Aquatic Botany 89 (2008) 297–302
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Aquatic Botany
journal homepage: www.elsevier.com/locate/aquabot
The potential role of climate in the distribution and zonation of
the introduced seagrass Zostera japonica in North America
Deborah J. Shafer a,*, Sandy Wyllie-Echeverria b, Timothy D. Sherman c
a
Engineer Research and Development Center, 3909 Halls Ferry Road, Vicksburg, MS 39180, USA
University of Washington, Friday Harbor Laboratories, 620 University Road, Friday Harbor, WA 98250, USA
c
University of South Alabama, Department of Biological Sciences, Life Sciences Building, Room 124, Mobile, AL 36688, USA
b
A R T I C L E I N F O
A B S T R A C T
Article history:
Received 6 November 2006
Received in revised form 20 February 2008
Accepted 7 March 2008
Available online 14 March 2008
The current distribution of the introduced seagrass Zostera japonica is restricted to the mid- to upper
intertidal zone in the coastal Pacific Northwest region of North America. The climate in this region is cool
and wet, becoming hotter and dryer with increasing distance southward. Since temperature is likely to be
an important factor affecting distribution of this species, growth of two populations located near the
northern and southern limits of its established range along the Pacific Coast of North America were
measured in an experimental setting across a range of temperatures typical of those in the field during
the growing season (10, 20, and 30 8C). The effects of temperature and population were both significant.
Leaf elongation, growth, and areal productivity rates of the northern population were consistently lower
than those of the southern population. Across the range of temperatures, mean leaf elongation rates
ranged from 0.47 to 1.40 cm2 shoot1 d1; mean growth rates ranged from 0.19 to
0.52 mg dry wt shoot1 d1. Mean areal productivity ranged from 0.54 to 1.92 g dry wt m2 d1.
Maximum rates of leaf elongation, growth, and areal productivity for both populations were observed
at 20 8C. However, leaf elongation, growth, and areal productivity of the northern population declined
markedly at 30 8C, whereas no comparable declines were observed for the southern population. This
suggests that Z. japonica populations near the southern limits of its established range may be better
adapted to warmer temperatures than populations near the northern range limits and further range
extensions southward along the California coast may be likely. These differences could be important in
predicting the outcome of competitive interactions between native and introduced seagrass species, and
in determining future patterns of distribution and zonation of Pacific Coast seagrasses.
ß 2008 Elsevier B.V. All rights reserved.
Keywords:
Zostera japonica
Temperature
Growth
Distribution
Exotic species
Climate change
1. Introduction
The presence of the non-indigenous seagrass Zostera japonica
Asch. & Graebn. in North America was first documented in 1957
(Hitchcock et al., 1969), although it is likely to have been
introduced decades earlier. For more than 50 years, distribution
of this species was limited to southern Oregon and Washington,
United States, and southern British Columbia, Canada (Fig. 1).
Within this range, dramatic expansions have occurred in some
areas (Posey, 1988; Baldwin and Lovvorn, 1994; Dumbauld and
Wyllie-Echeverria, 2003). However, the recent discovery of a small
population in Humboldt Bay near Eureka, California (Fig. 1),
represents a southerly extension of the range. Harrison and Bigley
(1982) suggested that this species had only colonized a small
* Corresponding author. Tel.: +1 601 634 3650; fax: +1 601 634 3205.
E-mail address: Shaferd@wes.army.mil (D.J. Shafer).
0304-3770/$ – see front matter ß 2008 Elsevier B.V. All rights reserved.
doi:10.1016/j.aquabot.2008.03.005
fraction of the available suitable habitat, and that dramatic
changes in the ecology of the intertidal flats were likely to result
from continued spread of this species throughout its potential
range. Concerns have been expressed regarding the potential for
displacement of the native eelgrass, Zostera marina, by Z. japonica,
and the impacts of this displacement on ecosystem structure and
function (Bando, 2006). In the case of Z. japonica, management
decisions are complicated by the shortage of information available
for this species either in its native range or on the Pacific Coast of
North America (Green and Short, 2003).
