marine mammals brief final
Repor t
October 2016
HIGHLIGHTS
Approaches to Understanding the Cumulative
Efects of Stressors on Marine Mammals
Marine mammals face a number of natural and human stressors that can harm
populations, such as noise and other pollutants, loss of habitat, and bycatch in
ishing. Much progress has been made in understanding the response of marine
mammals to some speciic stressors such as noise, but estimating risks to marine
mammal populations requires understanding how the full array of stressors
interact. This report offers a conceptual framework, research strategies, and
adaptive management suggestions to improve the ability to assess the cumulative
effects of stressors on marine mammal populations and identify which stressors
could be reduced to bring the population into a more favorable state.
Years of research and assessments, including four National Academies’ reports, have documented effects of human-induced sound on marine mammals. Based on this research,
environmental reviews now routinely assess the number of animals that may be injured or
disturbed by human-induced noise in the ocean.
There is growing recognition, however, that the effects of a single stressor such
as noise must be considered in the context of all other stressors in order to predict potential impacts on marine mammal populations. Advances in science are needed to better
assess the impact of repeated exposures to the same stressor, the cumulative effects from
all human stressors (e.g., noise and chemical pollution, marine debris, ishing), and the
complex interactions of human and natural stressors that alter ecological drivers such as
climate, prey, competitors, pathogens, and predators.
In recognition of this challenge, the Ofice of Naval Research, the National Marine
Fisheries Service (NMFS), the Bureau of Ocean Energy Management (BOEM), and the U.S.
Marine Mammal Commission funded this study to review the understanding of cumulative effects of human stressors on marine mammals and to identify new approaches that
may improve the ability to estimate cumulative effects.
SCIENTIFIC PROGRESS IN UNDERSTANDING SOUND
Efforts to understand the effects of sound on marine mammals are illustrative of the types
of research conducted to assess a speciic stressor. A main goal is to characterize the rela-
Beluga whale pod in the
Chukchi sea. Photo credit:
Laura Morse (NOAA)
There is growing recognition that the efects
of a single stressor such
as noise must be considered in the context
of all other stressors in
order to predict potential impacts on marine
mammal populations.
tionship between acoustic exposure level (the dosage)
and a behavioral or physiological response, such as a
temporary hearing loss. Dose-dependent functions
have been determined for physiological and behavioral
responses. Because of variation between individuals
and across species, the physiological effects of sound
cannot be generalized based on the amount of testing
conducted to date.
The variation in behavioral response is even
greater than that for physiological response. Location,
activity patterns, and social structure, among other
variables, affect the behavioral responsive of individuals. Generally, severity of response increases with
strength of stimulus. However, severe responses have
been observed at signal levels that are just dectectable,
and signals that are expected to exceed known thresholds have resulted in no observable response.
THE CHALLENGE OF ASSESSING
CUMULATIVE STRESSORS
Although the relationship between the dose and the
response of an individual animal can be determined
for some stressors, the addition of a second stressor
can add considerable complexity due to the potential
for interactions between the stressors or between their
effects. Stressors may interact in a synergistic or antagonistic manner, where the resulting response is larger
or smaller, respectively, than the sum of the individual
stressor responses.
The need to understand the cumulative effects
of multiple stressors has been illustrated in cases of
mammal populations that have suffered an unexplained
decline, or have failed to recover following the removal
of a stressor. One example is the Cook Inlet beluga
whale population, which is separated by the Alaska Pen-
Figure 1. The Population Consequences of Multiple Stressors (PCoMS) framework. The top slice
describes the model for one individual exposed to multiple (three in this case) stressors. Compartments are
connected by arrows that represent causal lows (“transfer functions” in the terminology of NRC, 2005). For each
individual and for each stressor, changes in physiology may result in changes in behavior (such as movement
away from a sound source and cessation of feeding), which may in turn affect physiological functions that could
simultaneously be stressed by contaminants or other factors. Health of the individual is an indicator of the effects
of multiple stressors which may inluence individual vital rates. The effects on multiple individuals, represented
by additional slices of the PCoMS, can lead to population consequences.
insula from other beluga populations in Alaskan waters.
