Four previous reports of the National Research Council (NRC)1 have documented effects of anthropogenic sound on marine mammals. It is now recognized that intense sounds from human activities such as seismic air guns can have direct physiological effects on marine mammals, and naval sonar triggers behavioral reactions that can lead to death by stranding. However, nonlethal behavioral disturbance is the most common effect of anthropogenic noise on marine mammals. Rather subtle behavioral changes experienced by many marine mammals may have greater population consequences than occasional lethal events. Environmental reviews of human activities that make noise2 in the ocean routinely assess the number of animals that may be injured or disturbed, and researchers have started to develop methods to estimate effects on populations.
Noise is a stressor for humans and wildlife, and its effects can interact with those of other stressors. Marine mammal populations exist in environments that are being altered simultaneously by various combinations of human activities and their effects, such as pollution and habitat degradation and loss. Natural factors interact in complex ways with effects of human activities to alter climate, the numbers of prey, competitors, pathogens, and predators, potentially contributing to the mix of threats that populations must withstand to remain viable.
Scientists, regulators, and managers have long recognized that the complexity of these interactions must be better understood in order to ensure that marine mammals will continue to be functioning components of their ecosystems. This has led to a strong desire to better understand marine mammal responses to cumulative effects of multiple stressors.
Terminology in the area of cumulative effects in scientific literature has been driven primarily by considerations of environmental chemicals. The U.S. Environmental Protection Agency (EPA, 2007) defines aggregate exposure as the combined exposure of a receptor (individual or population) to a single chemical. The chemical can originate from multiple sources and be present in multiple media, and exposures can occur by different routes and over different time periods. Cumulative risk is defined as the combined risk to a receptor (individual or population) from exposures to multiple agents (here, chemicals) that can come from many sources and exist in different media, and to which multiple exposures can be incurred over time to produce multiple effects. More than one chemical must be involved for the risk to be considered cumulative.
The term cumulative effect has been used in marine mammal literature to encompass both aggregate exposure and cumulative risk. For example, noise has been considered to have cumulative effects when an animal is exposed to multiple noise sources, such as shipping plus seismic. To be consistent with the much larger field of environmental chemical exposure, noise should be considered one of a number of stressors experienced by marine mammals. As such the effects of various noises on an individual or a population would be considered components of an overall aggregate exposure to noise. Cumulative effect would derive from the combination of noise and other anthropogenic stressors, such as chemical pollution, marine debris, introduced pathogens, and changes in temperature or pH induced by climate change, and also natural stressors, such as presence of predators, pathogens, parasites, or reduced availability of prey.
The committee defines aggregate exposure as the
1 Until 2015, reports were published under the authorship of the National Research Council.
2 Noise refers to sounds that are unwanted or are not useful for a receiver.
combined exposure to one stressor from multiple sources or pathways and cumulative effect as the combined effect of exposures to multiple stressors integrated over a defined relevant period: a day, a season, a year, or a lifetime.
When assessing cumulative effects, biologists focus on cumulative effects on an individual animal or population when they are repeatedly exposed to the same or different stressors. By contrast, definitions of “cumulative effects” used in relevant laws and regulations, particularly the National Environmental Policy Act of 1969 (NEPA) and the Endangered Species Act (ESA), focus on the effects of multiple “actions.” In addition to NEPA and ESA, there are a number of other acts and implementing regulations dealing with environmental impacts on marine mammals, which are summarized in Appendix B.
Finding 1.1: There is an important difference between the definition of cumulative effects as used by most biologists and cumulative effects as defined under the implementing regulations for the National Environmental Policy Act and the Endangered Species Act. The regulatory definition focuses on the incremental effect of a proposed human action when added to those of other human actions. Most biologists think of effects accumulating when individual animals or populations are repeatedly exposed to the same or different stressors, taking into consideration natural factors that may affect the response to human activities.
