Marine top predators as climate and ecosystem sentinels

I an era of unprecedented environmental change, developing a suite of tools for ecosystem monitoring is critical. This need is particularly urgent in marine ecosystems, given the rapid, climatedriven changes in marine populations and communities (Poloczanska et al. 2013). Comprehensive monitoring in marine ecosystems presents a challenge due to difficulties inherent in observing the highly dynamic ocean environment at relevant timescales. Traditional shipbased surveys are expensive, autonomous floats and underwater vehicles are still sparsely distributed, and remote sensing fails to capture threedimensional ocean structure. Furthermore, ecological monitoring in the open ocean is largely extractive and often involves lethal sampling of animal communities. In the undersampled marine realm, innovative and costeffective tools that can rapidly assess ecosystem responses to environmental change are vital. “Sentinel” species have been proposed as a means to provide information about unobserved components of the ecosystem (Zacharias and Roff 2001). Classic examples of sentinels include a domesticated variety of the canary (Serinus canaria), which was formerly used to monitor air quality in coal mines, and invertebrates, whose diversity has been used as an indicator of aquatic ecosystem health (Wilhm and Dorris 1968; Barry 2013). More recent studies show that vertebrate species can serve as sentinels of human health and environmental pollution (Bossart 2006; Smits and Fernie 2013), as well as coupled climate–ecosystem processes (Moore 2008). Useful sentinel species should integrate broader processes into rapidly interpretable metrics that reflect underlying ecosystem processes. Marine top predators (including certain species of predatory fish, seabirds, sea turtles, and marine mammals) have been proposed as ecosystem sentinels based on their conspicuous nature and capacity to indicate or respond to changes in ecosystem structure and function that would otherwise be difficult to observe directly (Figure 1; Bossart 2006; Boersma 2008; Moore 2008). Many marine top predators possess key characteristics of sentinel species, including (1) exhibiting clear responses to environmental variability or change (Sydeman et al. 2015; Fleming et al. 2016), (2) playing important roles in shaping marine food webs (Estes et al. 2016), and (3) indicating anthropogenic impacts on ecosystems (Sergio et al. 2008). Given these characteristics, there is a strong argument for using marine predators as ecosystem sentinels. Despite the contemporary use of marine predators as sentinels (relevant examples are listed in WebTable 1), the absence of a standardized framework for identifying sentinel Marine top predators as climate and ecosystem sentinels

[1]  Víctor M. Eguíluz,et al.  Animal-Borne Telemetry: An Integral Component of the Ocean Observing Toolkit , 2019, Front. Mar. Sci..

[2]  Michele Thums,et al.  Translating Marine Animal Tracking Data into Conservation Policy and Management. , 2019, Trends in ecology & evolution.

[3]  David W Johnston,et al.  Unoccupied Aircraft Systems in Marine Science and Conservation. , 2019, Annual review of marine science.

[4]  C. Wilcox,et al.  Using expert elicitation to rank ecological indicators for detecting climate impacts on Australian seabirds and pinnipeds , 2018, Ecological Indicators.

[5]  S. Hatch,et al.  Individual foraging location, but not dietary, specialization: implications for rhinoceros auklets as samplers of forage fish , 2018, Marine Ecology Progress Series.

[6]  D. Costa,et al.  The political biogeography of migratory marine predators , 2018, Nature Ecology & Evolution.

[7]  F. Mallard,et al.  Climate Sentinels Research Program: Developing Indicators of the Effects of Climate Change on Biodiversity in the Region of New Aquitaine (South West, France) , 2018, Climate Change Management.

[8]  A. Diamond,et al.  Seabird diets as bioindicators of Atlantic herring recruitment and stock size: a new tool for ecosystem-based fisheries management , 2018, Canadian Journal of Fisheries and Aquatic Sciences.

[9]  H. Weimerskirch,et al.  Massive decline of the world’s largest king penguin colony at Ile aux Cochons, Crozet , 2018, Antarctic Science.

[10]  K. Hunt,et al.  Quantifying hormones in exhaled breath for physiological assessment of large whales at sea , 2018, Scientific Reports.