Its population declined from around 1,300 whales in
1979 to 367 in 1999. It was assumed that the Alaskan
Native subsistence harvest was the major cause of the
observed decline over this period. However, the population has shown no sign of recovery since 1999 when
Alaskan Natives imposed a voluntary moratorium that
drastically reduced subsistence harvest.
A rigorous approach for testing interactive
effects of multiple stressors involves experiments that
use different intensities of each stressor coupled with
tests of some combinations of stressors. Both for practical and ethical reasons, however, such experimental
approaches are often not possible for marine mammals.
In those cases, inferences must be based on quasi-experiments that reveal patterns associated with variation in
the levels of stressors over space or time.
A NEW CONCEPTUAL FRAMEWORK FOR
ASSESSING CUMULATIVE RISKS
Recognizing the dificulty of quantitative prediction of
cumulative effects of stressors on marine mammals,
the report’s authoring committee developed the “Population Consequences of Multiple Stressors” (PCoMS)
framework (Figure 1). The framework documents the
pathways that are possible from exposures to stressors
to their effects on physiology, behavior and health and
from there to their effects on vital rates (e.g., survival)
and population dynamics. The framework considers
all of this in the context of ecological drivers, such as
climate change.
The PCoMS framework does not provide an
algorithm for predicting cumulative effects but instead
serves to identify the most important components for
evaluating cumulative effects. A key to the framework
is that the health of an individual marine mammal,
deined as the ability to adapt and self-manage, is used
as the summation point for the cumulative effects of
multiple stressors. The report discusses how a variety of
health indices, including allostatic load, energy stores,
immune status, organ status, stress levels, contaminant
burden and parasite load, play into the framework.
MANAGEMENT OF CUMULATIVE EFFECTS
Once populations or ecosystems are found to be at
risk of adverse impacts, the critical issue for selecting
management actions is to decide what combinations
of stressors could be reduced to bring the population
or ecosystem into a more favorable state. Even though
exposure to multiple stressors is an unquestioned
reality for marine mammals, the best current approach
for management and conservation is to identify which
stressor combinations could present the greatest risk
to populations. The Committee developed a decision
tree that could be used to identify situations where a
detailed study of potential cumulative effects should be
given a high priority. The decision tree was applied to
three case studies to demonstrate its utility.
Research Recommendations The report provides a number of research recommendations that
are designed to address the current challenges facing
researchers and managers involved in monitoring, managing, and protecting populations of marine mammals,
a subset of which are listed here.
Recommendation: Future
research
initiatives
should include efforts to develop case studies that
apply the PCoMS framework to actual marine
mammal populations. These studies will need to estimate exposure to multiple stressors, predict changes in
behavior and physiology from those stressors, assess
health, and measure vital rates in order to parameterize
the functional relationships between these components
of the framework. Where possible, the data on changes
in demography, population size, and the health of
individuals collected in these studies should be used
to improve estimates of the parameters of the PCoMS
model and reduce uncertainty.
Recommendation: Future
research
initiatives
should support evaluation of the range of emerging
technologies for sampling and assessing individual
health in marine mammals, and identiication of
a suite of health indices that can be measured for
diverse taxa and that best serves to predict future
changes in vital rates. Potentially relevant measures
include hormones, immune function, body condition,
oxidative damage, and indicators of organ status, as
well as contaminant burden and parasite load. New
technology for remotely obtaining respiratory, blood
and other tissue samples and for remote assessment
(e.g., visual assessment of body condition) should also
be pursued.
Recommendation: Agencies charged with monitoring and managing the effects of human activities
on marine mammals should identify baselines and
document exposures to stressors for high priority populations. High priority populations should be
selected to include those likely to experience extremes
(both high and low) of stressor exposure in order to
increase the probability of detecting relationships. This
will require stable, long-term funding to maintain a
record of exposures and responses that could inform
future management decisions. Information on base-
lines and contextual variables are critically important to
interpreting responses.
Recommendation: Responsible agencies should
develop relatively inexpensive surveillance systems
that can provide early detection of major changes
in population status. Surveillance systems should
be developed irst for populations that currently lack
adequate stock assessments. To be most effective in
providing an early warning, the variables monitored
will depend on the species and situation, and may
change over time with development of new technology
and increasing ecological knowledge.