This study is one of the first to investigate the potential role of
climate and temperature in the distribution of an introduced
marine plant. Poleward expansion of species is generally thought
to be limited by the effects of freezing on cellular structures
(Woodward, 1987). The predominantly annual life history and
high frequency and intensity of reproductive effort characteristic
of Z. japonica populations in the extreme northern limits of its
established range along the Pacific Coast (Harrison, 1979) may be
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D.J. Shafer et al. / Aquatic Botany 89 (2008) 297–302
Fig. 1. Distribution of the introduced seagrass Z. japonica along the Pacific Coast of
North America.
indicative of low temperature stress (Keddy and Patriquin, 1978;
Phillips and Backman, 1983; Phillips et al., 1983); therefore further
range extensions towards the north may be limited. Climatic
controls exerted on population expansion in a southerly direction
are less clear (Woodward, 1987).
There are strong correlations between plant physiognomy and
two particular aspects of climate, e.g. temperature and water
availability (Woodward, 1987). Although aquatic plants are not
subject to the same limitations on water supply as terrestrial
plants, intertidal seagrasses can become desiccated when exposed
to air and sunlight during low tide. Along the Pacific Coast of North
America, the area from southern British Columbia, Canada to
Humboldt Bay in northwestern California is known as the Pacific
Northwest region (Fig. 1) (Phillips, 1984). This area also defines the
current limits of distribution for Z. japonica (Fig. 1). In general, the
climate in this region is cool and wet, becoming progressively
hotter and dryer southward along the California Coast (Emmett
et al., 2000; Fig. 2). Average summer high temperatures in San
Diego, California are about 25 8C, while in Newport, Oregon,
summer high temperatures are only around 15 8C (Fig. 2).
The relationship between temperature and seagrass distribution patterns on a latitudinal scale was shown by McMillan (1979,
1984). The relatively narrow geographic range of Z. japonica along
the Pacific Coast of North America suggests there may be a
physiological basis for its distribution. Temperature is known to
exert a profound effect on rates of photosynthesis and growth in
seagrasses (Marsh et al., 1986; Bulthuis, 1987; Masini et al., 1995).
Lee et al. (2005) reported that growth of Z. japonica is regulated by
water temperature, and it has been suggested that distribution of Z.
japonica in the western Pacific is limited by high summer water
temperatures (Aioi and Nakaoka, 2003). However, the temperature
responses of this species have not been investigated.
The objectives of this study were to describe the range of
temperatures typical of Pacific Northwest intertidal Z. japonica
meadows during the growing season, and compare the growth
responses of two Z. japonica populations located near the northern
and southern limits of its established range in North America, across
Fig. 2. Monthly mean maximum air temperature (A), minimum air temperature (B),
and rainfall (C) at five selected sites along the Pacific Coast of North America (site
locations shown in Fig. 1).
the range of temperatures experienced by plants in situ during the
growing season. Since populations near the limits of their range may
exhibit different temperature tolerances (McMillan, 1979), experiments conducted at the boundaries of species’ distribution are
critical to understanding factors limiting the spread of introduced
species (Byers et al., 2002). The results of this study can be used to
predict the potential for further range extensions of this species
towards the south along the Pacific Coast of North America.
2. Methods
2.1. In situ temperature
In situ temperature data were collected in Padilla Bay,
Washington, in order to characterize the range of temperatures
typical of northern Z. japonica populations during the growing
season. Small temperature sensors (Vemco Mini-Log TDR and HOBO
Water Temp PRO) were attached to PVC stakes in mid- to upper
intertidal Z. japonica meadows. The instruments were set to record
D.J. Shafer et al. / Aquatic Botany 89 (2008) 297–302
temperature every 15 min over a period of several weeks in order to
capture the full range of tidal and weather conditions. Because the
plants are alternately submerged at high tide and exposed to air at
low tide on a daily basis, the data represent the full range of
temperatures experienced by the leaves of intertidal plants in situ
(in air during the daylight low tides, and in water during high tides).
Annual variability of in situ temperature for a southern population of
Z. japonica in Yaquina Bay, Oregon is described in Kaldy (2006). These
data provide a basis for subsequent laboratory experiments that
examined the effects of temperature on growth.
2.2. Effects of temperature on growth and production
Two populations of Z. japonica, located in Padilla Bay, Washington (488340 latitude, 1228320 longitude) and Yaquina Bay, Oregon
(448380 latitude, 1248030 longitude), located near the northern and
southern limits of its established range in the eastern Pacific,
respectively, were compared. For each population, three parameters,
leaf elongation (cm2 shoot1 d1), growth (mg dry wt shoot1 d1),
and areal productivity (g dry wt m2 d1), were evaluated.
