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Predatory disturbance and prey species diversity: the case of gray whale (Eschrichtius robustus) foraging on a multi-species mysid (family Mysidae) community

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Abstract

Why competitive exclusion does not limit the number of coexisting plankton species is a persistent question for community ecology. One explanation, the intermediate disturbance hypothesis (IDH), proposes that elevated species diversity is a product of moderate levels of disturbance that allow the subsequent invasion of less competitive species. Here, we assess the shifts in species diversity in a mysid (Mysidae Dana, 1850) zooplankton community, where at least 10 species have, over the last 15 years, have come to comprise the primary prey base of summer resident gray whales (Eschrictius robustus Lilljeborg, 1861) in Clayoquot Sound, British Columbia. We evaluate trends in the community structure of mysids (species dominance, diversity, and richness) across mysid habitat in the study area during the gray whale foraging season (May–September) for the period 1996 and 2008. Mysid species composition varies among years and diversity has increased as whales shifted their predatory focus from benthic amphipods (Ampeliscidae Costa, 1857) to mysids, near our starting point in 1996. Holmesimysis sculpta Tattersall, 1933 was the dominant species in early years; however, in 2007, the dominance shifted to Neomysis rayi Murdoch, 1885. The habitat restrictions and life history attributes of local populations of coastal mysids leave them vulnerable to the cumulative impacts of increased predation pressure by gray whales. This case study presents a unique examination implicating predation as an agent of disturbance capable of altering the species structure of a local prey community.

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References

  • Albertsson, J., 2004. Trophic interactions involving mysid shrimps (Mysidacea) in the near-bottom habitat in the Baltic Sea. Aquatic Ecology 38: 457–469.

    Article  Google Scholar 

  • Bender, E. A., T. J. Case & M. E. Gilpin, 1984. Perturbation experiments in community ecology: theory and practice. Ecology 65: 1–13.

    Article  Google Scholar 

  • Bowen, W. D., 1997. Role of marine mammals in aquatic ecosystems. Marine Ecology Progress Series 158: 267–274.

    Article  Google Scholar 

  • Clarke, K. R., 1993. Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology 18: 117–143.

    Article  Google Scholar 

  • Clutter, R. I., 1969. The microdistribution and social behaviour of some pelagic mysid shrimps. Journal of Experimental Marine Biology and Ecology 3: 125–155.

    Article  Google Scholar 

  • Connell, J., 1978. Diversity in tropical rainforests and coral reefs. Science 199: 1302–1310.

    Article  PubMed  CAS  Google Scholar 

  • Coyle, K. O., B. Bluhm, B. Konar, A. Blanchard & R. C. Highsmith, 2007. Amphipod prey of gray whales in the northern Bering Sea: comparison of biomass and distribution between the 1980s and 2002–2003. Deep-Sea Research Part II 54: 2906–2918.

    Article  Google Scholar 

  • Crawley, M. J., 2004. Timing of disturbance and coexistence in a species-rich ruderal plant community. Ecology 85: 3277–3288.

    Article  Google Scholar 

  • Croll, D. A., B. Marinovic, S. Benson, F. P. Chavez, N. Black, R. Temullo & B. R. Tershy, 2005. From wind to whales: trophic links in a coastal upwelling system. Marine Ecology Progress Series 289: 117–130.

    Article  Google Scholar 

  • DeMaster, D. P., A. Trites, P. Clapham, S. Mizroch, P. Wade, R. J. Small & J. Ver Hoef, 2006. The sequential megafaunal collapse hypothesis: testing with existing data. Progress in Oceanography 68: 329–342.

    Article  Google Scholar 

  • Duffus, D., 1996. The recreational use of grey whales in southern Clayoquot Sound, Canada. Applied Geography 16: 179–190.

    Article  Google Scholar 

  • Dunham, J. S. & D. A. Duffus, 2001. Foraging patterns of gray whales in central Clayoquot Sound, British Columbia, Canada. Marine Ecology Progress Series 223: 299–310.

    Article  Google Scholar 

  • Dunham, J. S. & D. A. Duffus, 2002. Diet of gray whales (Eschrichtius robustus) in Clayoquot Sound, British Columbia, Canada. Marine Mammal Science 18: 419–437.

    Article  Google Scholar 

  • Estes, J. A., M. T. Tinker, T. M. Williams & D. F. Doak, 1998. Killer whale predation on sea otters linking oceanic and nearshore ecosystems. Science 282: 473–476.

    Article  PubMed  CAS  Google Scholar 

  • Feyrer, L. J., 2010. Differences in embryo production between sympatric species of mysids (family Mysidae) in the shallow coastal waters off Vancouver Island, BC. Marine Biology 157: 2461–2465.

