Sea Otters And Wolves
Study area. (A) Temporal sequence of sea otter colonization of Glacier Bay National Park and Preserve and Pleasant Island in Icy Straight, Alaska, USA. (B) Sea otter consumption by wolves occurred in areas with the highest estimated sea otter densities (21, 24), but the relative frequency of sea otter in wolf scats was highest in Glacier Bay and Pleasant Island (26, 28).
________________________________________________
Recovery of a marine keystone predator transforms terrestrial predator–prey dynamics
Gretchen H. Roffler orcid.org/0000-0002-8534-3664 gretchen.roffler@alaska.gov, Charlotte E. Eriksson, Jennifer M. Allen, and Taal Levi orcid.org/0000-0003-1853-8311 taal.levi@oregonstate.eduAuthors Info & Affiliations
Edited by Mary Power, University of California Berkeley, CA; received May 25, 2022; accepted November 7, 2022
January 23, 2023
120 (5) e2209037120
doi.org/10.1073/pnas.2209037120
7,002
Metrics
7,002
Last 12 Months
7,002
Vol. 120 | No. 5
Significance
Abstract
Results
Discussion
Materials and Methods
Data, Materials, and Software Availability
Acknowledgments
Supporting Information
References
Significance
While there has been much effort to understand how sea otter recovery transforms nearshore ecosystems, the effects on terrestrial systems have remained uninvestigated. We documented a transboundary food web interaction resulting from the recolonization of sea otters in Icy Straight, Alaska, which provided an ample marine subsidy to island wolves, and subsequently caused extirpation of a terrestrial ungulate. This defies former predictions of predator–prey dynamics which do not account for increasingly abundant and predictable subsidies such that occur on the forefront of the sea otter recovery wave. Although disruption of terrestrial consumer-resource dynamics was previously unforeseen, it hints at both the possibility that these interactions occurred historically and could also become more widespread as sea otters continue to rebound.
Abstract
Sea otters (Enhydra lutris) and wolves (Canis lupus) are two apex predators with strong and cascading effects on ecosystem structure and function. After decades of recovery from near extirpation, their ranges now overlap, allowing sea otters and wolves to interact for the first time in the scientific record. We intensively studied wolves during 2015 to 2021 in an island system colonized by sea otters in the 2000s and by wolves in 2013. After wolf colonization, we quantified shifts in foraging behavior with DNA metabarcoding of 689 wolf scats and stable isotope analyses, both revealing a dietary switch from Sitka black-tailed deer (Odocoileus hemionus), the terrestrial in situ primary prey, to sea otters. Here we show an unexpected result of the reintroduction and restoration of sea otters, which became an abundant marine subsidy for wolves following population recovery. The availability of sea otters allowed wolves to persist and continue to reproduce, subsequently nearly eliminating deer. Genotypes from 390 wolf scats and telemetry data from 13 wolves confirmed island fidelity constituting one of the highest known wolf population densities and upending standardly accepted wolf density predictions based on ungulate abundance. Whereas marine subsidies in other systems are generally derived from lower trophic levels, here an apex nearshore predator became a key prey species and linked nearshore and terrestrial food webs in a recently deglaciated and rapidly changing ecosystem. These results underscore that species restoration may serve as an unanticipated nutrient pathway for recipient ecosystems even resulting in cross-boundary subsidy cascades.
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A widely recognized ecological phenomenon is the connection of ostensibly distinct systems through the transboundary movement of resources (1). Allochthonous subsidies such as marine resources commonly increase productivity of terrestrial systems through the transport of nutrients by physical or biotic agents, or through movement of organisms (1, 2), and may directly or indirectly affect terrestrial food webs and population dynamics (1, 3). The effect of allochthonous subsidies from a donor system depends upon characteristics of the consumer and the focal habitat; more mobile and generalist consumers inhabiting permeable ecosystem boundaries or landscapes with a higher edge to area ratio may receive increased subsidies (1, 4, 5). The magnitude and the timing of the availability of marine subsidies is also influential to predator–prey dynamics. Seasonal availability may result in prey switching, or temporarily satiate predators, easing pressure on resident prey (i.e., apparent mutualism) (6), whereas consistent availability is likely to decouple predator density from local prey availability, resulting in increased predation pressure on resident terrestrial prey (i.e., apparent competition, refs. 3, 7, and 8).
