Evolutions in Marine Mammal Noise Exposure Criteria

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Evolutions in Marine Mammal Noise Exposure Criteria
FEATURED ARTICLE

Evolutions in Marine Mammal Noise
         Exposure Criteria
                                               Brandon L. Southall

Foreword: The work summarized here represents the col-         “toothed” whales, dolphins, and porpoises (odonotocetes;
lective efforts of an international, interdisciplinary group    see bit.ly/3dfFYNv); the sirenians (manatees and dugongs;
of scientific experts to address potential underwater sound     see bit.ly/3fnKxs2); the amphibious pinnipeds (true seals,
impacts on marine mammals. The original group included          sea lions, and walrus; see bit.ly/2QB06SD); and other
Roger Gentry (who conceived of and convened the origi-          marine carnivores (otters and polar bears). Marine mam-
nal panel), Ann Bowles, William Ellison, James Finneran,        mals are exposed to diverse impulsive, continuous, and
Charles Greene Jr., David Kastak, Darlene Ketten, James         intermittent noise sources. This ever-changing situation
Miller, Paul Nachtigall, John Richardson, Brandon South-        creates myriad challenges for deriving comprehensive,
all, Jeanette Thomas, and Peter Tyack. Colleen Reichmuth,       empirically based exposure criteria for such a breadth
Doug Nowacek, and Lars Bejder were added subsequently.          of species and their potential risk from different sources.
All of these individuals contributed substantively to the       Extensive data gaps remain in many key areas, some of
evolving criteria for marine mammal noise exposure              which (e.g., direct measurements of auditory effects of
described herein.                                               noise for baleen whales) are difficult to envision ever fill-
                                                                ing. However, great progress has been made by a large and
Marine Mammal Noise Exposure Criteria:                          growing community of scientists working on these issues.
Emerging Needs
More than half a century ago, concerns were raised          Some species appear particularly sensitive to acoustic dis-
about the potential for human industrial noise to mask      turbance, including beaked whales (see bit.ly/3d9Tu5m)
whale communication (Payne and Webb, 1971). In the          that have stranded following exposure to military mid-
ensuing decades, multiple, increasingly complex tech-       frequency sonar (e.g., D’Amico et al., 2009). Events in
nological and scientific approaches have been developed     Greece, the Bahamas, Canary Islands, and other locations
to assess whether and how human noise can negatively        fueled awareness of how noise can harm marine mam-
affect ocean wildlife. In national jurisdictions and inter- mals (Ketten, 2014). Increasing attention and ensuing legal
national agreements, threatened and endangered species,     battles led to more and broader research efforts to obtain
which include most marine mammals, are often afforded       a better scientific basis for regulatory oversight and legal
legal protections intended to mitigate the noise impacts    compliance. Scientists now recognize that rare, yet dra-
of human activities. Much research has thus centered        matic and potentially locally important, stranding events
on marine mammals. Fair or not, “charismatic mega-          are just one among many potential effects of human noise.
fauna” also garner more public attention than other taxa,   Equally serious effects may parallel those seen for humans
although recent trends are broadening consideration to      and land mammals, such as noise-induced hearing losses,
fishes and invertebrates (e.g., Hawkins et al., 2015).      behavioral disturbances, communication disruption or
                                                            masking, and physiological stress (see Southall, 2017).
Marine mammals are a taxonomically and ecologically There is also the challenge, given the diversity of species
diverse aggregation of species, inhabiting coastal and open and their hearing abilities, that sounds that are noisome to
ocean waters from pole to pole. (For an excellent over- one species may be irrelevant or even inaudible to another.
view of marine mammals and sound, see www.dosits.org.)
They include the fully aquatic cetaceans, composed of Researchers and regulatory agencies have grappled for
large baleen whales (mysticetes; see bit.ly/3fpPOz8); the decades with the complexities of establishing “thresholds”