[11]  Ward Appeltans,et al.  Essential ocean variables for global sustained observations of biodiversity and ecosystem changes , 2018, Global change biology.

[12]  Liliane Lodi,et al.  Citizen science contributes to the understanding of the occurrence and distribution of cetaceans in southeastern Brazil – A case study , 2018 .

[13]  James V. Carretta,et al.  Population growth and status of california sea lions , 2018 .

[14]  James D. Scott,et al.  Forcing of Multiyear Extreme Ocean Temperatures that Impacted California Current Living Marine Resources in 2016 , 2018 .

[15]  Kristin N. Marshall,et al.  Competing tradeoffs between increasing marine mammal predation and fisheries harvest of Chinook salmon , 2017, Scientific Reports.

[16]  Fortune telling seabirds: sooty shearwaters (Puffinus griseus) predict shifts in Pacific climate , 2017 .

[17]  Patrick N. Halpin,et al.  Google Haul Out: Earth Observation Imagery and Digital Aerial Surveys in Coastal Wildlife Management and Abundance Estimation , 2017, Bioscience.

[18]  Kirstin K. Holsman,et al.  Defining ecosystem thresholds for human activities and environmental pressures in the California Current , 2017 .

[19]  Eric R. Dougherty,et al.  Suite of simple metrics reveals common movement syndromes across vertebrate taxa , 2017, Movement ecology.

[20]  S. Amstrup,et al.  Conservation status of polar bears (Ursus maritimus) in relation to projected sea-ice declines , 2016, Biology Letters.

[21]  M. Heithaus,et al.  Megafaunal Impacts on Structure and Function of Ocean Ecosystems , 2016 .

[22]  N. Holbrook,et al.  Fisheries management approaches as platforms for climate change adaptation: Comparing theory and practice in Australian fisheries , 2016 .

[23]  Elizabeth A. Fulton,et al.  Developing priority variables (“ecosystem Essential Ocean Variables” — eEOVs) for observing dynamics and change in Southern Ocean ecosystems , 2016 .

[24]  Irina Koester,et al.  Biological Impacts of the 2013–2015 Warm-Water Anomaly in the Northeast Pacific: Winners, Losers, and the Future , 2016 .

[25]  D. Grémillet,et al.  Seeing the ocean through the eyes of seabirds: a new path for marine conservation? , 2016 .

[26]  Kim Holland,et al.  Key Questions in Marine Megafauna Movement Ecology. , 2016, Trends in ecology & evolution.

[27]  M. Wikelski,et al.  Living sentinels for climate change effects , 2016, Science.

[28]  A. R. Thompson,et al.  Food limitation of sea lion pups and the decline of forage off central and southern California , 2016, Royal Society Open Science.

[29]  J. Calambokidis,et al.  Humpback whale diets respond to variance in ocean climate and ecosystem conditions in the California Current , 2016, Global change biology.

[30]  W. Sydeman,et al.  Climate change and marine vertebrates , 2015, Science.

[31]  J. George,et al.  Change in the Beaufort Sea ecosystem: Diverging trends in body condition and/or production in five marine vertebrate species , 2015 .

[32]  E. Ezcurra,et al.  Seabird diet predicts following-season commercial catch of Gulf of California Pacific Sardine and Northern Anchovy , 2015 .

[33]  K. Hyrenbach,et al.  Shearwaters as ecosystem indicators: Towards fishery-independent metrics of fish abundance in the California Current , 2015 .

[34]  M. Horn,et al.  A shallow-diving seabird predator as an indicator of prey availability in southern California waters: A longitudinal study , 2015 .

[35]  Laura A. Friedrich,et al.  Public perceptions of sharks: Gathering support for shark conservation , 2014 .

[36]  Carl Wunsch,et al.  Estimates of the Southern Ocean general circulation improved by animal‐borne instruments , 2013 .

[37]  Maeve Barry Canaries in the coal mine , 2013, European Respiratory Journal.

[38]  Carrie V. Kappel,et al.  Global imprint of climate change on marine life , 2013 .

