期刊论文详细信息
Annals of Occupational and Environmental Medicine
Novel species interactions: American black bears respond to Pacific herring spawn
Caroline Hazel Fox1  Paul Charles Paquet1  Thomas Edward Reimchen2 
[1] Department of Geography, University of Victoria, Victoria V8W 2Y2, BC, Canada
[2] Department of Biology, University of Victoria, Victoria V8W 2Y2, BC, Canada
关键词: Spawn;    Pacific Ocean;    Forage fish;    Intertidal zone;    Ursus americanus;    Clupea pallasii;    Species interactions;   
Others  :  1210166
DOI  :  10.1186/s12898-015-0045-9
 received in 2014-10-27, accepted in 2015-04-22,  发布年份 2015
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【 摘 要 】

Background

In addition to the decline and extinction of the world’s species, the decline and eventual loss of species interactions is one of the major consequences of the biodiversity crisis. On the Pacific coast of North America, diminished runs of salmon (Oncorhynchus spp.) drive numerous marine–terrestrial interactions, many of which have been intensively studied, but marine–terrestrial interactions driven by other species remain relatively unknown. Bears (Ursus spp.) are major vectors of salmon into terrestrial ecosystems, but their participation in other cross-ecosystem interactions is similarly poorly described. Pacific herring (Clupea pallasii), a migratory forage fish in coastal marine ecosystems of the North Pacific Ocean and the dominant forage fish in British Columbia (BC), spawn in nearshore subtidal and intertidal zones. Spawn resources (eggs, milt, and spawning adults) at these events are available to coastal predators and scavengers, including terrestrial species. In this study, we investigated the interaction between American black bears (Ursus americanus) and Pacific herring at spawn events in Quatsino Sound, BC, Canada.

Results

Using remote cameras to monitor bear activity (1,467 camera days, 29 sites, years 2010–2012) in supratidal and intertidal zones and a machine learning approach, we determined that the quantity of Pacific herring eggs in supratidal and intertidal zones was a leading predictor of black bear activity, with bears positively responding to increasing herring egg masses. Other important predictors included day of the year and Talitrid amphipod (Traskorchestia spp.) mass. A complementary analysis of black bear scats indicated that Pacific herring egg mass was the highest ranked predictor of egg consumption by bears. Pacific herring eggs constituted a substantial yet variable component of the early springtime diet of black bears in Quatsino Sound (frequency of occurrence 0–34%; estimated dietary content 0–63%). Other major dietary items included graminoids (grasses and sedges), Phaeophyta (brown algae), Zosteraceae (seagrasses), and Talitrid amphipods.

Conclusion

This research represents the first scientific evidence of a cross-ecosystem interaction between Pacific herring and American black bears. Our findings also expand knowledge of the ecological roles of both species. Combined, evidence of anthropogenic constraints on both black bears and Pacific herring suggests that bear-herring interactions were potentially stronger and more widespread in the past.