52   Acoustics Today • Summer 2021 | Volume 17, issue 2                ©2021 Acoustical Society of America. All rights reserved.
                                                                                           https://doi.org/10.1121/AT.2021.17.2.52
Evolutions in Marine Mammal Noise Exposure Criteria
for different effects of noise on marine mammals. Given
the evolving requirements, focus shifted from merely
documenting hearing to developing science-based noise-
exposure criteria. One such endeavor by the United States
National Marine Fisheries Service (NMFS) led to an expert
panel formed in 2003 to establish quantitative criteria for
auditory and behavioral effects. The resulting publication
(Southall et al., 2007) derived marine mammal noise-
exposure criteria, a first for any nonhuman mammalian
group. Innovations included the derivation of (1) species
groups based on hearing abilities rather than exclusively
taxonomy; (2) group- and frequency-specific auditory-              Figure 1. A harbor seal (Phoca vitulina) positioned at a listening
weighting functions; (3) temporary and permanent                   station within a hemianechoic chamber during a behavioral
threshold shift (TTS and PTS, respectively) onset levels;          hearing test. When the subject hears a test signal, it leaves
and (4) a descriptive spectrum of behavioral response              the station and presses a response paddle indicating it heard
severity from benign to lethal.                                    the signal. Photograph courtesy of D. Wharton, taken under
                                                                   National Marine Fisheries Service (NMFS) permit #14535.
Although an important step, the panel acknowledged
limitations to its conclusions, including the omission
of some species, simplistic approximation of hearing             mammal hearing and the effects of noise research in key
filters, lack of quantitative behavioral response criteria,      areas, thanks in part to earlier calls for targeted research.
and extensive assumptions and extrapolations underlying          These include experimental studies of hearing and TTS in
many predictions. The paper therefore included a sub-            controlled, laboratory settings like the trained harbor seal
stantial section on needed research in specific areas to         performing a behavioral hearing test (Figure 1).
address data gaps that would improve the criteria.
                                                                 Finneran (2016) provided a major step forward by develop-
National and international concerns and calls for action         ing a quantitative means of integrating hearing and TTS to
concerning ocean noise have not abated (see Chou et al.,         derive group-specific audiograms, auditory-weighting shapes,
2021) and new research continues to accumulate on both           and exposures predicted for different levels of TTS to occur.
the acute and cumulative effects of noise on marine species      Finneran’s approach retained the fundamental aspects of
(e.g., National Academies of Sciences and Medicine [NAS],        Southall et al. (2007), including the use of hearing groups,
2017; Southall, 2017). A decade after the initial panel, suf-    discrete criteria for impulsive and nonimpulsive exposures,
ficient new data were available to reassess exposure criteria.   multiple-exposure metrics, methods for estimating PTS onset
The expert panel was reassembled with added expertise,           (where direct measurements remain absent), and precaution-
resulting in three subpanels: (1) auditory impacts, (2)          ary approaches for taxa lacking direct hearing measurements
behavioral responses, and (3) impulsive noise categoriza-        (e.g., baleen whales). After a long progression of efforts to
tion. The remainder of this article summarizes progress          develop regulatory guidance that began during the process
and remaining data gaps in each area as well as two recent       leading up to Southall et al. (2007), the United States National
papers on associated topics (Southall et al., 2019a, 2021).      Oceanic and Atmospheric Administration (NOAA) largely
                                                                 adopted Finneran’s (2016) recommendations as the basis of
Hearing and Auditory Effects                                     their regulatory guidance on hearing effects (NMFS, 2016).
The Southall et al. (2007) noise-exposure criteria spurred
a number of follow-on assessments either adapting earlier        The current iteration of the noise-criteria panel subsequently
approaches within new quantitative approaches (Finneran,         presented updated marine mammal noise-exposure criteria
2016) or proposing alternate methods (e.g., Tougaard et          (Southall et al., 2019a), using the quantitative approach of
al., 2015). The original panel, augmented with additional        Finneran (2016) as a foundation. Southall et al. provides
experts, agreed to a broad reassessment of exposure criteria,    group-specific audiograms for most taxa and auditory-
given the substantial increase in scientific data on marine      weighting functions (filters). Examples of these functions

                                                                                             Summer 2021 • Acoustics Today          53
Evolutions in Marine Mammal Noise Exposure Criteria
NOISE EXPOSURE CRITERIA

                                                              how what is known about the functional anatomy relative
                                                              to proposed hearing groupings, underscoring remaining
                                                              data gaps, and suggesting potential new directions.

                                                              For example, Southall et al. (2019a) proposed the addi-
                                                              tion of two cetacean groups, segregating baleen whales
                                                              into “very low” and “low-frequency” categories and
                                                              denoting the largest of the toothed odontocetes (killer
                                                              whales [Orcinus orca]; see bit.ly/31mpBsX), sperm
                                                              whales (Physeter macrocephalus; see bit.ly/3lXzkiZ), and
                                                              beaked whales (family Ziphiidae; see bit.ly/3d9Tu5m) as
                                                              a new “mid-frequency” group. The remaining odontoce-
                                                              tes then comprise “high” and “very high frequency” groups.
                                                              These developments were regarded as a justified deviation
                                                              from the groups adopted by NMFS (2016), but they were
                                                              not made lightly. Substantial data gaps were identified, but
                                                              the new groupings were nevertheless proposed based on the
                                                              comprehensive integrated assessment of all forms of avail-
 Figure 2. Estimated underwater group audiograms. Top;        able data. Furthermore, the overall process led Southall et
 group estimates (black lines) from individual measurements   al. (2019a) to further research recommendations in emerg-
 (gray lines). Auditory-weighting functions (bottom) for      ing fields, including TTS growth rates, anatomical and
 phocid (true seal) marine carnivores in water (PCW; solid    functional modeling approaches (e.g., Tubelli et al., 2018),
 line) and other marine carnivores in water (OCW; dashed      and self-mitigation from intense exposure events whereby
 line). From Southall et al., 2019a, with permission.         animals reduce hearing sensitivity before anticipated noise
                                                              events (Nachtigall and Supin, 2015).

