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OSM Workshop on “Top predators as indicators of climate change:
Statistical techniques, challenges and opportunities”
by Elliott Hazen, Rob Suryan, Takashi Yamamoto and Steven Bograd Identify sentinel species and life history characteristics
that may best reveal responses to physical andbiological changes;
 Discuss synthetic approaches, beyond single measurement
types, that are needed to understand how climate
variability and change is integrated by top predator
behavior, distribution, abundance, and demography;
 Prepare a statement outlining the need for enhanced
sampling for top predator response to the predicted
2014–2015 El Niño event; Outline and write a review paper on a framework forassessing climate response in North Pacific top predators
 Realize the goal of an interdisciplinary, North Pacificwide funding proposal to synthesize top predator
datasets relative to potential climate change effects;
 Continue these efforts in collaboration with CLIOTOP
and IMBER at the 3rd PICES/ICES Symposium on the“Effects of climate change on the world’s oceans” in 2015.

Top predators such as fish, turtles, marine mammals, andseabirds integrate multiple lower trophic level processes
and can also exert top-down control of marine food webs.
Climate change and variability affect the timing andproductivity of pelagic ecosystems. This variability is
integrated into the life histories of top predators, potentiallyaffecting their breeding patterns, migration strategies, diets,and ultimately, fitness and reproductive success. PanPacific data about top predators are generated by surveys,
animal tracking studies, dietary analyses, and measurements of reproductive performance. Environmental andclimate data can be synthesized and compared to ecosystem
responses in many locations. To incorporate top predators
into our understanding of climate change impacts onmarine ecosystems and to support the objectives ofFUTURE, the PICES Advisory Panel on Marine Birds andMammals (AP-MBM) with joint support from IMBER’s
regional program, CLIOTOP (Climate Impacts on OceanicTop Predators), convened this workshop to examine how
top predators have responded, and are predicted to respond,to climatic variability and long term change.

With the primary goal of FUTURE, “To understand andforecast responses of North Pacific marine ecosystems toclimate change and human activities at basin and regional
scales, and to broadly communicate this scientificinformation to members, governments, resource managers,
stakeholders and the public”, top predators are particularly
useful given their integration across the physicalenvironment and multiple trophic levels, making their
responses a metric of ecosystem change. Also, there isstrong public interest in many top predators, making
outreach and engagement easier than for other ecosystemcomponents. Furthermore, a wide variety of data has beencollected on top predators, including multiple responses(behavior, distribution, fitness) to climatic events (e.g., ElNiños) that may give us insight to future long-term changes.

The primary goal of this workshop (W1) was to review
existing examples of observed and predicted top predator
responses to climate change and variability in the North
Pacific. More specifically, we had a number of goals thatcame to light via talks and workshop discussions: Identify existing top predator, ecological, and oceanographic datasets that can be used to examine response toclimate variability and change;
 Review statistical techniques that can be used todifferentiate top predator response from climate
variability and change;

Participants of the top predators workshop.

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There were 22 participants in the workshop. The workshop
included 4 invited talks, 7 contributed talks, and 2 hours ofdiscussion. The talks were organized largely by species
groups, starting with fish predictions as a function of climatechange and finishing with baleen whales.

This invited talk was followed by two more seabird
presentations from Takashi Yamamoto (University ofHokkaido, Japan) and Rob Suryan (Oregon StateUniversity, USA). Yamamoto’s presentation examinedboth tracking data and shipboard sighting surveys ofshearwaters in the Northwest Pacific. He used generalized
additive models to partition sightings data into likelycolony origination and sex, and also to predict changes insea distribution with increased temperatures up to 4°C.
Suryan used a 10-year time series to assess changes incommon murre chick stable isotope signatures and diets asa function of local- and basin-scale environmental forcing.
Specifically, he found a strong relationship between murrenitrogen isotope ratios and local upwelling intensity,suggesting possible trophic level shifts associated withupwelling regimes. It is unclear whether this represents achange in the length of the food chain or change in nitrogenvalues at the base of the food web. In contrast, carbon was
most strongly associated with basin-scale indices of watermass transport impacting nutrient sources.