Marine subsidies to large mammalian predators have the potential to be particularly influential given the strong effect apex predators have on their herbivore prey with consequences for vegetation structure and composition. Although wolves (Canis lupus) are considered to be obligate ungulate predators (9) with population densities consistently linked to ungulate density (9, 10), they display a high degree of dietary plasticity and consume a variety of alternative prey (10) including marine resources (11–15). If marine resources are abundant and predictable in space and time, and do not present a risk to obtain, they may allow canid populations to persist despite low abundance of primary prey, which may in effect uncouple their numerical response from ungulate abundance (16–18) leading to apparent competition through increased ungulate predation (19).
Sea otters were once nearly extirpated throughout their North Pacific range but have rapidly recovered in some areas due to reintroduction efforts and legal protection (20, 21). These conservation successes have been hailed not only for recovering an endangered species, but also for restoring a keystone species interaction in nearshore communities (22). Sea otters play an important role as predators of marine invertebrates such that their absence leads to the proliferation of sea urchins, which eliminate kelp forests with concomitant declines in biodiversity (23). Where sea otters recover, they can become extremely abundant. For example, after translocation from the Aleutian Islands in the 1960s, sea otters reached the southern fjord entrance to Glacier Bay National Park in the late 1980s and have continued to expand rapidly (Fig. 1A) before recently approaching local carrying capacity and a population estimate of 8,108 individuals (95% CIs = 6,374, 10,456) (Fig. 2B) in 2018 (24, 25).
Fig. 1.
Study area. (A) Temporal sequence of sea otter colonization of Glacier Bay National Park and Preserve and Pleasant Island in Icy Straight, Alaska, USA. (B) Sea otter consumption by wolves occurred in areas with the highest estimated sea otter densities (21, 24), but the relative frequency of sea otter in wolf scats was highest in Glacier Bay and Pleasant Island (26, 28).
Fig. 2.
Prey population and wolf diet trends. (A) Sitka black-tailed deer abundance and harvest declined on Pleasant Island after wolves became established in 2013. (B) Annual population estimates of sea otters (with 95% credible intervals) in Glacier Bay have increased dramatically since re-establishment. (C) The proportion of sea otters in Pleasant Island wolf diets increased as the proportion of deer decreased, measured by the relative frequency of occurrence of prey identified in scats (D) Isoplot of δ13C and δ15N for Pleasant Island wolf hair indicates increasing relative importance of marine resources in comparison to terrestrial resources coinciding temporally with declines in deer abundance.
We have recently discovered that this profusion of sea otters also serves as a substantial food resource for wolves in the archipelagic landscape of Southeast Alaska and particularly in areas adjacent to Glacier Bay (Fig. 1B) (26, 27) where sea otters are protected and the most abundant marine mammal (25). After decades of recovery, the ranges of wolves and sea otters now overlap allowing these species to interact for the first time in the scientific record. This presents the possibility that the ongoing recolonization of sea otters will, surprisingly, modify species interactions in terrestrial systems and would represent an unusual species interaction in which a keystone marine apex predator also serves as an important bottom-up resource to a terrestrial apex predator.
We report on a serendipitous opportunity to study sea otter-wolf-ungulate interactions focused on Pleasant Island and the adjacent mainland Gustavus Forelands on the periphery of Glacier Bay (Fig. 1A), beginning shortly after wolves became established on Pleasant Island in 2013. From 2015 to 2020, we used two complimentary methods to profile temporal dietary patterns of wolves—DNA metabarcoding of scats and stable isotope analysis of δ13C and δ15N ratios. We evaluated wolf dietary data in combination with population trends of wolves and ungulate prey, human harvest, and winter severity to provide insight on the factors driving predator–prey dynamics. Wolves are highly mobile and typically have a more dispersed home range than their ungulate prey, allowing them to take advantage of patchy resource distribution. To determine whether island wolves were accessing prey available in adjacent mainland systems, we assessed the spatial distribution and movement patterns of wolves by analyzing individual wolf relocation data obtained from GPS-collared wolves and wolf scats genotyped at 38 single nucleotide polymorphic markers (SNPs). In small and isolated populations, such as occur on islands, generalist predators may have large impacts on prey species even leading to local extinctions (5, 27, 28). We found that increasingly abundant marine subsidies decoupled predator–prey (i.e., wolf-ungulate) relationships, as predators switched from ungulates to marine resources. The continued annual reproduction of wolves on a primarily sea otter diet suggests that wolves are not currently energetically limited and that apparent competition between marine and terrestrial prey may prevent the recovery of deer.
