迁徙的北极鲑(Salvelinus alpinus)是北极海洋捕食者的猎物。

IF 4.3 2区 环境科学与生态学 Q1 ECOLOGY
Ecology Pub Date : 2025-08-10 DOI:10.1002/ecy.70177
Matthew J. H. Gilbert, Les N. Harris, Alexander L. Vail, Kristin L. Laidre, Mark L. Mallory, David J. Yurkowski
{"title":"迁徙的北极鲑(Salvelinus alpinus)是北极海洋捕食者的猎物。","authors":"Matthew J. H. Gilbert,&nbsp;Les N. Harris,&nbsp;Alexander L. Vail,&nbsp;Kristin L. Laidre,&nbsp;Mark L. Mallory,&nbsp;David J. Yurkowski","doi":"10.1002/ecy.70177","DOIUrl":null,"url":null,"abstract":"<p>Variation in resource distribution and phenology can necessitate that mobile animals move to track resource availability through space and time (Abrahms et al., <span>2021</span>; Furey et al., <span>2018</span>). Northern latitudes are characterized by extreme seasonality in temperature and food availability, making them rich in examples of species' capitalizing on resource waves or pulses (e.g., food and thermally suitable habitat) over the brief summer before either coping with or migrating to avoid resource limitations over winter. An iconic northern example is in Alaskan brown bears (<i>Ursus arctos gyas</i>) that track brief, asynchronous salmon migrations to extend their access to this vital resource (Schindler et al., <span>2013</span>). Marine examples include the bowhead whale (<i>Balaena mysticetus</i>), various seabirds that time feeding and life history events with the recession of the annual sea ice and subsequent production blooms (Mallory &amp; Forbes, <span>2007</span>), and polar bears (<i>Ursus maritimus</i>) that exhibit hyperphagia (strongly elevated appetite) in spring when weaned ringed seal (<i>Pusa hispida</i>) pups are accessible and at peak fatness (Stirling &amp; McEwan, <span>1975</span>). However, given the challenges of northern research (Mallory et al., <span>2018</span>), western scientific documentation of such events is lacking for many species. Here, we showcase images (Figures 1 and 2) of summer aggregations of migratory Arctic char (<i>Salvelinus alpinus</i>) with individual char being hunted and consumed by multiple marine mammal and seabird species. We hypothesize that these events may be examples of resource tracking by Arctic char and their marine predators.</p><p>The Arctic char are the most northerly distributed freshwater or anadromous fish whose range spans across coastal areas of the circumpolar Arctic (Reist et al., <span>2013</span>; Weinstein et al., <span>2024</span>). Anadromy is a common trait in many northern freshwater fishes that involves fish hatching in freshwater, living part of their life at sea, and returning to freshwater for reproduction (McDowall, <span>2008</span>). Adult anadromous Arctic char overwinter and spawn in freshwater, where the young rear under nutrient-poor conditions for several years before their first marine migration (~3–8 years and ~200 mm; Gilbert et al., <span>2016</span>; Johnson, <span>1980</span>). First-time migrants and adults migrate to the ocean in spring, which is in part dictated by the timing of river ice breakup (Figure 1a; Dutil, <span>1986</span>; Gilbert et al., <span>2016</span>; Johnson, <span>1980</span>; Menzies, <span>2024</span>, 23:10). At sea, Arctic char spend the short summer foraging (~4–6 weeks) in a relatively high productivity environment (Harris et al., <span>2022</span>; Johnson, <span>1980</span>). In late summer, they return to freshwater to access spawning and overwintering habitats before freeze-up, avoiding the frigid winter in the Arctic Ocean (Johnson, <span>1980</span>). After returning to freshwater, Arctic char generally cease feeding (Boivin &amp; Power, <span>1990</span>; Dutil, <span>1986</span>). Thus, after the onset of annual marine migrations, nearly all of their required annual energy intake can occur during their 4- to 6-week marine feeding periods, providing a striking example of dependence on resource pulses.</p><p>During marine migrations, Arctic char form predictable aggregations that are spatially and temporally condensed (Figure 1a,b). Even so, some studies have shown that these events may not be periods of high predator-related mortality for Arctic char (Caza-Allard et al., <span>2021</span>; Munaweera et al., <span>2022</span>), nor have they been documented as significant contributors to the overall diet of higher trophic level predators (e.g., seabirds and marine mammals). Here, however, we document numerous seabird and marine mammal predators foraging on aggregations of Arctic char as they enter and forage in the marine environment (Figures 1 and 2). This documentation includes rare observations of the capture of relatively large, anadromous Arctic char by glaucous gulls (<i>Larus hyperboreus</i>), red-throated loons (<i>Gavia stellata</i>), ringed seals, and narwhal (<i>Monodon monoceros</i>). These predators undertake significant migrations which, in this case, may target migratory Arctic char.</p><p>These observations were made in person (A.L. Vail) and from video recorded using a long lens camera (50–1000 mm), drones, and static cameras deployed on land and underwater at Kuuganajuk, Nunavut (Somerset Island; 72°41′0″ N, 93°25′0″ W) in the Canadian Arctic in summer, 2022. Video was captured by an author (A.L. Vail) and colleagues for the documentary, “Our Oceans” (Menzies, <span>2024</span>, 21:19–28:07). Observations of the Arctic char migration from the lake to the ocean and the associated predation events occurred from 25 June to 5 July 2022, during which time a crew filmed for ~14 h/day. Narwhal foraging was observed from 3 to 6 August 2022, during which time filming was limited to 2 days and ~8 h/day due to logistics of reaching the filming locations.</p><p>Arctic seabirds are typically predators with broad diets, but glaucous gulls are the quintessential generalists; they feed on terrestrial and marine prey and are also scavengers (Weiser &amp; Gilchrist, <span>2020</span>). Diets of Arctic loon species are poorly known, but most consume small fish along with freshwater and marine invertebrates during the breeding season (notably red-throated loons; Rizzolo et al., <span>2020</span>). Although diet studies of both glaucous gulls and red-throated loons are limited, the fish they consume are thought to primarily include smaller species such as Arctic cod (<i>Boreogadus saida</i>), capelin (<i>Mallotus villosus</i>), sculpins, sandlance (<i>Ammodytes</i> sp.), and Atlantic herring (<i>Clupea harengus</i>; Elliott &amp; Gaston, <span>2008</span>).