Marine mammal behavior response to sonars, a review

advertisement

Institutionen för fysik, kemi och biologi

Examensarbete 16 hp

Marine mammal behavior response to sonars, a review

Anna Linderhed

LiTH-IFM- Ex-13/2826 --SE

Handledare: Torbjörn Johansson, FOI

Examinator: Mats Amundin, Linköpings universitet

Institutionen för fysik, kemi och biologi

Linköpings universitet

581 83 Linköping

Språk /Language

Engelska /English

Institutionen för fysik, kemi och biologi

Department of Physics, Chemistry and Biology

Avdelningen för biologi

Instutitionen för fysik och mätteknik

Rapporttyp

Report category

Examensarbete

C-uppsats

ISBN

LITH-IFMA-EX — 13/2826 —SE

__________________________________________________

ISRN

__________________________________________________

Serietitel och serienummer ISSN

Title of series, numbering

Handledare/ Supervisor Torbjörn Johansson

Ort/ Location:

Kista

URL för elektronisk version

Datum /Date

20130901

Titel/ Title:

Marine mammal behavior response to sonars, a review

Författare/ Author:

Anna Linderhed

Sammanfattning/ Abstract:

During the last decades the problems caused by anthropogenic sound and noise in oceans have been recognized in public, by governments, and military. With the use of active sonar, different choices can be made to minimize the risk of damaging or disturbing marine mammals. For this purpose knowledge of sonar disturbance is crucial. There are methods for time or area planning, i.e. when and where to use active sonars, to avoid marine mammals. The purpose of this work is to find information in literature on marine mammal behaviour reactions to the sound of sonar pings, and to evaluate which of two different behavioural models used in risk assessment programs, the “varying response” model and the “avoidance” model, is more correct to use. Main focus is on sonars and marine mammals residing in Sweden, i.e. the harbour porpoise, grey seal, harbour seal and ringed seal. Behavioral results from other research areas such as bycatch, environmental, and strandings, together with other sound sources than sonars and other species, provide a broader picture of the situation in noisy oceans. For the harbor porpoise the “avoidance” model works well. It is a very shy species, which flees fast and far when it comes in contact with new things. With the seals however the “avoidance” model is probably less good, since their responses to sonar differ rather much. Hence, for these taxa we recommend to use the “various” model that takes into account such varying responses.

Nyckelord/ Keyword:

Marine mammal, anthropogenic noise, sonar, behaviour, risk assessment models.

Table of Contents

1 Abstract .................................................................................................................. 2

2 Introduction ............................................................................................................ 2

3 Method ................................................................................................................... 5

4 Results .................................................................................................................... 6

4.1

Behavioral response to underwater sound ..................................................... 7

4.1.1

Cetaceans ................................................................................................... 7

4.1.2

Pinniped ................................................................................................... 11

5 Discussion ............................................................................................................ 13

5.1

Conclusion ................................................................................................... 14

6 References ............................................................................................................ 15

1 Abstract

During the last decades the problems caused by anthropogenic sound and noise in oceans have been recognized in public, by governments, and military. With the use of active sonar, different choices can be made to minimize the risk of damaging or disturbing marine mammals. For this purpose knowledge of sonar disturbance is crucial. There are methods for time or area planning, i.e. when and where to use active sonars, to avoid marine mammals. The purpose of this work is to find information in literature on marine mammal behaviour reactions to the sound of sonar pings, and to evaluate which of two different behavioural models used in risk assessment programs, the “varying response” model and the “avoidance” model, is more correct to use. Main focus is on sonars and marine mammals residing in

Sweden, i.e. the harbour porpoise, grey seal, harbour seal and ringed seal. Behavioral results from other research areas such as bycatch, environmental, and strandings, together with other sound sources than sonars and other species, provide a broader picture of the situation in noisy oceans. For the harbor porpoise the “avoidance” model works well. It is a very shy species, which flees fast and far when it comes in contact with new things. With the seals however the “avoidance” model is probably less good, since their responses to sonar differ rather much. Hence, for these taxa we recommend to use the “various” model that takes into account such varying responses.

2 Introduction

Oceans are full of noise (Kumagai 2006). Natural sound sources have been there all the time and marine life is adapted to it. Anthropogenic sound and noise are fairly new and affect marine life (Southall et al. 2007). Noise disturbance can be as masking of natural functions (Soto 2006), changed behavior (Finneran et al. 2000,

Kastelein et al . 2011), and result in physical impact on hearing and body organs

(Johansson 2012). Mass strandings have received much recent attention and publicity

(Parsons et al. 2008, Dolman et al. 2011) and have led to a great deal of research being focused on what may have caused these strandings (Wright and Parsons 2011,

Kumagai 2006) (Weilgart 2006, Evans and Miller 2004). During the last decades the problems caused by anthropogenic sound and noise in oceans have been recognized in public, by governments, and military. Human underwater activity is an intrusion to marine mammal life and in particular the use of active sonar has been in focus, this because a number of marine mammal mass strandings have occurred in connection with military excercises using high-power, mid-frequency active sonar (Parsons et al

2008, Dolmanet al. 2011, Weilgart 2006, Evans and Miller 2004, Norman et al. 2004,

Nowacek et al. 2007, Tyack et al. 2006). Discussions regarding mass stranding have gone to the fullest extent in that a U.S. court has ordered the U.S. Navy to review their practices and produce an environmental plan in order to get permission to expand their sonar activities (Zirbel et al. 2011, Dalton 2003).

Different sources of anthropogenic noise are investigated with respect to the response from animals. Our main focus here is naval/military sonar but we also report on behavioural responses to other sound sources with similar sound pressure levels or frequency range.

Sonar is short for SOund Navigation And Ranging. It is based on active transmission of a sound pulse, and analysis of the echoes returning from an object/target hit by the sound pulse. The two-way transmission time provides information on the distance to the target, and the frequency content and time function of the echo provides

2

information on the size, material and shape of the target. This is the principle for cetacean echolocalization as well as for man-made sonar systems and echosounders.

Active man-made sonar uses a variety of ping types and frequencies. UK Naval sonar uses 1Hz - 1 kHz for low frequency active sonar (LFAS) and 100Hz-10 kHz for midfrequency active sonar (MFAS) (Dolman et al. 2009, OSPAR 2009). Swedish navy sonars use frequencies above 20 kHz (Kastelein et al. 2013-1).

Seal bombs (TNT) are used to scare seals away from equipment. They are depth bombs that explode under water and creates a flash of light and loud sounds below 1 kHz with sound pressure level (SPL) about 190 dB re 1

Pa at 1m. (Jefferson and

Curry 1996, Evans and Miller 2004).

Acoustic deterrent devices, ADDs, and acoustic harassment devices, AHDs, differ in output source levels and frequency range.

Low-level ADDs or pingers, are primarily designed to displace animals temporarily from a fishing net, to avoid entanglement. Typical ADDs vary a lot but most stay in the ultrasonic frequency range or operate in the pure-tonal around 10 kHz (possibly with harmonics) and variable, broad spectral 20-120 kHz with source level, SL, below

150 dB re 1

Pa at 1 m (Shapiro 2009). Another examples are from Teilmann et al.

