Introduced rats indirectly change marine rocky intertidal communities from algae- to invertebrate-dominated
Abstract
It is widely recognized that trophic interactions structure ecological communities, but their effects are usually only demonstrated on a small scale. As a result, landscape-level documentations of trophic cascades that alter entire communities are scarce. Islands invaded by animals provide natural experiment opportunities both to measure general trophic effects across large spatial scales and to determine the trophic roles of invasive species within native ecosystems. Studies addressing the trophic interactions of invasive species most often focus on their direct effects. To investigate both the presence of a landscape-level trophic cascade and the direct and indirect effects of an invasive species, we examined the impacts of Norway rats (Rattus norvegicus) introduced to the Aleutian Islands on marine bird densities and marine rocky intertidal community structures through surveys conducted on invaded and rat-free islands throughout the entire 1,900-km archipelago. Densities of birds that forage in the intertidal were higher on islands without rats. Marine intertidal invertebrates were more abundant on islands with rats, whereas fleshy algal cover was reduced. Our results demonstrate that invasive rats directly reduce bird densities through predation and significantly affect invertebrate and marine algal abundance in the rocky intertidal indirectly via a cross-community trophic cascade, unexpectedly changing the intertidal community structure from an algae- to an invertebrate-dominated system.
ACKNOWLEDGMENTS.
This article is dedicated to the memory of Captain Kevin Bell, in appreciation of his knowledge of and enthusiasm for the Aleutian Islands and his invaluable contribution to our work. We thank J. Figurski, S. Reisewitz, and A. Rose for help with field work; K. Bell and the crew of the M/V Tiglax for outstanding ship, logistic, and field support; G.V. Byrd, S. Ebbert, A. Sowls, K. Sundseth, J. Williams, and everyone at the Alaska Maritime National Wildlife Refuge for advice and logistical assistance; T. Klinger and D. Steller for assistance with identifying algal species; G. Bentall for illustrations; members of the D.A.C./B.R.T. lab for helpful discussion; and G.V. Byrd, J. Estes, M. Foster, M. Graham, P. Raimondi, E. Zavaleta and two anonymous reviewers for important comments on the manuscript. Work in the Aleutian Islands was supported by grants from the U.S. Fish and Wildlife Service (to C.M.K.), the M.C. Davis Memorial Fund (C.M.K.), and National Science Foundation Grant OPP-9985814 (to D.A.C.). Further support was provided by an Environmental Protection Agency STAR Fellowship (to C.M.K.), and grants from the Center for the Dynamics and Evolution of the Land–Sea Interface, the Myers Trust, U.S. Fish and Wildlife Service/National Fish and Wildlife Foundation, the STEPS Institute for Innovation in Environmental Research, and the Walt Disney Corporation.
References
1
NG Hairston, FE Smith, LB Slobodkin, Community structure, population control, and competition. Am Nat 94, 421–425 (1960).
2
DA Croll, J Maron, J Estes, EM Danner, GV Byrd, Introduced predators transform subarctic islands from grassland to tundra. Science 307, 1959–1961 (2005).
3
JA Estes, DO Duggins, Sea otters and kelp forests in Alaska: Generality and variation in a community ecological paradigm. Ecol Monogr 65, 75–100 (1995).
4
J Estes, M Tinker, T Williams, D Doak, Killer whale predation on sea otters linking oceanic and nearshore ecosystems. Science 282, 473–476 (1998).
5
JA Savidge, Extinction of an island avifauna by an introduced snake. Ecology 68, 660–668 (1987).
6
DR Towns, IAE Atkinson, CH Daugherty, Have the harmful effects of introduced rats on islands been exaggerated? Biol Invasions 8, 863–891 (2006).
7
HP Jones, et al., Global review of the severity of invasive rat impacts on susceptible seabirds. Conserv Biol 22, 16–26 (2008).
8
IAE Atkinson Conservation of Island Birds, ed PJ Moors (Smithsonian Institution Press for the ICBP, Washington, DC), pp. 35–81 (1985).