</p><p>In the documented interactions between predators and Arctic char (Figure 1d,e; Menzies, <span>2024</span>, 23:57), loons can be seen swimming with numerous adult Arctic char. We used the typical bill length of these birds (60 and 50 mm, respectively) to estimate fish length from the footage. Many Arctic char were about the same length as the loon (~600 mm; Rizzolo et al., <span>2020</span>), meaning that those fish were likely &gt;2000 g (Dutil, <span>1986</span>; Gilbert et al., <span>2016</span>). While these fish are too large for gulls and loons to catch, the largest fish captured were &gt;300 mm or &gt;230 g with an estimated energy content of &gt;1000 kJ (Figure 2c,d; Dutil, <span>1986</span>). Consuming one fish that size would meet the daily maintenance energetic need for adult glaucous gulls (Weiser &amp; Gilchrist, <span>2020</span>) or the daily energy expenditure for post-natal growth of loon chicks (Rizzolo et al., <span>2020</span>) and contain far more energy than the smaller fish typically consumed by these species in the Arctic (Elliott &amp; Gaston, <span>2008</span>). Thus, the pulse of migrating char provides an enormous opportunity for Arctic seabirds during the breeding season or pre-fall migration, periods of high energetic need.</p><p>The life history of ringed seals has been strongly shaped by sea ice dynamics where seals forage more intensively in the productive summer and fall periods to rebuild lost energy stores during the less productive overwintering period (McLaren, <span>1958</span>). Ringed seals are generalist and opportunistic consumers with diets consisting of numerous invertebrate and fish species (Gjertz &amp; Lydersen, <span>1986</span>), which vary with latitude and resource availability (Yurkowski et al., <span>2016</span>). It is general knowledge in some northern communities that ringed seals will consume migrating Arctic char, but char have rarely been documented in western scientific studies of seal stomach contents (e.g., Gjertz &amp; Lydersen, <span>1986</span>). The interactions documented herein depict a pursuit predation event where an individual Arctic char is isolated from a larger aggregation and consumed (Figure 2a,b; Menzies, <span>2024</span>, 24:11 and 24:48). These observations provide additional support that opportunistic foraging by ringed seals on an Arctic char migration pulse may be a regional phenomenon that requires further study.</p><p>The narwhal is a deep-diving cetacean that is endemic to the Arctic (Laidre et al., <span>2015</span>). The narwhal range covers the eastern Canadian high Arctic, West and East Greenland, Svalbard, and Franz Joseph Land (Heide-Jørgensen et al., <span>2013</span>). Narwhals follow the formation and retreat of annual sea ice over the course of extensive annual migrations, and their feeding intensity is generally higher during the over-wintering period. In summer, narwhals spend their time in ice-free bays and fjords of the high Arctic or at glacial fronts (especially around Greenland) consuming shrimp (<i>Pandalus</i> spp.), Arctic cod, polar cod (<i>Arctogadus glacialis</i>), and capelin (Watt et al., <span>2013</span>). In autumn, they migrate to overwintering areas that are deep, offshore, and ice-covered, usually along the continental slope (Laidre et al., <span>2003</span>, <span>2004</span>), where they feed more intensively on Greenland halibut (<i>Reinhardtius hippoglossoides</i>), boreoatlantic armhook squid (<i>Gonatus fabricii</i>), or capelin (Laidre &amp; Heide-Jørgensen, <span>2005</span>; Watt et al., <span>2013</span>). The observations here confirm that narwhals may opportunistically feed on the summer pulse of Arctic char (Figure 2; Menzies, <span>2024</span>, 25:56). However, the extent to which narwhals rely on Arctic char as an annual food source is unknown given the limited spatial and temporal availability, and that such pulses are not available to all summering subpopulations. The images also show narwhals using their tusks to stun Arctic char before consumption (Figure 2e), which agrees with contemporaneous observations by others in the same area (O'Corry-Crowe et al., <span>2025</span>). Footage collected by researchers in the Eastern Canadian Arctic showed narwhals stunning Arctic cod with their tusks, and these independent observations suggest that this is a tactic used by male narwhals.</p><p>Of the four marine predators we describe here, only ringed seals have previously been described in the literature as active predators of anadromous Arctic char (Gjertz &amp; Lydersen, <span>1986</span>). While adult Arctic char are often too large for loons or gulls to consume whole, gulls may still opportunistically feed on large adult char that become stranded in shallow water during their upriver migration (e.g., Gilbert et al., <span>2016</span>), an occurrence that is likely to change in frequency as climate change continues to alter hydrological regimes. Additionally, Arctic char have been anecdotally reported in the diet of loons in Greenland (Weiser &amp; Gilchrist, <span>2020</span>). Marine mammal predator-related mortality is assumed to be low for anadromous adult Arctic char, and such events have rarely been documented despite extensive overlap with piscivorous marine mammals (Finley &amp; Gibb, <span>1982</span>; Matley et al., <span>2015</span>; Moore, <span>1975</span>). For instance, separate studies examined ringed seal diets in spring and summer in the Cumberland Sound region of Nunavut, Canada, and in northwestern Spitsbergen, Svalbard, and found Arctic char in gut contents of only 8% and 4% of seals, respectively (Gjertz &amp; Lydersen, <span>1986</span>; Moore, <span>1975</span>). We could not find any scientific documentation of