[OANNES Foro] Indirect effects of invasive rat removal result in recovery of island rocky intertidal community structure

[Mario Cabrejos]

Scientific Reports <https://www.nature.com/srep> volume 11,
Article number: 5395 (2021)

Published: 08 March 2021
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#article-info>

https://doi.org/10.1038/s41598-021-84342-2



*Indirect effects of invasive rat removal result in recovery of island
rocky intertidal community structure*

Carolyn M. Kurle
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#auth-Carolyn_M_-Kurle>
, Kelly M. Zilliacus
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#auth-Kelly_M_-Zilliacus>
, Jenna Sparks
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#auth-Jenna-Sparks>
, Jen Curl
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#auth-Jen-Curl>
, Mila Bock
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#auth-Mila-Bock>
, Stacey Buckelew
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#auth-Stacey-Buckelew>
, Jeffrey C. Williams
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#auth-Jeffrey_C_-Williams>
, Coral A. Wolf
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#auth-Coral_A_-Wolf>
, Nick D. Holmes
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#auth-Nick_D_-Holmes>
, Jonathan Plissner
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#auth-Jonathan-Plissner>
, Gregg R. Howald
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#auth-Gregg_R_-Howald>
, Bernie R. Tershy
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#auth-Bernie_R_-Tershy>
 & Donald A. Croll
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#auth-Donald_A_-Croll>


*Abstract*

Eleven years after invasive Norway rats (*Rattus norvegicus*) were
eradicated from Hawadax Island, in the Aleutian Islands, Alaska, the
predicted three-level trophic cascade in the rocky intertidal, with native
shorebirds as the apex predator, returned, leading to a community
resembling those on rat-free islands with significant decreases in
invertebrate species abundances and increases in fleshy algal cover. Rats
had indirectly structured the intertidal community via their role as the
apex predator in a four-level trophic cascade. Our results are an excellent
example of an achievable and relatively short-term community-level recovery
following removal of invasive animals. These conservation successes are
especially important for islands as their disproportionately high levels of
native biodiversity are excessively threatened by invasive mammals.



*Introduction*

Invasive animals are a main driver of global biodiversity loss and can
impact ecosystem function1
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#ref-CR1>
,2
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#ref-CR2>
,3
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#ref-CR3>
,4
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#ref-CR4>
,5 <https://www.nature.com/articles/s41598-021-84342-2#ref-CR5>. Invasive
animal impacts are particularly disruptive on islands because islands
usually have small numbers of species resulting in simplified food chains
and limited functional redundancy, and those species typically have limited
evolved defenses against herbivory, predation, and competition6
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR6>. The direct
effects of invasive animals on islands are well documented7
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#ref-CR7>
,8
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#ref-CR8>
,9
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#ref-CR9>
,10
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#ref-CR10>
,11 <https://www.nature.com/articles/s41598-021-84342-2#ref-CR11>, and
there is increasing evidence of their multiple indirect effects as well6
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR6>, 12
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#ref-CR12>
,13
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#ref-CR13>
,14
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#ref-CR14>
,15 <https://www.nature.com/articles/s41598-021-84342-2#ref-CR15>.

Invasive rats (*Rattus spp.*) are the most widespread and damaging invasive
animals16 <https://www.nature.com/articles/s41598-021-84342-2#ref-CR16>,17
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR17>. They are
present on perhaps 90% of islands18
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR18>,19
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR19>, influence
island biota both directly as competitors, predators, herbivores, and
frugivores19
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#ref-CR19>
,20
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#ref-CR20>
,21 <https://www.nature.com/articles/s41598-021-84342-2#ref-CR21>, and
indirectly via trophic cascades, cross ecosystem subsidies, propagule
dispersal, and mutualist networks9
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR9>,13
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR13>,14
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR14>,22
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#ref-CR22>
,23
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#ref-CR23>
,24 <https://www.nature.com/articles/s41598-021-84342-2#ref-CR24>.

