IQOE Oceanography

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    R E G U L A R I S S U E F E A U R E

    AnInternational

    Quiet Ocean Experiment

    ABS RAC .Te effect o noise on marine li e is one o the big unknowns ocurrent marine science. Considerable evidence exists that the human contributionto ocean noise has increased during the past ew decades: human noise hasbecome the dominant component o marine noise in some regions, and noise isdirectly correlated with the increasing industrialization o the ocean. Sound is animportant actor in the lives o many marine organisms, and theory and increasingobservations suggest that human noise could be approaching levels at which negativeeffects on marine li e may be occurring. Certain species already show symptomso the effects o sound. Although some o these effects are acute and rare, chronicsublethal effects may be more prevalent, but are difficult to measure. We need toidenti y the thresholds o such effects or different species and be in a position topredict how increasing anthropogenic sound will add to the effects. o achieve suchpredictive capabilities, the Scientic Committee on Oceanic Research (SCOR) andthe Partnership or Observation o the Global Oceans (POGO) are developing anInternational Quiet Ocean Experiment (IQOE), with the objective o coordinatingthe international research community to both quanti y the ocean soundscape andexamine the unctional relationship between sound and the viability o key marineorganisms. SCOR and POGO will convene an open science meeting to gathercommunity input on the important research, observations, and modeling activitiesthat should be included in IQOE.

    made, anthropogenic noise in the oceanhas been increasing across much o the

    requency spectrum (Andrew et al.,2002; McDonald et al., 2008), and espe-cially at lower requencies (< 500 Hz;Frisk, 2007). Increases in noise romhuman activities add to the many naturalsources o sound in the ocean, such aswaves breaking, rain, and ice movement,and the sounds o the marine animalsthemselves (Figure 1). Given the spatialand temporal complexity and variabilityin all sound sources, the relative contri-bution o anthropogenic noise is notalways readily distinguishable.

    Te combined effects o temperatureand pressure in the deep ocean create asound channel by which acoustic wavescan be transmitted over large distances,sometimes hundreds o kilometers,and ofen much urther. Te complexpathways taken by this sound affect thenal received levels, but i they are aver-aged through time at the receiver, theyprovide an integrated signal dened bythe relative locations o all the sound

    1Te authors of this article were the attendees at a meeting, held at the University of Rhode Island from October 2729, 2010, to discuss the feasibility of conducting aexperiment to examine the effects of sound on life in the ocean.

    IN RODUC IONDoes the noise made by humans harmmarine li e? At present, we can offer onlypreliminary answers to this importantquestion, or only a ew species. We

    know that the ocean has become moreindustrialized and that the noise levelsassociated with human activities haveincreased (NRC, 2003). For example, inareas where measurements have been

    B Y I A N L . B O Y D , G E O R G E F R I S K , E D U R B A N , P E E R YA C K , J E S S E A

    S O P H I E S E E YAV E , D O U G C A O , B R A N D O N S O U H A L L , M I C H A E L W E I S E , R E X A

    O M O N A R I A K A M A S U , R E N D E K E L I N G , C H R I S I N E E R B E , D AV I D F

    R O G E R G E N RY, O M G R O S S , A N H O N Y H AW K I N S , F E N G H U A L I , K A H Y M E

    J A M E S H . M I L L E R , D AV I D M O R E I , C R I S I A N R O D R I G O , A N D O M I O S1

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    producers, the architecture o the oceanbasin, and the properties o the waterthrough which the sound has passed.It is sometimes possible to distinguishamong different sound sources based on

    sound characteristics.Humans introduce noise to the

    ocean through many different activities.Each source may have different effects,depending upon the requency range, itsintensity, and whether it is an intermit-tent, pulsed, or continuous sound. Someanthropogenic soundssuch as somemilitary sonars, seismic air guns usedextensively or oil and gas exploration,

    and pile drivingare both impulsiveand high intensity. Such sounds canelicit strong negative reactions, oreven physical injury, in some species,a concern that has led to higher levelso scrutiny or many o those sources.Recently, military sonars have been aparticular ocus o attention becauseo their association with the strandingo beaked whales (Cox et al., 2006).Nevertheless, the acute effects o sonarsupon beaked whales probably occur onlyrarely because the effects o sonars them-selves co-vary with other actors, such ascontext o the exposure (i.e., bathymetry,presence o sur ace temperature ducts,behavior, and number o naval vessels).Animal strandings are probably the mosteasily observed end point o a syndromeo behavioral responses to sound (Boydet al., 2007), leading through someunknown progression to physical harmand/or mortality. Tere is a strong suspi-cion, supported by increasing evidence,that a similar syndrome o reducedcapacity to per orm normal li e unctionsis present across a wide range o marine