narwhal hunting Arctic char. Recent studies using archival pop-off tags and traditional and local knowledge from hunters have documented predation events of Arctic char and the closely related Dolly Varden char (<i>Salvelinus malma malma</i>) by beluga whale (<i>Delphinapterus leucas</i>) in the western Canadian Arctic (Gallagher et al., <span>2021</span>; Loseto et al., <span>2018</span>). Cumulatively, these observations and those documented here suggest that large marine mammals, including whales and seals, do occasionally consume anadromous salmonids in the Arctic and are a source of mortality that could be important for some populations. In general, however, marine predation of Arctic salmonids is not well documented, and future studies should focus on populations that may be likely to experience these potentially brief but intense predation events to (1) determine how these events impact mortality rates and population dynamics and (2) understand the broad ecological importance of the fish in their ecosystem.</p><p>The images discussed here depict remarkable behaviors and trophic interactions shaped by the high spatiotemporal variation in resource availability that defines high-latitude environments. The Arctic char are themselves in pursuit of greater food availability as they migrate to the marine environment where they can become predictable prey for several marine predators ready to capitalize on the influx of food. The events discussed here may be examples of intentional resource tracking by these marine predators or may be examples of opportunistic foraging strategies. These possibilities and the relative paucity of western scientific research in the region raise several questions that warrant further investigation. For instance, do these predators track the timing of the Arctic char migration to sea? Does access to these resources influence predator habitat selection? Are these indeed rare events or are they just rarely documented? How important are these prey pulses to predator energy budgets? How are these events going to be shaped by shifts in species' ranges (e.g., killer whales; <i>Orcinus orca</i>) and the timing of seasonal events with ongoing environmental change? While relevant western scientific research in the north has been relatively limited, local people have lived in these regions for millennia, interacting closely with these animals. As such, studies of traditional and local knowledge are a natural starting point for further exploration.</p><p>The authors declare no conflicts of interest.</p>","PeriodicalId":11484,"journal":{"name":"Ecology","volume":"106 8","pages":""},"PeriodicalIF":4.3000,"publicationDate":"2025-08-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://esajournals.onlinelibrary.wiley.com/doi/epdf/10.1002/ecy.70177","citationCount":"0","resultStr":"{\"title\":\"Migratory Arctic char (Salvelinus alpinus) as a prey pulse for Arctic marine predators\",\"authors\":\"Matthew J. H. Gilbert,&nbsp;Les N. Harris,&nbsp;Alexander L. Vail,&nbsp;Kristin L. Laidre,&nbsp;Mark L. Mallory,&nbsp;David J. Yurkowski\",\"doi\":\"10.1002/ecy.70177\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p>Variation in resource distribution and phenology can necessitate that mobile animals move to track resource availability through space and time (Abrahms et al., <span>2021</span>; Furey et al., <span>2018</span>). Northern latitudes are characterized by extreme seasonality in temperature and food availability, making them rich in examples of species' capitalizing on resource waves or pulses (e.g., food and thermally suitable habitat) over the brief summer before either coping with or migrating to avoid resource limitations over winter. An iconic northern example is in Alaskan brown bears (<i>Ursus arctos gyas</i>) that track brief, asynchronous salmon migrations to extend their access to this vital resource (Schindler et al., <span>2013</span>). Marine examples include the bowhead whale (<i>Balaena mysticetus</i>), various seabirds that time feeding and life history events with the recession of the annual sea ice and subsequent production blooms (Mallory &amp; Forbes, <span>2007</span>), and polar bears (<i>Ursus maritimus</i>) that exhibit hyperphagia (strongly elevated appetite) in spring when weaned ringed seal (<i>Pusa hispida</i>) pups are accessible and at peak fatness (Stirling &amp; McEwan, <span>1975</span>). However, given the challenges of northern research (Mallory et al., <span>2018</span>), western scientific documentation of such events is lacking for many species. Here, we showcase images (Figures 1 and 2) of summer aggregations of migratory Arctic char (<i>Salvelinus alpinus</i>) with individual char being hunted and consumed by multiple marine mammal and seabird species. We hypothesize that these events may be examples of resource tracking by Arctic char and their marine predators.</p><p>The Arctic char are the most northerly distributed freshwater or anadromous fish whose range spans across coastal areas of the circumpolar Arctic (Reist et al., <span>2013</span>; Weinstein et al., <span>2024</span>). Anadromy is a common trait in many northern freshwater fishes that involves fish hatching in freshwater, living part of their life at sea, and returning to freshwater for reproduction (McDowall, <span>2008</span>). Adult anadromous Arctic char overwinter and spawn in freshwater, where the young rear under nutrient-poor conditions for several years before their first marine migration (~3–8 years and ~200 mm; Gilbert et al., <span>2016</span>; Johnson, <span>1980</span>). First-time migrants and adults migrate to the ocean in spring, which is in part dictated by the timing of river ice breakup (Figure 1a; Dutil, <span>1986</span>; Gilbert et al., <span>2016</span>; Johnson, <span>1980</span>; Menzies, <span>2024</span>, 23:10). At sea, Arctic char spend the short summer foraging (~4–6 weeks) in a relatively high productivity environment (Harris et al., <span>2022</span>; Johnson, <span>1980</span>). In late summer, they return to freshwater to access spawning and overwintering habitats before freeze-up, avoiding the frigid winter in the Arctic Ocean (Johnson, <span>1980</span>). After returning to freshwater, Arctic char generally cease feeding (Boivin &amp; Power, <span>1990</span>; Dutil, <span>1986</span>). Thus, after the onset of annual marine migrations, nearly all of their required annual energy intake can occur during their 4- to 6-week marine feeding periods, providing a striking example of dependence on resource pulses.