Recommendation: Adaptive management should
be used to identify which combinations of stressors
pose risks to marine mammal populations, and to
select which stressors to reduce once a risk is identiied. Once a population of marine mammals has been
found to be at risk, managers need to identify a stressor
or suite of stressors whose reduction can reduce this risk.
This suggests a new form of effect study – “subtractive
experiments” that remove or reduce one or more stressors to characterize the effect of the reduction. This
experimental design may be more appropriate for
adaptive management than the more traditional experiments that add stressors to the current baseline.
COMMITTEE ON ASSESSMENT OF THE CUMULATIVE EFFECTS ON ANTHROPOGENIC
STRESSORS ON MARINE MAMMALS
Peter Tyack (Chair), University of St. Andrews, UK; Helen Bailey, University of Maryland, Solomans; Daniel Crocker,
Sonoma State University, CA; James Estes, University of California, Santa Cruz; Clinton Francis, California Polytechnic State University; John Harwood, University of St. Andrews, Ceres Cupar, UK; Lori Schwacke, NOAA Hollings
Marine Laboratory, Charleston, SC; Len Thomas; University of St. Andrews, UK; Douglas Wartzok, Florida International University; Kim Waddell (Study Director, Gulf Research Program); Stacee Karras (Associate Program Oficer,
Ocean Studies Board), Payton Kulina (Senior Program Assistant, Ocean Studies Board)
For More Information . . . This Report Highlights was prepared by the Ocean Studies Board based on the report
Approaches to Understanding the Cumulative Effects of Stressors on Marine Mammals. The study was sponsored by the
Bureau of Ocean Energy Management, Marine Mammal Commission, National Oceanic and Atmospheric Administration, and Ofice of Naval Research. Any opinions, indings, conclusions, or recommendations expressed in this
publication are those of the authoring committee and do not necessarily relect those of the sponsors. Copies of the
report are available from the National Academies Press, (800) 624-6242; http://www.nap.edu.
Division on Earth and Life Studies
Copyright 2016 by the National Academy of Sciences. All rights reserved.
October 2016
HIGHLIGHTS
Approaches to Understanding the Cumulative
Efects of Stressors on Marine Mammals
Marine mammals face a number of natural and human stressors that can harm
populations, such as noise and other pollutants, loss of habitat, and bycatch in
ishing. Much progress has been made in understanding the response of marine
mammals to some speciic stressors such as noise, but estimating risks to marine
mammal populations requires understanding how the full array of stressors
interact. This report offers a conceptual framework, research strategies, and
adaptive management suggestions to improve the ability to assess the cumulative
effects of stressors on marine mammal populations and identify which stressors
could be reduced to bring the population into a more favorable state.
Years of research and assessments, including four National Academies’ reports, have documented effects of human-induced sound on marine mammals. Based on this research,
environmental reviews now routinely assess the number of animals that may be injured or
disturbed by human-induced noise in the ocean.
There is growing recognition, however, that the effects of a single stressor such
as noise must be considered in the context of all other stressors in order to predict potential impacts on marine mammal populations. Advances in science are needed to better
assess the impact of repeated exposures to the same stressor, the cumulative effects from
all human stressors (e.g., noise and chemical pollution, marine debris, ishing), and the
complex interactions of human and natural stressors that alter ecological drivers such as
climate, prey, competitors, pathogens, and predators.
In recognition of this challenge, the Ofice of Naval Research, the National Marine
Fisheries Service (NMFS), the Bureau of Ocean Energy Management (BOEM), and the U.S.
Marine Mammal Commission funded this study to review the understanding of cumulative effects of human stressors on marine mammals and to identify new approaches that
may improve the ability to estimate cumulative effects.
SCIENTIFIC PROGRESS IN UNDERSTANDING SOUND
Efforts to understand the effects of sound on marine mammals are illustrative of the types
of research conducted to assess a speciic stressor. A main goal is to characterize the rela-
Beluga whale pod in the
Chukchi sea. Photo credit:
Laura Morse (NOAA)
There is growing recognition that the efects
of a single stressor such
as noise must be considered in the context
of all other stressors in
order to predict potential impacts on marine
mammal populations.
tionship between acoustic exposure level (the dosage)
and a behavioral or physiological response, such as a
temporary hearing loss. Dose-dependent functions
have been determined for physiological and behavioral
responses. Because of variation between individuals
and across species, the physiological effects of sound
cannot be generalized based on the amount of testing
conducted to date.
