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Kurle et al 08
Introduced rats indirectly change marine rocky
intertidal communities from algae- to
invertebrate-dominated
Carolyn M. Kurle*, Donald A. Croll, and Bernie R. Tershy†
Department of Ecology and Evolutionary Biology, University of California, 100 Shaffer Road, Santa Cruz, CA 95060
Communicated by Donald Kennedy, Stanford University, Stanford, CA, January 22, 2008 (received for review September 10, 2007)
It is widely recognized that trophic interactions structure ecological test the hypothesis that rats are driving a landscape-level trophic
communities, but their effects are usually only demonstrated on a cascade that alters the marine rocky intertidal community
small scale. As a result, landscape-level documentations of trophic structure.
cascades that alter entire communities are scarce. Islands invaded by Worldwide, rats (Rattus spp.) are known to extirpate marine
animals provide natural experiment opportunities both to measure birds on islands primarily through direct predation on their eggs,
general trophic effects across large spatial scales and to determine the chicks, and sometimes adults (6–14). Available data indicate that
trophic roles of invasive species within native ecosystems. Studies predation by R. norvegicus on gull species on islands can reduce
addressing the trophic interactions of invasive species most often breeding populations by 19–47% depending on the species and
focus on their direct effects. To investigate both the presence of a location (7). In addition, gulls are known to leave islands that
landscape-level trophic cascade and the direct and indirect effects of become infested with rats, moving their breeding grounds else-
an invasive species, we examined the impacts of Norway rats (Rattus where (15). In the Aleutian Islands, Norway rats significantly
norvegicus) introduced to the Aleutian Islands on marine bird densi- reduce densities of both burrow- and ground-nesting marine
ties and marine rocky intertidal community structures through sur- birds, including intertidal foraging birds such as Glaucous-
veys conducted on invaded and rat-free islands throughout the entire winged gulls (Larus glaucescens) and Black Oystercatchers
1,900-km archipelago. Densities of birds that forage in the intertidal (Haematopus bachmani), primarily through predation on chicks
were higher on islands without rats. Marine intertidal invertebrates (16–19). However, the indirect impacts of rats on other com-
were more abundant on islands with rats, whereas fleshy algal cover munities are unknown. Gulls and oystercatchers are ground-
was reduced. Our results demonstrate that invasive rats directly nesting, year-round residents of the Aleutian Islands, with gulls
reduce bird densities through predation and significantly affect in- occurring throughout the archipelago and oystercatchers occur-
vertebrate and marine algal abundance in the rocky intertidal indi- ring east of 176° E (20). They forage extensively in the
rectly via a cross-community trophic cascade, unexpectedly changing intertidal, significantly decreasing densities of intertidal inver-
the intertidal community structure from an algae- to an invertebrate- tebrates through predation and indirectly influencing the pres-
dominated system. ence of fleshy algae (21–24). In the summer, oystercatchers
establish combined nesting and feeding territories, thereby for-
community structure invasive species Rattus norvegicus aging in the intertidal near their nesting sites (20), whereas gulls
trophic cascade marine birds feed almost exclusively in the intertidal starting in mid-July after
their young begin to fledge (25). We hypothesized that islands
H airston et al. (1) laid the theoretical framework for the role
of trophic interactions in structuring ecological communi-
ties, whereby carnivores keep herbivores in check via predation
with rats would have considerably lower bird densities and
therefore reduced predation by birds on certain intertidal in-
vertebrates. This would be reflected in substantial differences
that releases plants from heavy grazing pressure, thus resulting in the community structure of the rocky intertidal on islands
in a ‘‘green world.’’ As a result of their article and other seminal with rats.
publications on the topic, much attention in community ecology We measured the marine rocky intertidal community struc-
has focused on the role of predators in structuring communities. ture in July and August 2002–2004 on 8 islands with rats and 15
Thus, the direct and indirect effects of top-level predators on islands without rats (see Materials and Methods) at a landscape
community composition have repeatedly been demonstrated at level spanning nearly the entire Aleutian archipelago (Fig. 1).
the population or community level, but landscape-level illustra- We assessed gull and oystercatcher abundances by using counts
tions of communities transformed by top predators via trophic conducted by the U.S. Fish and Wildlife Service (USFWS) (26).
cascades are still scarce (but see refs. 2–4). Vertebrate predators Gulls were counted on 8 islands with rats and 89 islands without
introduced to oceanic islands throughout an archipelago provide rats, and oystercatchers were counted on 8 islands with rats and
ecologists with opportunities to investigate the presence and 85 islands without rats (excluding islands west of 176° E, where
extent of such cascades over larger spatial scales. Studies of oystercatchers do not occur). Our results provide clear and
invasive species on islands often demonstrate direct reductions compelling evidence of a landscape-level trophic cascade,
in native species abundances (5–7), but it has proven more whereby rats indirectly determine the marine rocky intertidal
difficult to determine the indirect trophic effects mediated by community structure on invaded Aleutian Islands through pre-
invaders and the extent to which these trophic interactions alter dation on birds that forage in the intertidal.
native community composition. The presence of invaded and
noninvaded islands within a single archipelago allows for the
quantification of both direct and indirect impacts on native Author contributions: C.M.K., D.A.C., and B.R.T. designed research; C.M.K. performed
communities imposed by introduced species and provides an research; C.M.K. analyzed data; and C.M.K. wrote the paper.
opportunity to test for the persistence of community-level The authors declare no conflict of interest.
structuring induced by trophic interactions over landscape-level *To whom correspondence should be addressed. E-mail: kurle@biology.ucsc.edu.
scales. We designed a natural comparison to examine the direct †Present address: Island Conservation, Center for Ocean Health, University of California,
and indirect effects of invasive Norway rats (Rattus norvegicus) Santa Cruz, CA 95060.