【 授权许可】

   
2015 Fox et al.

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【 参考文献 】
  • [1]Soulé ME, Estes JA, Berger J, Del Rio CM. Ecological effectiveness: conservation goals for interactive species. Conserv Biol. 2003; 17:1238-1250.
  • [2]Estes JA, Terborgh J, Brashares JS, Power ME, Berger J, Bond WJ et al.. Trophic downgrading of planet earth. Science. 2011; 333:301-306.
  • [3]Quinn TP. The behavior and ecology of Pacific salmon and trout. University of Washington Press, Seattle; 2005.
  • [4]Polis GA, Anderson WB, Holt RD. Toward an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Annu Rev Ecol Evol Syst. 1997; 28:289-316.
  • [5]Reimchen TE, Mathewson D, Hocking MD, Moran J. Isotopic evidence for enrichment of salmon-derived nutrients in vegetation, soil and insects in riparian zones in coastal British Columbia. Am Fish Soc Symp. 2003; 34:59-69.
  • [6]Ben-David M, Hanley TA, Klein DR, Schell DM. Seasonal changes in diets of coastal and riverine mink: the role of spawning Pacific salmon. Can J Zool. 1997; 75:803-811.
  • [7]Christie KS, Reimchen TE. Presence of salmon increases passerine density on Pacific North-west streams. Auk. 2008; 125:51-59.
  • [8]Bennetts E, McClelland BR. Influence of age and prey availability on Bald Eagle foraging behavior at Glacier National Park, Montan. Wilson Bull. 1997; 109:393-409.
  • [9]Reimchen TE. Some ecological and evolutionary aspects of bear—salmon interactions in coastal British Columbia. Can J Zool. 2001; 78:448-457.
  • [10]Quinn TP, Carlson SM, Gende SM, Rich HB. Transportation of Pacific salmon carcasses from streams to riparian forests by bears. Can J Zool. 2009; 87:195-203.
  • [11]Darimont CT, Reimchen TE. Intra-hair stable isotope analysis implies seasonal shift to salmon in gray wolf diet. Can J Zool. 2002; 80:1-5.
  • [12]Ben-David M, Hanley TA, Schell DM. Fertilization of terrestrial vegetation by spawning Pacific salmon: the role of flooding and predator activity. Oikos. 1998; 83:47-55.
  • [13]O’Keefe TC, Edwards RT. Evidence for hyporheic transfer and removal of marine-derived nutrients in a sockeye stream in southwest Alaska. Am Fish Soc Symp. 2002; 33:99-108.
  • [14]Hilderbrand GV, Schwartz CC, Robbins CT, Jacoby ME, Hanley TA, Arthur SM et al.. The importance of meat, particularly salmon, to body size, population productivity, and conservation of North American brown bears. Can J Zool. 1999; 77:132-138.
  • [15]Helfield JM, Naiman RJ. Keystone interactions: salmon and bear in riparian forests of Alaska. Ecosystems. 2006; 9:167-180.
  • [16]Ziegltrum GJ, Nolte DL. Black bear forest damage in Washington State, USA: economic, ecological, social aspects. Ursus. 2001; 12:169-172.
  • [17]Van Daele LJ, Barnes VG, Belant JL. Ecological flexibility of brown bears on Kodiak Island, Alaska. Ursus. 2012; 23:21-29.
  • [18]Smith TS, Partridge ST. Dynamics of intertidal foraging by coastal brown bears in southwestern Alaska. J Wildl Manag. 2004; 68:233-240.
  • [19]Carlton JT, Hodder J. Maritime mammals: terrestrial mammals as consumers in marine intertidal communities. Mar Ecol Prog Ser. 2003; 256:271-286.
  • [20]Orr M, Zimmer M, Jelinski DE, Mews M. Wrack deposition on different beach types: spatial and temporal variation in the pattern of subsidy. Ecology. 2005; 86:1496-1507.
  • [21]Willson MF, Gende SM, Marston BH. Fishes and the forest: expanding perspectives on fish-wildlife interactions. BioScience. 1998; 48:455-462.
  • [22]Schweigert JF, Boldt JL, Flostrand L, Cleary JS. A review of factors limiting recovery of Pacific herring stocks in Canada. ICES J Mar Sci. 2010; 67:1903-1913.
  • [23]Thornton TF, Moss ML, Butler VL, Herbert J, Funk F. Local and traditional knowledge and the historical ecology of Pacific herring in Alaska. J Ecol Anthropol. 2010; 14:81-88.
  • [24]McKechnie I, Lepofsky D, Moss ML, Butler VL, Orchard TJ, Coupland G et al.. Archaeological data provide alternative hypotheses on Pacific herring (Clupea pallasii) distribution, abundance, and variability. Proc Natl Acad Sci. 2014; 111:807-816.
  • [25]Purcell JE. Predation on fish larvae and eggs by the hydromedusa Aequorea victoria at a herring spawning ground in British Columbia. Can J Fish Aquat Sci. 1989; 46(141):5-1427.