The leaf-clipping method (Kaldy, 2006) was used in an
experimental setting to compare the effects of temperature on
growth and production within and between populations. Using a
PVC corer 7.6 cm in diameter, plugs containing intact plants with
root material and associated sediments were harvested at low tide
from intertidal beds of Z. japonica. Thirty plugs were harvested
from Padilla Bay, Washington, transported to the laboratory
facility at Newport, Oregon, and placed in prepared 95 L aquaria
within 8 h of collection. An additional 30 plugs were collected from
Yaquina Bay, Oregon and placed in aquaria within 1 h of collection.
The shoot density of each core was recorded and used to calculate a
mean shoot density for each population. Plants were allowed to
acclimate at ambient temperature (22 8C) for 24–48 h prior to the
beginning of the experiment.
Growth rates were measured under controlled temperature
conditions using a completely randomized split-plot experimental
design. Four replicate 95 L aquaria were used in each of three
temperature treatments (10, 20, and 30 8C). Ten samples from each
location were exposed to each of the three temperature
treatments. Within each temperature treatment, individual
samples were randomly assigned to one of the four replicate
aquaria. The aquaria were supplied with flow-through filtered
seawater with an average temperature of 10 8C and a salinity of
35 psu. Submersible aquarium heaters were used to maintain
appropriate temperatures (1 8C) in the 20 and 30 8C treatments.
Metal halide lights (1000 W; Sunlight Supply, Inc.) above each set of
four aquaria supplied illumination at an average irradiance of
400 mmol m2 s1 at the water surface for a period of 12 h each day.
At the beginning of the experiment, all plants were clipped just
above the top of the leaf sheath and temperatures adjusted to the
appropriate level for each treatment. Re-growth was monitored for
a period of 14 d. During this period, accumulations of epiphytes
were gently wiped from the leaves on a daily basis, as needed.
At the end of the growth period, the number of shoots in each
core was counted; samples were clipped again at the same point
and tissue collected for further analysis. The length and width of
each leaf was measured to the nearest mm and recorded. The
lengths of all leaves in each core were summed and divided by the
number of shoots per core to estimate leaf elongation rates
(cm2 shoot1 d1). Samples were dried at 65 8C for 48 h to obtain
dry wt biomass measurements. Growth rates were calculated by
dividing the total biomass per core by the number of shoots per
core (mg dry wt shoot1 d1). These growth rates were used along
with estimates of mean shoot density for each population to
express production on an areal basis (g dry wt m2 d1).
299
3. Data analysis
The data failed to meet the assumption of homogeneity of
variances required for standard Analysis of Variance (ANOVA)
techniques, due to the positive relationship between increasing
temperature and sample variance. A number of transformations
were applied, but all failed to successfully stabilize the group
variances. Therefore, the final analysis was conducted using a
weighted nested factorial ANOVA design, in which the reciprocals
of the within-group sample variances were used as weighting
factors (Freund and Wilson, 1993); a group was defined as each
Temperature Population combination. The ANOVA model was
constructed with Temperature and Population as the main effects.
Aquaria and Aquaria Population were both included in the
model as nested effects within Temperature to estimate the
proportion of the variance attributable to individual aquaria
effects. A series of five orthogonal linear and quadratic contrasts
were used to compare differences between groups. Significance
was interpreted as a 0.05. Values between 0.05 and 0.10 are
reported as marginally significant.
4. Results
4.1. In situ temperature
In situ temperatures in intertidal Pacific Northwest Z. japonica
meadows are controlled by daily tidal cycles (Fig. 3). In late spring
and summer, low tides occur during the day, and plants are
exposed to extremely variable temperatures on a daily basis,
ranging from near 10 8C when submerged, to more than 30 8C
when exposed to air for several hours on a sunny day (Fig. 3). This
daily range of temperature during the summer growing season
formed the basis of subsequent laboratory experiments that
compared growth of the two populations at 10, 20, and 30 8C.
4.2. The effects of temperature on growth and production
Both temperature and population, the main effects in the
weighted nested ANOVA model, were significant for all three
response variables (i.e. leaf elongation, growth, and areal production rates) (Table 1). Due to a lack of significant interaction effects,
conclusions regarding differences in populations also hold for each
temperature treatment. Additional support for these results is
Fig. 3. Variation in daily in situ temperatures and tidal elevation during the growing
season in a northern population of Z. japonica in Padilla Bay, Washington.