on marine communities in the Aleutian Islands, Alaska, and to © 2008 by The National Academy of Sciences of the USA
3800 –3804 PNAS March 11, 2008 vol. 105 no. 10 www.pnas.org cgi doi 10.1073 pnas.0800570105
A 25
*
Gull density
20
Alaska
15
Bering Sea 10
5
*
0
Aleutian Islands
B 0 .3 0 *
Oystercatcher
0 .2 5
Island Type
density
Alaid 0 .2 0
Nizki Rat-free 0 .1 5
Agattu Rat-infested 0 .1 0
Buldir 0 .0 5
*
Kiska Davidof 0 .0 0
Rocks off Davidof
Little Kiska Khvostof Ugamak
Rat Adak/Bay of *
Kaligagen
C
invertebrates
1800
Snails
Herbivorous
Amchitka Islands Kanu 1600
Kasatochi Aiktak 1400 Limpets
m-2
Sedanka
Amatignak Kagalaska Ogangen
Tagadak Vsevidof 400
200 * *
Fig. 1. The Aleutian archipelago with sample islands indicated in red 0 *
(rat-infested, n 8) and blue (rat-free, n 15).
D 50 *
Fleshy algae
% cover
40
Results 30 *
20
Rats significantly reduced the densities of two important inter- 10
tidal invertebrate predators. Glaucous-winged gulls and Black 0
Oystercatchers km 1 of shoreline were an order of magnitude
higher on rat-free islands than rat-infested islands (Fig. 2 A and E * Mussels
invertebrates
Non-grazing
600
B) (separate variance t tests: t 2.4, df 92.2, P 0.017; t Sea Stars
m-2
400
4.6, df 91.0, P 0.001, respectively). *
The species composition in the marine rocky intertidal com- 10
*
munities were significantly different between islands with and 0 *
without rats (MANOVAs; counts m 2 of individual inverte-
brates: Pillai Trace value 0.850, F6,16 15.152, P 0.001; F 20
*
percent cover of algae and aggregating invertebrates: Pillai Trace Barnacles
% cover
15
value 0.593, F6,16 3.878, P 0.014). The jackknifed 10
classification matrices from the discriminant analyses using the 5
*
classification factors derived from the percent cover data and 0
from the count m 2 data assigned 83% and 96% of islands,
respectively, to the correct category of rat or rat-free.
not in bird diets
G
Invertebrates
60
Sea Anemones
Densities of herbivorous snails and limpets were several times *
m-2
greater (1319.0 m 2 SE 541.1 vs. 223.7 m 2 SE 89.8 and 40
182.4 m 2 SE 79.0 vs. 30.2 m 2 SE 9.3, respectively) on 20 *
islands with rats than without (t 2.70, df 21, P 0.014; t
0
2.63, df 21, P 0.016, respectively) (Fig. 2C). The percent-
age of rocky intertidal area covered by fleshy algae on islands 8
H *
not in bird diets
Tunicates
Invertebrates
with rats was nearly half (31.2% SE 4.2 vs. 52.4% SE 4.2) 6
% cover
* Sponges
that observed on islands without rats (t 3.24, df 21, P 4
0.004) (Fig. 2D). 2 *
Densities of nongrazing invertebrates eaten by gulls and 0 *
oystercatchers also varied between island types. On islands with
Rat Infested Rat Free
rats, densities of mussels and sea stars were 30 (434.7 m 2
SE 277.0 vs. 13.2 m 2 SE 5.5) and 50 times greater (4.0 m 2 Fig. 2. Mean ( SE) values for parameters sampled on (n 8) rat-infested (red)
SE 2.5 vs. 0.1 m 2 SE 0.1), respectively, as on islands without and (n 15) rat-free (blue) islands in the Aleutian Islands. * indicates a significant
rats (t 2.13, df 21, P 0.045; t 2.16, df 21, P 0.043) difference at the P 0.05 level. Bird densities (birds km 1 of shoreline) were
(Fig. 2E), whereas barnacles covered nearly six times as much estimated from population counts made by the U.S. Fish and Wildlife Service of
area (17.5% SE 5.4 vs. 3.3% SE 1.2) in the rocky intertidal rat-infested (n 8) and rat-free (n 89) islands. Invertebrate densities
on islands with rats (t 3.41, df 21, P 0.003) (Fig. 2F). (invertebrates m 2) were estimated from total counts of individuals from 480 cm2
Densities of sessile invertebrates not eaten by gulls and photo quadrats. Aggregating invertebrate and algal densities (percent cover of
ECOLOGY
rocky intertidal) were estimated from point counts of species from 480 cm2 photo
oystercatchers also were significantly higher on islands with rats.
quadrats. (A) Densities of Glaucous-winged gulls. (B) Densities of Black Oyster-
Sea anemones were over three times greater (48.5 m 2 SE 19.9 catchers. (C) Densities of algal grazing invertebrates that are known bird dietary
vs. 14.6 m 2 SE 6.0) on rat-infested islands (t 2.06, df items. (D) Percent cover of fleshy algae. (E) Densities of nongrazing invertebrates
21, P 0.052) (Fig. 2G), whereas the percent cover of tunicates that are known bird dietary items. (F) Percent cover of barnacles, nongrazing
and sponges was 340 (3.4% SE 1.8 vs. 0.01% SE 0.01) and invertebrates, and known bird dietary items. (G) Densities of sea anemones,
three times greater (5.6% SE 2.2 vs. 1.7% SE 0.8), nongrazing invertebrates that are not bird dietary items. (H) Percent cover of
respectively, on rat-infested islands (t 2.62, df 21, P nongrazing aggregating invertebrates that are not bird dietary items.
0.016; t 2.05, df 21, P 0.054, respectively) (Fig. 2H).