</p><p>During marine migrations, Arctic char form predictable aggregations that are spatially and temporally condensed (Figure 1a,b). Even so, some studies have shown that these events may not be periods of high predator-related mortality for Arctic char (Caza-Allard et al., <span>2021</span>; Munaweera et al., <span>2022</span>), nor have they been documented as significant contributors to the overall diet of higher trophic level predators (e.g., seabirds and marine mammals). Here, however, we document numerous seabird and marine mammal predators foraging on aggregations of Arctic char as they enter and forage in the marine environment (Figures 1 and 2). This documentation includes rare observations of the capture of relatively large, anadromous Arctic char by glaucous gulls (<i>Larus hyperboreus</i>), red-throated loons (<i>Gavia stellata</i>), ringed seals, and narwhal (<i>Monodon monoceros</i>). These predators undertake significant migrations which, in this case, may target migratory Arctic char.</p><p>These observations were made in person (A.L. Vail) and from video recorded using a long lens camera (50–1000 mm), drones, and static cameras deployed on land and underwater at Kuuganajuk, Nunavut (Somerset Island; 72°41′0″ N, 93°25′0″ W) in the Canadian Arctic in summer, 2022. Video was captured by an author (A.L. Vail) and colleagues for the documentary, “Our Oceans” (Menzies, <span>2024</span>, 21:19–28:07). Observations of the Arctic char migration from the lake to the ocean and the associated predation events occurred from 25 June to 5 July 2022, during which time a crew filmed for ~14 h/day. Narwhal foraging was observed from 3 to 6 August 2022, during which time filming was limited to 2 days and ~8 h/day due to logistics of reaching the filming locations.</p><p>Arctic seabirds are typically predators with broad diets, but glaucous gulls are the quintessential generalists; they feed on terrestrial and marine prey and are also scavengers (Weiser &amp; Gilchrist, <span>2020</span>). Diets of Arctic loon species are poorly known, but most consume small fish along with freshwater and marine invertebrates during the breeding season (notably red-throated loons; Rizzolo et al., <span>2020</span>). Although diet studies of both glaucous gulls and red-throated loons are limited, the fish they consume are thought to primarily include smaller species such as Arctic cod (<i>Boreogadus saida</i>), capelin (<i>Mallotus villosus</i>), sculpins, sandlance (<i>Ammodytes</i> sp.), and Atlantic herring (<i>Clupea harengus</i>; Elliott &amp; Gaston, <span>2008</span>).</p><p>In the documented interactions between predators and Arctic char (Figure 1d,e; Menzies, <span>2024</span>, 23:57), loons can be seen swimming with numerous adult Arctic char. We used the typical bill length of these birds (60 and 50 mm, respectively) to estimate fish length from the footage. Many Arctic char were about the same length as the loon (~600 mm; Rizzolo et al., <span>2020</span>), meaning that those fish were likely &gt;2000 g (Dutil, <span>1986</span>; Gilbert et al., <span>2016</span>). While these fish are too large for gulls and loons to catch, the largest fish captured were &gt;300 mm or &gt;230 g with an estimated energy content of &gt;1000 kJ (Figure 2c,d; Dutil, <span>1986</span>). Consuming one fish that size would meet the daily maintenance energetic need for adult glaucous gulls (Weiser &amp; Gilchrist, <span>2020</span>) or the daily energy expenditure for post-natal growth of loon chicks (Rizzolo et al., <span>2020</span>) and contain far more energy than the smaller fish typically consumed by these species in the Arctic (Elliott &amp; Gaston, <span>2008</span>). Thus, the pulse of migrating char provides an enormous opportunity for Arctic seabirds during the breeding season or pre-fall migration, periods of high energetic need.</p><p>The life history of ringed seals has been strongly shaped by sea ice dynamics where seals forage more intensively in the productive summer and fall periods to rebuild lost energy stores during the less productive overwintering period (McLaren, <span>1958</span>). Ringed seals are generalist and opportunistic consumers with diets consisting of numerous invertebrate and fish species (Gjertz &amp; Lydersen, <span>1986</span>), which vary with latitude and resource availability (Yurkowski et al., <span>2016</span>). It is general knowledge in some northern communities that ringed seals will consume migrating Arctic char, but char have rarely been documented in western scientific studies of seal stomach contents (e.g., Gjertz &amp; Lydersen, <span>1986</span>). The interactions documented herein depict a pursuit predation event where an individual Arctic char is isolated from a larger aggregation and consumed (Figure 2a,b; Menzies, <span>2024</span>, 24:11 and 24:48). These observations provide additional support that opportunistic foraging by ringed seals on an Arctic char migration pulse may be a regional phenomenon that requires further study.