for the true (phocid) seals and other marine carnivores are   As intended by Southall et al. (2007), these recent develop-
shown in Figure 2.                                            ments represent subsequent steps in what will continue to
                                                              be an evolving, challenging, and extensive journey. Future
The resulting group- and frequency-specific hearing,          noise-exposure criteria for marine mammals should con-
frequency weighting, and TTS onset functions are quan-        tinue to evolve, incorporating new minds and new science
titatively identical to those for species groups considered   in this fast-moving field and considering effects not yet
in Finneran (2016) and adopted by the NMFS (2016).            considered, such as auditory masking and nonauditory
However, Southall et al. (2019a) offered several substan-     physiological effects (e.g., increases in stress hormones
tive additions and is in a peer-reviewed publication rather   and associated impacts on the immune or other systems).
than an unpublished guidance document specific to regu-
lations and subject to the politics of one nation.          Behavioral Response Severity
                                                            Another subgroup of the new panel addressed behavioral
For instance, only underwater noise was addressed by responses to noise on marine mammals, building from the
the NMFS (2016), whereas Southall et al. (2019a) con- earlier severity assessments in Southall et al. (2007). Consid-
sidered both airborne and underwater hearing impacts erations for this group were fundamental differences in the
for amphibious marine mammals. Furthermore, South- nature and severity of the behavioral effects of noise in captive
all et al. comprehensively reviewed the available data on and field settings, how effects can be studied for individuals
hearing and the auditory effects of noise, with additional and populations, and how best to evaluate the rapidly expand-
insight from auditory anatomy and sound commu- ing literature in this area (Southall et al., 2021).
nication. The extensive, integrated data syntheses are
included as detailed appendices, summarizing relevant Regulators have long sought and, in some cases, applied a
information for each marine mammal species, clarifying simple, overarching step-function threshold (i.e., 160 dB)

54   Acoustics Today • Summer 2021
Evolutions in Marine Mammal Noise Exposure Criteria
below which no behavioral response is assumed and above           and applying novel analytical concepts on a strategic subset
which responses would occur for all individuals. More             of a vast and growing literature. The need for more system-
recent efforts have considered exposure-response proba-           atic, standardized data in behavioral response studies is
bilistic functions. Neither a step-function threshold nor a       highlighted, along with key variables to describe subject- or
single probabilistic function was provided by Southall et         group-specific metadata (e.g., behavioral state, group size),
al. (2007) or appears in Southall et al. (2021) because of        exposure contextual variables (e.g., spatiotemporal features,
the well-documented variance in responses across spe-             exposure novelty), and acoustic exposure metrics (e.g., dura-
cies, sound types, and exposure contexts (see Ellison et al.,     tion, rise time, sound pressure and sound exposure levels).
2012; Southall, 2017). There is simply no single overarching      A major conclusion is that meta-analyses integrating results
applicable level or function spanning all species and expo-       across studies will be strengthened where such data are sys-
sure types. The situation is not, however, intractable; it just   tematically collected and reported.
requires more nuanced, evidence-based, and context- and
group-specific means of predicting response probability.        For captive animals, an assessment of response severity
                                                                based on Southall et al. (2007) is proposed with more
Southall et al. (2021) proposes novel, distinct approaches explicit consideration of conditioning, habituation, and
for deriving probabilistic response functions within the very potential physiological effects. For free-ranging animals,
different contexts for free-ranging marine mammals and however, Southall et al. (2021) propose a fundamen-
those in captivity. For field conditions, sound sources were tally different approach. Although similarly identifying
distinguished not by impulsive or nonimpulsive features but progressively severe response categories, Southall et
rather by practical, real-world categories (active sonar, seis- al. propose three explicit parallel tracks (see Figure 3)
mic surveys, continuous/industrial noise, and pile driving). for behaviors associated with the vital functions of sur-
Southall et al. (2021) is largely methodological, proposing vival (e.g., resting, navigation, defense), feeding (e.g.,

 Figure 3. Behavioral response severity spectrum. Examples of observable responses are shown for behaviors relating to survival,
 feeding, and reproduction in categories of increasing presumed severity (0-9). Severity assessments such as these have been used
 in systematic expert elicitation of behavioral response severity in noise-exposure studies. From Southall et al., 2021.