9
KA Hobson, MC Drever, GW Kaiser, Norway rats as predators of burrow-nesting seabirds: Insights from stable isotope analyses. J Wildlife Manage 63, 14–25 (1999).
10
J Burger, M Gochfeld Seabirds on Islands: Threats, Case Studies, and Action Plans, eds DN Nettleship, J Burger, M Gochfeld (Bird Life International, Cambridge, UK), pp. 39–67 (1994).
11
PJ Moors, IAE Atkinson Status and Conservation of the World's Seabirds, eds JP Croxall, PGH Evans, RW Schreiber (International Council for Bird Preservation, Cambridge, UK, 1984).
12
PJ Moors, IAE Atkinson, GH Sherley Prohibited Immigrants: The Rat Threat to Island Conservation (World Wildlife Fund for Nature, Wellington, New Zealand, 1989).
13
Y Osa, Y Watanuki, Status of seabirds breeding in Hokkaido. J Yamashina Institute for Ornithol 33, 107–141 (2002).
14
WB King Conservation of Island Birds: Case Studies for the Management of Threatened Island Species, ed PJ Moors (International Council of Bird Preservation, Cambridge, UK, 1985).
15
AP Moller, Damage by rats Rattus norvegicus to breeding birds on Danish Islands. Biol Conserv 25, 5–18 (1983).
16
SE Ebbert, GV Byrd, eds CR Veitch, MN Clout (IUCN Species Species Survival Commission, Gland, Switzerland, 2002).
17
HL Major, IL Jones, Distribution, biology and prey selection of the introduced Norway Rat Rattus norvegicus at Kiska Island, Aleutian Islands, Alaska Pacific. Conserv Biol 11, 105–113 (2005).
18
EP Bailey Introduction of Foxes to Alaskan Islands: History, Effects on Avifauna, and Eradication (U.S. Department of the Interior, Fish, and Wildlife Service, Washington, DC), pp. 54 (1993).
19
GV Byrd, HM Renner, M Renner, Distribution patterns and population trends of breeding seabirds in the Aleutian Islands. Fish Oceanogr 14, 139–159 (2005).
20
BA Andres, GA Falxa, Black Oystercatcher: Haematopus bachmani. The Birds of North America 155, 1–20 (1995).
21
PW Frank, Effects of winter feeding on limpets by Black Oystercatchers, Haematopus bachmani. Ecology 63, 1352–1362 (1982).
22
JT Wootton, Effects of birds on sea urchins and algae: A lower-intertidal trohic cascade. Ecoscience 2, 321–328 (1995).
23
JT Wootton, Indirect effects, prey susceptibility, and habitat selection: Impacts of birds on limpets and algae. Ecology 73, 981–991 (1992).
24
CP Marsh, Rocky intertidal community organization: The impact of avian predators on mussel recruitment. Ecology 67, 771–786 (1986).
25
DB Irons, RG Anthony, JA Estes, Foraging strategies of Glaucous-winged Gulls in a rocky intertidal community. Ecology 67, 1460–1474 (1986).
26
Beringian Seabird Colony Catalog Computer Database (U.S. Fish and Wildlife Service, Migratory Bird Management, Homer, Alaska, 2004).
27
GD Parry, The evolution of the life histories of four species of intertidal limpets. Ecol Monogr 52, 65–91 (1982).
28
J Lubchenco, Plant species diversity in a marine intertidal community: Importance of herbivore food preference and algal competitive abilities. Am Nat 112, 23–39 (1978).
29
T Norton, S Hawkins, N Manley, G Williams, D Watson, Scraping a living: A review of littorinid grazing. Hydrobiologia 193, 117–138 (1990).
30
H Chenelot, B Konar, Lacuna vincta (Mollusca, Neotaenioglossa) herbivory on juvenile and adult Nereocystis leutkeana (Heterokontophyta, Laminariales). Hydrobiologia 583, 107–118 (2007).