</p><p>The narwhal is a deep-diving cetacean that is endemic to the Arctic (Laidre et al., <span>2015</span>). The narwhal range covers the eastern Canadian high Arctic, West and East Greenland, Svalbard, and Franz Joseph Land (Heide-Jørgensen et al., <span>2013</span>). Narwhals follow the formation and retreat of annual sea ice over the course of extensive annual migrations, and their feeding intensity is generally higher during the over-wintering period. In summer, narwhals spend their time in ice-free bays and fjords of the high Arctic or at glacial fronts (especially around Greenland) consuming shrimp (<i>Pandalus</i> spp.), Arctic cod, polar cod (<i>Arctogadus glacialis</i>), and capelin (Watt et al., <span>2013</span>). In autumn, they migrate to overwintering areas that are deep, offshore, and ice-covered, usually along the continental slope (Laidre et al., <span>2003</span>, <span>2004</span>), where they feed more intensively on Greenland halibut (<i>Reinhardtius hippoglossoides</i>), boreoatlantic armhook squid (<i>Gonatus fabricii</i>), or capelin (Laidre &amp; Heide-Jørgensen, <span>2005</span>; Watt et al., <span>2013</span>). The observations here confirm that narwhals may opportunistically feed on the summer pulse of Arctic char (Figure 2; Menzies, <span>2024</span>, 25:56). However, the extent to which narwhals rely on Arctic char as an annual food source is unknown given the limited spatial and temporal availability, and that such pulses are not available to all summering subpopulations. The images also show narwhals using their tusks to stun Arctic char before consumption (Figure 2e), which agrees with contemporaneous observations by others in the same area (O'Corry-Crowe et al., <span>2025</span>). Footage collected by researchers in the Eastern Canadian Arctic showed narwhals stunning Arctic cod with their tusks, and these independent observations suggest that this is a tactic used by male narwhals.</p><p>Of the four marine predators we describe here, only ringed seals have previously been described in the literature as active predators of anadromous Arctic char (Gjertz &amp; Lydersen, <span>1986</span>). While adult Arctic char are often too large for loons or gulls to consume whole, gulls may still opportunistically feed on large adult char that become stranded in shallow water during their upriver migration (e.g., Gilbert et al., <span>2016</span>), an occurrence that is likely to change in frequency as climate change continues to alter hydrological regimes. Additionally, Arctic char have been anecdotally reported in the diet of loons in Greenland (Weiser &amp; Gilchrist, <span>2020</span>). Marine mammal predator-related mortality is assumed to be low for anadromous adult Arctic char, and such events have rarely been documented despite extensive overlap with piscivorous marine mammals (Finley &amp; Gibb, <span>1982</span>; Matley et al., <span>2015</span>; Moore, <span>1975</span>). For instance, separate studies examined ringed seal diets in spring and summer in the Cumberland Sound region of Nunavut, Canada, and in northwestern Spitsbergen, Svalbard, and found Arctic char in gut contents of only 8% and 4% of seals, respectively (Gjertz &amp; Lydersen, <span>1986</span>; Moore, <span>1975</span>). We could not find any scientific documentation of narwhal hunting Arctic char. Recent studies using archival pop-off tags and traditional and local knowledge from hunters have documented predation events of Arctic char and the closely related Dolly Varden char (<i>Salvelinus malma malma</i>) by beluga whale (<i>Delphinapterus leucas</i>) in the western Canadian Arctic (Gallagher et al., <span>2021</span>; Loseto et al., <span>2018</span>). Cumulatively, these observations and those documented here suggest that large marine mammals, including whales and seals, do occasionally consume anadromous salmonids in the Arctic and are a source of mortality that could be important for some populations. In general, however, marine predation of Arctic salmonids is not well documented, and future studies should focus on populations that may be likely to experience these potentially brief but intense predation events to (1) determine how these events impact mortality rates and population dynamics and (2) understand the broad ecological importance of the fish in their ecosystem.</p><p>The images discussed here depict remarkable behaviors and trophic interactions shaped by the high spatiotemporal variation in resource availability that defines high-latitude environments. The Arctic char are themselves in pursuit of greater food availability as they migrate to the marine environment where they can become predictable prey for several marine predators ready to capitalize on the influx of food. The events discussed here may be examples of intentional resource tracking by these marine predators or may be examples of opportunistic foraging strategies. These possibilities and the relative paucity of western scientific research in the region raise several questions that warrant further investigation. For instance, do these predators track the timing of the Arctic char migration to sea? Does access to these resources influence predator habitat selection? Are these indeed rare events or are they just rarely documented? How important are these prey pulses to predator energy budgets? How are these events going to be shaped by shifts in species' ranges (e.g., killer whales; <i>Orcinus orca</i>) and the timing of seasonal events with ongoing environmental change? While relevant western scientific research in the north has been relatively limited, local people have lived in these regions for millennia, interacting closely with these animals. As such, studies of traditional and local knowledge are a natural starting point for further exploration.</p><p>The authors declare no conflicts of interest.</p>\",\"PeriodicalId\":11484,\"journal\":{\"name\":\"Ecology\",\"volume\":\"106 8\",\"pages\":\"\"},\"PeriodicalIF\":4.3000,\"publicationDate\":\"2025-08-10\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://esajournals.onlinelibrary.wiley.com/doi/epdf/10.1002/ecy.70177\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Ecology\",\"FirstCategoryId\":\"93\",\"ListUrlMain\":\"https://esajournals.onlinelibrary.wiley.com/doi/10.1002/ecy.70177\",\"RegionNum\":2,\"RegionCategory\":\"环境科学与生态学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q1\",\"JCRName\":\"ECOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Ecology","FirstCategoryId":"93","ListUrlMain":"https://esajournals.onlinelibrary.wiley.com/doi/10.1002/ecy.70177","RegionNum":2,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"ECOLOGY","Score":null,"Total":0}
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摘要