  • [26]Tanasichuk RW, Ware DM, Shaw W, McFarlane GA. Variations in diet, daily ration, and feeding periodicity of Pacific hake (Merluccius productus) and spiny dogfish (Squalus acanthias) off the lower west coast of Vancouver Island. Can J Fish Aquat Sci. 1991; 48:2118-2128.
  • [27]Livingston PA. Importance of predation by groundfish, marine mammals and birds on walleye pollock Theragra chalcogramma and Pacific herring Clupea pallasi in the eastern Bering Sea. Mar Ecol Prog Ser. 1993; 102:205-215.
  • [28]Bishop MA, Green SP. Predation on Pacific herring (Clupea pallasi) spawn by birds in Prince William Sound, Alaska. Fish Oceanogr. 2001; 10 Suppl 1:149-158.
  • [29]Anderson EM, Lovvorn JR, Esler D, Boyd WS, Stick KC. Using predator distributions, diet, and condition to evaluate seasonal foraging sites: sea ducks and herring spawn. Mar Ecol Prog Ser. 2009; 386:287-302.
  • [30]Thomas AC, Lance MM, Jeffries SJ, Miner BG, Acevedo-Gutiérrez A. Harbor seal foraging response to a seasonal resource pulse, spawning Pacific herring. Mar Ecol Prog Ser. 2011; 441:225-239.
  • [31]Hay DE. Reproductive biology of Pacific herring (Clupea harengus pallasi). Can J Fish Aquat Sci. 1985; 42:111-126.
  • [32]Fuiman LA, Connelly TL, Lowerre-Barbieri SK, McClelland JW. Egg boons: central components of marine fatty acid food webs. Ecology. 2015; 96:153-156.
  • [33]Fox CH, El-Sabaawi R, Paquet PC, Reimchen TE. Pacific herring (Clupea pallasii) and wrack macrophytes subsidize semi-terrestrial detritivores. Mar Ecol Prog Ser. 2014; 495:49-64.
  • [34]Willson MF, Womble JN. Vertebrate exploitation of pulsed marine prey: a review and the example of spawning herring. Rev Fish Biol Fish. 2006; 16:183-200.
  • [35]Polis GA, Hurd SD. Linking marine and terrestrial food webs: allochthonous input from the ocean supports high secondary productivity on small islands and coastal land communities. Am Nat. 1996; 147:396-423.
  • [36]Varpe Ø, Fiksen Ø, Slotte A. Meta-ecosystems and biological energy transport from ocean to coast: the ecological importance of herring migration. Oecologia. 2005; 146:443-451.
  • [37]Garman GC, Macko SA. Contribution of marine-derived organic matter to an Atlantic coast, freshwater, tidal stream by anadromous clupeid fishes. J N Am Benthol Soc. 1998; 17:277-285.
  • [38]Walters AW, Barnes RT, Post DM. Anadromous alewives (Alosa pseudoharengus) contribute marine-derived nutrients to coastal stream food webs. Can J Fish Aquat Sci. 2009; 66:439-448.
  • [39]Breiman L. Random forests. Mach Learn. 2001; 45:5-32.
  • [40]Stock assessment report on Pacific herring in British Columbia in 2011. Can Sci Advis Sec Sci Advis Rep. 2011; 2011(061):1-15.
  • [41]Stock assessment report on Pacific herring in British Columbia in 2012. Can Sci Advis Sec Sci Advis Rep. 2012; 2012(062):1-17.
  • [42]Schweigert JF, Haegele CW, Stocker M. Optimizing sampling design for herring spawn surveys in the Strait of Georgia, BC. Can J Fish Aquat Sci. 1985; 42:1806-1814.
  • [43]Haegele CW, Humphreys RD, Hourston AS. Distribution of eggs by depth and vegetation type in Pacific herring (Clupea harengus pallasi) spawnings in southern British Columbia. Can J Fish Aquat Sci. 1981; 38:381-386.
  • [44]Schweigert JF, Haegele CW, Stocker M. Evaluation of sampling strategies for scuba surveys to assess spawn deposition by Pacific herring. N Am J Fish Manag. 1990; 10:185-195.
  • [45]Fox CH (2013) Pacific herring and salmon: ecological interactions across the land–sea interface. Ph.D. dissertation. University of Victoria, Department of Biology
  • [46]Alderdice DF, Hourston AS. Factors influencing development and survival of Pacific herring (Clupea harengus pallasii) eggs and larvae to beginning of exogenous feeding. Can J Fish Aquat Sci. 1985; 42:56-68.
  • [47]Haegele CW, Schweigert JF: Egg loss in herring spawns in Georgia Strait, British Columbia, Canada. In: Proceedings of the international herring symposium, Alaska Sea Grant College Program Report 1991, 91-01, pp 309–322
  • [48]Keeling BE (2013) Quantifying the magnitude and mechanisms driving Pacific herring (Clupea pallasi) egg loss on the Central Coast of British Columbia, Canada. M.Sc. thesis. Simon Fraser University, School of Resource and Environmental Management
  • [49]Shardlow TF, Hyatt KD. Quantifying associations of large vertebrates with salmon in riparian areas of British Columbia streams by means of camera-traps, bait stations, and hair samples. Ecol Indic. 2013; 27:97-107.