The presentation by M. Gadea Pérez-Andújar (Universityof Hawaii, USA) reviewed tagging results and verticalmovement of deep-water sharks relative to the oxygen
minimum zone (OMZ). By comparing species withdifferent movement patterns (deep water activity within theOMZ), we may be able to understand how different species
are likely to respond to more prevalent encounters with low
oxygen waters. Rachael Orben (University of California
Santa Cruz, USA) discussed winter movements of blacklegged kittiwake from the Pribilof Islands to the sub-arctic
North Pacific across three winter seasons. She foundhigher use of the Bering Sea during the El Niño conditionsof 2009/10 and that individuals traveled farther, flew more,and used more area in La Niña conditions in 2010/11.
Stable isotopes also showed greater individual variability incarbon isotopes in 2010/11, suggesting a use of a broader
geographic area and/or prey base in this year.
William Sydeman (Farallon Institute for Advanced
Ecosystem Research, USA) gave an invited presentation on
challenges and opportunities for assessment and attributionof climate impacts on North Pacific seabirds. A metaanalysis revealed that increased temperatures had mixedeffects on North Pacific seabirds, highlighting the need formore detailed examination of climate change mechanisms
and responses. Additional important points were that weneed more data and climate projections on mid-trophic
forage species that greatly influence these top predators,
and that we will likely need both mechanistic numericalmodels combined with statistical models to begin teasing
apart the effects of climate variability from change.

Takashi Yamamoto discussing streaked shearwater habitat use in theNorthwest Pacific.

Chandra Goetsch (University of California Santa Cruz,USA) presented results on northern elephant seal foraging
behavior changes and diet switching during the 2010
Central Pacific El Niño. Female elephant seals show
extreme fidelity to their migrations, so changes in diet arelikely a function of prey densities or selectivity by foraging
elephant seals. Diet estimates from fatty acid analysis
differed between ENSO states (negative, neutral, andpositive) with positive, or El Niño, conditions being
significantly different from neutral and negative (La Niña)
conditions. Future analyses will examine specific remotelysensed oceanographic conditions which may be driving thebehavioral and diet changes observed.
Our second invited speaker, Jeffrey Polovina (NOAA
Pacific Islands Fisheries Science Center, USA), spoke
about climate impacts on Hawaiian monk seals andloggerhead sea turtles relative to changes in the North
Pacific Transition Zone (NPTZ). One of the strongest
messages highlighted the complexity in predicting climate

Increased variability in Cassin’s auklet breeding success in recent years.
From W. Sydeman’s presentation.

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change effects on top predators, and why tagging studies
are critical to assess impacts on these species. Specifically,models predicting a northward migration of the NPTZ may
not have a large effect on sea turtles if the Kuroshio
Extension and Bifurcation also migrate northward ensuringthat the “highways” are still aligned with increased
productivity. Furthermore, central place foragers, likemonk seals, that are tied to land may no longer be able toreach critical foraging habitat after northward movement of
the NPTZ, which likely will create population level effects.

and attribute climate effects to top predator ecology anddemography; 3) The importance and need for the synthesis
and analysis of existing data, particularly in extreme years;
and 4) a need to identify life history characteristics andmetrics that are inherent to sentinel species. As part ofthese discussions, we came up with a suite of tasks
mentioned in the objectives above that we hope toaccomplish as part of AP-MBM, FUTURE, and CLIOTOP
upcoming activities.