Discussion foraging gulls and oystercatchers. Behavioral observations,
Our results demonstrate that the introduction of rats to the stomach contents, and stable isotope analyses (C.M.K., D.A.C.,
Aleutian Islands significantly reduces the densities of intertidal and B.R.T., unpublished data) confirmed that marine birds,
Kurle et al. PNAS March 11, 2008 vol. 105 no. 10 3801
Bottom–up processes such as increased exposure to nutrients
from seabird guano on islands without rats may be a small, but
insignificant, contributing factor to the differential algal cover
observed between island types. Evidence of enhanced algal
growth due to increased seabird guano in South Africa (35) was
confounded by differential bird predation on herbivores between
sites. Wootton (36) demonstrated that nutrients supplied to
intertidal marine algae via seabird guano positively influenced
fleshy algal growth in only 1 of 18 species.
There are several broad implications to our findings. We
provide an example of a landscape-level trophic cascade with
significant large-scale ecological impacts on plant abundance
and community structure in the tradition of Hairston et al. (1),
- whereby a top predator indirectly influences the abundance of
vegetation through predation on an intermediate organism. This
cascade is especially remarkable in that it is induced via intro-
duced rats that are among the most successful nonindigenous
animal pests on islands (8). The extirpation of native species
through predation by introduced rats is well known, but we
illustrate that invasive species can also have far-reaching and
surprising indirect consequences that extend beyond their more
obvious direct effects.
We also demonstrate an unexpected mechanism by which the
+ terrestrial and marine communities in the Aleutian Islands are
+ strongly linked. Marine birds nest on land while continuing to
forage in the marine environment, thus connecting marine and
terrestrial communities. Such connections are frequently pre-
sented as nutrient transfer from marine to terrestrial systems in
Fig. 3. Introduced Norway rats indirectly alter the intertidal community in the form of seabird guano (2), but we establish a link between
the Aleutian Islands through direct predation on birds that forage in the terrestrial and marine environments, whereby an invasive ter-
intertidal. Dotted arrows indicate indirect effects, whereas solid arrows indi- restrial omnivore reduces populations of marine predators
cate direct effects. Rats keep Glaucous-winged gull and Black Oystercatcher leading to significant changes in a marine community.
numbers low, which releases intertidal invertebrates such as barnacles and
herbivorous snails and limpets from foraging pressure. Greater numbers of Materials and Methods
grazing invertebrates leads to a significant decrease in algal cover, which Study Sites. The Aleutian archipelago is a remote series of islands extending
allows more settling space for sessile invertebrates. The marine rocky inter- 1,900 km west from the Alaska Peninsula (Fig. 1). These islands are ideal for
tidal is altered from an algae- to an invertebrate-dominated system. large-scale natural experiments to study the effects of introduced species (2)
for several reasons, including their homogenous floral, faunal, and weather
patterns; the lack of people; the large number of small islands for sampling;
along with terrestrial vegetation and marine amphipods, were rat and the random introduction of rats throughout the chain starting as early as
prey. Herbivorous snails and limpets are important components the late 1700s via shipwrecks, military, and other human activities (18). Rat-
of gull and oystercatcher diets (20, 21, 25, 27), and both are free islands sampled were Agattu, Aiktak, Alaid, Amatignak, Buldir, Davidof,
known to significantly reduce fleshy algal cover in the marine Kaligagen, Kanu, Kasatochi, Kvostof, Nizki, Rocks off Davidof, Tagadak, Uga-
rocky intertidal through grazing (21, 27–31). Therefore, rat mak, and Vsevidof. Rat-infested islands sampled were Amchitka, Bay of
predation on the birds indirectly changes the rocky intertidal Islands, Kagalaska, Kiska, Little Kiska, Ogangen, Rat, and Sedanka. The islands
sampled within the Bay of Islands were Black, Cormorant, Green, Sea Parrot,
community from an algal- to an invertebrate-dominated system
and South Islands. These islands were grouped into one sample due to their
by releasing intertidal herbivores from predation pressure, which close proximity for prevention of pseudoreplication. Islands were classified as
reduces fleshy algal cover via increased herbivory. The greater rat-free if rats were never introduced to the island. We classified islands as
percentage of area covered by nongrazing barnacles and mussels rat-infested if self-sustaining populations of rats were present on the islands
on islands with rats is likely a consequence of both decreased at the time of the surveys. Four of our rat-free islands lie west of 176° E out of
predation by birds and fewer algal plants because less algae the range of oystercatchers (Agattu, Alaid, Buldir, and Nizki); thus, gulls would
increases available space for aggregating invertebrates (32). be the only birds affecting the intertidal on these islands. Islands were chosen
Finally, the increase in settling space created by fewer algal for accessibility, presence or absence of rats, and absence of effects by intro-
duced foxes. Croll et al. (2) classified islands as fox-infested even if foxes had
plants likely contributed to the significantly higher densities of
been removed in previous years and they determined that these islands may
sessile invertebrates not eaten by birds on islands with rats, such still be experiencing the lingering effect of fewer birds due to past fox
as anemones, tunicates, and sponges (Fig. 3) (20, 25). Sea otters predation. We included nine of those islands in our study, seven of which were
(Enhydra lutris) are known to have a top–down effect on subtidal classified as rat-free and two of which were classified as having rats; all islands
kelp forests and low intertidal algal cover in the Aleutian Islands had foxes removed within the past 10 or more years. Several studies demon-
via their predation on sea urchins (3), important algal herbivores strate strong gull and oystercatcher recoveries within several years after fox
(3, 33). We did not consider a sea otter effect on the intertidal removal (18, 19, 37, 38). To determine whether there were residual effects of
community structure in our study because sea otters are eco- fox occupation influencing our results, we performed two-factor ANOVAs on
logically extinct in the Aleutian Islands (4, 34) and are uniformly all of our intertidal-dependent variables by using rat status and previous
occupation of the island by foxes as independent variables. If previous occu-
absent from all islands. Despite their important role in intertidal
pation by foxes had an effect on a dependent variable, there would be a
kelp abundance, sea urchins were not counted in this study significant effect of fox occupation or a significant interaction between fox
because urchins in the Aleutian Islands move with the tides and occupation and rat status. All such effects were nonsignificant (P 0.10 – 0.87),
are thus largely subtidal (B. Konar, personal communication) indicating that there were no effects resulting from the previous occupation
and impossible to accurately count during low-tide intertidal of the islands by foxes. Therefore, we feel confident that we have avoided any
surveys. potential complications from introduced foxes.