[39]  K. Fernie,et al.  Avian wildlife as sentinels of ecosystem health. , 2013, Comparative immunology, microbiology and infectious diseases.

[40]  Helen Bailey,et al.  Ontogeny in marine tagging and tracking science: technologies and data gaps , 2012 .

[41]  D. Madigan,et al.  Pacific bluefin tuna transport Fukushima-derived radionuclides from Japan to California , 2012, Proceedings of the National Academy of Sciences.

[42]  H. Weimerskirch,et al.  Changes in Wind Pattern Alter Albatross Distribution and Life-History Traits , 2012, Science.

[43]  J. A. van Franeker,et al.  Monitoring plastic ingestion by the northern fulmar Fulmarus glacialis in the North Sea. , 2011, Environmental pollution.

[44]  K. M. Schaefer,et al.  Tracking apex marine predator movements in a dynamic ocean , 2011, Nature.

[45]  G. Bossart,et al.  Marine Mammals as Sentinel Species for Oceans and Human Health , 2011, Veterinary pathology.

[46]  S. Edwards,et al.  Temporal increase in organic mercury in an endangered pelagic seabird assessed by century-old museum specimens , 2011, Proceedings of the National Academy of Sciences.

[47]  W. Trivelpiece,et al.  Variability in krill biomass links harvesting and climate warming to penguin population changes in Antarctica , 2011, Proceedings of the National Academy of Sciences.

[48]  Paul L. Koch,et al.  Using stable isotope biogeochemistry to study marine mammal ecology , 2010 .

[49]  Steven J. Bograd,et al.  Biologging technologies: new tools for conservation. Introduction , 2010 .

[50]  P. Levin,et al.  Integrated Ecosystem Assessments: Developing the Scientific Basis for Ecosystem-Based Management of the Ocean , 2009, PLoS biology.

[51]  J. Harvey,et al.  Temporal variability in ocean climate and California sea lion diet and biomass consumption: implications for fisheries management , 2008 .

[52]  M. Parsons,et al.  Seabirds as indicators of the marine environment , 2008 .

[53]  T. Caro,et al.  Top Predators as Conservation Tools: Ecological Rationale, Assumptions, and Efficacy , 2008 .

[54]  P. Boersma,et al.  Penguins as Marine Sentinels , 2008 .

[55]  Sue E. Moore,et al.  Marine mammals as ecosystem sentinels , 2008 .

[56]  S. Wanless,et al.  Seabirds as environmental indicators: the advantages of combining data sets , 2007 .

[57]  Suzann G. Speckman,et al.  Seabirds as indicators of marine food supplies: Cairns revisited , 2007 .

[58]  J. Lubchenco,et al.  Delayed upwelling alters nearshore coastal ocean ecosystems in the northern California current , 2007, Proceedings of the National Academy of Sciences.

[59]  Russell W. Bradley,et al.  Planktivorous auklet Ptychoramphus aleuticus responses to ocean climate, 2005: Unusual atmospheric blocking? , 2006 .

[60]  Michael J. Weise,et al.  Movement and diving behavior of male California sea lion (Zalophus californianus) during anomalous oceanographic conditions of 2005 compared to those of 2004 , 2006 .

[61]  G. Bossard Marine Mammals as Sentinel Species for Oceans and Human Health , 2006 .

[62]  Scott R. Benson,et al.  From wind to whales: trophic links in a coastal upwelling system , 2005 .

[63]  M. Zacharias,et al.  Use of focal species in marine conservation and management: a review and critique , 2001 .

[64]  R. Furness,et al.  Seabird-fishery interactions : quantifying the sensitivity of seabirds to reductions in sandeel abundance, and identification of key areas for sensitive seabirds in the North Sea , 2000 .

[65]  J. R. Nicolas,et al.  THE DISTRIBUTION OF THE HUMPBACK WHALE, MEGAPTERA NOVAEANGLIAE, ON GEORGES BANK AND IN THE GULF OF MAINE IN RELATION 10 DENSITIES OF THE SAND EEL, AMMODYTES AMERICANUS , 1986 .

[66]  J. Wilhm,et al.  Biological Parameters for Water Quality Criteria , 1968 .