Because of these deleterious impacts, the removal of invasive animals has
become an important global conservation strategy, with over 900 successful
animal eradications on almost 800 islands since 195025
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR25>. While the
number, rate, and size of invasive animal eradications is increasing8
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR8>, 26
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#ref-CR26>
,27
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#ref-CR27>
,28 <https://www.nature.com/articles/s41598-021-84342-2#ref-CR28>, studies
of the full benefits to island communities after invasive animal
eradications are limited (but see8
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR8>). Longer-term
post-eradication studies of island community recoveries from the direct and
indirect impacts of invaders are even more limited29
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR29>, as are
recoveries from the effects of cross-ecosystem (e.g. near-shore marine vs.
terrestrial) interactions.

Community recovery after invasive animal eradication is difficult to
measure for many reasons, including natural stochasticity and uncertain
baselines by which to compare altered landscapes. In addition,
demonstration of community recovery requires study of the indirect effects
of invaders, adequate measures of multiple community components, and a
commitment to long-term monitoring. Therefore, the extent to which entire
communities recover following invasive species eradication, and the time
required for recovery, are much less understood than the direct deleterious
effects of invaders and the recoveries of multiple native species once
invaders and their direct mechanisms of control (frequently predation) are
removed (but see30
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR30>,31
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR31>).

Hawadax Island (previously known as Rat Island) is in the central Aleutian
Island chain (Fig. 1
<https://www.nature.com/articles/s41598-021-84342-2#Fig1>). The island was
likely invaded by Norway rats (*R. norvegicus*) when a Japanese ship went
aground in the 1780′s, and invaded by Arctic foxes (*Vulpes lagopus*)
following intentional introductions by fur traders in the 1800s32
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR32>. The combined
impact of an introduced carnivore (foxes) and omnivore (rats) had multiple
direct and indirect impacts 33
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR33>. For example,
while archeological evidence from native Unangan (Aleut) habitation sites
indicate marine birds were once common on Hawadax Island, rats and
introduced foxes extirpated locally breeding seabirds, shorebirds, and land
birds32 <https://www.nature.com/articles/s41598-021-84342-2#ref-CR32>.

*Figure 1*

[image: figure1]
<https://www.nature.com/articles/s41598-021-84342-2/figures/1>

The (*A*) central Aleutian Archipelago, Alaska, USA contains the (*B*) Rat
Islands Group, including Hawadax Island. The (*C*) intertidal plots and
beach transects surveyed on Hawadax Island. Intertidal plot 6 was only
surveyed in 2008 and 201335
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR35>.

*Full size image*
<https://www.nature.com/articles/s41598-021-84342-2/figures/1>

Foxes were eradicated from Hawadax Island in 198434
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR34>, and rats
were eradicated in 2008 using aerially broadcast rodenticide (25-ppm
brodifacoum32 <https://www.nature.com/articles/s41598-021-84342-2#ref-CR32>).
Croll et al.33 <https://www.nature.com/articles/s41598-021-84342-2#ref-CR33>
reported
on the direct effects of rat eradication after five years, demonstrating
significant recoveries of terrestrial birds (Gray-crowned Rosy Finch
[*Leucosticte
tephrocotis*], Lapland Longspur [*Calcarius lapponi-cus*], Snow
Bunting [*Plectrophenax
nivalis*], and Song Sparrow [*Melospiza melodia*]) and shorebirds (Black
Oystercatcher [*Haematopus bachmani*] and Rock Sandpiper [*Calidris
ptilocnemis*], and the initial recolonization or recovery of marine birds
(Tufted Puffin [*Fratercula cirrhata*], Leach’s Storm-petrel [*Oceanodroma
leucohoa*], and Glaucous-winged Gull [*Larus glaucescens*]). However,
community-level changes resulting from indirect changes in trophic
structure post-rat eradication are likely to take longer than the recovery
of these directly impacted bird species30
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR30>.

To measure the time required and potential for passive community recovery
on an island after rat eradication, we measured abundances of shorebirds
and multiple rocky intertidal species before (2008), and five (2013) and 11
(2019) years post-rat eradication on Hawadax Island. Previous comparisons
in 2002–2004 by Kurle et al.12
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR12> of the rocky
intertidal community composition on Islands in the Aleutian archipelago
with and without invasive rats demonstrated a rat-mediated, four-level
trophic cascade in which rats extirpated the shorebirds that forage on
intertidal herbivores, leaving a system dominated by invertebrate
herbivores (Fig. 2 <https://www.nature.com/articles/s41598-021-84342-2#Fig2>).
Kurle et al.12 <https://www.nature.com/articles/s41598-021-84342-2#ref-CR12>
found
that 83% and 96% of islands could be assigned to their correct category of
rat-infested or rat-free, respectively, based on the species composition of
the rocky intertidal. Thus, we predicted that the rocky intertidal
community on Hawadax Island would return to a state resembling a rat-free
island given sufficient time for shorebird populations to recover to levels
necessary to maintain the three-trophic level cascade typical of Aleutian
Islands without rats.