Our third invited speaker, Kevin Weng (University ofHawaii, USA) gave a presentation on fish futures and howspecies are likely to adapt and respond to climate change.
His talk discussed physiological responses to climatechange and the potential interplay among CO2, O2 andtemperature on fitness. Kevin discussed the use of end-toend (E2E) ecosystem models such as SEAPODYM andAPECOSM that are predicting climate change effects on
distribution and abundance of top predatory fish.
Furthermore, the point was made that we need to seek
integrative funding calls to complete the research necessary
to understand top predator responses to climate variabilityand change. Kevin also discussed the role of CLIOTOP
and highlighted potential joint interests between theFUTURE and CLIOTOP programs on observing andpredicting the effects of climate on top predators.

Box 1. Climate predictions for 2014 suggest that astrong El Niño – potentially similar in magnitude to thestrongest previously recorded ENSO events – isdeveloping in the tropical Pacific that may have large
ecosystem effects throughout the North Pacific. Based ondiscussions from our PICES FUTURE workshop, weemphasize the importance of data collection to monitor
the ecosystem response to the impending El Niño.
Specifically, 1) ensure existing sampling and monitoringprograms on physical and biological oceanography, foragespecies, and top predators are continued, 2) implement
additional sampling to test key mechanistic hypotheses ofecosystem change that were generated during prior ENSO
events, and 3) obligate sufficient funding to compile andanalyze data with respect to previous El Niño events(1982–3/1997–8). Given the broad-reaching effects of El
Niño events on ocean ecosystems, data collection andanalyses should be coordinated throughout PICES
member countries. Understanding the response ofecosystems to extreme climate events is critical tounderstanding how ecosystems may respond in the future
under projected climate change scenarios.
http://www.cpc.ncep.noaa.gov/products/analysis_monitori
ng/enso_disc_apr2014/ensodisc.html.

Brianna Witteveen (University Alaska Kodiak, USA) talked
about the Gulf Apex Predator-Prey (GAP) integrated
research project which is documenting spatial and temporal
patterns in habitat use and consumption estimates of top
predators in the ecosystem around Kodiak Island. These
integrative surveys measured physical oceanography andlower trophic level species (zooplankton and fish) up to top
predator sightings.
Multi-scale data including aerial
surveys, stable isotopes, and individual tracking data werealso collected and can be used collectively to examine
ecological changes in baleen whales since 1997.
Our final presentation was by Kathy Kuletz (U.S. Fish andWildlife, USA) who provided an overview of available atsea survey data for the subarctic and arctic North Pacific.
A suite of studies are underway examining spatial shifts inseabird species and likely population changes such as fornorthern fulmars. Sightings data on seabirds are being
linked to prey and oceanographic data. Long-term datasets
and synthetic studies like these highlight the importance ofunderstanding both responses to climate variability (e.g.,extreme climatic events) but also long-term (20+ years)
trends in top predator distribution and abundance.

First, our use of the term “indicators” refers to sentinel
species that reflect (indicate) the impact of climate change
on upper trophic level species and may serve to highlight oreven lead certain biophysical processes that particularly
impact upper trophic level species. Inclusion of sentinel
species in FUTURE, therefore, fulfills a critical objectiveof assessing ecosystem impacts of climate change. The useof sentinel species to be early “indicators” of climatechange is most appropriate in situations where information

Summary and conclusions from the Workshop
There were several key takeaway messages from theworkshop discussion: 1) A need to define the term“indicator” particularly for top predators; 2) A need to
identify the mechanistic processes necessary to understand
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PICES Press Vol. 22, No. 2obtained from them is not being collected otherwise (e.g.,
top predators can be indicators of prey species such as theabundance of Pacific sand lance, Ammodytes hexapterus,
which is difficult to sample using traditional fisheries
methods).

past events, but also for targeting future research to fillknowledge gaps. It is essential to request adequate funds
for data synthesis in future funding of field data collection.
Fourth, and perhaps most importantly, there was muchdiscussion about understanding climate variability,
particularly extreme years and the top predator response tothese events. There is a suite of potential responses (e.g.,spatial shifts, temporal shifts, dietary changes, fitness anddemographic change). Furthermore, with a potentiallyextreme El Niño event developing in the second half of2014 (see Box 1), there is an urgent need to understandecosystem responses to this event. We have written astatement for distribution among the PICES community
stating the importance of continued measurements and,
where possible, additional data collection. We foresee theneed to collaborate across PICES committees to identify
physical, biological, top predator, and ecosystem dataneeds to measure the response of the North Pacific toclimatic extremes.