    Article  Google Scholar 

  • Feyrer, L. J & D. A. Duffus, 2011. Ecological, spatial and temporal linkages between gray whales and prey. Continental Shelf Research (in review)

  • Fox, W. J., 2007. The dynamics of top-down and bottom-up effects in food webs of varying prey diversity, composition, and productivity. Oikos 116: 189–200.

    Article  Google Scholar 

  • Gaedeke, A. & U. Sommer, 1986. The influence of the frequency of periodic disturbances on the maintenance of phytoplankton diversity. Oecologia 71: 25–28.

    Article  Google Scholar 

  • Gaston, K. J., 1994. Rarity. Chapman & Hall, London.

    Book  Google Scholar 

  • Gorokhova, E. & M. Lehtiniemi, 2007. A combined approach to understand the trophic interactions between Cercopagis pengoi (Cladocera: Onychopoda) and mysids in the Gulf of Finland. Limnology and Oceanography 52: 685–695.

    Article  Google Scholar 

  • Gray, J. S., 2000. The measurement of marine species diversity, with an application to the benthic fauna of the Norwegian continental shelf. Journal of Experimental Marine Biology and Ecology 250: 23–49.

    Article  PubMed  Google Scholar 

  • Grebmeier, J. M., J. E. Overland, S. E. Moore, E. V. Farley, E. C. Carmack, L. W. Cooper, K. E. Frey, J. H. Helle, F. A. McLaughlin & S. L. McNutt, 2006. A major ecosystem shift in the Northern Bering Sea. Science 311: 1461–1464.

    Article  PubMed  CAS  Google Scholar 

  • Green, J. M., 1970. Observation on the behavior and larval development of Acanthomysis sculpta (Tattersall), (Mysidacea). Canadian Journal of Zoology 48: 289–292.

    Article  PubMed  CAS  Google Scholar 

  • Hacker, S. D. & S. D. Gaines, 1997. Some implications of direct positive interactions for community species diversity. Ecology 78: 1990–2003.

    Article  Google Scholar 

  • Hairston, N. G., F. E. Smith & L. B. Slobodkin, 1960. Community structure, population control and competition. American Naturalist 94: 421–425.

    Article  Google Scholar 

  • Herbert, P. D. & T. J. Crease, 1980. Clonal coexistence in Daphnia pulex (Leydig): another planktonic paradox. Science 207: 1363–1365.

    Google Scholar 

  • Highsmith, R. C. & K. O. Coyle, 1992. Productivity of arctic amphipods relative to gray whale energy requirements. Marine Ecology Progress Series 83: 141–150.

    Article  Google Scholar 

  • Hixon, M. A. & W. Brostoff, 1983. Damselfish as keystone species in reverse: intermediate disturbance and diversity of reef algae. Science 220: 511–513.

    Article  PubMed  CAS  Google Scholar 

  • Huisman, J. & F. J. Weissing, 1999. Biodiversity of plankton species oscillations and chaos. Nature 402: 407–410.

    Article  Google Scholar 

  • Hunt, G. L. & S. McKinnel, 2006. Interplay between top-down, bottom-up, and wasp-waist control in marine ecosystems. Progress in Oceanography 68: 115–124.

    Article  Google Scholar 

  • Huston, M., 1979. A general hypothesis of species diversity. American Naturalist 113: 81–101.

    Article  Google Scholar 

  • Hutchinson, G. E., 1957. Concluding remarks. Cold Spring Harbor symposium. Quantitative Biology 22: 415–427.

    Google Scholar 

  • Hutchinson, G. E., 1961. The paradox of the plankton. American Naturalist 95: 137–145.

    Article  Google Scholar 

  • Jumars, P., 2007. Habitat coupling by mid-latitude, subtidal, marine mysids: import-subsidized omnivores. Oceanography and Marine Biology 45: 1–50.

    Google Scholar 

  • Kathman, R. D., W. C. Austin, J. C. Saltman & J. D. Fulton, 1986. Identification manual to the Mysidacea and Euphausiacea of the northeast Pacific. Canadian Special Publications in Fisheries and Aquatic Science 93.

  • Katona, S. & H. Whitehead, 1988. Are Cetacea ecologically important? Oceanography and Marine Biology Annual Review 26: 553–568.

    Google Scholar 

  • Kim, S. L. & J. S. Oliver, 1989. Swarming benthic crustaceans in the Bering and Chukchi Seas and their relation to geographic patterns in grey whale feeding. Canadian Journal of Zoology 67: 1531–1543.

    Article  Google Scholar 

  • Krebs, C. J., 1999. Ecological Methodology, 2nd ed. Harper & Row, New York.