NEPA recognized the importance of these interactions by requiring all federal agencies to assess the environmental impacts of their actions. At the heart of NEPA is a requirement that federal agencies “include in every recommendation or report on proposals for legislation and other major Federal actions significantly affecting the quality of the human environment, a detailed statement by the responsible official on—(i) the environmental impact of the proposed action, (ii) any adverse environmental effects which cannot be avoided should the proposal be implemented, (iii) alternatives to the proposed action, (iv) the relationship between local short-term uses of man’s environment and the maintenance and enhancement of long-term productivity, and (v) any irreversible and irretrievable commitments of resources which would be involved in the proposed action should it be implemented.”3 The detailed statement called for in NEPA is termed an Environmental Impact Statement (EIS). NEPA regulations require agencies to include in each EIS an evaluation of direct, indirect, and cumulative impacts associated with the action and proposed alternatives. Cumulative impact is defined for these purposes as “the impact on the environment which results from the incremental impact of the action when added to the other past, present, and reasonably foreseeable future actions regardless of what agency (federal or non-federal) or person undertakes such other actions.” The regulations add that “[c]umulative impacts can result from individually minor but collectively significant actions taking place over a period of time.”4
Section 7 of the ESA directs federal agencies to carry out programs for the conservation of threatened and endangered species. It further requires federal agencies to ensure that their actions (i.e., all actions authorized, funded, or carried out by the agency) are not likely to jeopardize the existence of a listed species or adversely modify the critical habitat of a listed species. As part of these assurances, Section 7 also requires agencies to consult with the U.S. Fish and Wildlife Service (FWS) or National Marine Fisheries Service (NMFS) (Steiger, 1994) regarding any activities that may affect listed species.5 “Procedurally, before initiating any action in an area that contains threatened or endangered species, federal agencies must consult with the FWS (for land based species and selected marine mammals) or NMFS (for all other marine species) to determine the likely effects of any proposed action on species and their critical habitat.”6
The text of the ESA does not directly address cumulative impacts or effects, but the implementing agencies (FWS and NMFS) and the courts have interpreted Section 7 as to require consideration of cumulative effects during the consultation process. The regulations promulgated under the ESA define “cumulative effects” as “those effects of future State or private activities, not involving Federal activities, that are reasonably certain to occur within the action area of the Federal action subject to consultation.”7 Guidance produced by the FWS and NMFS regarding Section 7 consultations specifically states that this more narrow definition should not be conflated with the broader definition of “cumulative impacts” used in NEPA and pertains only to ESA Section 7 analyses.8
The science is not currently in place to allow quantitative estimates of how different stressors will interact as they impact individuals and populations or what the impact will be of repeated exposure to stressors. For federal agencies that seek to continue to improve their consideration of cumulative effects, such as the U.S. Navy, the U.S. Department of the Interior’s Bureau of Ocean Energy Management (BOEM), and the National Oceanic and Atmospheric Administration’s
3 42 U.S.C. § 4332(2)(C).
4 40 C.F.R. § 1508.7.
5 16 U.S.C. § 1536(a). The agency first determines whether their proposed action “may affect” a listed species or its habitat. If the agency determines it may, then formal consultation with either FWS or NOAA Fisheries is automatically required. If the agency determines that the action is not likely to affect a listed species or its habitat and the consulting agency agrees with this assessment, then further formal consultation is not necessary. If, however, the consulting agency does not agree with the assessment, then a formal consultation is required. Conservation Congress v. USFS, 720 F.3d 1048 (9th Cir. 2013).
6Conservation Congress v. USFS 720 F.3d 1048 (9th Cir. 2013) citing Natural Resources Defense Council v. Houston, 146 F.3d 1118, 1125 (9th Cir. 1998) and Forest Guardians v. Johanns, 450 F.3d 455, 457 n.1.
7 50 C.F.R. § 1508.7.
(NOAA’s) NMFS, this presents a challenge. The U.S. Navy, BOEM, and NMFS each either fund and conduct noise-making activities, issue authorizations and permits for such activities, or regulate impacts of sound on most marine mammals. These agencies, along with the U.S. Marine Mammal Commission, funded the present study in order to review current understanding of cumulative effects of anthropogenic stressors, including sound, on marine mammals, to assess current methodologies, and to identify new approaches that may improve the ability to estimate cumulative effects.