                                                                                            Summer 2021 • Acoustics Today      55
Evolutions in Marine Mammal Noise Exposure Criteria
NOISE EXPOSURE CRITERIA

search, consumption, energetics), and reproduction (e.g.,based on methods developed by Samuels et al. (2000) for
mating, parenting). This framework is less qualitatively assessing longer term disturbance from wildlife tourism
descriptive of discrete responses and more focused on    was presented as a potential starting point, but further
expected longer term and ultimately population-level     development is needed. Insightful long-term studies are
consequences of responses affecting these vital functions.
                                                         providing critical measurements for how short-term
Southall et al. (2021) applies the new assessment method responses may or may not manifest in population-level
to a subset of studies in each of the four specified noise
                                                         consequences (e.g., Thompson et al., 2013). Efforts to
types using multiple independent observers.              link response studies and probabilities to energetic and
                                                         ultimately to the population consequences of distur-
This assessment demonstrates a high degree of con- bance offer important new insights and lessons for future
currence among assessors for studies where individual behavioral response studies (Pirotta et al., 2021). Finally,
responses to acute noise exposures were directly mea- major analytical advances are beginning to address the
sured and individually reported. This includes daunting challenges of multiple, interacting stressors and
increasingly complex controlled-exposure experi- behavioral and physiological effects (e.g., NAS, 2017).
ments using advanced tag sensors deployed on marine
mammals that measure fine-scale movement, sound “Impulsive” Exposure Criteria and
production, and noise exposure (see Figure 4). Such Sound Propagation
studies are providing novel, high-resolution data on Impulsive and nonimpulsive sounds have different audi-
acute responses, with more of the comprehensive subject, tory and behavioral effects. This is expected given what is
acoustic, and exposure contextual metrics required for known about the auditory systems of mammals, includ-
behavioral criteria (Southall et al., 2016, 2019b).      ing marine mammals (e.g., Finneran., 2015). However,
                                                         significant data limitations still exist in terms of under-
Southall et al. (2021) also conclude that fundamentally standing the physical features that cause impulsive
new perspectives on behavioral-response criteria for exposures to have greater auditory effects at comparable
data obtained on broader spatial and temporal scales are exposure levels. These differences have long been suffi-
needed. Their revised response-severity spectrum was ciently clear. Southall et al. (2007) established the need
limited in considering scenarios (and some well-designed for this distinct source categorization for marine noise
studies) where sustained or repeated disturbance occurs sources and it continues in the recent criteria (Southall
for many animals. A structured synthesis approach et al., 2019a).

                                                                   This distinction typically considers parameters associated
 Figure 4. Rissos dolphins (Grampus griseus) in a behavioral-      with the level of “impulsiveness” (e.g., rise time, crest
 response study. The gold tag affixed to the lead animal has       factor, kurtosis) measured in the near vicinity of the
 archival fine-scale movement and high bandwidth passive           source. Southall et al. (2007) categorized discrete events
 acoustic sensors. Photograph courtesy of A. Friedlaender, taken   such as an explosions or sonic booms as “single pulses,”
 under NMFS permit #19116.                                         repeated seismic airgun shots and pile strikes as “multiple
                                                                   pulses,” and continuous sounds like vessels, drilling, and
                                                                   many sonars as “nonpulses.”

                                                                   Of course, sound propagation alters the extent to which
                                                                   impulsive signals retain those characteristics at distant
                                                                   receivers. Southall et al. (2007) initially categorized noise
                                                                   sources by source features given the lack of direct audi-
                                                                   tory data for meaningful distinctions, particularly in light
                                                                   of variable acoustic interactions occurring over space,
                                                                   time, and spectra. This was a precautionary approach
                                                                   driven by data limitations and practical complexity. More
                                                                   protective (lower effect onset levels) impulsive criteria