北极海鸟是典型的食肉动物,饮食广泛,但白嘴鸥是典型的多面手;它们以陆地和海洋猎物为食,也是食腐动物(Weiser & Gilchrist, 2020)。北极潜鸟的饮食鲜为人知,但大多数在繁殖季节食用小鱼以及淡水和海洋无脊椎动物(特别是红喉潜鸟;Rizzolo等人,2020)。尽管对白嘴鸥和红喉鹭的饮食研究有限,但它们所吃的鱼被认为主要包括较小的物种,如北极鳕鱼(Boreogadus saida)、毛鳞鱼(Mallotus villosus)、石斑鱼、山鳞鱼(Ammodytes sp.)和大西洋鲱鱼(Clupea harengus; Elliott & Gaston, 2008)。在有记载的捕食者与北极char之间的相互作用中(图1d,e; Menzies, 2024, 23:57),可以看到潜鸟与许多成年北极char一起游泳。我们使用这些鸟类的典型喙长(分别为60和50毫米)来估计鱼类的长度。许多北极鲑的长度与潜龙差不多(~600毫米;Rizzolo等人,2020),这意味着这些鱼可能有2000克(Dutil, 1986; Gilbert等人,2016)。虽然这些鱼太大,海鸥和潜水器无法捕获,但捕获的最大鱼为300毫米或230克,估计能量含量为1000千焦耳(图2c,d; Dutil, 1986)。食用一条这样大小的鱼可以满足成年白头鸥的日常能量维持需求(Weiser & & Gilchrist, 2020),也可以满足长尾海鸥出生后的日常能量消耗(Rizzolo et al., 2020),而且含有的能量远远超过北极地区这些物种通常消耗的小鱼(Elliott & & Gaston, 2008)。因此,在繁殖季节或秋季前的迁徙期间,迁徙炭的脉动为北极海鸟提供了巨大的机会,这是能量需求旺盛的时期。环斑海豹的生活史在很大程度上受到海冰动态的影响,海豹在多产的夏季和秋季更密集地觅食,以便在生产力较低的越冬期间重建失去的能量储存(McLaren, 1958)。环斑海豹是多面手和机会主义消费者,其饮食包括许多无脊椎动物和鱼类(Gjertz & Lydersen, 1986),其饮食随纬度和资源可用性而变化(Yurkowski et al., 2016)。在一些北方群落中,人们普遍知道环海豹会食用迁徙的北极炭,但在西方对海豹胃内容物的科学研究中,很少有关于炭的记录(例如,Gjertz & Lydersen, 1986)。这里记录的相互作用描述了一个追捕捕食事件,在这个事件中,单个北极char从更大的聚集中被隔离并被吃掉(图2a,b; Menzies, 2024, 24:11和24:48)。这些观察结果提供了额外的支持,即环斑海豹在北极炭迁移脉冲上的机会性觅食可能是一种区域现象,需要进一步研究。独角鲸是北极特有的深潜鲸类动物(Laidre et al., 2015)。独角鲸的活动范围包括加拿大东部的北极高地、格陵兰岛的西部和东部、斯瓦尔巴群岛和弗朗茨约瑟夫地(heade - j ørgensen et al., 2013)。在广泛的年度迁徙过程中,独角鲸跟随每年海冰的形成和消退,在越冬期间,它们的摄食强度通常更高。夏季,独角鲸在北极高纬度的无冰海湾和峡湾或冰川前沿(尤其是格陵兰岛附近)度过时间,食用虾(Pandalus spp.)、北极鳕鱼、极地鳕鱼(Arctogadus glacialis)和毛鳞鱼(Watt et al., 2013)。在秋季,它们迁移到深海、近海和冰雪覆盖的越冬地区,通常沿着大陆斜坡(Laidre等人,2003年,2004年),在那里它们更密集地捕食格陵兰大比目鱼(Reinhardtius hippoglossoides)、北大西洋臂钩鱿鱼(Gonatus fabricii)或毛鳞鱼(Laidre & Heide-Jørgensen, 2005; Watt等人,2013)。这里的观察证实,独角鲸可能会机会性地以北极木炭的夏季脉冲为食(图2;Menzies, 2024, 25:56)。然而,考虑到有限的空间和时间可用性,独角鲸依赖北极炭作为年度食物来源的程度尚不清楚,而且并非所有夏季亚群都能获得这种脉冲。这些图像还显示,独角鲸在食用北极鲑之前会用它们的长牙击晕它们(图2e),这与同一地区其他人的同期观察结果一致(O'Corry-Crowe et al., 2025)。研究人员在加拿大东部北极地区收集的视频显示,独角鲸用它们的长牙震惊了北极鳕鱼,这些独立的观察表明,这是雄性独角鲸使用的一种策略。在我们这里描述的四种海洋捕食者中,只有环斑海豹在以前的文献中被描述为北冰洋鲑鱼的活跃捕食者(Gjertz & Lydersen, 1986)。 虽然成年北极炭通常太大,使潜鸟或海鸥无法吃掉整个,但海鸥仍可能会机会主义地以在上游迁徙过程中搁浅在浅水中的大型成年炭为食(例如,Gilbert等人,2016),随着气候变化继续改变水文制度,这种情况可能会发生频率变化。此外,格陵兰岛的潜水器饮食中也有北极炭的轶事报道(Weiser & Gilchrist, 2020)。海洋哺乳动物与捕食者相关的死亡率被认为是低的,尽管与鱼食性海洋哺乳动物有广泛的重叠,但这种事件很少有记录(Finley & Gibb, 1982; Matley et al., 2015; Moore, 1975)。例如,单独的研究分别在加拿大努纳维特的坎伯兰海峡地区和斯瓦尔巴群岛的斯匹次卑尔根群岛西北部调查了环斑海豹在春季和夏季的饮食,分别发现只有8%和4%的海豹在肠道内容物中含有北极碳(Gjertz & Lydersen, 1986; Moore, 1975)。我们找不到任何独角鲸捕杀北极鲑的科学文献。最近的研究利用档案标签和猎人的传统和当地知识,记录了加拿大北极西部白鲸(Delphinapterus leucas)捕食北极鲑和密切相关的Dolly Varden鲑(Salvelinus malma malma)的事件(Gallagher等人,2021;Loseto等人,2018)。总的来说,这些观察和记录表明,包括鲸鱼和海豹在内的大型海洋哺乳动物偶尔会在北极吃掉产卵的鲑鱼,这对某些种群来说可能是一个重要的死亡来源。然而,总的来说,北极鲑鱼的海洋捕食并没有得到很好的记录,未来的研究应该集中在可能经历这些潜在的短暂但强烈的捕食事件的种群上,以(1)确定这些事件如何影响死亡率和种群动态,(2)了解鱼类在其生态系统中的广泛生态重要性。这里讨论的图像描绘了由高纬度环境中资源可用性的高时空变化所塑造的显著行为和营养相互作用。北极鲑本身就是为了寻找更多的食物,因为它们迁徙到海洋环境中,在那里它们可以成为一些海洋捕食者的猎物,随时准备利用大量的食物。这里讨论的事件可能是这些海洋捕食者有意追踪资源的例子,也可能是机会主义觅食策略的例子。这些可能性和西方科学研究在该地区的相对缺乏提出了几个值得进一步调查的问题。例如,这些捕食者会追踪北极鲑鱼迁徙到海洋的时间吗?获取这些资源是否会影响捕食者的栖息地选择?这些确实是罕见的事件,还是只是很少有记录?这些猎物脉冲对捕食者的能量预算有多重要?这些事件将如何被物种范围的变化(例如,虎鲸;逆戟鲸)和季节性事件的时间与持续的环境变化所影响?虽然西方在北方的相关科学研究相对有限,但当地人已经在这些地区生活了数千年,与这些动物密切互动。因此,对传统和地方知识的研究是进一步探索的自然起点。作者声明无利益冲突。
本文章由计算机程序翻译,如有差异,请以英文原文为准。