    Google Scholar 

  • Kvitek, R. G. & J. S. Oliver, 1986. Side-scan sonar impressions of gray whale feeding grounds along Vancouver Island, Canada. Continental Shelf Research 6: 639–654.

    Article  Google Scholar 

  • Lande, R., P. J. DeVries & T. Walla, 2000. When species accumulation curves intersect: implications for ranking diversity using small samples. Oikos 89: 601–605.

    Article  Google Scholar 

  • Laskin, D., D. A. Duffus & D. J. Bender, 2010. Mysteries of the not so deep: an investigation into gray whale habitat use along the west coast of Vancouver Island, British Columbia. In Breman, J. (ed.), Ocean Globe. ESRI Press, Redlands.

    Google Scholar 

  • Lindholm, M., D. O. Hessen & L. Ramberg, 2009. Diversity, dispersal and disturbance: cladoceran species composition in the Okavango Delta. African Zoology 44: 24–35.

    Article  Google Scholar 

  • Magurran, A., 2004. Measuring Biological Diversity. Blackwell Publishing, Malden.

    Google Scholar 

  • Mauchline, J., 1980. The biology of mysids and euphausiids. Advanced Marine Biology 18: 1–444.

    Google Scholar 

  • McGuinness, K. A., 1987. Disturbance and organisms on boulders. II. Causes of patterns in diversity and abundance. Oecologia 71: 420–430.

    Article  Google Scholar 

  • Menge, B. A. & J. P. Sutherland, 1976. Species diversity gradients: synthesis of the roles of predation, competition and temporal heterogeneity. American Naturalist 110: 351–369.

    Article  Google Scholar 

  • Moore, S. E. & H. P. Huntington, 2008. Arctic marine mammals and climate change: impacts and resilience. Ecological Applications 18: 157–165.

    Article  Google Scholar 

  • Moore, S. E., J. M. Grebmeier & J. R. Davies, 2003. Gray whale distribution relative to forage habitat in the northern Bering Sea: current conditions and retrospective summary. Canadian Journal of Zoology 81: 734–742.

    Article  Google Scholar 

  • Mulkins, L. M., D. E. Jelinski, J. D. Karagatzides & A. Carr, 2002. Carbon isotope composition of mysids at a terrestrial-marine ecotone, Clayoquot Sound, British Columbia, Canada. Estuarine and Coastal Shelf Science 54: 669–675.

    Article  CAS  Google Scholar 

  • Nelson, T. A., D. A. Duffus, C. Robertson & L. J. Feyrer, 2008. Spatial-temporal patterns in intra-annual gray whale foraging: characterizing interactions between predators and prey in Clayoquot Sound, BC. Marine Mammal Science 24: 356–370.

    Article  Google Scholar 

  • Nelson, T. A., D. A. Duffus, C. Robertson, C. Labree & L. J. Feyrer, 2009. Spatial-temporal analysis of marine wildlife. Journal of Coastal Research 56: 1537–1541.

    Google Scholar 

  • Nerini, M., 1984. A review of gray whale feeding ecology. In Jones, M. L., S. L. Swartz & S. Leatherwood (eds), The Gray Whale, Eschrichtius robustus. Academic Press, Orlando.

    Google Scholar 

  • Newell, C. L. & T. J. Cowles, 2006. Unusual gray whale (Eschrichtius robustus) feeding in the summer of 2005 off the central Oregon Coast. Geophysical Research Letters 33: 1–5.

    Article  Google Scholar 

  • O’Brien, D. P. & D. A. Ritz, 1988. Escape responses of gregarious mysids (Crustacea: Mysidacea): towards a general classification of escape responses in aggregated crustaceans. Journal of Experimental Marine Biology and Ecology 116: 257–272.

    Article  Google Scholar 

  • Paine, R. T., 1966. Food web complexity and species diversity. American Naturalist 100: 65–76.

    Article  Google Scholar 

  • Paine, R. T., 2006. Whales, interaction webs, zero-sum ecology. In Estes, J. A., D. E. Demaster, D. E. Doak, T. M. Williams & R. I. Brownell (eds), Whales, Whaling and Ocean Ecosystems. University of California Press, Berkley.

    Google Scholar 

  • Reynolds, C. S., J. Padisak & U. Sommer, 1993. Intermediate disturbance in the ecology of phytoplankton and the maintenance of species diversity: a synthesis. Hydrobiologia 249: 183–188.

    Article  Google Scholar 

  • Rice, D. W. & A. A. Wolman, 1971. The life history of the gray whale (Eschrichtius robustus). American Society of Mammalogists, Special Publication 3.