31
K Van Alstyne, J Ehlig, S Whitman, Feeding preferences for juvenile and adult algae depend on algal stage and herbivore species. Mar Ecol Prog Ser 180, 179–185 (1999).
32
PK Dayton, Competition, disturbance, and community organization: The provision and subsequent utilization of space in a rocky intertidal community. Ecol Monogr 41, 351–389 (1971).
33
C Harrold, DC Reed, Food availability, sea urchin grazing, and kelp forest community structure. Ecology 66, 1160–1169 (1985).
34
J Estes, M Tinker, A Doroff, D Burn, Continuing sea otter population declines in the Aleutian archipelago. MarMammal Sci 21, 169–172 (2005).
35
AL Bosman, PAR Hockey, Seabird guano as a determinant of rocky intertidal community structure. Mar Ecol Prog Ser 32, 247–257 (1986).
36
JT Wootton, Direct and indirect effects of nutrients on intertidal community structure: Variable consequences of seabird guano. J Exp Mar Biol Ecol 151, 139–153 (1991).
37
GV Byrd, EP Bailey, W Stahl, Restoration of island populations of Black Oyster-catchers and Pigeon Guillemots by removing introduced foxes. Colonial Waterbirds 20, 253–260 (1997).
38
GV Byrd, JL Trapp, CF Zeillemaker, Removal of introduced foxes: A case study in restoration of native birds. Transact North Am Wildlife Nat Res Conf 59, 317–321 (1994).
39
EN Kozloff Seashore Life of the Northern Pacific Coast: An illustrated guide to Northern California, Oregon, Washington, and British Columbia (Univ of Washington Press, Seattle, 1983).
40
S Drummond, S Connell, Quantifying percentage cover of subtidal organisms on rocky coasts: A comparison of the costs and benefits of standard methods. Mar Freshwater Res 56, 865–876 (2005).
41
D Pech, A Condal, E Bourget, P-L Ardisson, Abundance estimation of rocky shore invertebrates at small spatial scale by high-resolution digital photography and digital image analysis. J Exp Mar Biol Ecol 299, 185–199 (2004).
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© 2008 by The National Academy of Sciences of the USA.
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Received: September 10, 2007
Published online: March 11, 2008
Published in issue: March 11, 2008
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Acknowledgments
This article is dedicated to the memory of Captain Kevin Bell, in appreciation of his knowledge of and enthusiasm for the Aleutian Islands and his invaluable contribution to our work. We thank J. Figurski, S. Reisewitz, and A. Rose for help with field work; K. Bell and the crew of the M/V Tiglax for outstanding ship, logistic, and field support; G.V. Byrd, S. Ebbert, A. Sowls, K. Sundseth, J. Williams, and everyone at the Alaska Maritime National Wildlife Refuge for advice and logistical assistance; T. Klinger and D. Steller for assistance with identifying algal species; G. Bentall for illustrations; members of the D.A.C./B.R.T. lab for helpful discussion; and G.V. Byrd, J. Estes, M. Foster, M. Graham, P. Raimondi, E. Zavaleta and two anonymous reviewers for important comments on the manuscript. Work in the Aleutian Islands was supported by grants from the U.S. Fish and Wildlife Service (to C.M.K.), the M.C. Davis Memorial Fund (C.M.K.), and National Science Foundation Grant OPP-9985814 (to D.A.C.). Further support was provided by an Environmental Protection Agency STAR Fellowship (to C.M.K.), and grants from the Center for the Dynamics and Evolution of the Land–Sea Interface, the Myers Trust, U.S. Fish and Wildlife Service/National Fish and Wildlife Foundation, the STEPS Institute for Innovation in Environmental Research, and the Walt Disney Corporation.
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The authors declare no conflict of interest.
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Introduced rats indirectly change marine rocky intertidal communities from algae- to invertebrate-dominated, Proc. Natl. Acad. Sci. U.S.A.
105 (10) 3800-3804,
https://doi.org/10.1073/pnas.0800570105
(2008).
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