    auna, including sh (Slabbekoorn et al.,2010) and marine mammals (Southall

    et al., 2007; yack, 2008).A major unanswered question is

    whether anthropogenic noise has asignicant impact on the tness oindividuals within populations that jeopardizes the viability o those popula-tions. Te US National Research Counciladdressed this question in its 2005report on marine mammal populationsand ocean noise (NRC, 2005), but theprinciples apply equally to all ormso marine li e. We reect this issuediagrammatically in Figure 2. Te NRCreport developed an approach known asPopulation Consequences o AcousticDisturbance (PCAD), which dened arationale or developing assessments othe signicance o sublethal effects and

    or identi ying the most important gapsin our knowledge. Our problem now isto dene the unctional relationships

    between behavioral or physiologicalresponses to sound and populationeffects that are required or this assess-ment process to work.

    Shipping is an important anthro-pogenic sound source (Wenz, 1962).Te volume o cargo transported bysea has been doubling approximatelyevery 20 years (http://www.marisec.org/shipping acts/worldtrade/volume-world-trade-sea.php ), resulting in an increasein anthropogenic sound. Although thesystematic measurement o sound inrelation to these changes is incomplete,the current estimate is that expandedshipping, which is directly correlatedwith increased global economic activity,has been accompanied by an increasein anthropogenic sound or requen-cies below 500 Hz (Frisk, 2007). Overthe past ew decades, the shipping

    Figure 1. Te hearing ranges of differentkinds of sh and mammals together withthe overlap in frequency with differentsources of human-generated noise.Modied from Slabbekoorn et al. (2010), copyright(2010), with permission from Elsevier

    H e a r i n g r a n g e s o f s h a n

    d m a m m a l s

    A n t h r o p o g

    e n

    i c n o

    i s e

    0.01 0.10 1 10 100 200Frequency (kHz)

    http://www.marisec.org/shippingfacts/worldtrade/volume-world-trade-sea.phphttp://www.marisec.org/shippingfacts/worldtrade/volume-world-trade-sea.phphttp://www.marisec.org/shippingfacts/worldtrade/volume-world-trade-sea.phphttp://www.marisec.org/shippingfacts/worldtrade/volume-world-trade-sea.phphttp://www.marisec.org/shippingfacts/worldtrade/volume-world-trade-sea.phphttp://www.marisec.org/shippingfacts/worldtrade/volume-world-trade-sea.php
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    contribution to ambient noise hasincreased by as much as 12 dB above thenatural background level in some loca-tions (Andrew et al., 2002; Hildebrand,2009). We also know that offshore oil

    and gas exploration and production, aswell as development o renewable energy,have expanded during the same period,as has the shing industry.

    DEFINING HE QUES IONSMany animals use sound in the ocean,either passively to listen and orient rela-tive to their surroundings, or actively asthey produce sound to communicate or

    to search or prey or or objects; in somecases, their use o sound is a byproducto other activity. Active use o sound isrelatively easy to detect, but passive useis not. It is likely that most multicellularmarine organisms use sound passivelyas a way o sensing the environment,

    including listening or prey and preda-tors, and changing behavior in relationto weather and obstacles (includingmoving ships or static propellers such asare proposed or tidal turbines). Te idea

    that animals may use something analo-gous to acoustic daylight (Buckinghamet al., 1992) to gain an image o theirsurroundings is gaining momentum,even i it is difficult to demonstrateempirically. Te properties o sound inwater and the low levels o light penetra-tion below the sur ace in many circum-stances mean that, or some species,sound is more important than light as

    the principal source o environmentalin ormation. Much evidence points tosound in the low requencies (< 1 kHz)being most important, except in thecases o some invertebrates (e.g., snap-ping shrimp) and marine mammals(dolphins, some whales, and seals) that

    have developed the capacity to both hearand, in some cases, produce complexsounds at much higher requencies (upto > 200 kHz in smaller cetaceans). Ourbasic knowledge o the way in which

    the majority o marine organisms sensesound and then respond behavior-ally to different sound stimuli is quiterudimentary or most species andgroups. Similarly, the extent to whichthe introduction o higher backgroundsound levels masks the ability o marineanimals to interpret sound signals romthe environment is largely unknown, asis their reaction to acute anthropogenic

    sounds in their vicinity.For example, we now know thatseveral species o whales have adjustedtheir communication calls in a mannerthat suggests they are raising their voices or otherwise changing their callsin order to be heard (e.g., Holt et al.,