  • Richerson, P., R. Armstrong & C. R. Goldman, 1970. Contemporaneous disequilibrium, a new hypothesis to explain the “paradox of the plankton”. PNAS 67: 1710–1714.

    Article  PubMed  CAS  Google Scholar 

  • Roast, S. D., J. Widdows & M. B. Jones, 1999. Respiratory responses of the estuarine mysid Neomysis integer (Peracarida: Mysidacea) in relation to a variable environment. Marine Biology 133: 643–649.

    Article  Google Scholar 

  • Romanuk, T. N., R. J. Vogt & J. Kolasa, 2009. Ecological realism and mechanisms by which diversity begets stability. Oikos 118: 819–828.

    Article  Google Scholar 

  • Scheffer, M., S. Rinaldi, J. Huisman & F. J. Weissing, 2003. Why plankton communities have no equilibrium: solutions to the paradox. Hydrobiologia 491: 9–18.

    Article  Google Scholar 

  • Schoener, T. W., 1974. Resource partitioning in ecological communities. Science 185: 27–39.

    Article  PubMed  CAS  Google Scholar 

  • Sousa, W. P., 2001. Natural disturbance and the dynamics of marine benthic communities. In Bertness, M. D., S. D. Gaines & M. E. Hay (eds), Marine Community Ecology. Sinauer Associates, Sunderland.

    Google Scholar 

  • Springer, A. M., J. A. Estes, G. B. van Vliet, T. M. Williams, D. F. Doak, E. M. Danner, K. A. Forney, & B. P. Fister, 2003. Sequential megafaunal collapse in the North Pacific Ocean: an ongoing legacy of industrial whaling? PNAS. 100(21): 12223–12228.

  • Steele, J. H., 1998. From carbon flux to regime shift. Fisheries and Oceanography 7: 176–181.

    Article  Google Scholar 

  • Stelle, L. L., W. M. Megill & M. R. Kinzel, 2008. Activity budget and diving behavior of gray whales (Eschrichtius robustus) in feeding grounds off coastal British Columbia. Marine Mammal Science 24: 462–478.

    Article  Google Scholar 

  • Svensson, J. R., M. Lindegarth & H. Pavia, 2009. Equal rates of disturbance cause different patterns of diversity. Ecology 90: 496–505.

    Article  PubMed  Google Scholar 

  • Svensson, J. R., M. Lindegarth & H. Pavia, 2010. Physical and biological disturbances interact differently with productivity: effects on floral and faunal richness. Ecology 91: 3069–3080.

    Article  PubMed  Google Scholar 

  • Turpen, S., J. W. Hunt, B. S. Anderson & J. S. Pearse, 1994. Population structure, growth and fecundity of the kelp forest mysid Holmesimysis costata in Monterey Bay, California. Journal of Crustacean Biology 14: 657–664.

    Article  Google Scholar 

  • Wittmann, J. K., 1984. Ecophysiology of marsupial development and reproduction in Mysidacea (Crustacea). Oceanography and Marine Biology Annual Review 22: 393–428.

    Google Scholar 

  • Worm, B. & R. A. Myers, 2003. Meta-analysis of cod–shrimp interactions reveals top-down control in oceanic food webs. Ecology 84: 162–173.

    Article  Google Scholar 

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Acknowledgments

Research was conducted in the traditional territory of the Ahousaht First Nation. Thanks to the late Chief Earl George and the residents of Ahousaht, Huey Clarke and family. M. O. Jangles, T. Lawson, R. Brushett, G. Lotz, K. Muirhead. C. Tombach, J. “Scotty” Dunham, H. Patterson, J. Maud, W. Megill, R. Burnham, C. Dedels, H. Mitchell, and the volunteers who assisted us in the field. Support for this research was generously provided by the Province of British Columbia Pacific Leaders Fellowship, the American Cetacean Society Puget Sound Chapter, the Department of Geography at the University of Victoria, the Society for Coastal and Ecological Research (SEACR), and the Derek Sewell Foundation.

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  1. Whale Research Lab, Department of Geography, University of Victoria, PO 3060 STN CSC, Victoria, BC, V8W 3P5, Canada

    Laura Joan Feyrer & David A. Duffus

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  1. Laura Joan Feyrer
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Correspondence to Laura Joan Feyrer.

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Handling editor: Sigrún Huld Jónasdóttir

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Feyrer, L.J., Duffus, D.A. Predatory disturbance and prey species diversity: the case of gray whale (Eschrichtius robustus) foraging on a multi-species mysid (family Mysidae) community. Hydrobiologia 678, 37–47 (2011). https://doi.org/10.1007/s10750-011-0816-z

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  • DOI: https://doi.org/10.1007/s10750-011-0816-z

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