56   Acoustics Today • Summer 2021
were recommended for impulsive noise, regardless of             threshold be used for marine mammals, noting the general
propagation distance.                                           consistency from a study in one species (harbor porpoise;
                                                                see bit.ly/31oncy2) using recorded pile-driving noise at
This oversimplification led to practical challenges and a single kurtosis level (Kastelein et al., 2016) that yielded
unintended consequences for both those establish- TTS results for harbor porpoises similar to those predicted
ing and enforcing regulations and for those seeking to by the impulse criteria from Southall et al. (2019a). Finally,
comply with them. For instance, it proved difficult to based on these assumptions and assessments, Martin et
effectively categorize certain rapid-onset sonar signals. al. (2020) postulated that propagation-related changes for
Additionally, when onset criteria levels were applied to signals are effectively not relevant considerations in a real-
relatively high-intensity impulsive sources (e.g., pile driv- world application.
ing), TTS onset was predicted in some instances at ranges
of tens of kilometers from the sources. In reality, acous- Although providing new data on propagation effects,
tic propagation over such ranges transforms impulsive developing novel applications of existing concepts,
characteristics in time and frequency (see Hastie et al., and proposing several testable hypotheses, Martin et
2019; Amaral et al., 2020; Martin et al., 2020). Changes al. (2020) is arguably overreaching and consequently
to received signals include less rapid signal onset, longer potentially misleading. At present, there are no properly
total duration, reduced crest factor, reduced kurtosis, and designed, comparative studies evaluating TTS for any
narrower bandwidth (reduced high-frequency content). marine mammal species with various noise types, using
A better means of accounting for these changes can avoid a range of impulsive metrics to determine either the
overly precautionary conclusions, although how to do best metric or to define an explicit threshold with which
so is proving vexing. Several recent studies address this to delineate impulsiveness. More substantial research
issue, which was taken up by a noise sources subgroup similar to that in human studies (Hamernik, 2010) for
of the reassembled criteria panel.                              multiple species in controlled conditions is needed to
                                                                support such explicit conclusions.
Hastie et al. (2019) evaluated field recordings of seismic
airguns and pile-driving at different ranges and compared Such studies should be conducted under testing condi-
received parameters (rise time, peak pressure and duration tions involving more realistic presentation of stimuli than
interactions, duration, and crest factor). They found range- can be achieved in traditional laboratory settings. The
dependent changes and that signals generally began to lose most needed relevant studies would avoid artificial near-
impulsive characteristics at ranges of several kilometers, field, highly reverberant testing contexts. These are often
especially beyond 10 km. However, they noted that the associated with the use of a scaled source projector very
lack of direct hearing data precluded determining the most close to the animals, intending to simulate high-intensity
appropriate metric(s) for defining impulsiveness.               sources by matching received levels at some presumed
                                                                range. This does not account for range-induced changes
Martin et al. (2020) suggested a novel effective quiet calcu- in spectral and temporal features. The most appropriate
lation to compare accumulated exposures to group-specific environments for such studies are arguably less reflec-
TTS onset estimates. After calculating crest factor, kurto- tive open ocean conditions and with full-scale projectors
sis, and the Harris impulse factor (applied by Southall et located at several to tens of kilometer ranges over which
al., 2007) for noise exposures measured or estimated at these potential transitions may be occurring. However,
variable ranges, Martin et al. (2020) compared values with such studies are challenging to conduct, especially for
those associated with residual auditory effects in humans multiple individuals and species, and the desired data
and some terrestrial mammals. They concluded that kurto- may thus be unavailable for some time.
sis (see Qiu et al., 2020) is the most appropriate indicator of
impulsiveness for their scenarios but similarly note the lack Although the predictions of Martin et al. (2020) may
of direct supporting empirical data in marine mammals. ultimately be validated for marine mammals, a sim-
Martin et al. (2020) further proposed a kurtosis threshold pler interim approach is possible. Namely, members of
for distinguishing impulsiveness using auditory studies in the noise sources subgroup noted that the presence of
humans (Hamernik et al., 2010). They suggested that this high-frequency noise energy could be used as a proxy