  • [50]Quinn TP, Wirsing AJ, Smith B, Cunningham CJ, Ching J. Complementary use of motion-activated cameras and unbaited wire snares for DNA sampling reveals diel and seasonal activity patterns of brown bears foraging on adult sockeye salmon. Can J Zool. 2014; 92:893-903.
  • [51]Dahle B, Sørensen OJ, Wedul EH, Swenson JE, Sandegren F. The diet of brown bears Ursus arctos in central Scandinavia: effect of access to free- ranging domestic sheep Ovis aries. Wildl Biol. 1998; 4:147-158.
  • [52]Persson IL, Wikan S, Swenson JE, Mysterud I. The diet of the brown bear Ursus arctos in the Pasvik Valley, northeastern Norway. Wildl Biol. 2001; 7:27-37.
  • [53]Mattson DJ, Blanchard BM, Knight RR. Food habits of Yellowstone grizzly bears, 1977–1987. Can J Zool. 1991; 69:1619-1629.
  • [54]Hewitt DG, Robbins CT. Estimating grizzly bear food habits from fecal analysis. Wildl Soc Bull. 1996; 24:547-550.
  • [55]Iverson M (2011) The diet of polar bears (Ursus maritimus) from Svalbard, Norway, inferred from scat analysis. M.Sc. thesis, University of Tromso, Department of Biosciences, fisheries and economics
  • [56]Pritchard GT, Robbins CT. Digestive and metabolic efficiencies of grizzly and black bears. Can J Zool. 1990; 68:1645-1651.
  • [57]McLellan BN. Implications of a high-energy and low-protein diet on the body composition, fitness, and competitive abilities of black (Ursus americanus) and grizzly (Ursus arctos) bears. Can J Zool. 2011; 89:546-558.
  • [58]Gray A (2005) The salmon river estuary: restoring tidal inundation and tracking ecosystem response. Ph.D. dissertation, University of Washington, School of Aquatic and Fishery Sciences
  • [59]Baldwin JR, Lovvorn JR. Expansion of seagrass habitat by the exotic Zostera japonica, and its use by dabbling ducks and brant in Boundary Bay, British Columbia. Mar Ecol Prog Ser. 1994; 103:119-127.
  • [60]Liaw A, Wiener M. Classification and regression by randomForest. R News. 2002; 2(3):18-22.
  • [61]R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/. Accessed 7 Jan 2015
  • [62]Fox CH, Paquet PC, Reimchen TE. Active American black bear dens adjacent to a marine beach used for foraging. Ursus. 2010; 21(2):195-197.
  • [63]Powell RA, Zimmerman JW, Seaman DE. Ecology and behaviour of North American black bears: home ranges, habitat and social organization. Chapman and Hall Wildlife Ecology and Behaviour Series, London; 1997.
  • [64]Reimchen TE. Nocturnal foraging behaviour of Black Bear, Ursus americanus, on Moresby Island, British Columbia. Can Field Nat. 1998; 112:446-450.
  • [65]Ellis DW, Wilson S (1981) The knowledge and usage of marine invertebrates by the Skidegate Haida people of the Queen Charlotte Islands. Monograph Series 1. Queen Charlotte Islands Museum Society, BC, Canada
  • [66]Kistchinski AA. Life history of the brown bear (Ursus arctos L.) in north-east Siberia. Bears Biol Manag. 1972; 2:67-73.
  • [67]Noyce KV, Kannowski PB, Riggs MR. Black bears as ant-eaters: seasonal associations between bear myrmecophagy and ant ecology in north-central Minnesota. Can J Zool. 1997; 75(10):1671-1686.
  • [68]Swenson JE, Jansson A, Riig R, Sandgren F. Bears and ants: myrmecophagy by brown bears in central Scandinavia. Can J Zool. 1999; 77:551-561.
  • [69]Laliberte AS, Ripple WJ. Range contractions of North American carnivores and ungulates. BioScience. 2004; 54:123-138.
  • [70]Smith TS, Oyster O, Partridge SD, Martin IE, Sisson A. Assessing American black bear response to human activity at Kenai Fjords National Park, Alaska. Ursus. 2012; 23:179-191.
  • [71]Taylor FCH. Life history and present status of British Columbia herring stocks. Bull Fish Res Board Can, Ottawa; 1964.
  • [72]Stock assessment and management advice for British Columbia Pacific herring: 2013 status and 2014 forecast. Can Sci Advis Sec Sci Advis Rep. 2014; 2014(003):1-18.
  • [73]Mandamin LS (2014) The Ahousaht, Ehattesaht, Hesquiaht, Mowachaht/Muchalaht and Tla-o-qui-aht Indian Bands and Nations and Minister of Fisheries and Oceans. Federal Court, Docket T-404-14, Ottawa
  • [74]Ware BM, Tanasichuk WW. Biological basis of maturation and spawning waves in Pacific herring (Clupea harengus pallasi). Can J Fish Aquat Sci. 1989; 46:1776-1784.
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