D.J. Shafer et al. / Aquatic Botany 89 (2008) 297–302
300
Table 1
Results of the nested ANOVA comparing leaf elongation, growth, and production rates between populations across temperatures
Source
d.f.
Leaf elongation (cm2 shoot1 d1)
Growth (mg dw shoot1 d1)
Areal production (g dw m2 d1)
Temperature
Aquarium [temperature]
Population
Temperature Population
Aquarium Population [temperature]
2
9
1
2
9
p < 0.0001
p = 0.0920
p = 0.0004
p = 0.3665
p = 0.5342
p < 0.0001
p = 0.1263
p = 0.0217
p = 0.3453
p = 0.3706
p = 0.0028
p = 0.1832
p < 0.0001
p = 0.0752
p = 0.5364
Table 2
Results of orthogonal linear contrasts between populations across temperature and non-linear contrasts within populations
Leaf elongation (cm2 shoot1 d1)
Growth (mg dw shoot1 d1)
Areal production (g dw m2 d1)
Linear contrasts between populations across temperature
Padilla vs. Yaquina @ 10 8C
p < 0.0001
Padilla vs. Yaquina @ 20 8C
p = 0.021
Padilla vs. Yaquina @ 30 8C
p = 0.031
p = 0.0024
p = 0.6337
p = 0.0576
p = 0.0013
p = 0.0067
p = 0.0009
Non-linear (Quadratic) contrasts within populations
Padilla Bay
p < 0.0001
Yaquina Bay
p = 0.0148
p = 0.0001
p = 0.3288
p = 0.0002
p = 0.0557
Contrast
provided by the linear contrasts comparing populations at each of
the three temperatures (Table 2).
Across the range of temperatures, mean leaf elongation rates
ranged from 0.47 to 1.40 cm2 shoot1 d1. Leaf elongation rates of
the northern population, Padilla Bay, were 23–40% lower than
those of the southern population, Yaquina Bay. Differences
between populations were significant at all three temperatures
(Table 2). Within each population, leaf elongation rates at 20 8C
were roughly double those observed at 10 8C. Leaf elongation rates
of both populations declined at 30 8C, as indicated by the quadratic
contrast, although this trend was more pronounced in the Padilla
Bay population (Table 2).
Mean growth rates ranged from 0.19 to 0.52 mg dry
wt shoot1 d1. Growth rates exhibited a slightly different pattern
across the range of temperatures than leaf elongation rates.
Growth rates of the northern population were significantly lower
than the southern population at 10 8C. At 20 8C, no significant
differences between populations could be detected. At 30 8C,
differences in growth were marginally significant (Table 2). Unlike
the northern Padilla Bay population, there was no apparent decline
in growth of the Yaquina Bay population at 30 8C (Fig. 4).
Patterns in areal productivity across the range of temperatures
were similar to those of leaf elongation (Fig. 4C and A). Mean areal
productivity ranged from 0.54 to 1.92 g dry wt m2 d1. Significant
differences between populations were noted at all three temperatures (Table 2). Although productivity of both populations was
generally lower at 30 8C, this trend was only significant for the
Padilla Bay population.
Although there are similarities in the temperature responses of
both populations, at higher temperatures, differences became
more apparent. Both populations exhibited low rates of growth at
10 8C. Maximum rates for both populations were observed at 20 8C.
However, leaf elongation, growth, and areal productivity of the
northern Padilla Bay population declined markedly at 30 8C,
whereas no comparable declines were observed for the Yaquina
Bay population (Fig. 4).
5. Discussion
In situ temperatures recorded in Padilla Bay, Washington were
similar to those reported from field studies in Yaquina Bay, Oregon
(Kaldy, 2006), therefore we are reasonably confident that
experimental treatment values correspond to the range of
temperatures plants would experience in situ. Although other
environmental conditions (e.g. continual submergence and fixed
irradiance) are most likely different than plants would have
experienced during the 14 d period of the experiment, leaf
elongation and maximum growth rates reported here are similar
to the range of values reported from the field evaluation of Z.
japonica shoots in Yaquina Bay (Kaldy, 2006) and in Korea (Lee
et al., 2005, 2006), which further supports our confidence that
these results can inform assumptions regarding the response of Z.
japonica leaf growth, from both sites, to temperature variation.