(2006) with signals of 100 kHz to 140 kHz, 200 ms long, SL of 153 dB re 1

Pa at

1m and the experimental set up of Kastelein et al . ( 2008) using pure tone signal of 70 kHz or 120 kHz and different signal durations.

High-level AHDs or seal scarers, use SL’s high enough to cause pain, but not harm

(Jefferson and Curry 1996) and are used to keep seals away from fishing gear. AHDs are needed because seals are more motivated to approach the fishing gear, to eat the fish. AHDs produces irregular wideband acoustic pulses within the seal's hearing range (12-17 kHz) between 5 and 30 kHz with source levels above 170 dB re 1

Pa at

1 m (Shapiro 2009). .

Echosounders, e.g. used to look for fish or explore the seabed, transmit variable frequencies depending on system and application, as illustrated in figure 1.

Figure 1. Echosounders (from Cochrane N.A., (1996)).

Industrial impulse noise from pile driver hammers, i.e. impulsive sounds generated when steel monopile foundations for offshore wind turbines is driven into hard sand in shallow water, has high sound pressures, SPL 235 dB re 1

Pa at 1 m, and can be

3

as loud as SPL 131 to 135 dB re 1

Pa measured 1km away. Sound pressure levels were measured over the frequency range of 50–26 000 Hz and were highest for center frequencies 200–800 Hz and progressively falling due for loss over distance for frequencies 12.8–25.6 kHz (David 2006).

Behavioral response from ship noise is also investigated (Ellison et al . 2011, OSPAR

2009) as well as from the noise produced by seismic surveys with airguns (Harris

2001). Nominal SPL for airguns, for downward propagation, is typically 245 to 255 dB re 1

Pa at 1m. Most emitted sound energy is at frequencies below 125 Hz with a safety radius of 150-250 m based on a 190 dB re 1

Pa criterion for broadband received level. A single airgun or a set of 8-11 airguns are used.

Although physical injuries caused by anthropogenic noise (e.g. permanent hearing loss) usually appear at very high energy levels, behavioral response and masking appear at much lower levels (Kastelein et al. 2000, 2006, 2008, 2011). Over time research has changed direction from physical impact to behavioral changes and focus now specifically on behavioral response. Even though direct response to a sonar ping is easier to evaluate it is necessary also to evaluate long term behavior changes as a result of disturbances. If the animals are driven out of their natural habitat, are forced to stop their foraging, or are disturbed at sensitive locations for breeding, it is a serious intervention in their natural life. Immediate impact of disturbance is e.g. when young animals are separated from their parent, a potentially life-threatening condition.

Also population survival may be impaired if animals are prevented from access to breeding areas or cannot search for food undisturbed.

Impairment of marine mammals’ welfare by marine active sonar is a growing international concern. Different agreements exist for the implementation of detailed conservation plans for cetaceans; ACCOBAMS (Agreement on the Conservation of

Cetaceans in the Black Sea Mediterranean Sea and Contiguous Atlantic Area) is dealing with the protection of marine mammals in the Mediterranean whilst

ASCOBANS (Agreement on the Conservation of Small Cetaceans of the Baltic,

North East Atlantic, Irish and North Seas) focus on the protection and conservation of

Northern Europe's small whales, dolphins and porpoises (ASCOBANS 2009).

According to the Marine Environment Directive (DIRECTIVE 2008) all marine ecosystems within EU shall have a good environmental status; USA and Australia have similar directives (Finneran and Jenkins 2012). The EU Marine directive includes all marine waters within the EU. Although this Directive does not apply to military activities in war, in peacetime the directive includes a recommendation also for the Navy with regards to the use of active sonar. Citing one paragraph in the directive; "Introduction of energy, including underwater noise, is at levels that do not affect the marine environment in a negative way”, this leaves the member states with no other option than to investigate how sonars affect marine mammals. Of special interest for Sweden is the local species; harbor seal ( Phoca vitulina ; Naturvårdsverket

2011b), gray seal (Halichoerus grypus; Naturvårdsverket 2011c), ringed seal ( Pusa hispida ; Naturvårdsverket 2011d), and porpoises ( Phocoena phocoena ;

Naturvårdsverket 2011a).

With the use of active sonar, different choices can be made to minimize the risk of disturbing or damaging marine mammals. For this purpose knowledge of how sonar might affect or act on cetaceans is crucial. This is partly depending on the species, some are always under water (porpoise) or partially under water (seals). There are different methods used to moderate the potentially negative effects of military sonars on the life of marine mammals. One is time or area closure, i.e. when and where to

4

use active sonars, to avoid affecting marine mammals or affecting them during sensitive periods, another is the use of different technical solutions e.g. soft start (or

‘‘ramp-up”) where the sound pressure levels are gradually increased over time; and yet another is to visually or acoustically monitoring animal groups, and avoid transmitting the sound in the presence of the animals, in order to keep a safe zone around the sonar or other noise sources (Dolman et al 2009).

The present work is done as a part of the project “Skydd av marint liv vid användning av aktiv sonar” (Protection of marine life in connection with the use of active sonar) at Swedish Defence Research Agency FOI (Johansson 2012). This project is a part of the EDA (European Defence Agency) project “Protection of Marine Mammals”,

PoMM, a collaboration between Sweden, Germany, Norway, the Netherlands, Italy and the UK. This project deals with, among other tasks, the building of a common database on marine mammals in European waters, and the development of methods for classification and/or detecting marine mammal vocalizations. In addition to this international commitment the FOI project also aims at building knowledge specific for Swedish conditions (Johansson 2012). Methods for time or area planning has to take the welfare of marine life into considerations and therefore several countries have developed simulation programs to support the planning of military operations in order to show necessary/suitable respect for the environment. Sigg (2013) has evaluated two tools. These tools work with different effects from sonar, such as

Temporary Threshold Shift (TTS) and Permanent Threshold Shift (PTS), i.e. different levels of hearing impairments. The programs estimate the degree of influence by modeling the transfer and distribution of sound, i.e., by performing the same calculations as done by a tactical support system for active sonar. They model the density of animals of different species in the area, their sensitivity to the transmitted pulses and their reaction. The threshold for eliciting escape behavior, avoidance, or other behavioral responses to the sonar signals is species specific. Risk estimates are based on a model of behavior that assumes that an animal reacts to the transmitted sonar signals in some way. Based on this, a calculated risk for PTS and TTS is obtained. There are distinct differences between the risk calculation algorithms used in the two programs evaluated; ERMC (BAE Systems, UK) and SAKAMATA (TNO, the Netherlands) (Sigg 2013). Both of the programs takes into account the behavioral reactions to a sonar ping. The first model, called the “various” model, assumes that when the animal perceives a sonar pulse, they may exhibit a variety of behaviors according to the pulse strength and the individual animal, taxa, age, sex, previous experience and current activities. The second tool, called the “avoidance” model, assumes that all animals are affected in the same way, i.e. when the sound pulse is stronger than a threshold all animal moves away from the sound source. This threshold can vary between species and ping type.