There has been a consistent expansion of focus in the series of NRC reports on marine mammals and sound from 1994 to 2005. Aside from scientific concern that noise from shipping might reduce the range over which whales may communicate (Payne and Webb, 1971) and studies on the impact of noise from offshore oil industry activities (Malme et al., 1983, 1984), there was little interchange before 1990 between marine mammal biologists and the ocean acoustics community, which understood how well low-frequency sound propagates in the deep ocean. The first NRC report on low-frequency sound and marine mammals (NRC, 1994) was motivated in large measure by a single ocean acoustics experiment designed to monitor changes in ocean temperature by measuring the speed with which a sound travels across ocean basins (Baggeroer and Munk, 1992). Four federal agencies funded a $1.7 million feasibility test for this project, which would involve sending a ship with powerful underwater loudspeakers to a site in the Indian Ocean where a low-frequency sound projected from the ship could be heard in Bermuda and California. When a report in Science (Gibbons, 1990) showed how the sound could be detected over much of the global oceans, the executive director of the U.S. Marine Mammal Commission could not understand how this federal action had not required permitting for effects of sound on marine mammals, because it covered such large ranges. His concerns led to the addition of a program to monitor effects on marine mammals, and the transmissions were permitted as marine mammal research (Cohen, 1991). This feasibility test succeeded in precisely timing how long sounds took to travel as far as 16,000 km (Munk et al., 1994). This success led to plans to operate a low-frequency source over a decade or more to measure changes in ocean temperature (in a project called Acoustic Thermometry of Ocean Climate, or ATOC). The long period of operation of such a long-range sound source raised concern about the impact of ATOC on marine mammals. The 1994 NRC report was tasked to review the effects of these kinds of low-frequency sounds on marine mammals and “to consider the trade-offs between the benefits of underwater sound as a research tool and the possibility of its having harmful effects on marine mammals” (NRC, 1994, p. 1). The NRC (1994) report addressed the state of knowledge on the effect of low-frequency sound on marine mammals and found very little relevant data. The 1994 report provided a number of research recommendations to close these data gaps.
The second NRC report, Marine Mammals and Low-Frequency Sound (NRC, 2000), was specifically tasked with assessing progress in research on effects of low-frequency sound on seals and cetaceans since 1994, with an evaluation of the marine mammal research program associated with ATOC. Given that the Marine Mammal Protection Act was coming up for reauthorization, NRC (2000) made specific recommendations for changes in the Act, along with recommendations to NOAA for setting priorities for regulating effects of noise, and recommendations for research sponsors. The 2000 report made a suite of recommendations calling for research that could address the uncertainty around the effects of different types and sources of sound on various marine mammal species, both in the context of biological consequences and for monitoring and regulatory purposes (NRC, 2000).
The third NRC report was tasked to evaluate all frequencies and sources of anthropogenic sound that could affect marine mammals, rather than simply low-frequency sound, to identify data gaps in ocean noise databases, and to recommend research to develop a model of ocean noise (NRC, 2003a). Consistent with this charge, the NRC (2003a) expanded the work of prior committees to recommend monitoring noise and marine mammal populations globally. This NRC report (2003a) also recommended that research on effects of sound on marine mammals be structured to test for population-level effects. This latter problem became the primary focus of the fourth NRC report (NRC, 2005), titled Marine Mammal Populations and Ocean Noise: Determining When Noise Causes Biologically Significant Effects. In order to begin to address the question of when a behavioral response will become significant to the individual animal, and, more importantly, significant to the population, the NRC (2005) developed a conceptual heuristic9 model that outlined how behavioral changes could have population consequences. This model, named the Population Consequences of Acoustic Disturbance (PCAD) model, identified a series of stages for relating the effects of acoustic disturbance on the life history of marine mammals, through to the impact on populations. The only stressor this model focused on was sound, and the model recognized that population-level consequences would be likely only when the stressor was repeatedly encountered. Specifically it looked at the aggregate effect of anthropogenic noise as a stressor over a sufficient period—a season or year—that could result in changes in life-history parameters for the exposed animals. These
9 A qualitative model informed by expert opinion that links processes and states, in this case the linking of acoustic disturbance through behavior and physiology to its impact on individuals and populations. The heuristic model informs research that can quantify the processes so the qualitative model is turned into a predictive model.
aggregate effects were modeled on the concept of allostatic load/overload (McEwen and Wingfield, 2003).
The model has subsequently been expanded to consider the population consequences of all forms of disturbance (PCoD). New et al. (2014) describe the PCoD model and present an early attempt to quantify fitness effects of behavioral disturbance. The recognition of the importance of identifying intermediate scales between short-term disturbance and population effects was a key element of the 2005 report that is taken up again by this report.
This report develops a metric of health of the individual that can integrate effects which can be related to survival or reproduction over periods of seasons up to the lifetime. The model defines how the distribution of the health of individuals can be used to determine the cumulative risk to the stock, population, or species.
The statement of task for this report is provided in Box 1.1.
