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Marine Mammal Populations and Ocean Noise: Determining When Noise Causes Biologically Significant Effects 1 Introduction DEFINING THE PROBLEM Throughout human history, the oceans have been important for transportation and commerce, for their biological and physical resources, and for defense. The vast expanse of the oceans precluded significant human impact until the coming of the industrial revolution when the transition from wind-driven to mechanized shipping became the first step in what was to be a continued increase in the unintentional and then—with the development of sonar—intentional introduction of sound into the oceans. Because of the low loss characteristic of sound transmission compared with light transmission, the use of sound had developed evolutionarily as the predominant long-range sensory modality for marine mammals. As engineers and scientists learned to appreciate the properties of acoustic propagation in the sea, they introduced sound sources to communicate and to detect objects in the oceans or on or below the seafloor. At some point, as humans use the oceans more and increase anthropogenic sound in the oceans, the conflict with evolutionarily adapted marine animals’ sound-sensing systems seems inevitable. Over 90% of global trade uses the sea for transportation. Shipping is the dominant source of sound in the world’s oceans in the range from 5 to a few hundred Hertz. At other frequencies, anthropogenic sound does not predominate in the ocean sound-energy budget, but it can have important local effects (NRC, 2003b). Seismic air guns associated with geophysical
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Marine Mammal Populations and Ocean Noise: Determining When Noise Causes Biologically Significant Effects exploration for locating new oil and gas deposits run hundreds of thousands of miles of survey lines in the Gulf of Mexico alone each year. Commercial sonar systems are on all but the smallest pleasure craft and permit safer boating and shipping and more productive fishing. Military sonar systems are important for national defense. Ocean noise from human and natural sources can also originate in the air, as in sonic booms, lightning, and wind (NRC, 2003b). The intentional and unintentional introduction of sound in the oceans associated with activities beneficial to humans has known deleterious effects on individual marine mammals. Mass strandings of beaked whales, defined as strandings involving two or more animals other than female-calf pairs (Geraci and Lounsbury, 1993), in some cases have clearly been associated with the use of midrange tactical military sonar (D’Amico, 1998; Evans and England, 2001; Jepson et al., 2003). Beluga whales (Delphinapterus leucas) have strong and prolonged behavioral responses to icebreakers 50 km away under some circumstances (LGL and Greeneridge, 1986; Cosens and Dueck, 1988; Finley et al., 1990). Gray whales (Eschrichtius robustus) and killer whales (Orcinus orca) have shown multiyear abandonment of critical habitats in response to anthropogenic noise (Bryant et al., 1984; Morton and Symonds, 2002). Although there are many documented, clearly discernible responses of marine mammals to anthropogenic sound, responses are typically subtle, consisting of shorter surfacings, shorter dives, fewer blows per surfacing, longer intervals between blows, ceasing or increasing vocalizations, shortening or lengthening vocalizations, and changing frequency or intensity of vocalizations. Some of those changes become statistically significant for a given exposure, such as increases in descent rate and increases or decreases in ascent rate of northern elephant seals (Mirounga angustriostris) in response to Acoustic Thermometry of the Ocean Climate (ATOC) signals (Costa et al., 2003). But it remains unknown when and how these changes translate into biologically significant effects—effects that have repercussions for the animal beyond the time of disturbance, effects on the animal’s ability to engage in essential activities, and effects that have potential consequences at the population level. The basic goal of marine mammal conservation is to prevent human activities from harming marine mammal populations. The threat from commercial whaling was obvious, but it is more difficult to estimate the population consequences of activities that have less immediately dramatic outcomes, such as those with indirect or small but persistent effects. The life histories and habitat of marine mammals compound the difficulties.
