synergies between climate anomalies and hydrological modifications facilitate estuarine biotic...

L E T T E RSynergies between climate anomalies and hydrological

modifications facilitate estuarine biotic invasions

Monika Winder,1* Alan D. Jassby2

and Ralph Mac Nally3

AbstractEnvironmental perturbation, climate change and international commerce are important drivers for biological

invasions. Climate anomalies can further increase levels of habitat disturbance and act synergistically to elevate

invasion risk. Herein, we use a historical data set from the upper San Francisco Estuary to provide the first

empirical evidence for facilitation of invasions by climate extremes. Invasive zooplankton species did not

become established in this estuary until the 1970s when increasing propagule pressure from Asia coincided with

extended drought periods. Hydrological management exacerbated the effects of post-1960 droughts and

reduced freshwater inflow even further, increasing drought severity and allowing unusually extreme salinity

intrusions. Native zooplankton experienced unprecedented conditions of high salinity and intensified benthic

grazing, and life history attributes of invasive zooplankton were advantageous enough during droughts to

outcompete native species and colonise the system. Extreme climatic events can therefore act synergistically

with environmental perturbation to facilitate the establishment of invasive species.

KeywordsClimate extremes, habitat perturbation, river flow, species introduction, zooplankton.

Ecology Letters (2011) 14: 749–757

INTRODUCTION

Movement of animals and plants by human activity is an inevitable

consequence of the globalised economy that poses a primary threat to

biodiversity and ecological and economic risks to native ecosystems

(Elton 2000). Understanding the mechanisms by which non-native

species become established in invaded habitats is central to

formulating effective management responses. Coastal and estuarine

ecosystems are especially susceptible to species invasion mediated by

high inputs of non-indigenous propagules from ships� ballast water

(Cohen & Carlton 1998; Ruiz et al. 2000; Verling et al. 2005), which

typically contains high densities of diverse organisms from the source

water body (Choi et al. 2005; Cordell et al. 2008). Although most

invading species fail to establish in the recipient region (Elton 2000;

Ruiz et al. 2000), environmental perturbations that alter ecosystem

processes such as resource availability, habitat modification and

climate change can facilitate naturalisation of non-native species

(Cohen & Carlton 1998; Stachowicz et al. 2002). The processes that

lead to successful invasions are difficult to predict (Carlton 1996), but

extreme climate events such as heat waves, storms and floods may also

alter the distribution and prevalence of invasive species by creating

novel environmental conditions in which exotic species can proliferate

and outcompete native species (Brook 2008; Bradley et al. 2010).

While there is a theoretical basis for climate extremes and their

amplifying impacts with other stressors in facilitating species invasion

(Brook 2008; Walther et al. 2009), empirical evidence for such

synergies in natural systems is rare because the sequence of events

that lead to successful establishment of invasions are often unknown

(Bradley et al. 2010).

An invaded aquatic ecosystem of great importance – ecologically,

economically and socially – is the San Francisco Estuary (California,

USA), consisting of the Bay and Delta (Fig. 1), which has experienced

an accelerating rate of non-native species appearances since the

California Gold Rush of 1849, broadly related to expansion in

international trade (Cohen & Carlton 1998). The high incidence of

invasive species plausibly might be due to several factors, including

(1) the lack of a diverse native fauna that could resist invasions,

(2) inoculation through diverse vectors from ships, aquaculture or

intentional stocking and (3) extensive habitat modification that altered

ecosystem processes and promoted invasions (Nichols et al. 1986;

Cohen & Carlton 1998). Anomalies in freshwater inflow also have

been suggested to play a critical role in successful establishment of

invasive species. It has been speculated that the drought years from

1959 to 1961 facilitated spread of the invasive Asian shrimp Palaemon

macrodactylus throughout the upper part of the estuary (Newman 1963).

The invasive clam Mya arenaria migrated upstream during the 1976–

1977 drought and temporarily intensified benthic grazing impacts

and substantially reduced phytoplankton biomass (Nichols 1985). An

extreme flood event followed by a long dry period that disturbed

the local benthic community may have been the major cause of

1Tahoe Environmental Research Center, John Muir Institute of the Environ-

ment, University of California, Davis, CA 95616, USA and Leibniz-Institute of

Marine Sciences at Kiel University (IFM-GEOMAR), Dusternbrooker Weg 20,

24105 Kiel, Germany2Department of Environmental Science and Policy, University of California,

Davis, CA 95616, USA

3Australian Centre for Biodiversity, School of Biological Sciences, Monash

University, Victoria 3800, Australia and Department of Zoology, The University

of Cambridge, Downing St, Cambridge, CB2 3EJ, UK

*Correspondence: E-mail: [email protected]

Ecology Letters, (2011) 14: 749–757 doi: 10.1111/j.1461-0248.2011.01635.x

� 2011 Blackwell Publishing Ltd/CNRS

proliferation of the introduced clam Corbula amurensis in 1986 (Carlton

et al. 1990; Nichols et al. 1990). Herein, we present evidence for the

effect of climate anomalies acting through freshwater flow on the

success, in particular, of invasive zooplankton species in the upper

San Francisco Estuary.