Experiments designed to evaluate the response of exotic species
to environmental conditions found at the boundaries of the
invaded territory are critical to understand factors that may limit
or augment spread (Byers et al., 2002). Moreover, Mau-Crimmins
et al. (2006) demonstrate that models constructed to predict
expansion of exotic species are more accurate if parameterized
with data collected from within the invaded range. This may be
especially true during periods of dynamic environmental change as
studies in terrestrial systems demonstrate that the distribution
and dispersal patterns of exotic plants can be affected by altered
climate regimes (Sasek and Strain, 1990; Walther, 2000).
An important finding of our study involves the apparent
differences in temperature tolerances between populations near
the established range limits of Z. japonica in North America. It has
been suggested that high summer water temperatures limit Z.
japonica distribution in its native range (Aioi and Nakaoka, 2003).
The results of this study indicate that Z. japonica from northern and
southern sites in North America exhibit different temperature
tolerances. While plants from the northern site are stressed at
temperatures of 30 8C, those from the south appear to be better
adapted to warmer temperatures. This adaptation could lead to
further expansion of Z. japonica along the California coast. The
invasion rate of Z. japonica, defined as ‘the mean rate of linear
expansion of an advancing colonization front in kilometers per
year’, has been estimated at 6 km yr1 (Kinlan and Gaines, 2003;
Shanks et al., 2003). However, it is possible that differences in
climate along the Pacific Coast could alter this rate of advance.
Just beyond the current southern limit of Z. japonica distribution, there is an abrupt climate transition from the cool, moist
climate conditions of the Pacific Northwest, to the hotter, dryer
climate conditions prevalent along the California Coast. While the
relatively cool and damp climate of the Pacific Northwest region
ameliorates the effects of temperature and desiccation to some
D.J. Shafer et al. / Aquatic Botany 89 (2008) 297–302
Fig. 4. Comparison of laboratory leaf elongation (A), growth (B), and areal
production (C) rates of Z. japonica populations in Padilla Bay, Washington, and
Yaquina Bay, Oregon across a range of temperatures (error bars represent least
squares means standard errors (S.E.)).
extent, expansion southward along the California Coast will expose
plants to progressively hotter and dryer conditions. Because of the
position of Z. japonica within the upper intertidal zone, exposure to
high air temperatures during daylight low tides coincides with
increased potential for desiccation. Since air and water temperature also limit the upper distribution limits of seagrass meadows
(Campbell et al., 2006), this difference in climate could render the
upper intertidal environment unsuitable for Z. japonica survival
along the southern Pacific Coast, possibly resulting in a shift in
species zonation into lower intertidal zones. Therefore, climate
may affect zonation patterns as well as the distribution of this
species on a latitudinal scale.
If the zonation of Z. japonica is shifted lower in the intertidal and
shallow subtidal zones as populations expand southward, this
scenario could lead to increasing overlap and competition with the
301
native eelgrass, Z. marina. In the Pacific Northwest, Z. japonica often
co-occurs with Z. marina, although these two species usually occupy
different niches within the intertidal and upper subtidal zones. Z.
marina occupies the lower intertidal to upper subtidal zones, and Z.
japonica typically occupies the mid- to upper intertidal zone
(Phillips, 1984; Thom, 1990; Bulthuis, 1995). Competitive interactions with Z. marina play a role in determining the boundary
between the lower limit of Z. japonica and the upper limit of Z. marina
where both species co-exist. Above-ground biomass and density of
either species may be reduced in the presence of the other (Harrison,
1982; Hahn, 2003; Bando, 2006). However, Z. japonica remains
limited to the upper and mid-intertidal zones even in the absence of
Z. marina at its lower boundary, suggesting that it is not interspecific
competition that controls the lower limit of Z. japonica zonation. The
mid- to upper intertidal zonation of Z. japonica cannot be explained
by a higher desiccation tolerance, as we have shown that Z. japonica
is physiologically more sensitive to desiccation than Z. marina
(Shafer et al., 2007). Our preliminary data (unpublished) also suggest
that photosynthetic efficiency is similar in both species; therefore
light limitation is unlikely to control the lower limits of Z. japonica
zonation.