The purpose of this work is to find information in the scientific literature on marine mammal behaviour reactions to sonar pings and other anthropogenic noise, and to evaluate which of the two risk assessment models used in the evaluated programs is more correct to use with marine mammals in Swedish waters. Main focus is on military sonars.

3 Method

This review is made solely by compiling information published in scientific literature.

Articles are searched for in data bases available at the library of Linköping

University: ScienceDirect is searched with the following key words: marine mammal,

5

seal, cetacean, dolphin, whale, porpoise, behavior effect, noise, naval sonar, and in

Pubmed in which the search profile (marine[All Fields] AND mammal[All Fields]OR cetacean[All Field]) AND sonar[All Fields] AND behaviour[All Fields]) was used.

As introduction and motivation to the work, project presentations and FOI reports are used (Johansson 2012; Sigg 2013). In some cases references found in the articles have been further investigated. Focus has been on finding information as input to a suitable model for marine mammal behaviour responses to naval/military sonar pings.

4 Results

In this section the result from the literature survey is presented. First a table of the sound sources presented above, it is compiled from the literature. Second we present information on marine mammal hearing. This because the relation between hearing range, noise bandwidth and SPL (received level ) is connected to possible behavioral response. Thereafter the behavioral responses are presented sorted by animal.

Table 1 Sound source characteristics.

Sound Sound pressure level (SPL)

(dB re 1 μPa)

272 - 287Peak

Bandwidth

(Hz)

Duration

(ms) ref

TNT(0,5-50kg) 2 - 1000 ~ 1 - 10

50

(Jefferson and

Curry 1996, Evans and Miller 2004).

(David 2006).

Pile driving

Swedish navy sonars

Echosounders

228 Peak /

243 – 257 P-to-P

215 Peak

20 ->20 000

Military sonar low- frequency (LFAS

Military sonar midfrequency MFAS

223 - 235

Peak

214-220

235 Peak

100 - 500

2800 - 8200

20 000 --500000

Variable

600 - 1000

500 - 2000

<1 -1000

5 - 10 ms

(Dolman et al.

2009, OSPAR

2009)

(Dolman et al.

2009, OSPAR

2009)

(Kastelein et al.

2013-1).

Cochrane N.A.,

(1996)

(Harris 2001).

(Shapiro 2009)

(Jefferson and

Curry 1996)

Airgun array

Acoustic deterrent

/harassment devices

260 - 262P-to-P

132 - 200 Peak

10 – 100 000

5000 -30 000

30 - 60

Variable 15 – 500 ms

Functional hearing limits for different marine mammals are listed by Finneran and

Jenkins (2012) and Nedwell et al.

(2004). Information on cetacean hearing can also be found in (Mooney et al. 2012). Information on the animal’s hearing ability is vital to the understanding of the reactions to sound. LF cetaceans such as humpback whale hear in the range of 7 Hz – 22 kHz. Most delphinid species have a U-shaped audiogram (fig 2), with a hearing range between from 150 Hz to 160 kHz, with best hearing in the 20-120 kHz range, while porpoises hear between 200 Hz and 180 kHz, with best hearing around 130 kHz. Phocids or “true seals,” hear between 75 Hz – 30 kHz in air and 75 Hz – 75 kHz in water (best hearing 20-30 kHz; fig 2), Otariids or

”eared seals” hear 100 Hz – 35 kHz in air and 100 Hz – 50 kHz in water (ref?). These boundaries are approximate; there are differences between species within the same families. Figure 2 show audiograms for Grey seal and Harbour Porpoise to illustrate the differences in hearing ability. The different curves for each species are from

6

different measuring methods. Audiograms can be obtained by behavioral studies and by measuring the electrical brain activity, so called auditory brainstem response

(ABR). An easy to read, non-technician friendly explanation of underwater acoustic measurements and units can be found in (Chapman 1998).

Figure 2. Audiogram of Gray seal (left) and Porpoise (right) (from Nedwell et al.

2004). Note the different level of scale on vertical axis.

4.1

Behavioral response to underwater sound

Effects of anthropogenic noise can vary depending on noise generating system, sound pressure levels(SPL) and environment among other things. Effects can be divided into masking, behavioral disturbance, hearing loss (TTS and PTS), discomfort, injury, death (OSPAR, 2009). In this section we present the behavioral response findings from the literature review sorted by species.

4.1.1

Cetaceans

Mysticeti (baleen whales)

Baleen whales have only been studied in the wild, by visual observations in combination with acoustic recordings. Male humpback whales ( Megaptera novaeangliae ) changed their vocal behavior when exposed to LFAS (low frequency active sonar) at SPL max 150 dB re 1

Pa at 1 m. On average, the songs were 29% longer during LFAS playbacks. The duration of the songs returned to normal after exposure. The limited effect on the duration of the song suggests that humpback whales sang longer songs during LFAS transmissions to compensate for acoustic interference (Miller et al. 2000). Regarding fishing gear alarms of various sorts,

Jefferson and Curry (1996) reported that the number of humpback whales found entangled in fishing gear was inversely proportional to the amount of noise made by the net.

Clark and Altman (2006) analyzed acoustic recordings made during naval sonar exercises. They found that there was an increased chance of detecting sound from fin whale ( Balaenoptera physalus ) during periods when there were no LFAS broadcasts than during periods of broadcasting. This may have been due either to the whales decreased vocal activity in response to LFAS transmissions or the effect of applying the rules described in the mitigation protocol, i.e. pushing the whales out of the area before transmitting the LFAS, or a combination of these two (Clark and Altman

2006).

7

Blue whales ( Balaenoptera musculus ) vocalization response to MFAS (mid frequency active sonar) sources was studied by Melcón et al. (2012). Blue whales were less likely to communicate when MFAS was active. This decrease was more pronounced at higher received SPLs, i.e., when the source was closer to the animal. The animals showed no diurnal variation in the response to the sonar or vessel noise (Melcon et al.

2012). Croll et al. (2001) studied blue whales foraging behavior when exposed to

LFAS, and found no effect even though received levels were estimated to be over

140 dB re 1

Pa. It was assumed that the diving behavior of the blue whales was more strongly linked to changes in eating habits and food supply than to the sound disturbance (Croll et al. 2001).

Odontoceti (toothed whales)

Long-finned pilot whales ( Globicephala melas ) and sperm whales ( Physeter macrocephalus ) were tagged with a so called D-tag for a free swimming controlled sound exposure study (Sivle et al. 2012). The D-tag is a recording device attached to the whale by a suction cup and is storing information on 3-D movements and sound generation. Analysis of the tag data showed that both species had normal deep foraging dives under MFAS exposure, while during the LFAS exposures, long-finned pilot whales performed fewer deep foraging dives and some sperm whales changed to shallower and shorter dives without foraging.

