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We thank the following collaborators for providing purified proteins
and antibodies: R. Jahn, C. Griesinger, B. Shwaller, and A. Roux. We
thank H. Martens for technical help and support, B. Rizzoli
for helpful comments on the manuscript, and T. Sargeant for
providing the carve source code for creation of the voltage-
dependent anion channel (VDAC)-based mitochondrial membrane
cut-outs. B.G. W. was supported by a Boehringer Ingelheim Fonds
PhD Fellowship. S. T. was supported by an Excellence Stipend of
the Göttingen Graduate School for Neurosciences, Biophysics, and
Molecular Biosciences (GGNB). The work was supported by grants
to S.O.R. from the European Research Council (FP7 NANOMAP and
ERC-2013-CoG NeuroMolAnatomy) and from the Deutsche
Forschungsgemeinschaft (DFG) Cluster of Excellence Nanoscale
Microscopy and Molecular Physiology of the Brain, as well as from
DFG grants RI 1967 2/1, RI 1967 3/1, and SFB 889/A5. We
acknowledge support by the DFG to V.H. (Exc-257-Neurocure and
SFB 958/A01), H.U. (SFB 889), and M.K. (SFB 958/A11). Author
contributions: B.G. W. prepared the synaptosomes and performed
all immunoblotting experiments. K.K. performed the electron
microscopy imaging and all neuromuscular junction imaging. C.S.
performed the hippocampal culture imaging. S. T. performed the
synaptosome imaging. B.R. generated the synapse model. S.J.K.,
G.A.C., and M.K. participated in the biochemistry experiments. S.M.
and H.U. designed and performed all mass spectrometry
experiments. S.O.R., B.G. W., and V.H. designed the experiments.
All authors analyzed the data and contributed to writing
Materials and Methods
Figs. S1 to S7
Tables S1 to S3
3 March 2014; accepted 6 May 2014
Optimal approaches for balancing
invasive species eradication and
endangered species management
Adam Lampert,1 Alan Hastings,1 Edwin D. Grosholz,1 Sunny L. Jardine,2 James N. Sanchirico1,3
Resolving conflicting ecosystem management goals—such as maintaining fisheries while
conserving marine species or harvesting timber while preserving habitat—is a widely
recognized challenge. Even more challenging may be conflicts between two conservation
goals that are typically considered complementary. Here, we model a case where
eradication of an invasive plant, hybrid Spartina, threatens the recovery of an endangered
bird that uses Spartina for nesting. Achieving both goals requires restoration of native
Spartina. We show that the optimal management entails less intensive treatment over
longer time scales to fit with the time scale of natural processes. In contrast, both
eradication and restoration, when considered separately, would optimally proceed as
fast as possible. Thus, managers should simultaneously consider multiple, potentially
conflicting goals, which may require flexibility in the timing of expenditures.
Ecosystem-based management recognizes that managing individual species does not account for trade-offs and interactions with natural and human communities (1, 2). Yet, the development of this approach has been
limited by an absence of attempts to address con-
flicting goals and interactions. Conflicting goals
may occur when two or more species or entities
are being manipulated, such as when harvest of
commercial fishes threatens endangered marine
species via by-catch (3–7), when timber harvest
destroys habitats of endangered wildlife species
(8, 9), and when supplying water at a high quan-
tity reduces water quality at the source reservoir
(10). Here, we focus on a particularly instructive
example, where eradication of an invasive spe-
cies (11–13) threatens the recovery of an endan-
gered species (14–16). By modeling this case study,
Species of cordgrass in the genus Spartina
have invaded many salt marshes around the
world, which has resulted in changes to physical,
biogeochemical, and biological processes that sup-
port benthic food webs and ecosystem produc-
tivity (17, 18). Spartina invasions have also had
an impact on human economies by altering shore-
line geomorphology, affecting aquaculture, and
reducing property values (19). Consequently, ef-
forts to eradicate invasive Spartina have occurred
worldwide (19). In San Francisco Bay, California,
S. alterniflora was introduced from the eastern
United States in the mid-1970s (20). It then hybrid-
ized with native S. foliosa and ultimately invaded
~800 acres (21) (Fig. 1A). Eradication of hybrid
invasive Spartina began in 2005 and, to date,
~92% has been removed (Fig. 1B) (22). However,
native Spartina has been slow to recover after
eradication of the invader.
During the invasive Spartina eradication period, between 2005 and 2011, populations of the
federally endangered California clapper rail (Rallus
longirostris obsoletus) in San Francisco Bay declined by nearly 50% (23), presumably because of
the overall decline in cover of Spartina in which
clapper rail nests and forages. Thus, the U.S. Fish
and Wildlife Service prohibited further eradication of invasive Spartina in the remaining untreated infested areas, which cover ~8% of the
originally infested area. To allow completion of
invasive Spartina eradication within the areas
currently off limits without further losses of clapper rail habitat, restoration of native Spartina
using nursery plants began in 2012.
To determine whether restoring native Spartina
is cost-effective, and if so, how to best allocate
efforts and a budget over time to combine native Spartina restoration with invasive Spartina
eradication, we developed a theoretical model of
Spartina management and estimated parameters
for the model based on field data that was
collected over several years (Fig. 2) (24). In addition to the distinction between native and invasive Spartina, we used a density-structured model
(25) and further distinguished between two types
of each Spartina species, “isolates” and “meadows.”
For invasive Spartina, isolates include individual
plants that remain after treatment and new seedlings produced by remaining plants, whereas
meadows are dense mature stands of untreated
invasive Spartina that cover large areas. For native
Spartina, isolates include naturally produced seedlings and restored individual plants, whereas meadows are dense mature stands covering larger areas.
This distinction is important because clapper rails
prefer larger meadows and are less willing to use
individual plants as their habitat (21). Therefore,
constraining the total amount of meadows (of either
invasive or native Spartina) to remain above a certain
limit is a plausible approach to promote the recovery
of clapper rail while still allowing cost-effective
management planning for the eradication program.
1University of California, Davis, One Shield Avenue, Davis, CA
95616, USA. 2University of Delaware, Newark, DE 19716, USA.
3Resources for the Future, Washington, DC 20036, USA.
*Corresponding author. E-mail: firstname.lastname@example.org