*Figure 2*

[image: figure2]
<https://www.nature.com/articles/s41598-021-84342-2/figures/2>

The presence of invasive rats on Aleutian Islands in Alaska creates a (*A*)
four-level trophic cascade wherein rats negatively impact primary
productivity, indirectly (dotted line) turning the rocky intertidal
community into an invertebrate dominated system by depredating shorebirds
and releasing intertidal grazers from bird predation pressure. On islands
without rats, and presumably on islands in recovery after rat removal, such
as Hawadax, the rocky intertidal becomes a (*B*) three-level trophic
cascade wherein shorebirds depredate herbivorous invertebrates, thereby
releasing algae from grazing pressure, and indirectly creating an algal
dominated community. Birds also consume invertebrate non-grazers (e.g.,
mussels, anemones, seastars, and sponges), and their decreased abundances
following rat removal may lead to increased availability of space in the
rocky intertidal, further facilitating increases in algal cover. Figure
modified from Kurle et al.12
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR12>., Gena
Bentall drew the images and C. Kurle created the figure.

*Full size image*
<https://www.nature.com/articles/s41598-021-84342-2/figures/2>

We compared our long-term monitoring data collected on Hawadax Island pre-
(2008) and post- (2013 and 2019) rat eradication to data contrasting
rat-infested and rat-free Aleutian Islands measured in 2002–2004 from Kurle
et al.12 <https://www.nature.com/articles/s41598-021-84342-2#ref-CR12>.
Specifically, we sought to: (1) document longer-term recovery of breeding
intertidal-feeding marine birds (Black Oystercatchers and Glaucous-winged
Gulls), (2) examine changes in the marine rocky intertidal community
related to the direct and indirect impacts of marine bird recovery, and (3)
better understand the time required for recovery of marine rocky intertidal
communities on islands after rat removal.

*Results*

Intertidal community

Predicted changes in the rocky intertidal community12
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR12> were largely
not evident five years post-rat eradication (Table 1
<https://www.nature.com/articles/s41598-021-84342-2#Tab1>, Fig. 3
<https://www.nature.com/articles/s41598-021-84342-2#Fig3>, and
Supplementary Fig. 1
<https://www.nature.com/articles/s41598-021-84342-2#MOESM1>). However, by
11 years post-eradication, seven of 13 intertidal taxonomic groups showed
significant predicted changes (Table 1
<https://www.nature.com/articles/s41598-021-84342-2#Tab1>, Fig. 3
<https://www.nature.com/articles/s41598-021-84342-2#Fig3>, Supplementary
Fig. 1 <https://www.nature.com/articles/s41598-021-84342-2#MOESM1>). Three
species (anemones, mussels, and snails) met or exceeded the expected
percent changes in abundance over time observed between islands with and
without rats. One (sponges) was within less than 10% of the expected
abundance

*Table 1 The relative abundance of intertidal organisms measured before and
after rat eradication (Mean* *±* *SE) (2008 and 2013: n* *=* *8; 2019: n*
*=* *7).*

*Full size table*
<https://www.nature.com/articles/s41598-021-84342-2/tables/1>

*Figure 3*

[image: figure3]
<https://www.nature.com/articles/s41598-021-84342-2/figures/3>

The percent change in algal, barnacle, sponge, and tunicate percent cover
and mean number per m2 of invertebrates pre- vs. post-eradication (2008 vs.
2013 and 2019) measured from intertidal photo quadrats. * indicates
significantly different data between 2008 and 2013 or 2008 and 2019,
*p* < 0.05.
The red diamonds indicate the percent change between islands with rats and
without rats from Kurle et al.12
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR12>. No red
diamond indicates an organism that was not measured in Kurle et al.12
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR12>.