The variation in behavioral response is even
greater than that for physiological response. Location,
activity patterns, and social structure, among other
variables, affect the behavioral responsive of individuals. Generally, severity of response increases with
strength of stimulus. However, severe responses have
been observed at signal levels that are just dectectable,
and signals that are expected to exceed known thresholds have resulted in no observable response.
THE CHALLENGE OF ASSESSING
CUMULATIVE STRESSORS
Although the relationship between the dose and the
response of an individual animal can be determined
for some stressors, the addition of a second stressor
can add considerable complexity due to the potential
for interactions between the stressors or between their
effects. Stressors may interact in a synergistic or antagonistic manner, where the resulting response is larger
or smaller, respectively, than the sum of the individual
stressor responses.
The need to understand the cumulative effects
of multiple stressors has been illustrated in cases of
mammal populations that have suffered an unexplained
decline, or have failed to recover following the removal
of a stressor. One example is the Cook Inlet beluga
whale population, which is separated by the Alaska Pen-
Figure 1. The Population Consequences of Multiple Stressors (PCoMS) framework. The top slice
describes the model for one individual exposed to multiple (three in this case) stressors. Compartments are
connected by arrows that represent causal lows (“transfer functions” in the terminology of NRC, 2005). For each
individual and for each stressor, changes in physiology may result in changes in behavior (such as movement
away from a sound source and cessation of feeding), which may in turn affect physiological functions that could
simultaneously be stressed by contaminants or other factors. Health of the individual is an indicator of the effects
of multiple stressors which may inluence individual vital rates. The effects on multiple individuals, represented
by additional slices of the PCoMS, can lead to population consequences.
insula from other beluga populations in Alaskan waters.
Its population declined from around 1,300 whales in
1979 to 367 in 1999. It was assumed that the Alaskan
Native subsistence harvest was the major cause of the
observed decline over this period. However, the population has shown no sign of recovery since 1999 when
Alaskan Natives imposed a voluntary moratorium that
drastically reduced subsistence harvest.
A rigorous approach for testing interactive
effects of multiple stressors involves experiments that
use different intensities of each stressor coupled with
tests of some combinations of stressors. Both for practical and ethical reasons, however, such experimental
approaches are often not possible for marine mammals.
In those cases, inferences must be based on quasi-experiments that reveal patterns associated with variation in
the levels of stressors over space or time.
A NEW CONCEPTUAL FRAMEWORK FOR
ASSESSING CUMULATIVE RISKS
Recognizing the dificulty of quantitative prediction of
cumulative effects of stressors on marine mammals,
the report’s authoring committee developed the “Population Consequences of Multiple Stressors” (PCoMS)
framework (Figure 1). The framework documents the
pathways that are possible from exposures to stressors
to their effects on physiology, behavior and health and
from there to their effects on vital rates (e.g., survival)
and population dynamics. The framework considers
all of this in the context of ecological drivers, such as
climate change.
The PCoMS framework does not provide an
algorithm for predicting cumulative effects but instead
serves to identify the most important components for
evaluating cumulative effects. A key to the framework
is that the health of an individual marine mammal,
deined as the ability to adapt and self-manage, is used
as the summation point for the cumulative effects of
multiple stressors. The report discusses how a variety of
health indices, including allostatic load, energy stores,
immune status, organ status, stress levels, contaminant
burden and parasite load, play into the framework.
MANAGEMENT OF CUMULATIVE EFFECTS
Once populations or ecosystems are found to be at
risk of adverse impacts, the critical issue for selecting
management actions is to decide what combinations
of stressors could be reduced to bring the population
or ecosystem into a more favorable state. Even though
exposure to multiple stressors is an unquestioned
reality for marine mammals, the best current approach
for management and conservation is to identify which
stressor combinations could present the greatest risk
to populations. The Committee developed a decision
tree that could be used to identify situations where a
detailed study of potential cumulative effects should be
given a high priority. The decision tree was applied to
three case studies to demonstrate its utility.