3802 www.pnas.org cgi doi 10.1073 pnas.0800570105 Kurle et al.
Sampling of Rocky Intertidal Communities. Study sites were chosen based on anemones, and sea stars. The second MANOVA and DFA were conducted with
the expanse of available rocky intertidal accessible by skiff. Surveys were the species counted as percent cover that were the fleshy algae and the
conducted in July and August 2002–2004. Surveys consisted of taking system- aggregating invertebrates (barnacles, sponges, and tunicates). To test for
atic digital photos of 480-cm2 quadrats in the rocky intertidal in the low, differences between islands with and without rats in invertebrate numbers
middle, and high intertidal (corresponding to zones 4 –2, respectively, in ref. and percent cover of algae and aggregating invertebrates, we used t tests. To
39). Photos were taken every 5 m along a 30- to 50-m transect. If the area to test for possible residual effects of introduced foxes on intertidal variables, we
be sampled at 5 m was unable to be photographed due to excessive water or performed two-factor ANOVAs on all of our intertidal dependent variables
other natural factors that would render the photograph illegible, the next using rat status and previous occupation of the island by foxes as independent
available site along the transect was chosen instead. Where large kelp or algal variables. To test for differences in bird densities between islands with and
fronds obscured the underlying intertidal bench, we clipped the plants to 1 without rats, mean numbers of birds km 1 of shoreline were compared on
cm and took additional photographs, removing subsequent layers of algal islands that were controlled for foxes and that were surveyed between 1970
cover with each photograph. These additional photos allowed us to estimate and 2007 for the USFWS database [89 without rats, 8 with rats for gulls, 85
the percent cover of algal species revealed with each layer and to estimate without rats, 8 with rats for oystercatchers (excluding islands west of 176° E,
densities of invertebrates hidden by overlying algae. where oystercatchers do not occur)]. This provided the most robust test of the
All digital photos were analyzed by using Adobe Photoshop version 6.0 hypothesis that rats affect bird abundances at the landscape level. Further, not
(Adobe Systems). A digital grid was overlaid on each photo with grid line all islands that we sampled were surveyed by the USFWS, and logistic con-
preferences set to 2.5 inches. Aggregating invertebrate and smaller algal straints (i.e., mismatches in the timing of our intertidal surveys and USFWS bird
species were counted as percent cover by counting their occurrence if they fell surveys conducted during peak bird abundance) precluded us from adding
below an intersection of the grid lines and then dividing that number by the additional bird survey data to the USFWS dataset. We used separate variance
total number of intersections (60). The percentage of area covered by larger t tests because variance terms and sample sizes were different for each island
kelps was estimated by counting the percent cover of holdfasts that remained type. The high proportion of islands with zero birds counted on shorelines
after the removal of the kelp blades. Once all kelp and algae were removed, prevented normalizing the data through transformation. However, because
we counted individual invertebrates and estimated percent cover of aggre- the high proportion of zeroes inflates the variance terms, we considered our
gating invertebrates. Invertebrates counted as percent cover were barnacles, statistics to be overly conservative and, thus, indicative of a true difference in
sponges, and tunicates; all fleshy algae and kelp were counted as percent bird densities among islands. All tests were conducted with Systat version 10.2
cover and included Alaria sp., Cladophora sp., Endocladia sp., Fucus sp., (Systat), and significance was tested at the 0.05 level.
Halosaccion sp., Laminaria sp., Leathesia sp., Mazzaella sp., Odonthalia sp.,
Palmaria sp., Porphyra sp., and Ulva sp. Not all numbers from the percent cover ACKNOWLEDGMENTS. This article is dedicated to the memory of Captain
estimates added to 100% because some areas contained rock, sand, or inver- Kevin Bell, in appreciation of his knowledge of and enthusiasm for the
tebrate species that were not counted as percent cover. Aleutian Islands and his invaluable contribution to our work. We thank J.
To estimate actual numbers of species, the occurrence of each individual Figurski, S. Reisewitz, and A. Rose for help with field work; K. Bell and the crew
within the photo was counted, and that number was divided by 0.048 to 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
estimate the number of invertebrates per square meter. Species counted as
Maritime National Wildlife Refuge for advice and logistical assistance; T.
individuals per square meter were anemones, chitons, herbivorous snails, Klinger and D. Steller for assistance with identifying algal species; G. Bentall
limpets, mussels, and sea stars. The use of digital photographs is widely for illustrations; members of the D.A.C./B.R.T. lab for helpful discussion; and
accepted as an appropriate technique to estimate the abundance of marine G.V. Byrd, J. Estes, M. Foster, M. Graham, P. Raimondi, E. Zavaleta and two
subtidal and intertidal organisms (40, 41). anonymous reviewers for important comments on the manuscript. Work in
the Aleutian Islands was supported by grants from the U.S. Fish and Wildlife
Statistical Testing. To test for differences in the species composition of the 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 pro-
rocky intertidal between islands with and without rats and to determine how
vided by an Environmental Protection Agency STAR Fellowship (to C.M.K.),
well the intertidal data predicted whether an island had rats, we used multi- and grants from the Center for the Dynamics and Evolution of the Land–Sea
variate ANOVAs (MANOVAs), followed by discriminant function analyses Interface, the Myers Trust, U.S. Fish and Wildlife Service/National Fish and
(DFAs). One MANOVA and a DFA were conducted with the invertebrates Wildlife Foundation, the STEPS Institute for Innovation in Environmental
counted as number per m 2 that were herbivorous snails, limpets, mussels, sea Research, and the Walt Disney Corporation.
