The rise of an apex predator following deglaciation

AIM: Sea otters (Enhydra lutris) are an apex predator of the nearshore marine community and nearly went extinct at the turn of the 20th century. Reintroductions and legal protection allowed sea otters to re‐colonize much of their former range. Our objective was to chronicle the colonization of this apex predator in Glacier Bay, Alaska, to help understand the mechanisms that governed their successful colonization. LOCATION: Glacier Bay is a tidewater glacier fjord in southeastern Alaska that was entirely covered by glaciers in the mid‐18th century. Since then, it has endured the fastest tidewater glacier retreat in recorded history. METHODS: We collected and analysed several data sets, spanning 20 years, to document the spatio‐temporal dynamics of an apex predator expanding into an area where they were formerly absent. We used novel quantitative tools to model the occupancy, abundance and colonization dynamics of sea otters, while accounting for uncertainty in the data collection process, the ecological process and model parameters. RESULTS: Twenty years after sea otters were first observed colonizing Glacier Bay, they became one of the most abundant and widely distributed marine mammal. The population grew exponentially at a rate of 20% per year. They colonized Glacier Bay at a maximum rate of 6 km per year, with faster colonization rates occurring early in the colonization process. During colonization, sea otters selected shallow areas, close to shore, with a steep bottom slope, and a relatively simple shoreline complexity index. MAIN CONCLUSIONS: The growth and expansion of sea otters in Glacier Bay demonstrate how legal protection and translocation of apex predators can facilitate their successful establishment into a community in which they were formerly absent. The success of sea otters was, in part, a consequence of habitat that was left largely unperturbed by humans for the past 250 years. Further, sea otters and other marine predators, whose distribution is limited by ice, have the potential to expand in distribution and abundance, reshaping future marine communities in the wake of deglaciation and global loss of sea ice.

[1]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[2]  J. Straley,et al.  Natural history, population dynamics, and habitat use of humpback whales over 30 years on an Alaska feeding ground , 2017 .

[3]  Simon A. Levin,et al.  The Spread of a Reinvading Species: Range Expansion in the California Sea Otter , 1988, The American Naturalist.

[4]  Benjamin Engel,et al.  Biological Invasions: Theory and Practice , 1998 .

[5]  Simon A. Levin,et al.  Spread of invading organisms , 1990, Landscape Ecology.

[6]  P. Turchin Quantitative analysis of movement : measuring and modeling population redistribution in animals and plants , 1998 .

[7]  A. Arendt,et al.  Rapid Wastage of Alaska Glaciers and Their Contribution to Rising Sea Level , 2002, Science.

[8]  M. Hooten,et al.  A general science-based framework for dynamical spatio-temporal models , 2010 .

[9]  C. Fastie,et al.  Causes and Ecosystem Consequences of Multiple Pathways of Primary Succession at Glacier Bay, Alaska , 1995 .

[10]  G. Pendleton,et al.  Harbor seal (Phoca vitulina richardii) decline continues in the rapidly changing landscape of Glacier Bay National Park, Alaska 1992―2008 , 2009 .

[11]  C. Cosner,et al.  Spatial Ecology via Reaction-Diffusion Equations: Cantrell/Diffusion , 2004 .

[12]  J. G. Skellam Random dispersal in theoretical populations , 1951, Biometrika.

[13]  M. Soulé,et al.  Mesopredator release and avifaunal extinctions in a fragmented system , 1999, Nature.

[14]  Mevin B. Hooten,et al.  Homogenization of Large-Scale Movement Models in Ecology with Application to the Spread of Chronic Wasting Disease in Mule Deer , 2012 .

[15]  Mevin B. Hooten,et al.  Computationally Efficient Statistical Differential Equation Modeling Using Homogenization , 2013 .

[16]  Tinker,et al.  Killer whale predation on sea otters linking oceanic and nearshore ecosystems , 1998, Science.

[17]  J. Estes,et al.  Prey choice and habitat use drive sea otter pathogen exposure in a resource-limited coastal system , 2009, Proceedings of the National Academy of Sciences.

[18]  M. Hebblewhite,et al.  A spatially explicit model for an Allee effect: why wolves recolonize so slowly in Greater Yellowstone. , 2006, Theoretical population biology.

[19]  S. Moore,et al.  Arctic marine mammals and climate change: impacts and resilience. , 2008, Ecological applications : a publication of the Ecological Society of America.

[20]  J. Bodkin,et al.  Population Demographics and Genetic Diversity in Remnant and Translocated Populations of Sea Otters , 1999 .

[21]  K. Kenyon The sea otter in the eastern Pacific Ocean , 1975 .

[22]  J. V. Ver Hoef,et al.  Quasi-Poisson vs. negative binomial regression: how should we model overdispersed count data? , 2007, Ecology.

[23]  M. Bigg,et al.  Sea Otters Reestablished in British Columbia , 1978 .

[24]  J. Estes,et al.  Sea Otters and Kelp Forests in Alaska: Generality and Variation in a Community Ecological Paradigm , 1995 .

[25]  Js Oliver,et al.  Influenoe of sea otters on soft-bottom prey communities in southeast Alaska , 1992 .

[26]  Mevin B Hooten,et al.  An integrated data model to estimate spatiotemporal occupancy, abundance, and colonization dynamics. , 2017, Ecology.

[27]  D. Murray,et al.  Modeling the reintroduction of lynx to the southern portion of its range , 2004 .

[28]  J. Bodkin Historic and Contemporary Status of Sea Otters in the North Pacific , 2015 .

[29]  明 大久保,et al.  Diffusion and ecological problems : mathematical models , 1980 .

[30]  R. Veit,et al.  Partial Differential Equations in Ecology: Spatial Interactions and Population Dynamics , 1994 .