    Ian L. Boyd ([email protected]) is Director, Scottish Oceans Institute and NERC Sea Mammal Research Unit, University of St. Andrews,Scotland, UK.George Frisk is Professor of Ocean and Mechanical Engineering, Florida Atlantic University, Dania Beach, FL, USA.Ed Urban

    is Executive Director, Scientic Committee on Oceanic Research, based at University of Delaware, Newark, DE, USA.Peter Tyack is SeniorScientist, Woods Hole Oceanographic Institution, Woods Hole, MA, USA. Jesse Ausubel is Vice President for Programs, Alfred P. Sloan

    Foundation, New York, NY, USA.Sophie Seeyave is Scientic Coordinator, Partnership for Observation of the Global Oceans, PlymouthMarine Laboratory, Plymouth, UK. Doug Cato is Principal Scientist, Marine Environment, Maritime Operations Division, Defence Science

    and echnology Organisation (DS O), Eveleigh, New South Wales, Australia.Brandon Southall is President, SEA, Inc., Aptos, CA, USA, andResearch Associate, Long Marine Laboratory, University of California, Santa Cruz, CA, USA.Michael Weise is Manager, Marine Mammals

    and Biological Oceanography Program, US Office of Naval Research, Arlington, VA, USA.Rex Andrew is Senior Engineer, Applied PhysicsLaboratory, University of Washington, Seattle, Washington, USA.Tomonari Akamatsu is Head, Bioacoustics Group, Fishing echnology

    and Information Science Division, National Research Institute of Fisheries Engineering, Fisheries Research Agency, Ibaraki, Japan.

    Ren Dekeling is manager of the research program on sound in the marine environment at Defence Materiel Organisation, Te Hague,Te Netherlands. Christine Erbe is Director, JASCO Australia, Brisbane, Queensland, Australia.David Farmer is Dean, Graduate School

    of Oceanography, University of Rhode Island, Narragansett, RI, USA.Roger Gentry is Consultant, ProScience Consulting, Dickerson,MD, USA.Tom Gross is Programme Specialist, Global Ocean Observing System for the Intergovernmental Oceanographic Commission,

    UNESCO, Paris, France.Anthony Hawkins is Owner, Loughine Ltd., Aberdeen, Scotland, UK.Fenghua Li is Professor and Deputy Director,Institute of Acoustics, Chinese Academy of Sciences, Beijing, China.Kathy Metcalf is Director of Maritime Affairs, Chamber of Shipping

    of America, Washington, DC, USA. James H. Miller is Professor of Ocean Engineering, University of Rhode Island, Narragansett, RI, USA.David Moretti is Principal Investigator, Chief of Naval Operations Marine Mammal Monitoring on Navy Ranges (M3R) Program, Naval

    Undersea Warfare Center (NUWC), Newport, RI, USA.Cristian Rodrigo is Oceanographer, Chilean Antarctic Institute, Punta Arenas, Chile.Tomio Shinke is Director, Research and Development Center, System Intech Co. Ltd. , okai University, Shizuoka, Japan.

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    Fitness effects leading tochanges in populations

    of sound producers and users

    2008; Parks et al., 2010). Tis Lombardeffect (Lombard, 1911) was originallyreported or humans, but it is also seenin terrestrial species such as birds thatuse sound in social activities (Lengagne,

    2008; Slabbekoorn et al., 2010). Tereis evidence that, in the presence ohigh levels o background sound, somespecies simply stop vocalizing, eitherbecause they are being disturbed orbecause, like humans trying to talk inthe presence o loud background noise,they give up because communicationbecomes ineffective. Acoustic maskingo marine mammal sounds by increased

    ambient noise is o particular concernin low- requency specialists, such as thelarge baleen whales (Clark et al., 2009).Although it is possible that whales couldbe especially sensitive (and we knowthat not all whale species share the samesensitivities), the presence o maskingand the Lombard effect leads to twoadditional questions: (1) are these generaleffects widespread among marine organ-isms and, (2) even i they are widespread,are they important to the unction andsurvival o viable populations?

    WHY SHOULD WE BE BO HEREDWI H NOISE IMPAC S ONMARINE ORGANISMS?Tis question is important or two mainreasons. Te rst is that the industrial-ization o the ocean is likely to increasein the next ew decades. A very largeproportion o the manu actured goodsand raw materials needed by a growingglobal economy is being shipped aroundthe world on the ocean. Te demand orhydrocarbons is also pushing explora-tion and production urther offshoreinto deep waters at continental sheledges. Energy extraction rom the ocean,

    although relatively small at present, isexpected to expand rapidly over thenext ew decades. In coastal areas, recre-ation is also bringing with it increasingnoise levels rom pleasure boats. Tere

    are real concerns that this process oexpanding industrialization and recre-ation will lead us in small steps towardan intolerable acoustic environment ormany marine organisms.