                                                                                     Summer 2021 • Acoustics Today    57
NOISE EXPOSURE CRITERIA

for impulsiveness. A high-stimulus bandwidth is corre-          possible) to use different spectral bands as proxies for
lated to some degree with most, if not all, the impulsive       impulsiveness for different groups. But although there
features that have been identified in prior studies, includ-    are extensive acknowledged data limitations, as a simple,
ing kurtosis, crest factor, and rise time. Put simply, it is    tractable, interim measure, the presence of noise energy at
difficult to generate a stimulus that has a relatively high     10 kHz and higher could be applied. Practically speaking,
kurtosis, high crest factor, or rapid signal onset that lacks   the range at which noise from an impulsive source lacks
high-frequency spectral content.                                discernable energy (relative to ambient noise at the same
                                                                location) at frequencies ≥ 10 kHz could be used to distin-
Price (1983) demonstrated that the correspondence               guish when the relevant hearing effect criteria transitions
between the spectra of a finite transient impulse and           from impulsive to nonimpulsive.
hearing sensitivity can effectively predict human thresh-
old shifts. Studies of chinchillas using impulsive stimuli      To be clear, measurements of noise exposure at various
demonstrate similar auditory and physiological relation-        ranges should continue to be made, ideally including
ships related to noise spectrum (e.g., Ahroon et al., 1996).    the suite of impulsive metrics measured and considered
Although we lack such measurements for marine mam-              by Martin et al. (2020). Kurtosis is clearly a useful and
mals, the conceptual basis of auditory weighting and            insightful metric that should continue to be obtained in
exposure functions is that auditory effects are likely and      real-world measurements. The suggestion here is simply
occur at the lowest exposure levels at frequencies where        to use a readily quantifiable broadband measurement
the hearing is most sensitive (Figure 4) (Finneran, 2015).      of spectral energy without distinguishing a specific
Presuming that the absence of high-frequency energy is a        impulsive metric and threshold that cannot at present
reasonable proxy for reduced impulsiveness for multiple         be sufficiently prescribed. This approach could also yield
metrics, evaluating how spectral content changes from           directly testable predictions using currently available
source to receiver could provide insight into which criteria    experimental scenarios. Field recordings of impulsive
(impulsive or nonimpulsive criteria) is more appropriate.       (near-source) noise obtained at ranges where the prop-
                                                                agation effects have occurred have yielded insightful
We are confident that there are broad differences in hear- results when in laboratory hearing studies (e.g., Sills et
ing across the frequency spectrum for different marine al., 2017). A comparable paradigm could be applied for
mammal groups. These may result in differences in whether laboratory TTS studies using impulsive noise recorded at
and how impulsive exposures lose those features that define ranges where energy above 10 kHz was absent to evaluate
impulsivity. Although direct measurements to make that TTS onset relative to impulsive and nonimpulsive criteria.
determination definitively for any group are again lacking,
one consideration for reasoned practical assessments is to Regardless of whether or how regulators or noise pro-
identify regions of the frequency spectrum where most taxa ducers consider the interim approach proposed in this
overlap in terms of best relative hearing sensitivity and are article, it should be recognized that the use of impulsive
thus most liable to noise impacts.                              exposure criteria for receivers at greater ranges (tens of
                                                                kilometers) is almost certainly an overly precautionary
It is noted that above about 10 kHz, several things occur interpretation of existing criteria. This interim measure
both in terms of sound propagation and sound reception. is presented as a simple, reasonable proxy that could help
First, broadband stimuli are substantially degraded at this avoid gross misapplication of auditory criteria until more
and higher frequencies with increasing range, restricting direct empirical audiometric data are obtained.
the overall noise spectrum and thus reducing associated
impulsive metrics. Second, this frequency region either Synthesis
overlaps or is fairly similar to best hearing sensitivity rela- This article, which considers auditory and behavioral
tively (not absolutely) speaking across all marine mammal noise-exposure criteria for different marine mammals
taxa (see Southall et al., 2019a, Figures 1-9). Below this and noise sources, marks the conclusion of the second
region, high-frequency specialists hear relatively poorly, iteration of the noise criteria panel first convened in 2003
whereas at higher frequencies, low-frequency hearers by Dr. Roger Gentry. Given rapidly evolving issues sur-
are less sensitive. It may be necessary (and eventually rounding marine noise and protected species, Gentry