*Full size image*
<https://www.nature.com/articles/s41598-021-84342-2/figures/3>

change and three (fleshy algae, limpets, and sea stars) were within 17 to
35%. The abundances of two (barnacles and tunicates) did not change as
predicted, and the remaining four taxa were not measured in Kurle et al.12
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR12> (Fig. 3
<https://www.nature.com/articles/s41598-021-84342-2#Fig3>, Supplementary
Table 1 <https://www.nature.com/articles/s41598-021-84342-2#MOESM1>), so
were not compared.

*Beach transects*

Glaucous-winged Gulls and Black Oystercatchers were significantly more
abundant post-eradication in 2013 and even more so in 2019 (Table 2
<https://www.nature.com/articles/s41598-021-84342-2#Tab2>, Fig. 3
<https://www.nature.com/articles/s41598-021-84342-2#Fig3>, Supplementary
Table 1 <https://www.nature.com/articles/s41598-021-84342-2#MOESM1>,
Supplementary Fig. 1
<https://www.nature.com/articles/s41598-021-84342-2#MOESM1>). Kurle et al.12
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR12> observed that
Black Oystercatcher and Glaucus-winged Gull abundances were greater by 984%
(0.246 ± SD 0.44 vs. 0.025 ± SD 0.04 per km of shoreline) and 1014% (17.643
± SD 60.89 vs. 1.740 ± SD 3.09 per km of shoreline), respectively, on
islands without rats, whereas we observed 900% and 291% increases in their
abundances between 2008 and 2019 (Table 2
<https://www.nature.com/articles/s41598-021-84342-2#Tab2>). In addition, we
detected 19 active Glaucous-winged Gull nests and five active Black
Oystercatcher nests post-eradication in 2019 compared to five nests and one
nest, respectively, pre-eradication in 2008.

*Table 2 The mean number km**−1* *±* *SE of Black Oystercatchers and
Glaucous-winged Gulls detected on beach transects “Pre” (2008; n* *=* *16)
and “Post” rat eradication (2013; n* *=* *16 and 2019; n* *=* *16).*

*Full size table*
<https://www.nature.com/articles/s41598-021-84342-2/tables/2>

*Discussion*

Multiple studies document significant restoration of plant and animal
species on islands following invasive animal removal5
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR5>,8
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR8>, 36
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#ref-CR36>
,37
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#ref-CR37>
,38
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#ref-CR38>
,39 <https://www.nature.com/articles/s41598-021-84342-2#ref-CR39>. In
particular, positive growth in bird abundances post-eradication is
especially well-documented31
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR31>, 40
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR40>,41
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR41>, including in
the Aleutian Islands, where bird abundances increased significantly
5–10 years after invasive fox and/or rat eradication33
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR33>, 42
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#ref-CR42>
,43
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#ref-CR43>
,44 <https://www.nature.com/articles/s41598-021-84342-2#ref-CR44>. However,
most of these studies focus on the reestablishment of individual native
vertebrate or plant species. It is more difficult to assess the long-term
responses of entire communities or ecosystems, whose recoveries are
frequently tied to the return of native species known to structure
communities via their foraging patterns and other activities (but see4
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR4>,45
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR45>).

Based on previous work by Kurle et al.12
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR12> comparing
rocky intertidal communities on islands with and without rats in the
Aleutian archipelago, we hypothesized that rat removal would eventually
return the marine rocky intertidal community on Hawadax Island to a three
trophic level system with shorebirds as apex predators, instead of a four
trophic level system with rats as apex predators, and thus change from
algae- to invertebrate-dominated (Fig. 2
<https://www.nature.com/articles/s41598-021-84342-2#Fig2>). Consistent with
this hypothesis, we found a dramatic shift in invertebrate and algal cover
dominating the rocky intertidal community on Hawadax Island after rat
eradication. Specifically, 11 years post rat eradication, we found: 1) a
significant increase in percent cover of fleshy algae, 2) significant
decreases in grazers of fleshy algae (isopods, limpets, and snails), as
well as four other invertebrate groups (anemones, mussels, seastars, and
sponges), and 3) significant increases in the shorebird predators
(Glaucous-winged Gulls and Black Oystercatchers) of these intertidal
invertebrates both five and 11 years post-rat eradication. Isopods were the
only invertebrate that showed a statistically significant decrease in
abundance five years post-rat eradication.