Miller et al. (2011) studied the behavioral effects of killer whales ( Orcinus orca ), sperm whales, and long-finned pilot whales when exposed to naval sonar signals in

Norwegian waters. Each experiment was performed with multiple exposures, with 1-2 kHz (LFAS) and 6-7 kHz (MFAS) upsweep signals. Some animals were also tested with silent approach, conducted as a control for the possible effect of the vessel approach itself, and some with 1-2 kHz down-sweep echosounder signals. Each tested whale was tagged with a D-tag and was also the focal animal for visual tracking. The project collected baseline data for each tagged subject, and implemented a controlled sound exposure regime in which a realistic sonar source started operating at a distance of 6-8 km from the animal, increasing to maximum source level through a ramp-up procedure. The source then approached the subject, creating a “worst-case scenario” by making turns always towards the subject. At 1 km distance, the source stopped the approach, and passed and moved away from the subject and then ceased the transmissions about 5 minutes after the point of closest approach. The comprehensive results presented in the report include detailed observations to examine whether and how the behavior may have been affected when each subject was subjected to such a controlled exposure of sonar sounds. The whales showed a large number of changes in behavior during these sonar exposures. Mostly the animals chose to avoid the sound source or move away from the path of the source. At one point the unexpected effect was that a killer whale calf was separated from the herd. Also changes in diving and surfacing behavior was seen in some cases, and details on diving behavior differed by species. Similar conclusions hold for changes in the acoustic behavior.

Changes tended to be less during periods with quiet sonar.

Tyack et al. ( 2011) documented Blainville’s beaked whales ( Mesoplodon densirostris ) in a sea area where sonar is used regularly. Behavioral responses were investigate by using two methods, one monitoring the direct whale responses to naval exercises of tactical MFAS over several days, another one using an experimental approach with playbacks of simulated sonar and whales tagged with D-tags. Both experiments showed that beaked whales stopped their echolocation during deep foraging dives and instead moved away from the sound source when exposed to

8

sonar. During sonar exposure the whales maintained a distance of 16 km from the sonar source and did not return to the original area until after 2 to 3 days. The results suggest that such evasive actions and disruption of foraging behavior can occur at exposures below the previously known levels of disturbance. The received SPLs collected by the D-tag with such behavioral responses were between undetected to

142 dB re 1

Pa and ceased clicking were detected at received levels of 138 dB re 1

Pa. Previous studies showed that D-tagged Cuvier’s beaked whales ( Ziphius cavirostris ) and Blainville’s beaked whales made foraging dives deeper and longer than expected when exposed to sonar (Tyack et al., 2006).

McCarthy et al. (2011) studied Blainville’s beaked whales concerning the number of vocalizing groups in connection with foraging and their distribution during multi-ship

MFAS operations.These surveys were carried out by using existing data routinely recorded during military exercises. Reduced phonic/acoustic activity in the whales was observed during active sonar exercises and increased vocal activity was observed when the sonar transmissions stopped. Received sound levels for several groups of whales were calculated and indicated that the animals continued to eat when exposed to sonar at levels as high as 157 dB re 1

Pa. Possible explanations were given for this decrease in vocalization, either the animals had moved outside the area but continued to vocalize, or the animals went silent during the military operations. These results are consistent with those of Clark and Altman (2006) for fin whale. Another possible explanation for the findings of McCarthy et al. (2011) may be that masking has occurred, i.e. whale sound is drowned out by the sond produced by multi-ship

MFAS operations and that the system could not detect whale vocalizations because of the noise (Soto 2006).

Carretta et al. (2008) report that pingers (acoustic deterrent devices) are extremely efficient to prevent bycatch of beaked whales in driftnets. Such bycatch dropped to zero when pingers were put on to the nets. Cox et al. (2007) found that even though these alarms (details not specified in the reference) were moderately effective in reducing bycatches of marine mammals, there was no significant change in the number of dolphin near the net when the alarms were turned on or off. On the other hand, according to Bordino et al. (2002), dolphins responded well to the intensions of the use of pingers (Dukane Netmark 1000 emitted a multi-harmonic signal centered at

10 kHz every four seconds, with a source level of 132 dB re 1

Pa at 1 m) to keep the mammals from the net, meaning that dolphins avoid pingers. The reason for these somehow contradictory results can be that the alarms, seal scareres and pingers operate at different frequencies and SPL.

Finneran et al. (2000) examined the effects of distant underwater explosions on the hearing sensitivity of one captive and trained beluga ( Delphinapterus leucas ) and two captive and trained bottlenose dolphins ( Tursiops truncatus ) by exposing them to impulsive underwater sounds. The impulse noise was designed to simulate distant underwater explosions. Behavioral changes indicating impact on masked thresholds for underwater hearing was demonstrated at exposures equivalent to 500 kg TNT at a distance of 1.9 km [ sic!

] for the beluga whale and equivalent to 5 kg TNT at 9.3 km for the dolphins (Finneran et al. 2000).

Houser et al. (2013) performed a controlled study using a large sample of trained bottlenose dolphins and a simulated tactical sonar signals. The study was performed in a 9.1 × 18.3 m netted enclosure where the dolphins performed their trained duty when exposed to the sonar signals. The dolphins habituated to the exposure quickly as long as the received SPLs was not higher than 160 dB re 1

Pa. When the received

9

SPLs was increased to 175 dB re 1

Pa and above no habituation could be observed and no dolphin completed the requested trained behavioral sequence when exposures reached 185 dB re 1

Pa.

The normal acoustic behavior of Harbor porpoises ( Phocoena phocoena ) is described by Carlström (2005) and Clausen et al. (2011). The Harbor porpoise is considered to be a shy species that rather avoids vessels and are hard to observe in the wild.

Frequencies from standard sonars are often within the hearing range of porpoises and some fishfinder ehosounders use pulses almost identical to porpoise sonar clicks

(Naturvårdsverket 2011a).

Brandt et al. (2013) studied wild porpoise reactions to seal scarers (Lofitech

(www.lofitech.no) through passive acoustic monitoring using C-POD recordings in the German North Sea. The seal scarer emitted 0.5 s long pulsed signals at a main frequency of 14 kHz with weak harmonics and SL (source level) 189 dB re 1

Pa at

1m and repetition rate randomized in the range of 0.6 s to 90 s) C-PODs are ultrasound loggers collecting tonal clicks and record the time, duration, center frequency and other features of each click. The experiment showed that the seal scarers had a significant deterrent effect on porpoises up to 7.5 km away (equivalent to a received SPL of about 113 dB re 1

Pa), much longer than previously reported.

Harbor porpoise reactions to Dukane NetMark ™ 1000 (10 kHz, 132 dB re 1

Pa at 1 m) pingers were studied by Cox et al. (2001). It was shown that the probability of porpoise presence within 125 m from a pinger fell initially when pingers were turned on, but then increased to equal to the control after 10-11 days. These results indicate that the porpoise habituated to this kind of pinger.

Kastelein et al. (2006) exposed a striped dolphin ( Stenella coeruleoalba ) and a

Harbor porpoise, both kept in the same sea pen, to the sound of a XP-10 experimental acoustic alarm. The alarm produced 0.3s tonal signals randomly selected from a set of

16 with fundamental frequencies between 9 and 15kHz, with a constant pulse interval of 4.0s (duty cycle 8%) and a SL range of 133-163dB re 1

Pa at 1m. The effect of the alarm was assessed by comparing the animal breathing rate and their surfacing positions relative to the transducer during the test periods with those during the baseline period. The striped dolphin showed no reaction to the alarm in these trials.

The porpoise responded to the alarm with avoidance and increased respiration rate.