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3804 www.pnas.org cgi doi 10.1073 pnas.0800570105 Kurle et al.
intertidal communities from algae- to
invertebrate-dominated
Carolyn M. Kurle*, Donald A. Croll, and Bernie R. Tershy†
Department of Ecology and Evolutionary Biology, University of California, 100 Shaffer Road, Santa Cruz, CA 95060
Communicated by Donald Kennedy, Stanford University, Stanford, CA, January 22, 2008 (received for review September 10, 2007)
It is widely recognized that trophic interactions structure ecological test the hypothesis that rats are driving a landscape-level trophic
communities, but their effects are usually only demonstrated on a cascade that alters the marine rocky intertidal community
small scale. As a result, landscape-level documentations of trophic structure.
cascades that alter entire communities are scarce. Islands invaded by Worldwide, rats (Rattus spp.) are known to extirpate marine
animals provide natural experiment opportunities both to measure birds on islands primarily through direct predation on their eggs,
general trophic effects across large spatial scales and to determine the chicks, and sometimes adults (6–14). Available data indicate that
trophic roles of invasive species within native ecosystems. Studies predation by R. norvegicus on gull species on islands can reduce
addressing the trophic interactions of invasive species most often breeding populations by 19–47% depending on the species and
focus on their direct effects. To investigate both the presence of a location (7). In addition, gulls are known to leave islands that
landscape-level trophic cascade and the direct and indirect effects of become infested with rats, moving their breeding grounds else-
an invasive species, we examined the impacts of Norway rats (Rattus where (15). In the Aleutian Islands, Norway rats significantly
norvegicus) introduced to the Aleutian Islands on marine bird densi- reduce densities of both burrow- and ground-nesting marine
ties and marine rocky intertidal community structures through sur- birds, including intertidal foraging birds such as Glaucous-
veys conducted on invaded and rat-free islands throughout the entire winged gulls (Larus glaucescens) and Black Oystercatchers
1,900-km archipelago. Densities of birds that forage in the intertidal (Haematopus bachmani), primarily through predation on chicks
were higher on islands without rats. Marine intertidal invertebrates (16–19). However, the indirect impacts of rats on other com-
were more abundant on islands with rats, whereas fleshy algal cover munities are unknown. Gulls and oystercatchers are ground-
was reduced. Our results demonstrate that invasive rats directly nesting, year-round residents of the Aleutian Islands, with gulls
reduce bird densities through predation and significantly affect in- occurring throughout the archipelago and oystercatchers occur-
vertebrate and marine algal abundance in the rocky intertidal indi- ring east of 176° E (20). They forage extensively in the
rectly via a cross-community trophic cascade, unexpectedly changing intertidal, significantly decreasing densities of intertidal inver-
the intertidal community structure from an algae- to an invertebrate- tebrates through predation and indirectly influencing the pres-
dominated system. ence of fleshy algae (21–24). In the summer, oystercatchers
establish combined nesting and feeding territories, thereby for-
community structure invasive species Rattus norvegicus aging in the intertidal near their nesting sites (20), whereas gulls
trophic cascade marine birds feed almost exclusively in the intertidal starting in mid-July after
their young begin to fledge (25). We hypothesized that islands
H airston et al. (1) laid the theoretical framework for the role
of trophic interactions in structuring ecological communi-
ties, whereby carnivores keep herbivores in check via predation
with rats would have considerably lower bird densities and
therefore reduced predation by birds on certain intertidal in-
vertebrates. This would be reflected in substantial differences
that releases plants from heavy grazing pressure, thus resulting in the community structure of the rocky intertidal on islands
in a ‘‘green world.’’ As a result of their article and other seminal with rats.
publications on the topic, much attention in community ecology We measured the marine rocky intertidal community struc-
has focused on the role of predators in structuring communities. ture in July and August 2002–2004 on 8 islands with rats and 15
Thus, the direct and indirect effects of top-level predators on islands without rats (see Materials and Methods) at a landscape
community composition have repeatedly been demonstrated at level spanning nearly the entire Aleutian archipelago (Fig. 1).
the population or community level, but landscape-level illustra- We assessed gull and oystercatcher abundances by using counts
tions of communities transformed by top predators via trophic conducted by the U.S. Fish and Wildlife Service (USFWS) (26).
cascades are still scarce (but see refs. 2–4). Vertebrate predators Gulls were counted on 8 islands with rats and 89 islands without
introduced to oceanic islands throughout an archipelago provide rats, and oystercatchers were counted on 8 islands with rats and
ecologists with opportunities to investigate the presence and 85 islands without rats (excluding islands west of 176° E, where
extent of such cascades over larger spatial scales. Studies of oystercatchers do not occur). Our results provide clear and
invasive species on islands often demonstrate direct reductions compelling evidence of a landscape-level trophic cascade,
in native species abundances (5–7), but it has proven more whereby rats indirectly determine the marine rocky intertidal
difficult to determine the indirect trophic effects mediated by community structure on invaded Aleutian Islands through pre-
invaders and the extent to which these trophic interactions alter dation on birds that forage in the intertidal.
native community composition. The presence of invaded and
noninvaded islands within a single archipelago allows for the
quantification of both direct and indirect impacts on native Author contributions: C.M.K., D.A.C., and B.R.T. designed research; C.M.K. performed
communities imposed by introduced species and provides an research; C.M.K. analyzed data; and C.M.K. wrote the paper.
opportunity to test for the persistence of community-level The authors declare no conflict of interest.
structuring induced by trophic interactions over landscape-level *To whom correspondence should be addressed. E-mail: kurle@biology.ucsc.edu.
scales. We designed a natural comparison to examine the direct †Present address: Island Conservation, Center for Ocean Health, University of California,
and indirect effects of invasive Norway rats (Rattus norvegicus) Santa Cruz, CA 95060.