Second, understanding mechanisms (for example, PICES2011 Topic Session S2, convened by Alheit, Hazen,
Katugin, Suryan, Watanuki, Yasuda, 2011; Marine Ecology
Progress Series Theme Section 487: 176–304, 2013) of
how sentinel species are affected by climate change iscritical to modeling ecosystem impacts to upper trophic
levels. This effort will require a combination of statistical,numerical, and energy flow modeling approaches toidentify mechanisms. The group also acknowledged that
understanding all mechanisms is unrealistic given the suiteof variables integrated by top predators, but identifying a
few dominant mechanisms is realistic and should be a goalin the future. Particular life history traits may cause various
top predators to respond differently to climate change suchas a) central place forager vs. migratory species, b) trophic
position in the food web, c) specialist vs. generalist
foragers, d) air breather vs. gilled organism. Considerationof these traits have important implications when testing
response mechanisms. We proposed that a subset of theworkshop participants develop a review paper thatexamines the framework needed and mechanisms involved
to understand responses of top predators to climate change.

Acknowledgements We thank the speakers for taking thetime to travel to attend the workshop, summarizing andsharing their data, and contributing to a fruitful discussion.
We would especially like to thank those individuals who
contributed additional time to analyze new datasets
specifically for this workshop. We thank the BIO and POC
Committees, Science Board and the PICES Secretariat for
supporting the workshop and for providing travel funds forour invited speakers. We also thank CLIOTOP for cosponsoring an invited speaker for the session.

Third, there is still much to be learned by compiling andanalyzing existing datasets, particularly in response toextreme climatic events. This is critical for learning fromDr. Elliott Hazen (elliott.hazen@noaa.gov) is an ecologist at NOAA’s Southwest Fisheries Science Center, Environmental Research
Division, in Pacific Grove, California. His research interests include a range of topics from fine-scale foraging ecology of top predators
to modeling the effects of climate change on top predator habitat and biodiversity. In addition, he is currently working on creatingecosystem indicators for the California Current large marine ecosystem.
Dr. Steven Bograd (steven.bograd@noaa.gov) is a physical oceanographer (with Elliott Hazen) at NOAA’s Southwest Fisheries ScienceCenter, Environmental Research Division, in Pacific Grove, California. Steven is currently involved in a number of research projects
studying climate variability and its impacts on the marine ecosystems of the North Pacific Ocean, and is Editor-in-Chief of Fisheries
Oceanography. Steven has been active in PICES for many years, and is a member of the Physical Oceanography Committee and WG 27
on North Pacific Climate Variability and Change. He chairs the Advisory Panel on Anthropogenic Influences on Coastal Ecosystems.
Dr. Takashi Yamamoto (taka.y@nipr.ac.jp) is a postdoctoral fellow of Arctic Environment Research Center at National Institute of Polar
Research (working at Hokkaido University) in Japan. His research specialty is the spatial ecology of top predators, especially seabirds.
Recently his research interests include behavioural and morphological adaptations of animals to local marine environment, and also
understanding the factors influencing species distribution and predicting species response to climate-related changes using habitat
modelling techniques.
Dr. Rob Suryan (rob.suryan@oregonstate.edu) is an Associate Professor - Senior Research in the Department of Fisheries and Wildlife
at Oregon State University. His research focuses on marine ecosystem processes and their effect on foraging, reproduction, andpopulation dynamics of mid to upper trophic-level predators and human-resource interactions.

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