Based on the audiogram of this specific striped dolphin and published porpoise audiograms, together with the general noise levels during the experiment, it was concluded that both animals must have heard the alarm clearly. This study indicated that odontocetes are not equally affected by anthropogenic noise. In a previous study with two porpoises and the same alarm the porpoises responded heavily on the alarm by swimming away and by increase the respiratory rate (Kastelein et al. 2000). The results for the porpoise are consistent with those of Teilmann et al. (2006) although using a different sound, with a pulse duration of 200ms in the frequency band from

100 kHz to 140 kHz, and with those of Kastelein et al. (2008), although they used pure tone signals of 70 or 120 kHz with different signal durations.

Another experiment on a male porpoise in an outdoor pool was conducted by

Kastelein et al. (2013-2). This study measured the porpoise’s response to naval sonar at 25 kHz. The sound types used were frequency modulated (FM 25.5-24.5

kHz), continuous wave (CW) and a combination of these (Combo). These signals were presented to the animal at three different SL’s in random order. The behavioral parameters used to quantify the porpoise’s responses to the sound sequences were respiratory rate, distance from the transducer, swimming speed, and how many times

10

it jumped out of the water. Reactions by increased respiration rate was shown at SL

125 dB re 1

Pa at 1m FM, 118 dB re 1

Pa at 1m CW and Combo, by increased swimming speed at SPL 125 dB re 1

Pa at 1m FM, 136 dB re 1

Pa at 1m CW and118 dB re 1

Pa at 1m Combo. Jumping started at SPL 125 dB re 1

Pa at 1m

FM, 118 dB re 1

Pa at 1m CW and Combo. To determine whether habituation or desensitization had occurred during the 30-minutes trials, the data were analyzed separately for three ten-minute section of each trial, by examination the respiratory rate. After each session, the animal's behavior returned to normal immediately

A study by Sivle et al. (2012) showed that killer whales can alter their dive behavior by switching from deep foraging dives to shallow travel dives when exposed to LFAS

(1-2 kHz) and MFAS (6 -7 kHz) signals. If the killer whales were travelling when the sonar was turned on, there were no changes in dive behavior.

4.1.2

Pinniped

Phocidae Earless seals ,

Kvadsheim et al. (2010) performed controlled exposure experiments on captive hooded seals ( Cystophora cristata ). The seals were tagged with data loggers; heart rate receiver and logger HRX/HTR and depth-time recorder MK9, (Wildlife

Computers, Redmond, WA, USA.) in addition to activity loggers (Actiwatch,

MiniMitter, Bend, OR, USA) to store swimming speed. Then they were released into a large net pen in the sea. The sonar exposures presented to the animals were mixed

"soft start"(consisting of a series of 1-s sonar pulses every 10 s (duty cycle 10%), gradually increasing in pressure level from SPL 134 to 194 dB re 1

Pa at 1 m) and

"slow start" (consisting of a series of 1-s signals at 194 dB re 1

Pa SPL at 1 m with increasing duty cycles from 1% (100-s signal interval) to 10% (10-s signal interval) in

10 min) to simulate sonar signals between 1-7 kHz at source levels of 134-194dB

RMS re 1

Pa at 1m. Inside the pen the SPL was 10-27 dB below the source level.

The seals responded initially with avoidance when exposed to received SPL over 160-

170 dB re 1

Pa. Emotional activation during sonar exposure was detected by the increase in heart rate(above normal) at the surface, but the lack of effect on heart rate during diving showed that physiological capacity of bradycardia remained intact during the sonar exposure.

(Kastelein et al. 2013-1) examined the behavior of two seals in a large quiet pool when subjected to sonar sound with a frequency of around 25 kHz. The sensitivity of the harbor seal to such sonar is expected to be relatively high because it is within the most sensitive hearing frequency range of harbor seals (Kastelein et al.

, 2009a, b;.

2010). Behavioral responses were recorded as no response, a slightly increased time in the water, increased number of jumps out of the water, and increased swimming speed. The animals' discomfort threshold was determined by exposing them to signal sequences at three received SPLs. The signals were either FM 25.5-24.5

kHz , CW, or

Combo. Mainly FM caused significant behavioral responses to received levels above

125 dB re 1

Pa. The CW and Combo sounds caused only minimal response. The results showed that the CW and Combo sound types should be preferred as sonar signals in order not to disturb this species.

Observations during seismic surveys with airguns showed behavioral responses of ringed seals ( Pusa hispida ). In full array firings, 18% of 143 observed seals looked what happened, 2% were approaching, 5% swam alongside the boat trails, 36% dived

11

and 39% swam away from the airgun blast. No seals were seen within 150 meters of the ship under full seismic array exposures and this may be due to the mitigation protocols which governs when and how to do experiments with respect to wildlife.

(Harris 2001)

12

5 Discussion

This literature review deals with how marine mammals change their behavior when exposed to anthropogenic sounds. The review focuses on sonar, but information from research on other sound sources is also included, since it widens the perspective and the understanding of variations in the behavioral responses.

The problem with by-catch mitigation is that it relies on the animals changing their behavior in order to avoid being entangled (Hodgson et al. 2007). What motivates the present report is to find scientific facts on how to adapt the sonar signals and the use of sonar to do the opposite, i.e. to minimize the negative effects on the animals, and therefore we need to know how the different animals respond to sonar (Sigg 2013).

The behavioral changes we have seen in the articles in this survey are avoidance behavior and changed vocalizations, both aborting vocalizations and increasing whistling, and modified respiratory rate and diving patterns. One can, in some cases, assume that modified feeding behavior is due to masking effects but also to prey being affected by the noise (Weilgart 2006, Croll et al. 2001; David 2006).

Mass strandings have received much attention and publicity in recent years (Parsons et al.

2008; Dolman et al. 2011) and this has led to a great deal of research focusing on what may have been the underlying causes. Temporary or permanent hearing

(TTS or PTS) loss or blast injury in connection with military LFAS and MFAS operations are suggested reasons for stranding (Weilgart 2006), other suggestions are induced stress in beaked whales and other marine mammals (Wright and Parsons

2011). Norman et al. (2004) could not find any direct sign of acoustic trauma on dead stranded porpoises when dissected, but was not able to totally rule out the possibility that military sonar energy had caused the death of these animals. More recent research argue that these stranding are caused by extreme diving behavior leading to decompression problems. These extreme diving behavior are likely to result of an abnormal behavioral response to sonar, but the cause is unknown (Tyack et al. (2011).

The results of Clark and Altman (2006) that fin whales reduced vocalization during

LFAS exposure agree with those of Melcon et al. (2012) for blue whale, but are opposite to those of Miller et al. ( 2000) for humpback whales. The latter increased their singing during LFAS exposure. Long-finned pilot whales and sperm whales seemed to be undisturbed by MFAS (Sivle 2012).

