of
low -frequency seismic sound (<300 Hz) on fish or invertebrates. These studies represented a total of
68 species of fish and 35 species of invertebrates. Of these, commercial species comprised 81% of fish
and 66% of invertebrates. Laboratory experiments made up 35% of all studies; caged field studies,
25%; and uncaged field studies, 40% (Carroll etaL 2017). Carroll etal. (2017) found the lack of sound
exposure standardization difficult, as well as translating laboratory results to field populations. Edmonds
et al. (2016) critically evaluated the literature and found that Norway lobster and closely related species,
including juvenile stages, were physiologically sensitive to underwater noise, especially local particle
motion. Tidau & Briffa (2016) reviewed research on crustaceans and discovered a variety of biological
and ecological impacts ranging from an increase in stress, slower antipredator behavior, changes in
feeding, and changes to social and aggressive behavior among individuals of the same species. Cox et
al. (2016) attempted to determine the impacts of human -caused noise on fish behavior and physiology
by conducting a meta-analysis (analysis of past studies). The review identified 3,174 potentially relevant
papers of which 27 were used. The analysis showed that anthropogenic noise has an adverse effect on
marine and freshwater fish behavior and physiology (Cox et al. 2016). They conclude that "...although
certain species may be more susceptible to anthropogenic noise than others, the vast majority of fish
have the potential to be negatively affected by noise pollution.' (Cox et al. 2016).
Shannon et al. (2016) conducted a systematic review of the scientific literature on the effects of
anthropogenic noise on wildlife (both terrestrial and aquatic) published between 1990 and 2013. Of
the 242 studies included in the review, 88% reported a statistical biological response to noise exposure
(Shannon etaL 2016). These included changes in vocal behavior in an attempt to overcome masking,
decreased abundance in noisy habitats, alterations in vigilance and foraging behavior, and impacts on
individual fitness and the structure of ecological communities (Shannon etaL 2016). Aquatic fishes,
invertebrates, and mammals reacted to noise across a wide range of noise levels (67-195 dB SPL re 1 NPa),
with half of the aquatic studies measuring a biological response at or below 125 dB re 1 µPa (Shannon et
al. 2016), a surprisingly low level.
Williams et al. (2015) reviewed case studies and concluded that "...non -injurious effects can still
accumulate to have population -level impacts mediated through physiological impacts and probably
other mechanisms" They believe there has been too much focus on high-level,'injurious' noise exposures
at the expense of population -level impacts (Williams etal. 2015). Peng etal. (2015)'s review on noise
impacts on marine organisms concludes that noise pollution is a threat to individuals but also"...may
affect the composition, and subsequently the health and service functions of the ecosystem" Kight &
Swaddle's (2011) review covers all animal species, not just fish and invertebrates. They conclude that
noise stress is particularly damaging to females and predict that "...if noise affects key developmental
processes, the consequences will persist over the long term.' Moreover, if animals are increasing their
vigilance and hiding as a response to noise, they may lose foraging time. Kight & Swaddle (2011) show
that environmental noise can cause DNA damage, changes in how genes are expressed, and alterations
that could affect neural, developmental, immunological and physiological functioning. In their review of
aquatic noise pollution impacts, Kunc etaL (2016) found "...comprehensive evidence that noise affects an
individual's development, physiology, and/or behaviour'
The Impact of Ocean Noise Pollutic ) on Fish and Invertebrate
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Scientific gaps and future studies
Carroll et al. (2017) noted the complete absence of research on the masking of natural signals by seismic
airguns. Also, elasmobranchs (sharks and rays) were very underrepresented in studies of the impacts
of seismic noise, and more research on invertebrates was needed, especially early life stages (Carroll et
aL 2017). Williams etaL (2015) further identified sea turtles as the most under -studied group regarding
noise impacts. Carroll et aL (2017) noted substantial knowledge gaps concerning "...the effects of seismic
sounds on important physiological and biological processes such as metabolic rate, reproduction, larval
development, foraging and intraspecific communication." Other needs identified by various authors
include:
1) Research on the ultimate consequences of noise, that is, on an individual's ability to survive and
reproduce which, in turn, will translate into population viability and ecosystem community function.
Studies on population and ecosystem impacts are vastly easier to do on fish and invertebrates than
most marine mammal species. Studies should measure vital rates such as survival, growth, and
reproductive rates (Nedelec etaL 2014; Normandeau Associates, Inc. 2012) and should be long-term
(Kunc etaL 2016) and over larger geographic scales (Shannon etaL 2016).
2) Experiments on repetitive or chronic noise exposure, as cumulative effects may produce differing
responses (Nedelec et al. 2014). Synergistic or aggregate effects and interactions from multiple, even -
non -noise, stressors are important (Normandeau Associates, Inc. 2012).
3) Determine reliable indicators of harmful stress (Normandeau Associates, Inc. 2012).
4) Research on the long-term or cumulative effects of noise on genes, cells, tissues, or physiological
processes associated with stress responses (Aguilar de Soto & Kight 2016).
5) More field-based experiments which address the spatial scale of impacts under the most ecologically
realistic scenarios, taking context into account (Bruintjes & Radford 2013).
6) Field studies examining vital rates of comparable populations in noisy and quiet conditions.
Differences in how fish and invertebrates are distributed in noisy and quiet environments should
be studied (Slabbekoorn etaL 2010). Gradients of noise exposure, rather than just noisy and quiet
scenarios, should be investigated (Shannon etaL 2016).