Migratory Arctic char (Salvelinus alpinus) as a prey pulse for Arctic marine predators

Migratory Arctic char (Salvelinus alpinus) as a prey pulse for Arctic marine predators

Migratory Arctic char (Salvelinus alpinus) as a prey pulse for Arctic marine predators

Variation in resource distribution and phenology can necessitate that mobile animals move to track resource availability through space and time (Abrahms et al., 2021; Furey et al., 2018). Northern latitudes are characterized by extreme seasonality in temperature and food availability, making them rich in examples of species' capitalizing on resource waves or pulses (e.g., food and thermally suitable habitat) over the brief summer before either coping with or migrating to avoid resource limitations over winter. An iconic northern example is in Alaskan brown bears (Ursus arctos gyas) that track brief, asynchronous salmon migrations to extend their access to this vital resource (Schindler et al., 2013). Marine examples include the bowhead whale (Balaena mysticetus), various seabirds that time feeding and life history events with the recession of the annual sea ice and subsequent production blooms (Mallory & Forbes, 2007), and polar bears (Ursus maritimus) that exhibit hyperphagia (strongly elevated appetite) in spring when weaned ringed seal (Pusa hispida) pups are accessible and at peak fatness (Stirling & McEwan, 1975). However, given the challenges of northern research (Mallory et al., 2018), western scientific documentation of such events is lacking for many species. Here, we showcase images (Figures 1 and 2) of summer aggregations of migratory Arctic char (Salvelinus alpinus) with individual char being hunted and consumed by multiple marine mammal and seabird species. We hypothesize that these events may be examples of resource tracking by Arctic char and their marine predators.

The Arctic char are the most northerly distributed freshwater or anadromous fish whose range spans across coastal areas of the circumpolar Arctic (Reist et al., 2013; Weinstein et al., 2024). Anadromy is a common trait in many northern freshwater fishes that involves fish hatching in freshwater, living part of their life at sea, and returning to freshwater for reproduction (McDowall, 2008). Adult anadromous Arctic char overwinter and spawn in freshwater, where the young rear under nutrient-poor conditions for several years before their first marine migration (~3–8 years and ~200 mm; Gilbert et al., 2016; Johnson, 1980). First-time migrants and adults migrate to the ocean in spring, which is in part dictated by the timing of river ice breakup (Figure 1a; Dutil, 1986; Gilbert et al., 2016; Johnson, 1980; Menzies, 2024, 23:10). At sea, Arctic char spend the short summer foraging (~4–6 weeks) in a relatively high productivity environment (Harris et al., 2022; Johnson, 1980). In late summer, they return to freshwater to access spawning and overwintering habitats before freeze-up, avoiding the frigid winter in the Arctic Ocean (Johnson, 1980). After returning to freshwater, Arctic char generally cease feeding (Boivin & Power, 1990; Dutil, 1986). Thus, after the onset of annual marine migrations, nearly all of their required annual energy intake can occur during their 4- to 6-week marine feeding periods, providing a striking example of dependence on resource pulses.

During marine migrations, Arctic char form predictable aggregations that are spatially and temporally condensed (Figure 1a,b). Even so, some studies have shown that these events may not be periods of high predator-related mortality for Arctic char (Caza-Allard et al., 2021; Munaweera et al., 2022), nor have they been documented as significant contributors to the overall diet of higher trophic level predators (e.g., seabirds and marine mammals). Here, however, we document numerous seabird and marine mammal predators foraging on aggregations of Arctic char as they enter and forage in the marine environment (Figures 1 and 2). This documentation includes rare observations of the capture of relatively large, anadromous Arctic char by glaucous gulls (Larus hyperboreus), red-throated loons (Gavia stellata), ringed seals, and narwhal (Monodon monoceros). These predators undertake significant migrations which, in this case, may target migratory Arctic char.

These observations were made in person (A.L. Vail) and from video recorded using a long lens camera (50–1000 mm), drones, and static cameras deployed on land and underwater at Kuuganajuk, Nunavut (Somerset Island; 72°41′0″ N, 93°25′0″ W) in the Canadian Arctic in summer, 2022. Video was captured by an author (A.L. Vail) and colleagues for the documentary, “Our Oceans” (Menzies, 2024, 21:19–28:07). Observations of the Arctic char migration from the lake to the ocean and the associated predation events occurred from 25 June to 5 July 2022, during which time a crew filmed for ~14 h/day. Narwhal foraging was observed from 3 to 6 August 2022, during which time filming was limited to 2 days and ~8 h/day due to logistics of reaching the filming locations.

Arctic seabirds are typically predators with broad diets, but glaucous gulls are the quintessential generalists; they feed on terrestrial and marine prey and are also scavengers (Weiser & Gilchrist, 2020). Diets of Arctic loon species are poorly known, but most consume small fish along with freshwater and marine invertebrates during the breeding season (notably red-throated loons; Rizzolo et al., 2020). Although diet studies of both glaucous gulls and red-throated loons are limited, the fish they consume are thought to primarily include smaller species such as Arctic cod (Boreogadus saida), capelin (Mallotus villosus), sculpins, sandlance (Ammodytes sp.), and Atlantic herring (Clupea harengus; Elliott & Gaston, 2008).

In the documented interactions between predators and Arctic char (Figure 1d,e; Menzies, 2024, 23:57), loons can be seen swimming with numerous adult Arctic char. We used the typical bill length of these birds (60 and 50 mm, respectively) to estimate fish length from the footage. Many Arctic char were about the same length as the loon (~600 mm; Rizzolo et al., 2020), meaning that those fish were likely >2000 g (Dutil, 1986; Gilbert et al., 2016). While these fish are too large for gulls and loons to catch, the largest fish captured were >300 mm or >230 g with an estimated energy content of >1000 kJ (Figure 2c,d; Dutil, 1986). Consuming one fish that size would meet the daily maintenance energetic need for adult glaucous gulls (Weiser & Gilchrist, 2020) or the daily energy expenditure for post-natal growth of loon chicks (Rizzolo et al., 2020) and contain far more energy than the smaller fish typically consumed by these species in the Arctic (Elliott & Gaston, 2008). Thus, the pulse of migrating char provides an enormous opportunity for Arctic seabirds during the breeding season or pre-fall migration, periods of high energetic need.