Some research have been based on experimental studies of captive marine mammals while other have studied reactions of free-ranging animals. Inevitably environmental conditions and also results differ between such studies, but on the whole, the results are consistent. Controlled captivity experiments give more detailed data on physical responses that can be obtained in the wild. Still, extrapolating behavior results from controlled studies on animals in captivity, to free-ranging wild animals should be done with caution (Kastelein et al. 2013-1). Laboratory experiments can be scientifically robust, but behavioral responses depend not only on hearing sensitivity, but also on many individual characteristics of the animals. It is also affected by the fact that the captive animals are in a different environment than their wild conspecifics, and is constrained so they cannot avoid a negative stimulus. Also experiments with captive animals are often restricted to few individuals who may become very familiar with the experimental situation and subject to repeated exposures. Götz and Janik (2010, 2011) analyzed how the acoustic startle reflex associated with stress and habituation effects and noted that in experiments with animals in captivity, where food is included in the context, seals habituate faster to

13

sound types presented with normalized received levels of 146 dB re 1

Pa than for experiments on animals tested in the wild without food rewards. Food presentation, in addition to the fact that that the test animals are unable to flee, is the most likely explanation for the rapid habituation of the avoidance behavior observed in captive animals exposed to received levels of 135-144 dB re. 1

Pa,

According to Hildebrand (2004) “Behavioral data must be collected in the wild in order to reveal potential effects”. Recent research using tagged wild animals is a way to go, but still often suffers from a low number of test animals (Miller et al. 2011;

Tyack et al. 2011; Sivle et al. 2012; DeRuiter et al. 2013; Linnenschmidt et al. 2013).

In-depth analysis of the data provided by Miller et al. (2011) showed that the free swimming killer whales, provided with D-tags, did not change their behavior when exposed to sonar below a received SPL of approximately 150 dB re 1

Pa, but for

SPL above this the whales moved away from the sound source with speed. This indicated that the ramp-up procedure recommended to make the animals move out of the area before dangerous levels are transmitted should start at these levels. This behavioral threshold level probably differs from species to species, and maybe between different specimens of the same species, due to different experiences to noise. Hence more knowledge from studying wild tagged animals is needed.

For Swedish conditions the findings in the reviewed literature can be summarized as follows:

1.

The harbor porpoise tend to respond by escape to novel sounds, to acoustic deterrent and harassment sounds and to military sonars.

2.

Swedish earless seals, e.g. grey seal, harbor seal and ringed seal, are more varying in their response to sounds, and may approach, ignore or avoid even powerful acoustic harassment sounds. They show behavioral and physiological reactions to some military sonars but not to others.

5.1

Conclusion

The goal of this study was to determine which of the two models used for sonar exposure risk assessment are the most appropriate to use for a particular species.

For the harbor porpoise the “avoidance model” works well. This is a very shy species and porpoises mostly flee fast and far when they come in contact with new things.

For seals, however, the avoidance model is probably less good because seals respond in a variety of ways to sonar, some even approaching the source. Hence, using this model could cause damage to animals that do not behave as expected by the

“avoidance” model. Since only one report of this survey indicate a percentage distribution between flight, approach and other reactions, we do not give a breakdown of the behavior into figures to put into a simulator. These results were also not responses to sonar but to impulse sound produced by airgun.

For Swedish conditions, we recommend managers and the military to use the model that takes into account the specific response of the species of concern, i.e. the

“avoidance” model with the harbor porpoise and the “various” model with seals.

14

6 References

ASCOBANS (2009).

“Report of the Intersessional Working Group on the assessment of acoustic disturbance,” Noise Working Group, ASCOBANS, Bonn,

24pp.

Bordino, P., Kraus, S., Albareda, D., Fazio, A., Palmerio, A., Mendez, M., and S.

Botta (2002), Reducing incidental mortality of franciscana dolphin pontoporia blainvillei with acoustic warning devices attached to fishing nets, Marine Mammal Science , Volume 18, Issue 4, October 2002, Pages:

833–842.

Brandt, Miriam J., Höschle, Caroline, Diederichs, Ansgar, Betke, Klaus, Matuschek,

Rainer, Witte, Sophia and Nehls, Georg (2012), Far-reaching effects of a seal scarer on harbour porpoises, Phocoena phocoena, Aquatic

Conservation: Marine And Freshwater Ecosystems . 23: 222–232 .

Carlström Julia (2005), Diel variation in echolocation behavior of wild harbor porpoises, Marine Mammal Science Volume 21, Issue 1, January 2005,

Pages: 1–12.

Carretta, James V, Barlow, Jay (2008), Acoustic pingers eliminate beaked whale bycatch in a gill net fishery, Marine Mammal Science , 24(4): 956–961

(October 2008).

Clark, C.W., Altman, N.S., (2006). Acoustic detections of blue whale (Balaenoptera musculus) and fin whale (B. physalus) sounds during a SURTASS LFA exercise. Journal of Oceanic Engineering , 31, 120–128.

Clausen, Karin Tubbert, Wahlberg, Magnus, Beedholm, Kristian, Deruiter, Stacy,

Teglberg Madsen, Peter, (2011): Click communication in harbour porpoises phocoena phocoena , Bioacoustics: The International Journal of

Animal Sound and its Recording , 20:1, 1-28.

Cochrane N.A., (1996), Cutting Edge Sonar Technologies Explored For Pelagic

Stock Assessment, availible online http://www2.mar.dfompo.gc.ca/science/review/1996/Cochrane/Cochrane_e.html

Cox, Tara M,. Read, Andrew J, Solow, Andrew, Tregenza, Nick, (2001) Will harbour porpoises (Phocoena phocoena) habituate to pingers? J. Cetacean Res.

Manage.

3(1):81–86, 2001.

Cox, T. M.,. Lewison, R. L,. Žydelis, R, Crowder, L. B., Safina, C., Read, A. J.,

(2007), Comparing Effectiveness of Experimental and Implemented

Bycatch Reduction Measures: the Ideal and the Real, Conservation

Biology , Volume 21, Issue 5, October 2007, Pages: 1155–1164.

Croll, Donald A., Clark Christopher, W., Calambokidis, John, Ellison, William T.,

Tershy, Bernie R. (2001), Effect of anthropogenic low-frequency noise on the foraging ecology of Balaenoptera whales, Animal Conservation (2001)

4, 13–27.

Dalton, Rex, (2003), Court ruling sounds note of caution for sonar system, Nature

Vol 425 4 September 2003. |

David J.A., (2006) Likely sensitivity of bottlenose dolphins to pile-driving noise,

WATER AND ENVIRONMENT JOURNAL, Volume 20, Issue 1, March

2006, Pages: 48–54.

DeRuiter, Stacy L., Boyd, Ian L., Claridge, Diane E., Clark, Christopher W., Gagnon,

Chuck, Southall, Brandon L. Tyack, Peter L., (2013), Delphinid whistle production and call matching during playback of simulated military sonar,

Marine Mammal Science , Volume 29, Issue 2, April 2013, Pages: E46–

E59.

15

Dolman, Sarah J., Weir, Caroline R., Jasny, Michael, (2009) , Comparative review of marine mammal guidance implemented during naval exercises, Marine

Pollution Bulletin 58 (2009) 465–477.

Dolman, Sarah J., Parsons, E.C.M., Wright, Andrew J., Cetaceans and military sonar:

A need for better management, Marine Pollution Bulletin Volume 63,

Issues 1–4, 2011, Pages 1–4.