    It is vital that industrialists engagewith solving the problem. I they are notinvolved, the inexorable march o the

    precautionary principle will slowly butprogressively constrain their ability tooperate (Gillespie, 2007). Environmentalnongovernmental organizations withmissions to protect the marine environ-

    ment will drive the regulatory process.But, while precautionary approachesmay be inconvenient to many who havenarrow commercial interests, precautionin the ace o uncertainty is rationaland is an approach that is now deeplyembedded in the way that society oper-ates. Reducing uncertainty by increasing

    Figure 2. A diagrammatic view of the problem being investigated by the International Quiet OceanExperiment (IQOE), which denes three major sources of sound in the ocean: physical, biological,and anthropogenic. Te sounds involved in marine animal communication and echolocation can bemasked by physical and other biological sound sources. Communication is likely to have evolvedcope with this type of masking. However, overlaid on this soundscape is new noise added by humamarine animals may not be able to handle the additional masking to the same extent. Te characterisof the sound received by organisms (receivers) will determine responses that could cascade throuphysiological or behavioral effects that affect an animals ability to feed, migrate, and breed and thturn, may lead to changes in reproduction and survival of the individual. Relatively few physiologibehavioral responses will have a direct effect on populations, but increasing effects of sound couldmulate across individuals, thus pushing these effects gradually to population-level effects.

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    PREDIC ING SOUNDFIELDS AND MANAGINGNOISE BUDGE SEstablishing the global ocean sound-scape, with appropriate statistical consid-

    eration o spatial and temporal variance,is a necessary step toward predictingocean sound elds in particular loca-tions. Sound eld predictions can thenbe challenged with in situ measurements

    rom existing data collection sites, and aprocess o tuning the sound eld modelsto maximize the t to the empiricalobservations will eventually rene oceansoundscape descriptions.

    Predicting sound elds in thisway should also eed directly into theemerging processes or regulation ooffshore human activities and generalindustrial development. In both theUnited States and Europe, or example,legislation is moving rapidly to embracemarine spatial planning and to set stan-dards or noise production, principallyon a precautionary basis. But, availablein ormation is insufficient to build therationale or spatial management oindustrial activities to reduce potentialnoise impacts on sensitive species orhabitats. Characterization o sound-scapes on the global scale will enableregional administrations to downscalethe soundscapes to reect their ownneeds at regional and local scales and tohelp dene the kinds o threshold valuesthat managers ofen need in order to beable to set legally binding conditionson ocean use. Tis nested approach tomodel development and validation isnecessary because noise is a problemthat needs to be tackled initially at largescales because o the long-range propa-gation o low- requency sound. Evenlocal models need to have boundary

    conditions specied in order to buildlocal noise budgets; it is hoped thatIQOE will provide this capability.

    EXPLORA ION IN DEEP IME

    So, what was the global ocean likebe ore humans arrived? Many haveexplored this question with respect tothe removal o marine mammals andsh, in particular, but we also want toknow how noisy the ocean was in thepast. In other words, can we back-castthe ocean soundscape to a preindustrialera? Similarly, can we predict the oceansoundscape in the uture i current

    trends continue? Can we create a kind oKeeling curve or ocean noise (Keelinget al., 1976)? What is the cost-benettrade-off i regulations are set to reducethe sound produced by human activities?Questions such as these, though inter-esting in their own right, have most rele- vance i they are accompanied by robust

    unctional relationships between soundand the growth or decline o populationso marine organisms.

    Te challenge and opportunityo IQOE is to coordinate scienticactivities on the effects o ocean noiseon marine organisms internationally,whether conducted in the academic,governmental, or industry (e.g., JointIndustry Program) sectors. Developmento a body o knowledge that begins toilluminate types o responses to differentlevels o noise in the li e unctions oindividual organismssuch as changesin reproductive rate, growth rate, use ohabitat, survival rate, and social struc-tureis an essential part o the strategybeing adopted or this experiment. Tespecies that need to be included varyacross the ull range o marine organ-isms, but perhaps could ocus principally

    on some o the keystone or indicatorspecies within major, or important,ecological systems, as well as speciesalready recognized as endangered. Manyo the resulting effects studies will be

    small scale and in situ, and some may bepossible in controlled conditions in thelaboratory. However, all will need to bedesigned care ully, with controls and alswith a view to ensuring that the effectsobserved can be built into larger-scalestrategic models o effects at populationand ecological levels, such as the PCADmodel re erred to previously.