58   Acoustics Today • Summer 2021
responded proactively to pressing regulatory, legal, and         et al. (2007) and the onset of the current efforts is prob-
scientific needs for objective application of available sci-     ably a realistic period for such reassessment given the
ence and identification of priority research to inform           pace of science and the enormity of the issues. Future
exposure criteria. He assembled and served as one of the         efforts should build on the solid foundations of exper-
complementary experts who contributed to the Southall            tise, knowledge, and methods to date and bring new
et al. (2007) criteria, and he guided the panel through          minds and new ideas to bear. Future criteria should
that process into the present one.                               consider potential significant population-level behavioral,
                                                                 masking, and physiological effects and perhaps other eco-
It was a bold vision by Gentry, given the expansive and          system considerations yet to be identified.
complex nature of the issues. Those of us involved from
the start, and those who joined later, were perhaps unpre-       Acknowledgments
pared for the challenges of this venture. Our scientific         This work would not have been possible without decades
training teaches us that firm conclusions often require          of almost entirely in-kind support by the scientists iden-
larger sample sizes than exist for nearly any of the topics      tified in the Foreword. Travel and logistical support for
considered. This work has taken us out of our comfort            different phases in the panel process were provided by the
zone to provide informed assessments where decisions             United States National Marine Fisheries Service, United
must be made before all desirable data are available. We         States National Science Foundation, and the Joint Indus-
recognized that decisions about the effects of noise will        try Program on Sound and Marine Life. The permitted
be made one way or another and that it is useful to have         use of images from Southall et al. (2019a) by Aquatic
experts familiar with the science work together through a        Mammals is appreciated.
transparent process to develop reasonable recommenda-
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effects, nonauditory physiological effects, or the inter-        Finneran, J. J. (2015). Noise-induced hearing loss in marine mammals:
                                                                  A review of temporary threshold shift studies from 1996 to 2015. The
action of multiple stressors for populations. Strategic           Journal of the Acoustical Society of America 138, 1702-1726.
thinking is needed, with an emphasis on more compre-             Finneran, J. J. (2016). Auditory Weighting Functions and TTS/PTS
hensive data and larger sample sizes for “representative”         Exposure Functions for Marine Mammals Exposed to Underwater
                                                                  Noise. Technical Report 3026, Prepared for Commander, US Fleet
species and integrating responses and vital life history
                                                                  Forces Command, Norfolk, VA, by the Space and Naval Warfare
parameters to consider longer term and potential popula-          Systems Center Pacific, San Diego, CA.
tion impacts (see Pirotta et al., 2021).                         Hamernik, R., Qiu, W., and Davis, R. (2010). The use of the kurtosis
                                                                  metric in the evaluation of industrial noise exposures. The Journal
                                                                  of the Acoustical Society of America 128, 2456.
The collective recent efforts of the panel are subsequent        Hastie, G., Merchant, N. D., Götz, T., Russell, D. J., Thompson, P., and Janik,
steps in an evolving, self-correcting process that will           V. M. (2019). Effects of impulsive noise on marine mammals: Investigat-
continue into the future. The decade between Southall             ing range‐dependent risk. Ecological Applications 29, Article e01906.