Ellison W. T., Southall, B. L., Clark, C. W., Frankel, A. S.

, (

2011), A New Context-

Based Approach to Assess Marine Mammal Behavioral Responses to

Anthropogenic Sounds, Conservation Biology , Volume 26, No. 1, 21–28

C , 2011.

DIRECTIVE 2008/56/EC OF THE EUROPEAN PARLIAMENT AND OF THE

COUNCIL of 17 June 2008 establishing a framework for community action in the field of marine environmental policy (Marine Strategy

Framework Directive), Available online http://eurlex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2008:164:0019:0040:

EN:PDF, 20130511.

Evans, P. G. H., and Miller, L. A. (2004). Proceedings of the workshop on active sonar and cetaceans. European Cetacean Society Newsletter Special Issue

No. 42.

Finneran, J. J., Schlundt, C. E., Carder, D. A., Clark, J. A., Young, J. A., Gaspin, J.

B., och Ridgway, S. H. (2000). Auditory and behavioral responses of bottlenose dolphins (Tursiops truncatus) and a beluga whale

(Delphinapteras leucas) to impulsive sounds, resembling distant signatures of underwaterexplosions, J. Acoust. Soc. Am . 108, 417-431.

Finneran, J. J., och Jenkins, A. K. (2012). Criteria and Thresholds for U.S. Navy

Acoustic and Explosive Effects Analysis , SSC Pacific, USA, Report, s 64.

Götz, T., och Janik, V. M. (2010). Aversiveness of sounds in phocid seals: psycho- physiological factors, learning processes and motivation, J. Exp. Biol.

213, 1536-1548.

Götz, T., Janik, V.M., (2011), Repeated elicitation of the acoustic startle reflex leads to sensation in subsequent avoidance behaviour and induces fear conditioning. BMC Neurosci . 12 (30), 13.

Harris, R. E., Miller, G. W., Rochardson, W. J. (2001). Seal response to airgun sounds during summer seismic surveys in the Alaskan Beaufort Sea, Mar. Mamm.

Sci ., 17 (4), 795-812.

Hildebrand, J. A. (2004). Impacts of Anthropogenic Sound on Cetaceans,

IWC/SC/56/E13, USA, Report, s 32.

Hildebrand, J. A. (2009), Anthropogenic and natural sources of ambientnoise in the ocean, Mar. Ecol. Prog. Ser . 395, 5–20.

Hodgson, A. J., Marsh, Delean, H., S., Marcus, L., (2007) , Is attempting to change marinemammal behaviour a generic solution to the bycatch problem? A dugong case study, Animal Conservation 10 (2007) 263–273

Houser, Dorian S., Martin, Steve W., Finneran, James J., (2013), Exposure amplitude and repetition affect bottlenose dolphin behavioral responses to simulated mid-frequency sonar signals, Journal of Experimental Marine Biology and Ecology , Volume 443, May 2013, Pages 123-133.

Jefferson, Thomas A., Curry, Barbara E., (1996), Acoustic methods of reducing or eliminating marine mammal-fishery interactions: do they work?, Ocean &

Coastal Management , Volume 31, Issue 1, 1996, Pages 41-70.

16

Johansson, Torbjörn, (2012)

Lägesrapport för projektet ”FOI medverkan PoMM",

Totalförsvarets forskningsinstitut (FOI), Stockholm, Memo 4154, 2012-

10-25, (in swedish). Stockholm, Sverige, s 65. http://www.foi.se/ReportFiles/foir_3469.pdf.

Kastelein, R. A., Rippe, H. T., Vaughan, N., Schooneman, N. M., Verboom, W. C., och de Haan, D. (2000), The effects of acoustic alarms on the behavior of harbor porpoises (Phocoena phocoena) in a floating pen, Mar. Mamm. Sci .

16, 46-64.

Kastelein, Ronald A., Bunskoek, Paulien, Hagedoorn, Monique, (2002), Audiogram of a harbor porpoise (Phocoena phocoena) measured with narrow-band frequency-modulated signals. J. Acoust. Soc. Am . 112 (1), July 2002.

Kastelein, R.A., Jennings, N., Verboom, W.C., de Haan, D., Schooneman, N.M.,

(2006), Differences in the response of a striped dolphin (Stenella coeruleoalba) and a harbour porpoise (Phocoena phocoena) to an acoustic alarm, Marine Environmental Research 61, 363–378.

Kastelein, R. A., Verboom, W. C., Jennings, N., de Haan, D., och van der Heul, S.

(2008), The influence of 70 and 120 kHz tonal signals on the behavior of harbor porpoises (Phocoena phocoena) in a floating pen, Mar. Env. Res .

66, 319–326.

Kastelein, R. A., Steen, N., de Jong, C., Wensveen, P., och Verboom, W. C. (2011),

Effect of broadband-noise masking on the behavioral response of a harbor porpoise (Phocoena phocoena) to 1-s duration 6–7 kHz sonar up-sweeps,

J. Acoust. Soc. Am . 129(4), 2307-2315.

Kastelein, Ronald A., Hoek, Lean, Janssens, Griet, Gransier, Robin, Johansson,

Torbjörn,( 2013), Behavioral responses of harbor seals (Phoca vitulina) to sonar signals in the 25 kHz range. Submitted to Marine Environmental

Research

Kastelein, Ronald A., Hoek, Lean, Janssens, Griet, Gransier, Robin, Johansson, (

2013), Behavioral responses of harbor porpoise to sonar signals in the 25 kHz range, Submitted to Marine Environmental Research

Kumagai Jean, (2006), Drowning In Sound, IEEE Spectrum April 2006.

Kvadsheim, P. H., Sevaldsen, E. M., Scheie, D., Folkow, L. P., och Blix, A. S.

(2010), Effects of naval sonar on seals, Norwegian Defence Research

Establishment, FFI-rapport 2010/02222, 10 November 2010, ISBN 978-

82-464-1842-1, s26. http://rapporter.ffi.no/rapporter/2010/02222.pdf

Linnenschmidt, Meike, Teilmann, Jonas, Akamatsu, Tomonari, Dietz, Rune Miller,

Lee A., Biosonar, dive, and foraging activity of satellite tracked harbor porpoises (Phocoena phocoena), Marine Mammal Science , Volume 29,

Issue 2, April 2013, Pages: E77–E97.

McCarthy, Elena, Moretti, David, Thomas, Len, DiMarzio, Nancy, Morrissey,

Ronald, Jarvis, Susan, Ward, Jessica, Izzi, Annamaria, Dilley, Ashley,

(2011), Changes in spatial and temporal distribution and vocal behavior of

Blainville's beaked whales (Mesoplodon densirostris) during multiship exercises with mid-frequency sonar, Marine Mammal Science , Volume

27, Issue 3, July 2011, Pages: E206–E226

Melcón ML, Cummins AJ, Kerosky SM, Roche LK, Wiggins SM, Hildebrand JA.,

(2012), Blue whales respond to anthropogenic noise., PLoS One .

2012;7(2)

Miller, P.J.O., Biassoni, N., Samuels, A., Tyack, P.L.,( 2000), Whale songs lengthen in response to sonar. Nature 405, 903.