Research Recommendations The report provides a number of research recommendations that
are designed to address the current challenges facing
researchers and managers involved in monitoring, managing, and protecting populations of marine mammals,
a subset of which are listed here.
Recommendation: Future
research
initiatives
should include efforts to develop case studies that
apply the PCoMS framework to actual marine
mammal populations. These studies will need to estimate exposure to multiple stressors, predict changes in
behavior and physiology from those stressors, assess
health, and measure vital rates in order to parameterize
the functional relationships between these components
of the framework. Where possible, the data on changes
in demography, population size, and the health of
individuals collected in these studies should be used
to improve estimates of the parameters of the PCoMS
model and reduce uncertainty.
Recommendation: Future
research
initiatives
should support evaluation of the range of emerging
technologies for sampling and assessing individual
health in marine mammals, and identiication of
a suite of health indices that can be measured for
diverse taxa and that best serves to predict future
changes in vital rates. Potentially relevant measures
include hormones, immune function, body condition,
oxidative damage, and indicators of organ status, as
well as contaminant burden and parasite load. New
technology for remotely obtaining respiratory, blood
and other tissue samples and for remote assessment
(e.g., visual assessment of body condition) should also
be pursued.
Recommendation: Agencies charged with monitoring and managing the effects of human activities
on marine mammals should identify baselines and
document exposures to stressors for high priority populations. High priority populations should be
selected to include those likely to experience extremes
(both high and low) of stressor exposure in order to
increase the probability of detecting relationships. This
will require stable, long-term funding to maintain a
record of exposures and responses that could inform
future management decisions. Information on base-
lines and contextual variables are critically important to
interpreting responses.
Recommendation: Responsible agencies should
develop relatively inexpensive surveillance systems
that can provide early detection of major changes
in population status. Surveillance systems should
be developed irst for populations that currently lack
adequate stock assessments. To be most effective in
providing an early warning, the variables monitored
will depend on the species and situation, and may
change over time with development of new technology
and increasing ecological knowledge.
Recommendation: Adaptive management should
be used to identify which combinations of stressors
pose risks to marine mammal populations, and to
select which stressors to reduce once a risk is identiied. Once a population of marine mammals has been
found to be at risk, managers need to identify a stressor
or suite of stressors whose reduction can reduce this risk.
This suggests a new form of effect study – “subtractive
experiments” that remove or reduce one or more stressors to characterize the effect of the reduction. This
experimental design may be more appropriate for
adaptive management than the more traditional experiments that add stressors to the current baseline.
COMMITTEE ON ASSESSMENT OF THE CUMULATIVE EFFECTS ON ANTHROPOGENIC
STRESSORS ON MARINE MAMMALS
Peter Tyack (Chair), University of St. Andrews, UK; Helen Bailey, University of Maryland, Solomans; Daniel Crocker,
Sonoma State University, CA; James Estes, University of California, Santa Cruz; Clinton Francis, California Polytechnic State University; John Harwood, University of St. Andrews, Ceres Cupar, UK; Lori Schwacke, NOAA Hollings
Marine Laboratory, Charleston, SC; Len Thomas; University of St. Andrews, UK; Douglas Wartzok, Florida International University; Kim Waddell (Study Director, Gulf Research Program); Stacee Karras (Associate Program Oficer,
Ocean Studies Board), Payton Kulina (Senior Program Assistant, Ocean Studies Board)
For More Information . . . This Report Highlights was prepared by the Ocean Studies Board based on the report
Approaches to Understanding the Cumulative Effects of Stressors on Marine Mammals. The study was sponsored by the
Bureau of Ocean Energy Management, Marine Mammal Commission, National Oceanic and Atmospheric Administration, and Ofice of Naval Research. Any opinions, indings, conclusions, or recommendations expressed in this
publication are those of the authoring committee and do not necessarily relect those of the sponsors. Copies of the
report are available from the National Academies Press, (800) 624-6242; http://www.nap.edu.
Division on Earth and Life Studies
Copyright 2016 by the National Academy of Sciences. All rights reserved.