                                                                                                Summer 2021 • Acoustics Today               59
NOISE EXPOSURE CRITERIA

Hawkins, A. D., Pembroke, A., and Popper, A. (2015). Information                Southall, B. L., Nowacek, D. P., Miller, P. J. O., and Tyack, P. L. (2016).
 gaps in understanding the effects of noise on fishes and invertebrates.         Synthesis of experimental behavioral response studies using human
 Reviews in Fish Biology and Fisheries 25, 39-64.                                sonar and marine mammals. Endangered Species Research 31, 291-
Kastelein, R. A., Helder-Hoek, L., Covi, J., and Gransier, R. (2016).            313. https://doi.org/10.3354/esr00764.
 Pile driving playback sounds and temporary threshold shift in                  Thompson, P. M., Brookes, K. L., Graham, I. M., Barton, T. R.,
 harbor porpoises (Phocoena phocoena): Effect of exposure duration.              Needham, K., Bradbury, G., and Merchant, N. D., (2013). Short-
 The Journal of the Acoustical Society of America 139, 2842-2851.                term disturbance by a commercial two-dimensional seismic
Ketten, D. R. (2014). Sonars and strandings: Are beaked whales the               survey does not lead to long-term displacement of harbour
 aquatic acoustic canary? Acoustics Today 10(3), 46-56.                          porpoises. Proceedings of the Royal Society. Series B: Biological Sci-
Martin, S. B., Lucke, K., and Barclay, D. R. (2020). Techniques for              ences 280(1771), 20132001.
 distinguishing between impulsive and non-impulsive sound in the                Tougaard, J., Wright, A. J., and Madsen, P. T. (2015). Cetacean noise
 context of regulating sound exposure for marine mammals. The Jour-              criteria revisited in the light of proposed exposure limits for harbour
 nal of the Acoustical Society of America 147, 2159-2176.                        porpoises. Marine Pollution Bulletin 90, 196-208.
Nachtigall, P. E., and Supin, A. Y. (2015). Conditioned frequency-depen-        Tubelli, A., Zosuls, A., Ketten, D., and Mountain, D. (2018). A middle
 dent hearing sensitivity reduction in the bottlenose dolphin (Tursiops          ear finite element model to predict the hearing range of the hump-
 truncatus). Journal of Experimental Biology 218, 999-1005.                      back whale (Megaptera novaeangliae). The Journal of the Acoustical
National Academies of Sciences and Medicine (NAS) (2017). Approaches             Society of America 144, 525-535.
 to Understanding the Cumulative Effects of Stressors on Marine Mam-
 mals. The National Academies Press, Washington, DC.
National Marine Fisheries Service (NMFS) (2016). Technical Guidance               About the Author
 for Assessing the Effects of Anthropogenic Sound on Marine Mammal
 Hearing: Underwater Acoustic Thresholds for Onset of Permanent
 and Temporary Threshold Shifts. National Oceanic and Atmospheric                                         Brandon L. Southall
 Administration (NOAA) Technical Memorandum NMFS-OPR-55,                                                  Brandon.Southall@sea-inc.net
 NOAA, US Department of Commerce, Washington, DC.
                                                                                                          Southall Environmental Associates and
Payne, R., and Webb, D. (1971). Orientation by means of long-range
 acoustic signaling in baleen whales. Annals of the New York Academy                                      University of California, Santa Cruz
 of Sciences 188(1), 110-141.                                                                             9099 Soquel Drive, Suite 8
Pirotta, E., Booth, C. G., Cade, D. E., Calambokidis, J., Costa, D. P., Fahl-                             Aptos, California 95003, USA
 busch, J. A., Friedlaender, A. S., Goldbogen, J. A., Harwood, J., Hazen, E.                           Brandon Southall has Master’s and PhD
 L. New, L., and Southall, B. L. (2021). Context-dependent variability in the
                                                                                 degrees from the University of California, Santa Cruz (Santa
 predicted daily energetic costs of disturbance for blue whales. Conservation
                                                                                 Cruz), studying marine mammal communication, hearing,
 Physiology 9(1), coaa137. https://doi.org/10.1093/conphys/coaa137.
Price, G. R. (1983). Relative hazard of weapons impulses. The Journal            and noise impacts. He has led basic and applied laboratory
 of the Acoustical Society of America 73, 556-566.                               and field research programs and contributed to national and
Qiu, W., Murphy, W. J., and Suter, A. (2020). Kurtosis: A new tool for           international policies, including the development of marine
 noise analysis. Acoustics Today 16(4), 39-47.                                   mammal noise-exposure criteria. He has directed large-scale,
 https://doi.org/10.1121/AT.2020.16.4.39.                                        multidisciplinary behavioral research programs on marine
Samuels, A., Bejder, L., and Heinrich, S. (2000). A Review of the Lit-           mammals around the world. He serves as a technical advisor
 erature Pertaining to Swimming with Wild Dolphins. Report prepared              to international corporations and environmental organiza-
 for the Marine Mammal Commission, Bethesda, MD.                                 tions and has testified before the US Congress and Supreme
Sills, J. M., Southall, B. L., and Reichmuth, C. (2017). The influence           Court and the United Nations. He has published over 175
 of temporally varying noise from seismic air guns on the detection
                                                                                 peer-reviewed scientific papers and technical reports.
 of underwater sounds by seals. The Journal of the Acoustical Society
 of America 141, 996-1008.
Southall, B. L. (2017). Noise. In B. Würsig and H. Thiewesson (Eds.),
 Encyclopedia of Marine Mammals, 3rd ed. Academic Press, New York,
 NY, pp. 699-707.
Southall, B. L. Bowles, A., Ellison, W., Finneran, J., et al. (2007).
 Marine mammal noise exposure criteria. Aquatic Mammals 33, 411-
                                                                                         BECOME INVOLVED
 521. https://doi.org/10.1578/AM.33.4.2007.411.
Southall, B. L., DeRuiter, S. L., Friedlaender, A., Stimpert, A. K., Gold-            Would you like to become more involved with
 bogen, J. A., Hazen, E., Casey, C., Fregosi, S., Cade, D. E., Allen, A. N.,
                                                                                      the ASA? Visit acousticalsociety.org/volunteer
 and Harris, C. M. et al. (2019b). Behavioral responses of individual
 blue whales (Balaenoptera musculus) to mid-frequency military                       to learn more about the Society's technical and
 sonar. Journal of Experimental Biology 222, Article jeb190637.                     administrative committees, and submit a form to
 https://doi.org/10.1242/jeb.190637.                                                       express your interest in volunteering!
Southall, B. L., Finneran, J. J., Reichmuth, C., Nachtigall, P. E., Ketten,
 D. R., Bowles, A. E., Ellison, W. T., Nowacek, D. P,. and Tyack, P.L
 (2019a). Marine mammal noise exposure criteria: Updated scientific
 recommendations for residual hearing effects. Aquatic Mammals 45,
 125-232. https://doi.org/10.1578/AM.45.2.2019.125.                                         acousticalsociety.org/volunteer
Southall, B. L., Nowacek, D. P., Bowles, A. E., Senigaglia, V., et al.
 (2021). Marine mammal noise exposure criteria: Assessing the sever-
 ity of marine mammal behavioral responses to human noise. Aquatic
 Mammals. In press.

60   Acoustics Today • Summer 2021
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