17

Miller, Patrick, Antunes, Ricardo, Alves, Ana Catarina, Wensveen, Paul, Kvadsheim,

Petter, Kleivane, Lars, Nordlund, Nina, Lam, Frans-Peter, van

Ijsselmuide, Sander, Visser, Fleur, Tyack Peter, (2011), The 3S experiments: studying the behavioural effects of naval sonar on killer whales (Orcinus orca), sperm whales (Physeter macrocephalus), and long-finned pilot whales (Globicephala melas) in Norwegian waters ,

Scottish Oceans Inst. Tech. Rept., SOI-2011-001

Mooney, T. Aran, Yamato, Maya, Branstetter, Brian K.,( 2012), Chapter Four -

Hearing in Cetaceans: From Natural History to Experimental Biology,

Advances in Marine Biology, Volume 63, 2012, Pages 197-246.

Naturvårdsverket (2011a). Åtgärdsprogram för tumlare 2008–2013, Rapport 5846 • augusti 2008. ISBN 978-91-620-5846-3.pdf, Stockholm, Sverige, s 63. http://www.naturvardsverket.se/Documents/publikationer/978-91-620-

5846-3.pdf (in swedish)

Naturvårdsverket (2011b). Knubbsäl, Phoca vitulina, EU-kod: 1365. Vägledning för svenska arter i habitatdirektivets bilaga 2 , NV-01162-10. Stockholm,

Sverige, s10. http://www.naturvardsverket.se/upload/stod-imiljoarbetet/vagledning/natura-2000/arter/ryggradsdjur/vl_knubbsal.pdf

(in swedish)

Naturvårdsverket (2011c). Gråsäl, Halichoerus grypus, EU-kod: 1364. Vägledning för svenska arter i habitatdirektivets bilaga 2 , NV-01162-10. Stockholm,

Sverige, s 8. http://www.naturvardsverket.se/upload/stod-imiljoarbetet/vagledning/natura-2000/arter/ryggradsdjur/vl_grasal.pdf (in swedish)

Naturvårdsverket (2011d). Vikare, Phoca hispida, EU-kod: 1938. Vägledning för svenska arter i habitatdirektivets bilaga 2, NV-01162-10. Stockholm,

Sverige, s 8. http://www.naturvardsverket.se/upload/stod-imiljoarbetet/vagledning/natura-2000/arter/ryggradsdjur/vl_vikare.pdf(in swedish)

Nedwell J.R., Edwards B., Turnpenny A.W.H., Gordon J.,(2004), Fish and Marine

Mammal Audiograms: A summary of available information,

Subacoustech Report ref: 534R0214, http://www.subacoustech.com/wpcontent/uploads/534R0214.pdf

Norman, S. A., Raverty, S., McLellan, B., Pabst, A., Ketten, D., Fleetwood, M.,

Gaydos, J. K., Norberg, B., Barre, L., Cox, T., Hanson, B., och Jeffries, S.

(2004), Multidisciplinary investigation of stranded harbor porpoises

(Phocoena phocoena) in Washington State with an assessment of acoustic trauma as a contributory factor (2 May–2 June 2003), U.S. Dep.

Commerce, NOAA Tech. Memo. NMFSNWR-34, s

120.http://docs.lib.noaa.gov/noaa_documents/NMFS/TM_NMFS_FNWR/

TM_NMFS_FNWR_34.pdf

OSPAR, (2009). Overview of the impacts of anthropogenic underwater sound in the marine environment , OSPAR rapport, s 134. http://www.ospar.org/documents/dbase/publications/p00441_noise%20ba ckground%20document.pdf

Parsons, E.C.M., Dolman, Sarah J., Wright, Andrew J.,. Rose, Naomi A, Burns,

W.C.G., Navy sonar and cetaceans: Just how much does the gun need to smoke before we act?, Marine Pollution Bulletin , Volume 56, Issue 7,

July 2008, Pages 1248-1257.

18

Shapiro Ari D., Tougaard Jakob, Jørgensen Poul Boel, Kyhn Line A., Dalgaard Balle

Jeppe, Bernardez Cristina, Fjälling Arne, Karlsen Junita , Wahlberg

Magnus,( 2009), Transmission loss patterns from acoustic harassment and deterrent devices do not always follow geometrical spreading predictions,

Marine Mammal Science , Volume 25, Issue 1, January 2009, Pages: 53–

67,

Sigg, Robert, Utvärdering av stödverktyg för riskuppskattning vid användning av aktiv sonar . Totalförsvarets forskningsinstitut (FOI), Stockholm, 2012.

FOI-R--3505-SE. (in swedish)

Sivle LD, Kvadsheim PH, Fahlman A, Lam FP, Tyack PL, Miller PJ., (2012),

Changes in dive behavior during naval sonar exposure in killer whales, long-finned pilot whales, and sperm whales., Front Physiol . 2012;3:400.

Soto, Natacha Aguilar, (2006), does intense ship noise disrupt foraging in deep-diving cuvier’s beaked whales(ziphius cavirostris)?

Marine Mammal Science,

22(3): 690–699 (July 2006)

Southall, B. L., Bowles, A. E., Ellison, W. T., Finneran, J. J., Gentry, R. L., Greene,

C. R., Jr., Kastak, D., Ketten, D. R., Miller, J. H., Nachtigall, P. E.,

Richardson, W. J., Thomas, J. A., och Tyack, P. L. (2007), Marine mammal noise exposure criteria: initial scientific recommendations,

Aquat. Mamm.

33, 411-521.

Teilmann, Jonas, Tougaard, Jakob, Miller, Lee A., Kirketerp, Tim, Hansen, Kirstin,

Brando, Sabrina,( 2006), Reactions of captive harbor porpoises (phocoena phocoena) to pinger-like sounds, Marine Mammal Science , Volume 22,

Issue 2, April 2006, Pages: 240–260,

Tyack, Peter L., Johnson, Mark, Soto, Natacha Aguilar, Sturlese, Albert, Madsen,

Peter T., (2006), Extreme diving of beaked whales, The Journal of

Experimental Biology 209, 4238-4253.

Tyack PL, Zimmer WM, Moretti D, Southall BL, Claridge DE, Durban JW, Clark

CW, D'Amico A, DiMarzio N, Jarvis S, McCarthy E, Morrissey R, Ward

J, Boyd IL., (2011), Beaked whales respond to simulated and actual navy sonar., PLoS One . 2011 Mar 14;6(3):e17009.

Weilgart, L S. (2006), The impacts of anthropogenic ocean noise on cetaceans and implications for management, Can. J. Zool . 85,

Wright AJ, Deak T, Parsons EC., (2011), Size matters: management of stress responses and chronic stress in beaked whales and other marine mammals may require larger exclusion zones., Mar Pollut Bull . 2011;63(1-4):5-9.

Zirbel, K., Balint, P., Parsons, E.C.M., Navy sonar, cetaceans and the US Supreme

Court: A review of cetacean mitigation and litigation in the US, Marine

Pollution Bulletin , Volume 63, Issues 1–4, 2011, Pages 40-48.

19

Download