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Marine Mammal Populations and Ocean Noise: Determining When Noise Causes Biologically Significant Effects Marine mammals are long-lived and slow to mature. The young of many species are dependent for long periods. They are highly social, have behavioral plasticity, and have complex processes of behavioral development. Many of their behaviors occur underwater, where they are difficult to document, and that makes it particularly hard to estimate the effects of a short-term exposure as they ripple through the lifetime of an individual or as the effects on different individuals ripple through the population. Even extreme effects, including death, are not necessarily observed. With the exception of the beaked whale strandings, connections between anthropogenic sound in the oceans and marine mammal deaths have not been documented. In the presence of clear evidence of lethal interactions between humans and marine mammals in association with fishing and vessel collisions (Clapham et al., 1999; Laist et al., 2001), the absence of such documentation has raised the question of the relative importance of sound in the spectrum of anthropogenic effects on marine mammal populations. Anthropogenic ocean noise is thought not to be a factor in any of the recent major declines in marine mammal populations, such as Steller sea lions (Eumetopias jubatus; NRC, 2003a), harbor seals (Phoca vitulina; Pitcher, 1990), fur seals (York, 1987), and Aleutian Island sea otters (Enhydra lutris; Doroff et al., 2003). No scientific studies have conclusively demonstrated a link between exposure to sound and adverse effects on a marine mammal population. These considerations have led to alternative assessments of the effects of sound on marine mammals. On the one hand, sound may represent only a second-order effect on the conservation of marine mammal populations; on the other hand, what we have observed so far may be only the first early warnings or “tip of the iceberg” with respect to sound and marine mammals. HISTORY OF NATIONAL RESEARCH COUNCIL REPORTS The National Research Council has produced three reports on the effects of noise on marine mammals, in 1994, 2000, and 2003. The primary goal of the first, Low-Frequency Sound and Marine Mammals: Current Knowledge and Research Needs, was to address the specific issues raised by the Heard Island Feasibility Test, which sought to “establish the limits of usable, long-range acoustic transmissions” (Munk et al., 1994). The feasibility test was preliminary to the ATOC experiment. The ATOC project proposed to measure the speed of sound across ocean basins as a way to monitor global climate change, and it required long-range transmissions of
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Marine Mammal Populations and Ocean Noise: Determining When Noise Causes Biologically Significant Effects underwater sound regularly from several sites for decades. The 1994 report recommended research with respect to low-frequency (1- to 1,000-Hz) sound and marine mammals that was needed before a full deployment of ATOC. The report also noted that regulation of marine mammal research impeded exactly the type of research needed to determine if anthropogenic noise is detrimental to the animals. The report included an entire chapter on regulatory issues (NRC, 1994). The Marine Mammal Protection Act (MMPA, 16 U.S.C. 1361-1401 et seq.) enacted in 1972 is the legal instrument of the US federal government for protection of marine mammals. The 1994 National Research Council report was concerned that the statutory term harassment, included in the MMPA but undefined in regulation, was “being interpreted through practice to include any action that results in an observable change in the behavior of a marine mammal” (Swartz and Hofman, 1991). The report pointed out (pg. 28) that As researchers develop more sophisticated methods for measuring the behavior and physiology of marine mammals in the field (e.g., via telemetry), it is likely that detectable reactions, however minor and brief, will be documented at lower and lower received levels of human-made sound…. In that case, subtle and brief reactions are likely to have no effect on the well-being of marine mammal individuals or populations. The report recommended that legislative distinctions be made between different types of taking and that the regulatory agencies streamline the permitting process for activities that do not kill or capture marine mammals. Additional streamlining should be considered for nonlethal activities that have negligible effects. Agencies were encouraged to regulate within the context of total human impacts on marine mammals—including fisheries, shipping, the oil and gas industry, and research activities—and to expend their primary effort on activities with the greatest potential for harm. The 2000 National Research Council report, Marine Mammals and Low-frequency Sound: Progress Since 1994, noted that the 1994 amendments to the MMPA addressed some of the issues raised in the 1994 report. The 1994 amendments introduced two levels of disturbance that are considered regulated takings—level A and level B harassment. Level A harassment is “any act of pursuit, torment, or annoyance which has the potential to injure a marine mammal or marine mammal stock in the wild.” Level B harassment is “any act of pursuit, torment, or annoyance which has the potential to disturb a marine mammal or marine mammal stock in the wild by causing disruption of behavioral patterns including, but not limited to,
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Marine Mammal Populations and Ocean Noise: Determining When Noise Causes Biologically Significant Effects migration, breathing, nursing, breeding, feeding, or sheltering.” However, the 2000 National Research Council report continued to emphasize the importance of a criterion for significance of disruption of behavior (pg. 68): It does not make sense to regulate minor changes in behavior having no adverse impact; rather regulations must focus on significant disruption of behaviors critical to survival and reproduction. The report recommended a redefinition of level B harassment as any act that (pg. 69) has the potential to disturb a marine mammal or marine mammal stock in the wild by causing meaningful disruption of biologically significant activities, including but not limited to, migration, breeding, care of young, predator avoidance or defense, and feeding. Since the report was issued, the term biologically significant has been used in discussions of the 2003-2004 reauthorization of the MMPA (House Report 108-464). The US National Marine Fisheries Service (now National Oceanic and Atmospheric Administration [NOAA] Fisheries) has used the term in decisions to grant incidental harassment authorizations, but scientific investigation and description of what would constitute “biologically significant” have not been pursued in a comprehensive manner. The 2003 National Research Council report, Ocean Noise and Marine Mammals, attempted to quantify the world ocean-noise budget between 1 and 200,000 Hz with particular attention to habitats that are important to marine mammals (NRC, 2003b). The basic question it addressed was the overall impact of human-made sound on the marine environment. The somewhat unsatisfactory answer was that the overall impact is unknown but there is cause for concern. It was noted that total energy contribution is not the best currency to use in determining the potential impact of human-made sound on marine organisms. The report offered a number of recommendations; the overarching one was the need to understand better the characteristics of ocean noise, particularly from human-made noise, and its potential effects on marine life, especially effects that may have population consequences. Thus, each of the three previous National Research Council reports has recommended research to resolve critical uncertainties about the effects of noise on marine mammals. All three highlighted the need for research in behavioral ecology, auditory physiology and anatomy, nonauditory effects of sound, effects of sound on prey of marine mammals, and development of new techniques for measuring the effects of
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Marine Mammal Populations and Ocean Noise: Determining When Noise Causes Biologically Significant Effects sound on marine mammals. The 2003 report also recommended research on sources and modeling of ocean noise. Some of the recommendations have led to research that has greatly reduced the data gap. For example, the 1994 and 2000 reports recommended experiments to determine acoustic exposures that would lead to temporary shifts in the threshold of hearing in marine mammals. In the last decade, several laboratories have conducted such experiments (Kastak et al., 1999; Finneran et al., 2000, 2002; Schlundt et al., 2000; Nachtigall et al., 2003, 2004), and there is much less uncertainty in modeling the exposures that start to cause physiological effects on hearing in the seal and small-toothed whale species that have been tested. There has been partial progress on other recommendations. For example, the 1994 report recommended the development of tags to record physiological characteristics, behavior, location, and sound exposure. In the last decade, tags have been developed to record all the features recommended (Burgess, 2001; Johnson and Tyack, 2003) except physiological measures. For many of the other research recommendations research is being conducted, but progress has been slow enough to warrant the establishment of a targeted research program. The 2000 and 2003 National Research Council reports recommended better coordination between federal regulatory agencies and science-funding agencies to develop a multidisciplinary research program that would judge the quality of proposals with peer review. There has been little progress on those programmatic recommendations, and the present committee reemphasizes that progress in critical research requires that the federal government develop and fund a dedicated multidisciplinary research program on the subjects in question. CALL FOR A NEW NATIONAL RESEARCH COUNCIL STUDY The recommendations of the 2000 National Research Council report have received great attention and been applied by regulators, legislators, and permit applicants to describe level B harassment under the MMPA. The vagaries associated with the term biologically significant behaviors and what constitutes “meaningful” disruption of those behaviors have been problematic. In light of the litigious and legislative environment of the issue of the disturbance of marine mammals, several federal agencies (including the Office of Naval Research, the National Science Foundation, the Minerals Management Service, and NOAA), working through the National Oceanographic Partnership Program, requested that the National
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Marine Mammal Populations and Ocean Noise: Determining When Noise Causes Biologically Significant Effects Research Council undertake a study to clarify the meaning of the term used in the 2000 report. Which possible effects have population consequences? If we don’t know, how can we determine them? The agencies, recognizing that effects will be biologically significant at individual and population levels, requested guidance from the present committee in making those determinations. At the individual level, the biological significance of an effect must be judged by changes in the ability of an animal to grow, survive, and reproduce. The population effect involves the cumulative impact on all individuals affected. The committee’s charge, developed with those considerations in mind is shown in Box 1-1. After discussion of and deliberation on the task statement, the committee recognized that the definition of level B harassment proposed in the 2000 report introduced two kinds of biological significance: one, with respect to animal activities, stated directly, and the other implied in the “meaningful disturbance” of those activities. On reflection, it became clear that animals in the wild rarely spend substantial amounts of time engaging in activities that are not biologically significant. Even seemingly frivolous BOX 1-1 Statement of Task In its 2000 report, Marine Mammals and Low-frequency Sound, the National Research Council recommended that the Marine Mammal Protection Act definition of “Level B harassment should be limited to meaningful disruption of biologically significant activities that could affect demographically important variables such as reproduction and longevity.” Recognizing that the term “biologically significant” is increasingly used in resource management and conservation plans, this study will further describe the scientific basis of the term in the context of marine mammal conservation and management related to ocean noise. Based on input from a scientific workshop, consideration of the relevant literature, and other sources, the committee will produce a brief report that reviews and characterizes the current scientific understanding of when animal behavior modifications induced by transient and non-transient ocean acoustic sources individually or cumulatively affect individuals in ways that have negative consequences for populations.