Nine committee members were selected, representing a broad range of expertise (marine mammalogy, ecology, animal behavior, biostatistics, physiology, global change biology, zoology, and bioacoustics). Beginning with its first meeting in June 2015, the committee held four meetings and a workshop. The workshop, held in October 2015, was an information-gathering opportunity designed to survey approaches and methodologies that have been developed to identify and measure animals’ exposure to stressors and their responses. The committee was particularly interested in efforts developed for human and terrestrial ecosystems because they wanted to hear how other disciplines addressed these same challenges and questions of assessing cumulative impacts. The workshop discussions also helped the committee members identify innovations (in thinking and application) that they could consider in their review of the current approaches and methods.
In this chapter, the committee begins by defining some of the terminology associated with cumulative effects and the contrasts in their interpretation by biologists and regulators. This is followed by a brief introduction of select U.S. legislation that provides the general legal framework for addressing impacts to marine mammals that the sponsors of this report also use to guide their programmatic activities and responsibilities relevant to marine mammals. The chapter closes with a review of earlier NRC studies that looked at marine mammals and sound.
The effects of sound on wildlife are the focus of Chapter 2 and the committee examines the various sources and the variations in time, frequency, and intensity of sound. Both terrestrial and marine studies are reviewed, and particular attention is given to the perception of or responses to sound by animals. The chapter discusses auditory sensitivities, shifts in hearing (both temporary and permanent), and dose–response relationships in the context of stressors. Characterizing these relationships is an essential step in understanding exposure and outcomes, an approach that is revisited in the remaining chapters in the reviews of other types of stressors and their effects. The chapter includes an explanation of how dose–response functions, properly obtained, can provide much more accurate estimates and variances of marine mammal “take” in association with sound-generating activities.
Chapter 3 transitions away from sound to explore the current state of knowledge regarding the many other types
and sources of stressors, with a particular focus on extrinsic stressors (factors in the animal’s external environment that create stress). The committee reviewed the effects of extrinsic stressors associated with anthropogenic activities, such as pollutants or ship strikes, and ones that are associated with natural factors. The chapter concludes with a discussion of how the spatial and temporal variation among stressors affects the potential for cumulative effects of individual and combined stressors.
Understanding how the effects of extrinsic stressors might interact to create cumulative effects is the focus of Chapter 4. The committee reviewed studies of interactions of multiple stressors and discussed the challenges of applying the findings from these studies to management of marine mammals and their environment. The chapter examines how multiple stressors are likely to interact, and then identifies approaches for prioritizing stressors for cumulative effects analysis with the use of a decision tree. The committee also explored a set of case studies involving marine mammal population declines that illustrate the difficulty of inferring causes—but also provided the committee an opportunity to investigate what conclusions might have been drawn if the decision tree had been used with these case studies.
Chapter 5 provides a conceptual framework via a new model, titled Population Consequences of Multiple Stressors (PCoMS), developed for assessing the risks associated with aggregate exposures to one kind of stressor, such as sound, and the cumulative exposure associated with sound and other stressors. The PCoMS model documents the pathways from exposure to stressors through their effects on health to their effects on vital rates and population dynamics. A key component of this framework is an assessment of the health of an individual. The chapter discusses a suite of measures that the committee identifies as useful for assessing health in the target populations.
In Chapter 6 the committee broadened its review from cumulative effects of stressors on individuals and populations to consider how interactions among stressors may affect multiple species and entire ecosystems. In doing so, committee members review the components of an interaction web and the various species or abiotic elements that affect the distribution and abundance of species of interest, and specifically how interaction webs can help identify the factors that need to be considered in evaluating cumulative effects on populations and ecosystems.
Chapter 7 acknowledges the challenges of detecting and anticipating the cumulative effects of multiple stressors on marine mammal populations and discusses a suite of population-monitoring parameters that could facilitate the early detection of unexpected population declines and, where possible, the rapid diagnosis of the main factors contributing to them.
In the final chapter of the report (Chapter 8), the committee reviews a broad range of approaches for assessing cumulative impacts that include approaches with limited use for marine mammals as well as those with more utility. The committee identifies the use of comprehensive health assessment as a broadly applicable approach that can serve as a key component of the PCoMS model framework as well as an early warning indicator of population risk prior to population decline.
The tasks asked of this committee span a broad range of scientific disciplines from toxicology to marine ecology. Terms such as interaction have different meanings to different specialties, and the dose–response functions discussed in the report span many levels of biological organization from molecules to ecosystems. Nearly every reader may have questions about the usage of some terms. The committee has included a glossary of important terms used throughout this report (Appendix D).
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