In rocky intertidal communities, marine birds can control abundances of
invertebrate grazers via predation46
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR46>,47
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR47>, and
intertidal invertebrate herbivores reduce algal cover through grazing
pressure48 <https://www.nature.com/articles/s41598-021-84342-2#ref-CR48>,49
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR49>, leading, in
some cases, to three level trophic cascades50
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR50>,51
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR51> such as those
observed on rat-free islands in Kurle et al.12
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR12>. We expect
other processes such as upwelling, temperature, recruitment, and currents
also influenced the rocky intertidal community structure across the
Aleutian Islands48
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR48>, 52
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR52>. However,
given the many examples of top-down control in rocky intertidal systems
(see above), coupled with the patterns Kurle et al.12
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR12> observed
across 23 islands spanning nearly the entire Aleutian Island chain, we are
confident that the likely mechanism driving the rocky intertidal community
structure on Hawadax Island is the extirpation of rats followed by the
recovery of gulls and oystercatchers as the apex predators in a three level
trophic cascade.

Abundances of gulls and oystercatchers were significantly greater in 2013
(2.3 and 5 times higher, respectively) compared with 2008, indicating
passive recovery of the shorebird populations had already begun five years
post rat-eradication. However, the intertidal data suggest this level or
time for recovery was not sufficient to restore the rocky intertidal food
web to a shorebird-mediated state more resembling that of a rat-free
island. By 2019, gull and oystercatcher abundances had further increased to
2.9 and 9 times higher, respectively, than from 2008. These bird numbers
are still lower than earlier measures from Aleutian Islands with no history
of rat or fox invasions12
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR12> (n = 89
islands, oystercatchers = 0.25 ± SD 0.44 and gulls = 17.64 ± SD 60.88 birds
per km of shoreline). However, the bird numbers between this study and
Kurle et al.12 <https://www.nature.com/articles/s41598-021-84342-2#ref-CR12>
are
not directly comparable as they derived their estimates from bird counts
conducted by personnel circumnavigating islands in small boats rather than
the land-based beach transect counts used here.

A few rocky intertidal species measured in this study did not follow the
patterns observed in Kurle et al.12
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR12> between
islands with and without rats. First, the percent cover of barnacles and
tunicates were not different over time in this study, but their abundances
were significantly less on islands without rats than on islands with rats
in Kurle et al.12
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR12>. These
exceptions may simply reflect dietary choices by gulls and oystercatchers
as they do not appear to eat tunicates, and barnacles make up only a small
percentage of their preferred intertidal prey53
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#ref-CR53>
,54
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#ref-CR54>
,55
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#ref-CR55>
,56 <https://www.nature.com/articles/s41598-021-84342-2#ref-CR56>. Kurle et
al.12 <https://www.nature.com/articles/s41598-021-84342-2#ref-CR12> surmised
that the greater area covered by invertebrates not eaten by shorebirds on
islands with rats was due to less algal cover and the resultant increased
rocky intertidal substrate space available for invertebrate colonization.
If this is the case, it may take more time for intertidal community
differences related to competition, succession, and space availability to
become measurable. In addition, the percent cover of geniculate algae in
the intertidal showed no difference between 2008 and 2019. Coralline algal
species in the North Pacific are fairly slow to colonize newly opened space
57 <https://www.nature.com/articles/s41598-021-84342-2#ref-CR57> and are
initially outcompeted by fleshy algal species and certain invertebrates58
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR58>, which could
explain why their abundances did not change over the course of this study.

Further, we found no significant differences in the abundances of sea
urchins, a known diet component for shorebirds, between pre- and
post-eradication on Hawadax Island. Urchin abundance was not assessed in
Kurle et al.12 <https://www.nature.com/articles/s41598-021-84342-2#ref-CR12>.
Urchins are difficult to accurately measure in intertidal surveys as they
are largely subtidal organisms, remaining submerged throughout a tide cycle
by following the tidal flux or via confinement to shallow tide pools59
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR59>. In addition,
around the Aleutian Islands, urchin numbers are largely regulated by sea
otter (*Enhydra lutris*) predaton. Sea otters around the Aleutian Islands
have remained in steep decline since the 1990′s, likely from predation by
killer whales (*Orcinus orca*)60
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR60>, and are thus
reduced across much of the Archipelago. Therefore, sea urchin abundances
are high in many of the subtidal zones around the Aleutian Islands,
including around Hawadax61
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR61>,62
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR62>, and likely
not controlled by bird predation.