    WHERE, WHEN, WHO,AND HOW?IQOE is being developed under thesponsorship o the Scientic Committeeon Oceanic Research (SCOR) and thePartnership or Observation o theGlobal Oceans (POGO) as a potential joint project, with exploratory unding

    rom the Al red P. Sloan Foundation another sources. Trough this cooperation,IQOE aims to engage with the globaloceanographic community. Te intent oIQOE is to combine the talents o phys-ical oceanographers, acousticians, behavioral biologists, ecosystem modelers, andpopulation biologists.

    Although IQOE should have a globaloutreach, we oresee that specic sitesor regions will be used, either becausethey provide extreme examples o loca-tions where sound is likely to have largeimpacts, or because they are particularlyquiet and undisturbed by sound. Wepropose paying specic attention to areawhere relatively rapid changes in indus-trial activity are occurring or are likely,in order to assess and identi y changes iboth the soundscapes and responses inmarine biota in a comparative way.

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    IQOE provides a mechanism orocusing and coordinating existing

    activity. We recognize, or example, thatthe plans or construction o offshorewind arms in the North Sea represent

    an opportunity to observe and possiblyto carry out experiments on the effectso percussive noise rom pile driving.Tese types o in situ studies could be animportant part o the IQOE approach. Insome circumstances, planned shutdowno sound sources will add to the knowl-edge gained rom studies that examineanimal distribution and abundancebe ore, during, and afer disturbance

    events. Tere are also some very capabledeep ocean laboratories available or

    conducting experiments on the effectso sound, mainly in the orm o navalunderwater test ranges that have exten-sive arrays o acoustic sensors. Some othese acilities have already been used or

    innovative experimental studies on theeffects o sound on beaked whales.

    Te idea o experimentally shuttingdown anthropogenic sound sourcesand observing the effects was a centraldriver or IQOE development (Ausubel,2009). Recognizing that marine noisehas been increasing, experimentalapproaches to examining the effects osound need to involve the reduction, or

    removal, o anthropogenic sound as wellas the introduction o increased sound.

    However, as the space and time scalesget larger, the idea o reducing anthro-pogenic sound sources gets increasinglydifficult. Figure 3 depicts this trade-offbetween the capacity to carry out experi-

    mental manipulations and the size o thetemporal and spatial scales involved, andit shows the matrix o different experi-mental designs and time scales along agradient o increasing difficulty. In act,to shut down all human activity in theocean or only one daywhich would bebarely long enough or the sound ringingaround on the ocean to dissipatecouldhave a nancial cost o more than

    $10 billion. So, IQOE will ocus uponmore modest objectives or experimental

    Figure 3. Matrix of quieting feasibility. Te difficulty and nancial cost of a shutdown of noise sources increases from left toright in the matrix. Te feasible time that a noise shutdown could be accomplished decreases from left to right (orange row).Different experimental activities (blue row) might be possible at different spatial scales (green row). Te goal of IQOE would beto conduct activities at many different scales. Te relationship of the different temporal and spatial scales means that the mostfeasible approaches are likely to be several experiments carried out over long durations at small scales (i.e., toward the left of thediagram). wo roles that IQOE will play will be (1) to help reduce the difficulty of experiments from left to right in this diagram, and(2) to coordinate experiments of the type dened to the left of the diagram so that they will combine to deliver some of the benetsthat would emerge if we were able to carry out experiments lying to the right of the diagram.

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    manipulation. Tese objectives will carryeven more weight i the results can ndgeneral application through the parame-terization and/or validation o the globalsound eld model.

    IQOE should also drive technologyinnovation. Smaller instruments withgreater data storage and transmissioncapacity would allow sound measure-ment to become more routine and avail-able to a broader range o researchers ataffordable prices. In addition, properlypromoted, investigation o the ve-dimensional world o ocean soundthethree spatial dimensions plus time and

    the requency dimension (pitch)willbring a new depth o understanding tothe lives o people who may never havelooked at the ocean in this way be ore.

    SCOR and POGO will continueto develop the IQOE idea with anAugust 30September 1, 2011, openscience meeting (see http://www.IQOE-2011.org) to ensure broad input rom theacoustic and oceanographic communi-ties and to enable creation o a scienceplan or an international research projecton sound in the ocean. Tis plan willbuild on the work reported in Boyd et al.(2008) and NRC (2003, 2005). Te issueo sound in the ocean deserves to beadded to the list o global changes thatare monitored and studied.

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