on marine communities in the Aleutian Islands, Alaska, and to © 2008 by The National Academy of Sciences of the USA
3800 –3804 PNAS March 11, 2008 vol. 105 no. 10 www.pnas.org cgi doi 10.1073 pnas.0800570105
A 25
*
Gull density
20
Alaska
15
Bering Sea 10
5
*
0
Aleutian Islands
B 0 .3 0 *
Oystercatcher
0 .2 5
Island Type
density
Alaid 0 .2 0
Nizki Rat-free 0 .1 5
Agattu Rat-infested 0 .1 0
Buldir 0 .0 5
*
Kiska Davidof 0 .0 0
Rocks off Davidof
Little Kiska Khvostof Ugamak
Rat Adak/Bay of *
Kaligagen
C
invertebrates
1800
Snails
Herbivorous
Amchitka Islands Kanu 1600
Kasatochi Aiktak 1400 Limpets
m-2
Sedanka
Amatignak Kagalaska Ogangen
Tagadak Vsevidof 400
200 * *
Fig. 1. The Aleutian archipelago with sample islands indicated in red 0 *
(rat-infested, n 8) and blue (rat-free, n 15).
D 50 *
Fleshy algae
% cover
40
Results 30 *
20
Rats significantly reduced the densities of two important inter- 10
tidal invertebrate predators. Glaucous-winged gulls and Black 0
Oystercatchers km 1 of shoreline were an order of magnitude
higher on rat-free islands than rat-infested islands (Fig. 2 A and E * Mussels
invertebrates
Non-grazing
600
B) (separate variance t tests: t 2.4, df 92.2, P 0.017; t Sea Stars
m-2
400
4.6, df 91.0, P 0.001, respectively). *
The species composition in the marine rocky intertidal com- 10
*
munities were significantly different between islands with and 0 *
without rats (MANOVAs; counts m 2 of individual inverte-
brates: Pillai Trace value 0.850, F6,16 15.152, P 0.001; F 20
*
percent cover of algae and aggregating invertebrates: Pillai Trace Barnacles
% cover
15
value 0.593, F6,16 3.878, P 0.014). The jackknifed 10
classification matrices from the discriminant analyses using the 5
*
classification factors derived from the percent cover data and 0
from the count m 2 data assigned 83% and 96% of islands,
respectively, to the correct category of rat or rat-free.
not in bird diets
G
Invertebrates
60
Sea Anemones
Densities of herbivorous snails and limpets were several times *
m-2
greater (1319.0 m 2 SE 541.1 vs. 223.7 m 2 SE 89.8 and 40
182.4 m 2 SE 79.0 vs. 30.2 m 2 SE 9.3, respectively) on 20 *
islands with rats than without (t 2.70, df 21, P 0.014; t
0
2.63, df 21, P 0.016, respectively) (Fig. 2C). The percent-
age of rocky intertidal area covered by fleshy algae on islands 8
H *
not in bird diets
Tunicates
Invertebrates
with rats was nearly half (31.2% SE 4.2 vs. 52.4% SE 4.2) 6
% cover
* Sponges
that observed on islands without rats (t 3.24, df 21, P 4
0.004) (Fig. 2D). 2 *
Densities of nongrazing invertebrates eaten by gulls and 0 *
oystercatchers also varied between island types. On islands with
Rat Infested Rat Free
rats, densities of mussels and sea stars were 30 (434.7 m 2
SE 277.0 vs. 13.2 m 2 SE 5.5) and 50 times greater (4.0 m 2 Fig. 2. Mean ( SE) values for parameters sampled on (n 8) rat-infested (red)
SE 2.5 vs. 0.1 m 2 SE 0.1), respectively, as on islands without and (n 15) rat-free (blue) islands in the Aleutian Islands. * indicates a significant
rats (t 2.13, df 21, P 0.045; t 2.16, df 21, P 0.043) difference at the P 0.05 level. Bird densities (birds km 1 of shoreline) were
(Fig. 2E), whereas barnacles covered nearly six times as much estimated from population counts made by the U.S. Fish and Wildlife Service of
area (17.5% SE 5.4 vs. 3.3% SE 1.2) in the rocky intertidal rat-infested (n 8) and rat-free (n 89) islands. Invertebrate densities
on islands with rats (t 3.41, df 21, P 0.003) (Fig. 2F). (invertebrates m 2) were estimated from total counts of individuals from 480 cm2
Densities of sessile invertebrates not eaten by gulls and photo quadrats. Aggregating invertebrate and algal densities (percent cover of
ECOLOGY
rocky intertidal) were estimated from point counts of species from 480 cm2 photo
oystercatchers also were significantly higher on islands with rats.
quadrats. (A) Densities of Glaucous-winged gulls. (B) Densities of Black Oyster-
Sea anemones were over three times greater (48.5 m 2 SE 19.9 catchers. (C) Densities of algal grazing invertebrates that are known bird dietary
vs. 14.6 m 2 SE 6.0) on rat-infested islands (t 2.06, df items. (D) Percent cover of fleshy algae. (E) Densities of nongrazing invertebrates
21, P 0.052) (Fig. 2G), whereas the percent cover of tunicates that are known bird dietary items. (F) Percent cover of barnacles, nongrazing
and sponges was 340 (3.4% SE 1.8 vs. 0.01% SE 0.01) and invertebrates, and known bird dietary items. (G) Densities of sea anemones,
three times greater (5.6% SE 2.2 vs. 1.7% SE 0.8), nongrazing invertebrates that are not bird dietary items. (H) Percent cover of
respectively, on rat-infested islands (t 2.62, df 21, P nongrazing aggregating invertebrates that are not bird dietary items.
0.016; t 2.05, df 21, P 0.054, respectively) (Fig. 2H).