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Marine Mammal Populations and Ocean Noise: Determining When Noise Causes Biologically Significant Effects activities, such as play, can be biologically significant (Bekoff and Byers, 1998). Therefore, the primary concern should be with determining when human activity elicits behavioral or physiological responses in marine mammals that rise to the level of biological significance. Population consequences of behavioral change result from the accumulation of responses of individuals. In some cases, thousands of behavioral effects accumulated over years may be necessary for any population consequences; in other cases, a single instance of behavioral response may have the potential for population consequences. FINDING: As opposed to the definition of biologically significant activities, whose disruption can constitute harassment, the crucial determination is of when behavioral or physiological responses result in deleterious effects on the individual animals and the population. The statement of task incorporates two issues that had been concerns of earlier National Research Council reports. One is the difference between statistically significant and biologically significant changes in behavior. As more subtle behavioral changes become capable of being observed, it is inevitable that exposure to noise will result in statistically significant changes in one or more of the observed behaviors, but it is not equally certain that the changes will have any biological significance either for the individual or for the population. The second issue is the linking of short-term behavioral changes to possible consequences at the population level. How does one determine whether an acoustic disturbance can, or does, result in a change in population structure, distribution, or, ultimately, survival? In the absence of any comprehensive model for relating acoustic disturbance to population response with due consideration of all the intermediary steps and processes, the committee developed a conceptual model that, when supplemented with data, would facilitate the recognition of population effects of acoustic disturbance. The model includes an indication of the current state of knowledge and was designed to allow sensitivity analysis that can focus, stimulate, and direct research. To elaborate the model, identify deficiencies, and summarize current understanding, the committee held a focused public workshop (Appendix C). Workshop panel members were presented with the conceptual model, named the Population Consequences of Acoustic Disturbance (PCAD) model (Appendix D), described in Chapter 2, and asked to apply their
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Marine Mammal Populations and Ocean Noise: Determining When Noise Causes Biologically Significant Effects expertise in such fields as epidemiology and population biology. Workshop participants discussed the PCAD model—they related it to existing models, identified weaknesses in it, provided an assessment of data available to achieve its objectives, and evaluated the probability of achieving a predictive model in the next decade, given the current understanding of the processes linking behavior to vital rates and given the missing, but required, data. Participants agreed that the model provided a good basis for encompassing the components of the problem, defining needed data, and identifying the research agenda for the next decade. The consensus of the participants, both in their presentations and in breakout groups, was that the model incorporated the necessary components to become a predictive model when sufficient data became available. Workshop discussions of a number of topics improved the information and depth of analysis incorporated in this report, such as the examples of allostasis and the comparison of capital with income pinniped breeders. The initial model did not include the assessments of current knowledge of either the major categories of responses or the transfer functions. Those functions were assigned by the committee after the input of the workshop participants. This report is the culmination of the workshop presentations, the public dialogues that ensued, and the committee’s deliberations. The participants in the workshop made it clear that current empirical data and theoretical knowledge are insufficient to accomplish all the goals of the committee. Therefore, this report offers recommendations intended to provide a roadmap for the development of a predictive model of the effects of ocean noise on marine mammal populations and presents suggestions for temporary measures for regulating the effects until a predictive model is developed and tested. FINDING: A conceptual model can assist in the understanding of acoustic disturbance of marine mammals and possible effects on populations of them. However, the paucity of data prevents such a model from having a predictive role now.
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