A large marine heatwave (“The Blob”) began in the Gulf of Alaska in fall
2013, spread south to Baja California, and caused warm sea surface
temperature anomalies in the top ~ 100 m of the ocean until April 201563
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR63>. Long-term
monitoring of sites in the Gulf of Alaska (GOA) and the eastern Alaska
Peninsula (EAP) documented significant intertidal changes related to The
Blob, including decreases in sea stars, increases in mussels, and decreases
in fleshy algae64
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR64>. Coletti et
al.64 <https://www.nature.com/articles/s41598-021-84342-2#ref-CR64> related
the reduction in sea stars to Sea Star Wasting Disease (SSWD), a syndrome
causing mass mortality of sea stars from south-central Alaska to Baja
California over the last decade. Mussel densities in the GOA and EAP then
rose in response to a reduction in their sea star predators. The decreases
in fleshy algal cover in the GOA and EAP were attributed to reductions in
survival and/or recruitment of the brown algae *Fucus distichus* related to
warmer than normal temperatures65
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR65>. The range of
SSWD detected in sea stars does not include the Aleutian Islands66
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR66>, so is
unlikely a factor in the decrease in sea stars or mussels we observed. And
the trend of decreasing fleshy algal cover related to The Blob is the
opposite of the increases we observed, making it unlikely its effects
contributed to algal cover changes we observed on Hawadax.

Determining ecological community recovery following restoration is
challenging but is aided by the clear definition of a goal, a quantified
description of that state (e.g. equivalent monitoring data from
experimental or natural controls), and an understanding of other
environmental drivers that influence a restoration outcome. In addition,
while species compositions are fairly uniform within intertidal communities
across the Aleutian Islands, each island is subject to some variation in
recruitment, reproduction, competition, predation, wave-action, and other
factors influencing the densities and cover of intertidal species, further
complicating our ability to assess the degree of intertidal community
recovery 11 years after rat eradication on Hawadax Island. However,
comparisons of the percentage change over time for the densities and
percent cover values of intertidal organisms on Hawadax pre- vs.
post-eradication are similar to those observed between islands with and
without rats surveyed in 2002–2004 for Kurle et al.12
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR12> (Fig. 3
<https://www.nature.com/articles/s41598-021-84342-2#Fig3>, Supplementary
Table 1 <https://www.nature.com/articles/s41598-021-84342-2#MOESM1>),
indicating a high degree of recovery from rat impacts in the rocky
intertidal.

Across 60 + years of invasion ecology as a discipline67
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR67>,68
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR68>, research has
accumulated overwhelming evidence detailing the loss of biodiversity and
other threats to native species and ecosystems posed by non-native invaders
69 <https://www.nature.com/articles/s41598-021-84342-2#ref-CR69>,
especially on islands3
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR3>. When
mammalian invaders are removed from islands, conservation success, if
measured at all, is generally tracked by how well populations of native
(and largely terrestrial) species rebound8
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR8>. However, less
understood or even studied, are recoveries of entire communities,
particularly nearshore marine systems, and the biological parameters a
community must attain for it to be considered recovered (but see21
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR21>,70
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR70>). Community
recovery is especially difficult to quantify as communities are host to a
myriad of biological interactions, and invasive species can insert
themselves into those interactions, shaping community structure in
unexpected ways via direct and indirect mechanisms29
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR29>,45
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR45>. Finally, the
time required for community recovery after invasive species eradication is
uncertain, as is the variability of recovery for different components of
the system, requiring a long-term commitment to extensive monitoring.