Discussion foraging gulls and oystercatchers. Behavioral observations,
Our results demonstrate that the introduction of rats to the stomach contents, and stable isotope analyses (C.M.K., D.A.C.,
Aleutian Islands significantly reduces the densities of intertidal and B.R.T., unpublished data) confirmed that marine birds,
Kurle et al. PNAS March 11, 2008 vol. 105 no. 10 3801
Bottom–up processes such as increased exposure to nutrients
from seabird guano on islands without rats may be a small, but
insignificant, contributing factor to the differential algal cover
observed between island types. Evidence of enhanced algal
growth due to increased seabird guano in South Africa (35) was
confounded by differential bird predation on herbivores between
sites. Wootton (36) demonstrated that nutrients supplied to
intertidal marine algae via seabird guano positively influenced
fleshy algal growth in only 1 of 18 species.
There are several broad implications to our findings. We
provide an example of a landscape-level trophic cascade with
significant large-scale ecological impacts on plant abundance
and community structure in the tradition of Hairston et al. (1),
- whereby a top predator indirectly influences the abundance of
vegetation through predation on an intermediate organism. This
cascade is especially remarkable in that it is induced via intro-
duced rats that are among the most successful nonindigenous
animal pests on islands (8). The extirpation of native species
through predation by introduced rats is well known, but we
illustrate that invasive species can also have far-reaching and
surprising indirect consequences that extend beyond their more
obvious direct effects.
We also demonstrate an unexpected mechanism by which the
+ terrestrial and marine communities in the Aleutian Islands are
+ strongly linked. Marine birds nest on land while continuing to
forage in the marine environment, thus connecting marine and
terrestrial communities. Such connections are frequently pre-
sented as nutrient transfer from marine to terrestrial systems in
Fig. 3. Introduced Norway rats indirectly alter the intertidal community in the form of seabird guano (2), but we establish a link between
the Aleutian Islands through direct predation on birds that forage in the terrestrial and marine environments, whereby an invasive ter-
intertidal. Dotted arrows indicate indirect effects, whereas solid arrows indi- restrial omnivore reduces populations of marine predators
cate direct effects. Rats keep Glaucous-winged gull and Black Oystercatcher leading to significant changes in a marine community.
numbers low, which releases intertidal invertebrates such as barnacles and
herbivorous snails and limpets from foraging pressure. Greater numbers of Materials and Methods
grazing invertebrates leads to a significant decrease in algal cover, which Study Sites. The Aleutian archipelago is a remote series of islands extending
allows more settling space for sessile invertebrates. The marine rocky inter- 1,900 km west from the Alaska Peninsula (Fig. 1). These islands are ideal for
tidal is altered from an algae- to an invertebrate-dominated system. large-scale natural experiments to study the effects of introduced species (2)
for several reasons, including their homogenous floral, faunal, and weather
patterns; the lack of people; the large number of small islands for sampling;
along with terrestrial vegetation and marine amphipods, were rat and the random introduction of rats throughout the chain starting as early as
prey. Herbivorous snails and limpets are important components the late 1700s via shipwrecks, military, and other human activities (18). Rat-
of gull and oystercatcher diets (20, 21, 25, 27), and both are free islands sampled were Agattu, Aiktak, Alaid, Amatignak, Buldir, Davidof,
known to significantly reduce fleshy algal cover in the marine Kaligagen, Kanu, Kasatochi, Kvostof, Nizki, Rocks off Davidof, Tagadak, Uga-
rocky intertidal through grazing (21, 27–31). Therefore, rat mak, and Vsevidof. Rat-infested islands sampled were Amchitka, Bay of
predation on the birds indirectly changes the rocky intertidal Islands, Kagalaska, Kiska, Little Kiska, Ogangen, Rat, and Sedanka. The islands
sampled within the Bay of Islands were Black, Cormorant, Green, Sea Parrot,
community from an algal- to an invertebrate-dominated system
and South Islands. These islands were grouped into one sample due to their
by releasing intertidal herbivores from predation pressure, which close proximity for prevention of pseudoreplication. Islands were classified as
reduces fleshy algal cover via increased herbivory. The greater rat-free if rats were never introduced to the island. We classified islands as
percentage of area covered by nongrazing barnacles and mussels rat-infested if self-sustaining populations of rats were present on the islands
on islands with rats is likely a consequence of both decreased at the time of the surveys. Four of our rat-free islands lie west of 176° E out of
predation by birds and fewer algal plants because less algae the range of oystercatchers (Agattu, Alaid, Buldir, and Nizki); thus, gulls would
increases available space for aggregating invertebrates (32). be the only birds affecting the intertidal on these islands. Islands were chosen
Finally, the increase in settling space created by fewer algal for accessibility, presence or absence of rats, and absence of effects by intro-
duced foxes. Croll et al. (2) classified islands as fox-infested even if foxes had
plants likely contributed to the significantly higher densities of
been removed in previous years and they determined that these islands may
sessile invertebrates not eaten by birds on islands with rats, such still be experiencing the lingering effect of fewer birds due to past fox
as anemones, tunicates, and sponges (Fig. 3) (20, 25). Sea otters predation. We included nine of those islands in our study, seven of which were
(Enhydra lutris) are known to have a top–down effect on subtidal classified as rat-free and two of which were classified as having rats; all islands
kelp forests and low intertidal algal cover in the Aleutian Islands had foxes removed within the past 10 or more years. Several studies demon-
via their predation on sea urchins (3), important algal herbivores strate strong gull and oystercatcher recoveries within several years after fox
(3, 33). We did not consider a sea otter effect on the intertidal removal (18, 19, 37, 38). To determine whether there were residual effects of
community structure in our study because sea otters are eco- fox occupation influencing our results, we performed two-factor ANOVAs on
logically extinct in the Aleutian Islands (4, 34) and are uniformly all of our intertidal-dependent variables by using rat status and previous
occupation of the island by foxes as independent variables. If previous occu-
absent from all islands. Despite their important role in intertidal
pation by foxes had an effect on a dependent variable, there would be a
kelp abundance, sea urchins were not counted in this study significant effect of fox occupation or a significant interaction between fox
because urchins in the Aleutian Islands move with the tides and occupation and rat status. All such effects were nonsignificant (P 0.10 – 0.87),
are thus largely subtidal (B. Konar, personal communication) indicating that there were no effects resulting from the previous occupation
and impossible to accurately count during low-tide intertidal of the islands by foxes. Therefore, we feel confident that we have avoided any
surveys. potential complications from introduced foxes.