Since zonation patterns cannot be explained by interspecific
competition, differences in desiccation tolerances, or light
requirements, differences in their thermal optima may be
responsible for the observed zonation patterns of these two
species in the intertidal and shallow subtidal zones. The
temperature optima of 20 8C for Z. japonica observed in this study
is within the range of 18–23 8C reported by Lee et al. (2005) in
Korea. In contrast, the optimum temperature for the native Z.
marina in the Pacific Northwest ranges between 7.5 and 12.5 8C
(Phillips, 1972), and may be as low as 5–8 8C (Thom et al., 2001).
Above 15 8C, the productivity to respiration ratio of Z. marina
becomes very low, suggesting thermal stress (Biebel and McRoy,
1971; Thom et al., 2001). Since optimum growth of Z. japonica
occurs at temperatures that cause stress to Z. marina, and Z.
japonica grows very slowly at the low temperatures where Z.
marina thrives, differences in temperature optima may be
responsible in part for the zonation patterns of these two species
in the Pacific Northwest. Additional support for this hypothesis is
provided by Harrison (1982), who noted that Z. marina was able to
out-compete Z. japonica because it grew much more rapidly, and
the shading produced by its larger leaves and canopy resulted in
decreased density of Z. japonica. Therefore, as populations of Z.
japonica continue to expand southward along the California coast,
zonation patterns are likely to be affected by two factors: (1) the
upper boundary may be shifted lower in the intertidal zone by
increased desiccation associated with hotter and drier climate
conditions, and (2) cold water temperatures and interspecific
competition may limit expansion of the lower boundary into the
lower intertidal and shallow subtidal zones.
Results of this study also have important implications for
predicting the response of seagrass species to large-scale climatic
changes such as those associated with El Niño/La Niña events or
global warming. Analysis of long-term northeast Pacific climate
trends indicates that periods of relatively stable climate conditions, which may last decades, can be followed by abrupt
transitions to a different set of stable conditions. These changes,
known as regime shifts, are linked to the behavior of the Eastern
Pacific Boundary Current system (Swartzman and Hickey, 2003).
Regime shifts, which have probably been occurring for centuries,
but only recently recognized (Francis and Hare, 1994), are
characterized by large-scale fluctuation in climate, and associated
variation in marine species abundance, community composition,
and trophic organization (Swartzman and Hickey, 2003). The effect
of regime shifts on marine fisheries has been relatively well-
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D.J. Shafer et al. / Aquatic Botany 89 (2008) 297–302
documented (Benson and Trites, 2002); coastal and estuarine plant
distribution, abundance, growth, and reproduction may also be
affected. For example, climate changes associated with El Nino/La
Nina periods influence Z. marina biomass and productivity (Nelson,
1997) as well as abundance and flowering in the Pacific Northwest
(Thom et al., 2003).
Decadal scale patterns associated with regime shifts may be
superimposed on longer-term climate changes occurring due to
global warming. Increased global temperatures will probably
affect growth rates and other physiological processes within
seagrass leaves (Short and Neckles, 1999). Distribution patterns
are also likely to change as a result of thermal stress and altered
reproductive fitness and output (Short and Neckles, 1999). The
results presented here suggest that Z. japonica populations in
northern and southern sites respond differently to temperature.
These differences could be important in determining future
patterns of distribution and abundance, and in predicting the
outcome of competitive interactions with the native Z. marina.
Acknowledgements
This research was conducted under a Guest Worker Agreement
with the Environmental Protection Agency, Pacific Coastal Ecology
Branch, Newport, Oregon. The authors thank Walt Nelson,
Environmental Protection Agency, and Douglas Bulthuis, Padilla
Bay National Estuarine Research Reserve, for their support. Special
thanks are due to Jim Kaldy for his assistance with lab set-up and
for constructive comments provided on an earlier draft of this
manuscript. Dale Magoun provided advice on appropriate statistical procedures. Comments from the editor and two anonymous
reviewers contributed to the quality of the manuscript.
References
Aioi, K., Nakaoka, M., 2003. The seagrasses of Japan. In: Green, E.P., Short, F.T.
(Eds.), World Atlas of Seagrasses. University of California Press, Berkeley,
California, pp. 185–192.
Baldwin, J.R., Lovvorn, J.R., 1994. Expansion of seagrass habitat by the exotic Zostera
japonica, and its use by dabbling ducks and brant in Boundary Bay, British
Columbia. Mar. Ecol. Prog. Ser. 103, 119–127.
Bando, K.J., 2006. The roles of competition and disturbance in a marine invasion.
Biol. Inv. 8, 755–763.