Here, we move beyond demonstrating increases in native bird abundances
after removal of invasive rats, a finding repeatedly shown across multiple
studies detailing direct effects of rat eradication on native island
species. Our long-term intertidal monitoring data show the changes in
densities of rocky intertidal invertebrates and the percentage of
intertidal area covered by fleshy algae and aggregating invertebrates after
rats were removed from Hawadax Island largely followed the same patterns
observed between rat-infested and rat-free islands surveyed in Kurle et al.
12 <https://www.nature.com/articles/s41598-021-84342-2#ref-CR12> indicating
a high degree of passive recovery was achieved in a relatively short
11 years. With invasive rats removed, shorebirds have resumed their role as
top predator, indirectly shaping the rocky intertidal community (Fig. 2
<https://www.nature.com/articles/s41598-021-84342-2#Fig2>B; see12
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR12>).

More studies focused on understanding and measuring both direct and
indirect impacts of invaders, and how communities respond following removal
of those impacts, are needed to underscore the widespread conservation
successes associated with invasive species eradication, especially on
islands. In addition, our data demonstrate that continued eradication of
introduced rats from other infested islands in the Aleutian Chain would add
to increased bird and rocky intertidal community recoveries within the
Alaska Maritime National Wildlife Refuge, thereby contributing to the
Refuge’s mission of restoration and protection of natural biodiversity on
refuge lands.

*Methods*

Hawadax Island (51.80° N, 178.30° E), part of the Alaska Maritime National
Wildlife Refuge, is located within the Rat Islands group of the western
Aleutian Islands (Fig. 2
<https://www.nature.com/articles/s41598-021-84342-2#Fig2>). The 2,780 ha
(6,869 acres) island has steep cliffs along most of the coastline backed by
rolling hills and plateaus rising to a small ridge of mountains with a peak
elevation of 400 m. There are more than 30 offshore rock stacks and several
islets. The largest islet is approximately 4 ha (10 acres) in size and is
located 1.7 km off the southeast end of the island (Ayugadak Point).
Hawadax Island is a designated Wilderness and has no inhabitants or human
facilities.

Rats were introduced to different Aleutian Islands at different times.
However, while one island (Little Kiska) became infested in 1990, the rest
received rats before 1940 and as early as the 1700′s42
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR42>. Thus, rat
effects would currently be largely uniform across islands.

During September and October 2008, the U.S. Fish and Wildlife Service
partnered with The Nature Conservancy and Island Conservation to restore
seabird breeding habitat on Hawadax Island by removing introduced Norway
rats using aerially applied cereal-based bait containing brodifacoum32
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR32>. This was the
first aerial rat eradication program conducted in Alaska32
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR32>. Monitoring
teams conducted biological surveys from June 1–20, 2008 (pre-eradication),
and May 31–June 10, 2013 and June 1–16, 2019 (post-eradication), to
coincide with early seasonal breeding activity for most native island bird
species.

The protocols used in this study were approved by the Institutional Animal
Care and Use Committee (IACUC) of the University of California, Santa Cruz
(protocols Crold1004 and Crold1303). The research was performed in strict
accordance with the guidelines and regulations in these protocols.
Observers did not engage in any contact with the animals while recording
their natural behavior and no biological samples were collected.

*Intertidal community*

*Photo plots*

We conducted surveys to describe the community structure of intertidal
flora and fauna. We used methods similar to those developed by Kurle71
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR71>, who
previously conducted studies to document the impacts of Norway rats on
marine bird densities and rocky intertidal communities in the Aleutian
Islands, including Hawadax Island. In 2008 and 2013, we conducted surveys
on eight beaches: five on the north side of the island, and three on the
south side. In 2019, we revisited seven of the original eight beaches; due
to time constraints, we were unable to survey Beach 6 on the south side of
the island (Fig. 2 <https://www.nature.com/articles/s41598-021-84342-2#Fig2>
).

At each beach, we conducted two transects in both the low and mid
intertidal zones. The lower intertidal zones were dominated by algae from
the genera *Alaria* and *Laminaria*, whereas the mid zones were dominated
by algae from the genera *Fucus* and *Halosaccion*. For each 30 m transect,
we took digital photos of seven, 365 cm2 quadrats, located at 5 m
intervals. We took two photos every quadrat: the first of the surface
coverage, and a second photo after the overlying algal layer was removed to
reveal the understory community (Fig. 4
<https://www.nature.com/articles/s41598-021-84342-2#Fig4>).