3802 www.pnas.org cgi doi 10.1073 pnas.0800570105 Kurle et al.
Sampling of Rocky Intertidal Communities. Study sites were chosen based on anemones, and sea stars. The second MANOVA and DFA were conducted with
the expanse of available rocky intertidal accessible by skiff. Surveys were the species counted as percent cover that were the fleshy algae and the
conducted in July and August 2002–2004. Surveys consisted of taking system- aggregating invertebrates (barnacles, sponges, and tunicates). To test for
atic digital photos of 480-cm2 quadrats in the rocky intertidal in the low, differences between islands with and without rats in invertebrate numbers
middle, and high intertidal (corresponding to zones 4 –2, respectively, in ref. and percent cover of algae and aggregating invertebrates, we used t tests. To
39). Photos were taken every 5 m along a 30- to 50-m transect. If the area to test for possible residual effects of introduced foxes on intertidal variables, we
be sampled at 5 m was unable to be photographed due to excessive water or performed two-factor ANOVAs on all of our intertidal dependent variables
other natural factors that would render the photograph illegible, the next using rat status and previous occupation of the island by foxes as independent
available site along the transect was chosen instead. Where large kelp or algal variables. To test for differences in bird densities between islands with and
fronds obscured the underlying intertidal bench, we clipped the plants to 1 without rats, mean numbers of birds km 1 of shoreline were compared on
cm and took additional photographs, removing subsequent layers of algal islands that were controlled for foxes and that were surveyed between 1970
cover with each photograph. These additional photos allowed us to estimate and 2007 for the USFWS database [89 without rats, 8 with rats for gulls, 85
the percent cover of algal species revealed with each layer and to estimate without rats, 8 with rats for oystercatchers (excluding islands west of 176° E,
densities of invertebrates hidden by overlying algae. where oystercatchers do not occur)]. This provided the most robust test of the
All digital photos were analyzed by using Adobe Photoshop version 6.0 hypothesis that rats affect bird abundances at the landscape level. Further, not
(Adobe Systems). A digital grid was overlaid on each photo with grid line all islands that we sampled were surveyed by the USFWS, and logistic con-
preferences set to 2.5 inches. Aggregating invertebrate and smaller algal straints (i.e., mismatches in the timing of our intertidal surveys and USFWS bird
species were counted as percent cover by counting their occurrence if they fell surveys conducted during peak bird abundance) precluded us from adding
below an intersection of the grid lines and then dividing that number by the additional bird survey data to the USFWS dataset. We used separate variance
total number of intersections (60). The percentage of area covered by larger t tests because variance terms and sample sizes were different for each island
kelps was estimated by counting the percent cover of holdfasts that remained type. The high proportion of islands with zero birds counted on shorelines
after the removal of the kelp blades. Once all kelp and algae were removed, prevented normalizing the data through transformation. However, because
we counted individual invertebrates and estimated percent cover of aggre- the high proportion of zeroes inflates the variance terms, we considered our
gating invertebrates. Invertebrates counted as percent cover were barnacles, statistics to be overly conservative and, thus, indicative of a true difference in
sponges, and tunicates; all fleshy algae and kelp were counted as percent bird densities among islands. All tests were conducted with Systat version 10.2
cover and included Alaria sp., Cladophora sp., Endocladia sp., Fucus sp., (Systat), and significance was tested at the 0.05 level.
Halosaccion sp., Laminaria sp., Leathesia sp., Mazzaella sp., Odonthalia sp.,
Palmaria sp., Porphyra sp., and Ulva sp. Not all numbers from the percent cover ACKNOWLEDGMENTS. This article is dedicated to the memory of Captain
estimates added to 100% because some areas contained rock, sand, or inver- Kevin Bell, in appreciation of his knowledge of and enthusiasm for the
tebrate species that were not counted as percent cover. Aleutian Islands and his invaluable contribution to our work. We thank J.
To estimate actual numbers of species, the occurrence of each individual Figurski, S. Reisewitz, and A. Rose for help with field work; K. Bell and the crew
within the photo was counted, and that number was divided by 0.048 to 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
estimate the number of invertebrates per square meter. Species counted as
Maritime National Wildlife Refuge for advice and logistical assistance; T.
individuals per square meter were anemones, chitons, herbivorous snails, Klinger and D. Steller for assistance with identifying algal species; G. Bentall
limpets, mussels, and sea stars. The use of digital photographs is widely for illustrations; members of the D.A.C./B.R.T. lab for helpful discussion; and
accepted as an appropriate technique to estimate the abundance of marine G.V. Byrd, J. Estes, M. Foster, M. Graham, P. Raimondi, E. Zavaleta and two
subtidal and intertidal organisms (40, 41). anonymous reviewers for important comments on the manuscript. Work in
the Aleutian Islands was supported by grants from the U.S. Fish and Wildlife
Statistical Testing. To test for differences in the species composition of the 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 pro-
rocky intertidal between islands with and without rats and to determine how
vided by an Environmental Protection Agency STAR Fellowship (to C.M.K.),
well the intertidal data predicted whether an island had rats, we used multi- and grants from the Center for the Dynamics and Evolution of the Land–Sea
variate ANOVAs (MANOVAs), followed by discriminant function analyses Interface, the Myers Trust, U.S. Fish and Wildlife Service/National Fish and
(DFAs). One MANOVA and a DFA were conducted with the invertebrates Wildlife Foundation, the STEPS Institute for Innovation in Environmental
counted as number per m 2 that were herbivorous snails, limpets, mussels, sea Research, and the Walt Disney Corporation.
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