Sea Otters And Wolves
Study area. (A) Temporal sequence of sea otter colonization of Glacier Bay National Park and Preserve and Pleasant Island in Icy Straight, Alaska, USA. (B) Sea otter consumption by wolves occurred in areas with the highest estimated sea otter densities (21, 24), but the relative frequency of sea otter in wolf scats was highest in Glacier Bay and Pleasant Island (26, 28).
________________________________________________
Recovery of a marine keystone predator transforms terrestrial predator–prey dynamics
Gretchen H. Roffler orcid.org/0000-0002-8534-3664 gretchen.roffler@alaska.gov, Charlotte E. Eriksson, Jennifer M. Allen, and Taal Levi orcid.org/0000-0003-1853-8311 taal.levi@oregonstate.eduAuthors Info & Affiliations
Edited by Mary Power, University of California Berkeley, CA; received May 25, 2022; accepted November 7, 2022
January 23, 2023
120 (5) e2209037120
doi.org/10.1073/pnas.2209037120
7,002
Metrics
7,002
Last 12 Months
7,002
Vol. 120 | No. 5
Significance
Abstract
Results
Discussion
Materials and Methods
Data, Materials, and Software Availability
Acknowledgments
Supporting Information
References
Significance
While there has been much effort to understand how sea otter recovery transforms nearshore ecosystems, the effects on terrestrial systems have remained uninvestigated. We documented a transboundary food web interaction resulting from the recolonization of sea otters in Icy Straight, Alaska, which provided an ample marine subsidy to island wolves, and subsequently caused extirpation of a terrestrial ungulate. This defies former predictions of predator–prey dynamics which do not account for increasingly abundant and predictable subsidies such that occur on the forefront of the sea otter recovery wave. Although disruption of terrestrial consumer-resource dynamics was previously unforeseen, it hints at both the possibility that these interactions occurred historically and could also become more widespread as sea otters continue to rebound.
Abstract
Sea otters (Enhydra lutris) and wolves (Canis lupus) are two apex predators with strong and cascading effects on ecosystem structure and function. After decades of recovery from near extirpation, their ranges now overlap, allowing sea otters and wolves to interact for the first time in the scientific record. We intensively studied wolves during 2015 to 2021 in an island system colonized by sea otters in the 2000s and by wolves in 2013. After wolf colonization, we quantified shifts in foraging behavior with DNA metabarcoding of 689 wolf scats and stable isotope analyses, both revealing a dietary switch from Sitka black-tailed deer (Odocoileus hemionus), the terrestrial in situ primary prey, to sea otters. Here we show an unexpected result of the reintroduction and restoration of sea otters, which became an abundant marine subsidy for wolves following population recovery. The availability of sea otters allowed wolves to persist and continue to reproduce, subsequently nearly eliminating deer. Genotypes from 390 wolf scats and telemetry data from 13 wolves confirmed island fidelity constituting one of the highest known wolf population densities and upending standardly accepted wolf density predictions based on ungulate abundance. Whereas marine subsidies in other systems are generally derived from lower trophic levels, here an apex nearshore predator became a key prey species and linked nearshore and terrestrial food webs in a recently deglaciated and rapidly changing ecosystem. These results underscore that species restoration may serve as an unanticipated nutrient pathway for recipient ecosystems even resulting in cross-boundary subsidy cascades.
Sign up for PNAS alerts.
Get alerts for new articles, or get an alert when an article is cited.
A widely recognized ecological phenomenon is the connection of ostensibly distinct systems through the transboundary movement of resources (1). Allochthonous subsidies such as marine resources commonly increase productivity of terrestrial systems through the transport of nutrients by physical or biotic agents, or through movement of organisms (1, 2), and may directly or indirectly affect terrestrial food webs and population dynamics (1, 3). The effect of allochthonous subsidies from a donor system depends upon characteristics of the consumer and the focal habitat; more mobile and generalist consumers inhabiting permeable ecosystem boundaries or landscapes with a higher edge to area ratio may receive increased subsidies (1, 4, 5). The magnitude and the timing of the availability of marine subsidies is also influential to predator–prey dynamics. Seasonal availability may result in prey switching, or temporarily satiate predators, easing pressure on resident prey (i.e., apparent mutualism) (6), whereas consistent availability is likely to decouple predator density from local prey availability, resulting in increased predation pressure on resident terrestrial prey (i.e., apparent competition, refs. 3, 7, and 8).