Benson, A.J., Trites, A.W., 2002. Ecological effects of regime-shifts in the Bering Sea
and eastern North Pacific Ocean. Fish Fish. 3, 95–113.
Biebel, R., McRoy, C.P., 1971. Plasmatic resistance and rate of respiration and
photosynthesis of Zostera marina at different salinities and temperatures.
Mar. Biol. 8, 48–56.
Bulthuis, D.A., 1987. Effects of temperature on photosynthesis and growth of
seagrasses. Aquat. Bot. 27, 27–40.
Bulthuis, D.A., 1995. Distribution of seagrasses in a North Puget Sound estuary:
Padilla Bay, Washington, USA. Aquat. Bot. 50, 99–105.
Byers, J.E., Reichard, S., Randall, J.M., Parker, I.M., Smith, C.S., Lonsdale, W.M.,
Atkinson, I.A.E., Seastedt, T.R., Williamson, M., Chornesky, E., Hayes, D., 2002.
Directing research to reduce the impacts of nonindigenous species. Conserv.
Biol. 16, 630–640.
Campbell, S.J., McKenzie, L.J., Kerville, S.P., 2006. Photosynthetic responses of seven
tropical seagrasses to elevated seawater temperature. J. Exp. Mar. Biol. Ecol.
330, 455–468.
Dumbauld, B.R., Wyllie-Echeverria, S., 2003. The influence of burrowing thalassinid
shrimps on the distribution of intertidal seagrasses in Willapa Bay, Washington,
USA. Aquat. Bot. 77, 27–42.
Emmett, R., Llanso, R., Newton, J., Thom, R., Hornberger, M., Morgan, C., Levings, C.,
Copping, A., Fishman, P., 2000. Geographic signatures of North American West
Coast estuaries. Estuaries 23, 765–792.
Francis, R.C., Hare, S., 1994. Decadal-scale regime shifts in the large marine ecosystems
of the North-east Pacific: a case for historical science. Fish. Ocean. 3, 279–291.
Freund, R.J., Wilson, W.J., 1993. Statistical Methods. Academic Press, Inc. Harcourt
Brace Jovanovich, Publishers, Boston, Massachusetts.
Green, E.P., Short, F.T., 2003. World Atlas of Seagrasses. University of California
Press, Berkeley, California.
Hahn, D.R., 2003. Changes in community composition and ecosystem processes
associated with biological invasions: impacts of Zostera japonica in the marine
intertidal zone. Ph.D. Dissertation. University of Washington, Seattle,
Washington.
Harrison, P.G., 1979. Reproductive strategies in intertidal populations of two cooccurring seagrasses (Zostera spp.). Can. J. Bot. 57, 2635–2638.
Harrison, P.G., 1982. Comparative growth of Zostera japonica Aschers. & Graebn. and
Z. marina L. under simulated intertidal and subtidal conditions. Aquat. Bot. 14,
373–379.
Harrison, P.G., Bigley, R.E., 1982. The recent introduction of the seagrass Zostera
japonica Aschers. & Graebn to the Pacific coast of North America. Can. J. Fish. Aq.
Sc. 39, 1642–1648.
Hitchcock, C.L., Cronquist, A., Ownbey, M., Thompson, J.W., 1969. Vascular Plants of
the Pacific Northwest. Part I: Vascular Cryptograms, Gymnosperms, and Monocotyledons. University of Washington Press, Seattle, Washington.
Kaldy, J.E., 2006. Production ecology of the non-indigenous seagrass, dwarf eelgrass
(Zostera japonica Ascher. & Graeb.) in a Pacific Northwest estuary, USA. Hydrobiologia 553, 201–217.
Keddy, J., Patriquin, D.G., 1978. An annual form of eelgrass in Nova Scotia. Aquat.
Bot. 5, 163–170.
Kinlan, B.P., Gaines, S.D., 2003. Propagule dispersal in marine and terrestrial
environments: a community perspective. Ecology 84, 2007–2020.
Lee, S.Y., Oh, J.H., Choi, C.I., Suh, Y., Mukai, H., 2005. Leaf growth and population
dynamics of intertidal Zostera japonica on the western coast of Korea. Aquat.
Bot. 83, 263–280.
Lee, S.Y., Kim, J.B., Lee, S.M., 2006. Temporal dynamics of subtidal Zostera marina and
intertidal Zostera japonica on the southern coast of Korea. Mar. Ecol. 27, 133–
144.