7) Field studies documenting biological responses in environments that have experienced a noise
reduction, such as a change in ship traffic routes. This could help reveal how systems recover from
chronic noise exposure (Shannon etaL 2016).
8) More realistic masking experiments (Radford etaL 2014) and how masking relates to vital rates and
predator -prey relationships (Slabbekoorn et aL 2010).
9) Identify the most vulnerable species in a local ecosystem and those that play a key ecological role
(Hawkins & Popper 2017).
10) Research and development on quieting methods and technologies (Normandeau Associates, Inc.
2012).
11) Evaluate and test the effectiveness of mitigation tools and methods (Normandeau Associates, Inc.
2012, Shannon etaL 2016).
12) Employ more passive acoustic monitoring for mitigation, monitoring, and impact studies of essential
fish and invertebrate habitat, especially ocean -bottom sensors and gliders (Aguilar de Soto etal.
2016).
13) Further develop acoustic measures of habitat biodiversity and study the impact of noise on
biodiversity.
14) Identify biologically important fish and invertebrate habitat (Normandeau Associates, Inc. 2012) to
protect it from noise, using acoustic buffer zones as needed.
15) Identify which characteristics of sound make it injurious (Normandeau Associates, Inc. 2012).
16) Determine whether it is better to expose a habitat to louder noise for a shorter period of time vs.
quieter noise for a longer period of time.
17) Research on physical injuries other than hearing damage (Normandeau Associates, Inc. 2012) and
expand hearing damage studies to include noise -induced sensorineural hearing loss (death of
neurons).
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18) Better measurements, descriptions, and standardization of particle motion in studies (Hawkins &
Popper 2017; Normandeau Associates, Inc. 2012).
19) Liaise with fisheries managers to better determine the impacts of noise on fisheries (Normandeau
Associates, Inc. 2012).
Management and mitigation recommendations
1) Promote and further airgun alternatives and quieting technologies, such as Marine Vibroseis, which is
thought to lower particle motion acceleration as well. Also work to reduce vibration through the sea bed.
2) All noise sources should avoid biologically important areas (e.g. spawning grounds, nursery areas,
important foraging habitat) and times of year, such as spawning. Dawn or dusk fish choruses should
preferably also be avoided. A recovery period for females immediately after spawning should be
allowed, as females tend to be in very poor body condition at this time. Shipping lanes could be re-
routed to avoid important fish and invertebrate habitat.
3) Reduce commercial shipping and fishing vessel noise (e.g. dragging) through technological
innovation or quieter operation (e.g. slow steaming). Ships should avoid routes immediately parallel
to the continental shelf as noise can more easily enter the deep sound channel, travelling very
efficiently for large distances.
4) Vessels in port should avoid using their generators and use shore power instead to reduce biofouling
which adds to shipping noise and introduces invasive species. Noise insulation and dampening of
engines and generators should also occur.
5) Reduce recreational boat noise and promote quieter, surface -piercing drives such as Arneson
drives, as appropriate. Four-stroke outboard engines appear less impactful to some marine species
compared with two-stroke engines.
6) Dynamic Positioning (DP) is extremely loud and is often used by supply ships, among other vessels.
Alternative operation or technologies should be promoted.
7) All sonars, echosounders, and multibeams should use frequencies above at least 200 kHz.
8) The required, involuntary activation of echosounders on recreational boats upon turning on the
engine should be abolished. This appears to be the case for newer boats, where the GPS immediate
activates the echosounder and it cannot be turned off.
9) Reduce pile driving or construction noise through the water and vibration through the sea bed.
Alternative foundations such as suction caissons or gravity -based foundations may effectively
eliminate noise during construction. Quieter, new installation methods such as BLUE Piling which do
not require a hammer and have no moving parts, should be explored and promoted.
10) Naval sonar should also be kept away from biologically rich and productive areas. Dipping sonar
seems to be particularly problematic for marine mammals and may also be for fish and invertebrates
as there is no possibility of habituation.
11) Noise impacts should be incorporated into population modelling for fish and invertebrates.
12) Geophysical surveys of all kinds (including seabed mapping) should be required to use the lowest
possible source level.
13) Thorough Environmental Impact Assessments need to completed for all noise activities having the
potential to cause impacts. Analyses of the impacts on fish and invertebrates need to be included.
14) Marine Protected Areas should be managed with noise in mind, including acoustic buffer zones.
15) Acoustic refuges of still -quiet biologically important areas for noise -sensitive marine life should be
safeguarded and protected from noise.
16) The unproven assumption that all marine life will avoid noise must be jettisoned. Many species and
individuals do not consistently avoid even damaging noise, if the area is important to them. Even if
animals avoid noise, this is a costly behavior in terms of: a) lost foraging time; b) the energetic costs of
transiting and interrupted feeding; and c) predation and less efficient foraging in areas that are not as
well known.
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References
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CH -8820 Mclenswil
Switzerland
Tel: +41 (0) 44 780 66 88
Fax: +41 (0) 44 780 68 08
Email: infoCa)oceancare.ory
Web: www.oceancare.oro
Dalhousie University
Department of Biology
1355 Oxford St.
P.O. Box 15000
Halifax, Nova Scotia 63H 4132 Canada
Suggested citation: Weilgart L. 2018. The impact of ocean noise pollution on fish and invertebrates. Report
for OceanCare, Switzerland. 34 pp.
DALHOUSIE
ocean care TUNIVERSITY
Inspiring Minds