Marine subsidies to large mammalian predators have the potential to be particularly influential given the strong effect apex predators have on their herbivore prey with consequences for vegetation structure and composition. Although wolves (Canis lupus) are considered to be obligate ungulate predators (9) with population densities consistently linked to ungulate density (9, 10), they display a high degree of dietary plasticity and consume a variety of alternative prey (10) including marine resources (11–15). If marine resources are abundant and predictable in space and time, and do not present a risk to obtain, they may allow canid populations to persist despite low abundance of primary prey, which may in effect uncouple their numerical response from ungulate abundance (16–18) leading to apparent competition through increased ungulate predation (19).
Sea otters were once nearly extirpated throughout their North Pacific range but have rapidly recovered in some areas due to reintroduction efforts and legal protection (20, 21). These conservation successes have been hailed not only for recovering an endangered species, but also for restoring a keystone species interaction in nearshore communities (22). Sea otters play an important role as predators of marine invertebrates such that their absence leads to the proliferation of sea urchins, which eliminate kelp forests with concomitant declines in biodiversity (23). Where sea otters recover, they can become extremely abundant. For example, after translocation from the Aleutian Islands in the 1960s, sea otters reached the southern fjord entrance to Glacier Bay National Park in the late 1980s and have continued to expand rapidly (Fig. 1A) before recently approaching local carrying capacity and a population estimate of 8,108 individuals (95% CIs = 6,374, 10,456) (Fig. 2B) in 2018 (24, 25).
Fig. 1.
Study area. (A) Temporal sequence of sea otter colonization of Glacier Bay National Park and Preserve and Pleasant Island in Icy Straight, Alaska, USA. (B) Sea otter consumption by wolves occurred in areas with the highest estimated sea otter densities (21, 24), but the relative frequency of sea otter in wolf scats was highest in Glacier Bay and Pleasant Island (26, 28).
Fig. 2.
Prey population and wolf diet trends. (A) Sitka black-tailed deer abundance and harvest declined on Pleasant Island after wolves became established in 2013. (B) Annual population estimates of sea otters (with 95% credible intervals) in Glacier Bay have increased dramatically since re-establishment. (C) The proportion of sea otters in Pleasant Island wolf diets increased as the proportion of deer decreased, measured by the relative frequency of occurrence of prey identified in scats (D) Isoplot of δ13C and δ15N for Pleasant Island wolf hair indicates increasing relative importance of marine resources in comparison to terrestrial resources coinciding temporally with declines in deer abundance.
We have recently discovered that this profusion of sea otters also serves as a substantial food resource for wolves in the archipelagic landscape of Southeast Alaska and particularly in areas adjacent to Glacier Bay (Fig. 1B) (26, 27) where sea otters are protected and the most abundant marine mammal (25). After decades of recovery, the ranges of wolves and sea otters now overlap allowing these species to interact for the first time in the scientific record. This presents the possibility that the ongoing recolonization of sea otters will, surprisingly, modify species interactions in terrestrial systems and would represent an unusual species interaction in which a keystone marine apex predator also serves as an important bottom-up resource to a terrestrial apex predator.
We report on a serendipitous opportunity to study sea otter-wolf-ungulate interactions focused on Pleasant Island and the adjacent mainland Gustavus Forelands on the periphery of Glacier Bay (Fig. 1A), beginning shortly after wolves became established on Pleasant Island in 2013. From 2015 to 2020, we used two complimentary methods to profile temporal dietary patterns of wolves—DNA metabarcoding of scats and stable isotope analysis of δ13C and δ15N ratios. We evaluated wolf dietary data in combination with population trends of wolves and ungulate prey, human harvest, and winter severity to provide insight on the factors driving predator–prey dynamics. Wolves are highly mobile and typically have a more dispersed home range than their ungulate prey, allowing them to take advantage of patchy resource distribution. To determine whether island wolves were accessing prey available in adjacent mainland systems, we assessed the spatial distribution and movement patterns of wolves by analyzing individual wolf relocation data obtained from GPS-collared wolves and wolf scats genotyped at 38 single nucleotide polymorphic markers (SNPs). In small and isolated populations, such as occur on islands, generalist predators may have large impacts on prey species even leading to local extinctions (5, 27, 28). We found that increasingly abundant marine subsidies decoupled predator–prey (i.e., wolf-ungulate) relationships, as predators switched from ungulates to marine resources. The continued annual reproduction of wolves on a primarily sea otter diet suggests that wolves are not currently energetically limited and that apparent competition between marine and terrestrial prey may prevent the recovery of deer.