The life history of ringed seals has been strongly shaped by sea ice dynamics where seals forage more intensively in the productive summer and fall periods to rebuild lost energy stores during the less productive overwintering period (McLaren, 1958). Ringed seals are generalist and opportunistic consumers with diets consisting of numerous invertebrate and fish species (Gjertz & Lydersen, 1986), which vary with latitude and resource availability (Yurkowski et al., 2016). It is general knowledge in some northern communities that ringed seals will consume migrating Arctic char, but char have rarely been documented in western scientific studies of seal stomach contents (e.g., Gjertz & Lydersen, 1986). The interactions documented herein depict a pursuit predation event where an individual Arctic char is isolated from a larger aggregation and consumed (Figure 2a,b; Menzies, 2024, 24:11 and 24:48). These observations provide additional support that opportunistic foraging by ringed seals on an Arctic char migration pulse may be a regional phenomenon that requires further study.

The narwhal is a deep-diving cetacean that is endemic to the Arctic (Laidre et al., 2015). The narwhal range covers the eastern Canadian high Arctic, West and East Greenland, Svalbard, and Franz Joseph Land (Heide-Jørgensen et al., 2013). Narwhals follow the formation and retreat of annual sea ice over the course of extensive annual migrations, and their feeding intensity is generally higher during the over-wintering period. In summer, narwhals spend their time in ice-free bays and fjords of the high Arctic or at glacial fronts (especially around Greenland) consuming shrimp (Pandalus spp.), Arctic cod, polar cod (Arctogadus glacialis), and capelin (Watt et al., 2013). In autumn, they migrate to overwintering areas that are deep, offshore, and ice-covered, usually along the continental slope (Laidre et al., 2003, 2004), where they feed more intensively on Greenland halibut (Reinhardtius hippoglossoides), boreoatlantic armhook squid (Gonatus fabricii), or capelin (Laidre & Heide-Jørgensen, 2005; Watt et al., 2013). The observations here confirm that narwhals may opportunistically feed on the summer pulse of Arctic char (Figure 2; Menzies, 2024, 25:56). However, the extent to which narwhals rely on Arctic char as an annual food source is unknown given the limited spatial and temporal availability, and that such pulses are not available to all summering subpopulations. The images also show narwhals using their tusks to stun Arctic char before consumption (Figure 2e), which agrees with contemporaneous observations by others in the same area (O'Corry-Crowe et al., 2025). Footage collected by researchers in the Eastern Canadian Arctic showed narwhals stunning Arctic cod with their tusks, and these independent observations suggest that this is a tactic used by male narwhals.

Of the four marine predators we describe here, only ringed seals have previously been described in the literature as active predators of anadromous Arctic char (Gjertz & Lydersen, 1986). While adult Arctic char are often too large for loons or gulls to consume whole, gulls may still opportunistically feed on large adult char that become stranded in shallow water during their upriver migration (e.g., Gilbert et al., 2016), an occurrence that is likely to change in frequency as climate change continues to alter hydrological regimes. Additionally, Arctic char have been anecdotally reported in the diet of loons in Greenland (Weiser & Gilchrist, 2020). Marine mammal predator-related mortality is assumed to be low for anadromous adult Arctic char, and such events have rarely been documented despite extensive overlap with piscivorous marine mammals (Finley & Gibb, 1982; Matley et al., 2015; Moore, 1975). For instance, separate studies examined ringed seal diets in spring and summer in the Cumberland Sound region of Nunavut, Canada, and in northwestern Spitsbergen, Svalbard, and found Arctic char in gut contents of only 8% and 4% of seals, respectively (Gjertz & Lydersen, 1986; Moore, 1975). We could not find any scientific documentation of narwhal hunting Arctic char. Recent studies using archival pop-off tags and traditional and local knowledge from hunters have documented predation events of Arctic char and the closely related Dolly Varden char (Salvelinus malma malma) by beluga whale (Delphinapterus leucas) in the western Canadian Arctic (Gallagher et al., 2021; Loseto et al., 2018). Cumulatively, these observations and those documented here suggest that large marine mammals, including whales and seals, do occasionally consume anadromous salmonids in the Arctic and are a source of mortality that could be important for some populations. In general, however, marine predation of Arctic salmonids is not well documented, and future studies should focus on populations that may be likely to experience these potentially brief but intense predation events to (1) determine how these events impact mortality rates and population dynamics and (2) understand the broad ecological importance of the fish in their ecosystem.

The images discussed here depict remarkable behaviors and trophic interactions shaped by the high spatiotemporal variation in resource availability that defines high-latitude environments. The Arctic char are themselves in pursuit of greater food availability as they migrate to the marine environment where they can become predictable prey for several marine predators ready to capitalize on the influx of food. The events discussed here may be examples of intentional resource tracking by these marine predators or may be examples of opportunistic foraging strategies. These possibilities and the relative paucity of western scientific research in the region raise several questions that warrant further investigation. For instance, do these predators track the timing of the Arctic char migration to sea? Does access to these resources influence predator habitat selection? Are these indeed rare events or are they just rarely documented? How important are these prey pulses to predator energy budgets? How are these events going to be shaped by shifts in species' ranges (e.g., killer whales; Orcinus orca) and the timing of seasonal events with ongoing environmental change? While relevant western scientific research in the north has been relatively limited, local people have lived in these regions for millennia, interacting closely with these animals. As such, studies of traditional and local knowledge are a natural starting point for further exploration.

The authors declare no conflicts of interest.

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来源期刊
Ecology
Ecology 环境科学-生态学
CiteScore
8.30
自引率
2.10%
发文量
332
审稿时长
3 months
期刊介绍: Ecology publishes articles that report on the basic elements of ecological research. Emphasis is placed on concise, clear articles documenting important ecological phenomena. The journal publishes a broad array of research that includes a rapidly expanding envelope of subject matter, techniques, approaches, and concepts: paleoecology through present-day phenomena; evolutionary, population, physiological, community, and ecosystem ecology, as well as biogeochemistry; inclusive of descriptive, comparative, experimental, mathematical, statistical, and interdisciplinary approaches.
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