Marsh, J.A., Dennison, W.C., Alberte, R.S., 1986. Effects of temperature on photosynthesis and respiration in eelgrass (Zostera marina L.). J. Exp. Mar. Biol. Ecol.
101, 257–267.
Masini, R.J., Cary, J.L., Simpson, C.J., McComb, A.J., 1995. Effects of light and
temperature on the photosynthesis of temperate meadow-forming seagrasses
in Western Australia. Aquat. Bot. 49, 239–254.
Mau-Crimmins, T.M., Schussman, H.R., Geiger, E.L., 2006. Can the invaded range of a
species be predicted sufficiently using only native-range data? Lehmann lovegrass (Eragrostis lehmanniana) in the southwestern United States. Ecol. Model.
193, 736–746.
McMillan, C., 1979. Differentiation in response to chilling temperatures among
populations of three marine spermatophytes, Thalassia testudinum, Syringodium
filiforme and Halodule wrightii. Am. J. Bot. 66, 810–819.
McMillan, C., 1984. The distribution of tropical seagrasses with relation to their
tolerance of high temperatures. Aquat. Bot. 19, 369–380.
Nelson, T.A., 1997. Interannual variance in a subtidal eelgrass community. Aquat.
Bot. 56, 245–252.
Phillips, R.C., 1972. Ecological life history of Zostera marina L. (eelgrass) in Puget
Sound, Washington. Ph.D. Dissertation. University of Washington, Seattle,
Washington.
Phillips, R.C., 1984. The Ecology of Eelgrass Meadows in the Pacific Northwest: A
Community Profile. U.S. Dept. of the Interior, Washington, DC (FWS/OBS-84/
24).
Phillips, R.C., Backman, T.W., 1983. Phenology and reproductive biology of eelgrass
(Zostera marina L.) at Bahia Kino, Sea of Cortez, Mexico. Aquat. Bot. 17, 85–90.
Phillips, R.C., Grant, W.S., McRoy, C.P., 1983. Reproductive strategies of eelgrass
(Zostera marina L.). Aquat. Bot. 16, 1–20.
Posey, M.H., 1988. Community changes associated with the spread of an introduced
seagrass, Zostera japonica. Ecology 69, 974–983.
Sasek, T.W., Strain, B.R., 1990. Implications of atmospheric CO2 enrichment and
climatic change for the geographical distribution of two introduced vines in the
USA. Clim. Change 16, 31–51.
Shafer, D.J., Sherman, T., Wyllie-Echeverria, S., 2007. Do desiccation tolerances
control vertical distribution of seagrasses? Aquat. Bot. 87, 161–166.
Shanks, A.L., Grantham, B.A., Carr, M.H., 2003. Propagule dispersal distance and the
size and spacing of marine reserves. Ecol. Appl. 13, S159–S169.
Short, F.T., Neckles, H.A., 1999. The effects of global climate change on seagrasses.
Aquat. Bot. 63, 169–196.
Swartzman, G., Hickey, B., 2003. Evidence for a regime shift after the 1997–1998 El
Nino, based on 1995, 1998, and 2001 acoustic surveys in the Pacific Eastern
Boundary Current. Estuaries 26, 1032–1043.
Thom, R.M., 1990. Spatial and temporal patterns in plant standing stock and
primary production in a temperate seagrass system. Bot. Mar. 33, 497–510.
Thom, R.M., Borde, A.B., Blanton, S.L., Woodruff, D.L., Williams, G.D., 2001. The
influence of climate variation and change on structure and processes in nearshore vegetated communities of Puget Sound and other Northwest estuaries. In:
Droscher, T. (Ed.), Proceedings of 2001 Puget Sound Res. Conference. Puget
Sound Water Quality Action Team, Olympia, Washington.
Thom, R.M., Borde, A.B., Rumrill, S., Woodruff, D.L., Williams, G.D., Southard, J.A.,
Sargeant, S.L., 2003. Factors influencing spatial and annual variability in eelgrass (Zostera marina L.) meadows in Willapa Bay, Washington, and Coos Bay,
Oregon, estuaries. Estuaries 26, 1117–1129.
Walther, G.R., 2000. Climatic forcing on the dispersal of exotic species. Phytocoenologia 30, 409–430.
Woodward, F.I., 1987. Climate and Plant Distribution. Cambridge University Press,
Cambridge, UK.