[31]  P. Chesson,et al.  Community ecology theory as a framework for biological invasions , 2002 .

[32]  J. Estes,et al.  Aleuts, Sea Otters, and Alternate Stable-State Communities , 1978, Science.

[33]  M. Hebblewhite,et al.  Status and Ecological Effects of the World’s Largest Carnivores , 2014, Science.

[34]  F. Stuart Chapin,et al.  Mechanisms of Primary Succession Following Deglaciation at Glacier Bay, Alaska , 1994 .

[35]  Mevin B. Hooten,et al.  Bayesian Models: A Statistical Primer for Ecologists , 2015 .

[36]  Mevin B. Hooten,et al.  A guide to Bayesian model checking for ecologists , 2018, Ecological Monographs.

[37]  J. Bodkin,et al.  An aerial survey method to estimate sea otter abundance , 2021, Marine Mammal Survey and Assessment Methods.

[38]  G. Vogel,et al.  The Carnivore Comeback , 2006, Science.

[39]  Douglas W. Smith,et al.  Yellowstone after Wolves , 2003 .

[40]  Mevin B. Hooten,et al.  A guide to Bayesian model selection for ecologists , 2015 .

[41]  D. Marks,et al.  ATTACKS ON SEA OTTERS BY KILLER WHALES , 1998 .

[42]  Mevin B. Hooten,et al.  A hierarchical Bayesian non-linear spatio-temporal model for the spread of invasive species with application to the Eurasian Collared-Dove , 2008, Environmental and Ecological Statistics.

[43]  D. Monson,et al.  FORAGING DEPTHS OF SEA OTTERS AND IMPLICATIONS TO COASTAL MARINE COMMUNITIES , 2004 .

[44]  Christopher N. Johnson,et al.  Predator interactions, mesopredator release and biodiversity conservation. , 2009, Ecology letters.

[45]  N. S. Smith,et al.  Sea Otter Predation and Community Organization in the Western Aleutian Islands, Alaska , 1978 .

[46]  Denise L. Doolan,et al.  Killer Whale Predation on Sea Otters Linking Oceanic and Nearshore Ecosystems , 1998 .

[47]  Allen,et al.  HARBOR SEAL (Phoca vitulina richardii) , 2013 .

[48]  D. Esler,et al.  Monitoring population status of sea otters ( Enhydra lutris ) in Glacier Bay National Park and Preserve, Alaska: options and considerations , 2015 .

[49]  J. Bodkin,et al.  The Conservation of Sea Otters: A Prelude , 2015 .

[50]  Thorsten Wiegand,et al.  Assessing the suitability of central European landscapes for the reintroduction of Eurasian lynx , 2002 .

[51]  J. Estes,et al.  Life history plasticity and population regulation in sea otters , 2000 .

[52]  B. Weitzman Effects Of Sea Otter Colonization On Soft-Sediment Intertidal Prey Assemblages In Glacier Bay, Alaska , 2013 .

[53]  J. Estes,et al.  Growth and equilibrium in sea otter populations , 1990 .

[54]  Perry J. Williams,et al.  Monitoring dynamic spatio-temporal ecological processes optimally. , 2017, Ecology.

[55]  J. Estes,et al.  SEA OTTER POPULATION DECLINES IN THE ALEUTIAN ARCHIPELAGO , 2003 .

[56]  G. Pendleton,et al.  DECLINES IN HARBOR SEAL (PHOCA VITULINA) NUMBERS IN GLACIER BAY NATIONAL PARK, ALASKA, 1992–2002 , 2006 .

[57]  Sea otter studies in Glacier Bay National Park and Preserve: Aerial surveys, foraging observations, and intertidal clam sampling , 2001 .

[58]  K. Kenyon,et al.  History and status of translocated sea otter populations in North America , 1982 .

[59]  John M. Maniscalco,et al.  Population growth and colonization of Steller sea lions in the Glacier Bay region of southeastern Alaska: 1970s–2009 , 2011 .

[60]  G. Ellis,et al.  Estimating Carrying Capacity for Sea Otters in British Columbia , 2008 .

[61]  J. Bodkin,et al.  Status and Trends of Sea Otter Populations in Southeast Alaska, 1969-2003 , 2009 .

[62]  Mevin B. Hooten,et al.  Estimating occupancy and abundance using aerial images with imperfect detection , 2017 .

[63]  Christian P. Robert,et al.  Statistics for Spatio-Temporal Data , 2014 .

[64]  D. Duggins Kelp Beds and Sea Otters: An Experimental Approach , 1980 .

[65]  Josefino C. Comiso,et al.  A rapidly declining perennial sea ice cover in the Arctic , 2002 .

[66]  E. K. Pikitch,et al.  Trophic Downgrading of Planet Earth , 2011, Science.

[67]  Mevin B Hooten,et al.  When mechanism matters: Bayesian forecasting using models of ecological diffusion. , 2017, Ecology letters.

[68]  E. Revilla,et al.  Assessment of the Conservation Efforts to Prevent Extinction of the Iberian Lynx , 2011, Conservation biology : the journal of the Society for Conservation Biology.

[69]  R. Mcdonald,et al.  Ecosystem restoration with teeth: what role for predators? , 2012, Trends in ecology & evolution.

[70]  J. Estes,et al.  Sea Otters: Their Role in Structuring Nearshore Communities , 1974, Science.

[71]  R. Fisher THE WAVE OF ADVANCE OF ADVANTAGEOUS GENES , 1937 .

[72]  A. Laliberte,et al.  The Rise of the Mesopredator , 2009 .

[73]  K. Laidre,et al.  Spatial Habitat Use Patterns of Sea Otters in Coastal Washington , 2009 .