*Figure 4*

[image: figure4]
<https://www.nature.com/articles/s41598-021-84342-2/figures/4>

Example of digital photos of intertidal quadrats. A digital photo was taken
first of the surface coverage of the plot (*A*). A second photo of the
exact plot (*B*) was taken after the algal layer was removed to reveal the
under-story community. Photos by J. Curl.

*Full size image*
<https://www.nature.com/articles/s41598-021-84342-2/figures/4>

Seasonal, logistic, financial, and low-tide constraints all limited our
field time, precluding lengthy field identification of invertebrates to
species. Our major goal with this limited field time was to get clear and
accurate photos of our study plots to best replicate the earlier study of
Kurle et al.12 <https://www.nature.com/articles/s41598-021-84342-2#ref-CR12>.
As a result, we were not able to confidently identify our metrics to
species, but instead relied upon the broader taxonomic categorization.
While potentially interesting to have more taxonomic detail, the
conclusions in our manuscript based upon the broad taxonomic categories
are, we feel, robust.

We analyzed 2008 and 2013 intertidal photos using Adobe Photoshop 6.0. We
used Adobe Photoshop Elements 2019 to analyze all digital photos taken in
2019. We followed the same data analysis protocols in 2008, 2013, and 2019.
For all years, on each photo, we overlaid a digital 6 × 9 rectangular grid
and calculated percent cover as the ratio of the number of each species
lying below an intersection of the gridline to the total number of
intersections within each grid. We calculated percent cover of sessile
organisms (barnacles, sponges, and tunicates). We estimated the percent
cover of larger algae (coralline algae and all fleshy algal species) by
counting the percent cover of stipes that remained after the removal of the
algal blades. We counted the number of individual mobile invertebrates
(anemones, snails, limpets, mussels, urchins, and sea stars) in each photo
to estimate density. We pooled data by beach for statistical analyses and
compared the mean percent cover and mean number of individuals per m2 pre-
(2008) and post- (2013 and 2019) eradication using t-tests (α = 0.05).

*Beach transects*

Shorebirds, such as Black Oystercatchers and Glaucous-winged Gulls, are
important predators of intertidal organisms53
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#ref-CR53>
,54
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#ref-CR54>
,55
<https://www.nature.com/articles/s41598-021-84342-2?utm_source=Nature+Briefing&utm_campaign=cb18b1c8d3-briefing-dy-20210525&utm_medium=email&utm_term=0_c9dfd39373-cb18b1c8d3-45511414#ref-CR55>
,56 <https://www.nature.com/articles/s41598-021-84342-2#ref-CR56>. To
assess their relative abundance, we conducted beach surveys along the
entire length of all accessible beaches (n = 16; Fig. 2
<https://www.nature.com/articles/s41598-021-84342-2#Fig2>) on Hawadax
Island. Detailed methods are presented in Croll et al.33
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR33> and are
briefly summarized here. An observer slowly walked along each beach
transect during morning hours whenever possible (0700–1100), counting all
birds seen or heard between the water’s edge and 50 m inland from the storm
tide line. For each species, observers recorded aural and visual detections
separately. Observers recorded the time and GPS location at the start and
end of each transect. We measured the length of each transect following the
contour of the beach between waypoints using ArcGIS 10.772
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR72>. We conducted
four to five replicate surveys of each of the 16 beach transects to
minimize effects of variation in time and sampling conditions. We
calculated the relative abundances for Black Oystercatchers and
Glaucous-winged Gulls by dividing the total count of birds detected per
beach transect by the length of the transect (birds km−1). We then averaged
the five replicate surveys for each beach and used the averaged counts for
each beach each year as a sample. We then compared pre- (2008) and
post-eradication (2013, 2019) results using nonparametric Van der Waerden
tests, *α* = 0.05.

*Assessing status of rocky intertidal community recovery*

An island community may be considered recovered if the components are not
significantly different from an unperturbed reference island73
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR73>. To assess
the degree to which the rocky intertidal on Hawadax Island may have
recovered following rat eradication, we compared the percentage change over
time for abundances and percent cover values of intertidal organisms and
shorebirds on Hawadax Island pre- vs. post-rat eradication to those
observed between islands with and without rats surveyed for Kurle et al.12
<https://www.nature.com/articles/s41598-021-84342-2#ref-CR12>.



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