METHODS

Site description

The San Francisco Estuary provides crucial ecosystem services to the

state of California, including drinking water to 25 million people,

irrigation water for one of the world�s most productive agricultural

centres and open-water habitat for hundreds of plant and animal

species, including native fish species (CALFED 2001; Service 2007).

Large-scale hydrological modification of the estuary became possible

in 1945 with the completion of Shasta Dam on the Sacramento River

and was enhanced over the next three decades through additional

major dam projects such as the Oroville Dam on the Feather River

(completed 1968). This estuary is a major international shipping port

on the west coast of North America and receives nearly three million

tonnes of ballast water from foreign countries each year (Choi et al.

2005), almost certainly the major mechanism of non-native species

inoculations. More than 212 exotic and 123 cryptogenic (species that

are neither clearly native nor exotic) species were counted in this

estuary by the late 1990s (Cohen & Carlton 1998). Crustaceans and

bivalves comprise a large fraction of newly introduced species into the

estuary that have successfully colonised the system and displaced the

local fauna.

Data collection

We have analysed historical data from the upper part of the San

Francisco Estuary (i.e., the Sacramento-San Joaquin River Delta and

Suisun Bay; Fig. 1). This upper section of the San Francisco Estuary is

a low-salinity habitat, where abundances of certain fish and

invertebrates are negatively correlated with the amount of freshwater

inflow (Jassby et al. 1995; Mac Nally et al. 2010). This low-salinity

section has one of the longest, most complete estuarine zooplankton

records available, starting in 1972, which allowed identification of

temporal patterns of species invasions and the most probable driving

forces of invasions. The native crustacean zooplankton community

is relatively species-poor, dominated by freshwater cladocerans, the

copepods Acartia spp., Eurytemora affinis, Acanthocyclops vernalis and the

native opossum shrimp Neomysis mercedis (Winder & Jassby 2010).

These species were reported in a survey in 1912–1914 and 1963 in the

San Francisco estuary, suggesting that the community composition did

not undergo a major change before 1972 (Painter 1966).

Figure 1 Map of the San Francisco Estuary. Plankton and benthic sampling stations included in the present study are located in the upper estuary, consisting of Suisun Bay and

the Sacramento-San Joaquin Delta, as highlighted. The arrows mark different distances (km) of the positioning of the 2 & salinity zone (X2) from X2 = 0 at the Golden Gate

according to Monismith et al. (2002). X2 = 75 km corresponds approximately to the Sacramento-San Joaquin River Delta and Suisun Bay boundary, as well as the location at

which flow rates are estimated.

750 M. Winder, A. D. Jassby and R. Mac Nally Letter


Water-quality and zooplankton data were collected twice monthly

from April to October and monthly in March and November between

1972 and 1993, and afterwards at a monthly interval year-round.

Benthic samples were taken biannually from 1975 to 1979 and at a

monthly interval thereafter. Further details on sampling and analysis

are provided in Appendix S1.

River flow

Historical (1955–2009) mean daily flow rates were obtained with

Dayflow, a computer programme designed to estimate daily average

Delta outflow (http://www.water.ca.gov/dayflow/) (IEP 2006). The

programme uses daily river inflows, water exports, rainfall and

estimates of Delta agriculture depletions to estimate the �net� flow at

the confluence of the Sacramento and San Joaquin Rivers, nominally

at Chipps Island (see Fig. 1). In addition, back-calculated flow data

from 1930 to 1955 provided by Dayflow were included to compare

long-term actual flow with unimpaired (natural) flow. Unimpaired

flow is runoff that would have occurred, had water flow remained

unaltered in rivers and streams instead of being stored in reservoirs,

imported from other basins, exported or diverted, but otherwise at the

current level of development (Arora et al. 2006). Unimpaired flow data

are available from 1920 to 2003. The salinity field of the estuary can be

characterised by the positioning of the 2 & near-bottom salinity value

along the axis of the estuary (denoted as X2) (Jassby et al. 1995) and is

indexed as the distance from the Golden Gate up the axis of the

estuary (Fig. 1), described in Appendix S1. X2 was determined from

both actual flow and unimpaired flow using a steady-state model

suitable for monthly and longer time scales (Monismith et al. 2002).

International trade

As an index of international commerce, foreign trade values (export

and import) through California ports were obtained from http://

www.dof.ca.gov/HTML/FS_DATA/LatestEconData/FS_Trade.htm.

The Marine Exchange provided data on foreign shipping arrivals to

ports in the San Francisco Estuary; ship arrivals by last port of call

were available only for 1987–2009. Commercial export was used as a

surrogate for increase in propagule pressure and long-term commer-

cial increase because exporting ships are more likely to enter the ports

under ballast, and number of ships arriving from East-Asian countries

were not available before 1987. Total ship arrivals was not an

appropriate surrogate for increase in propagule pressure because total

ship arrivals declined (slope = )0.86% year)1; P < 0.001) despite

increasing international trade, which is due to several factors including

larger ships and decline of vehicle carriers from Japan as factories were

established in the US.

Statistical analyses

We explored links between numbers of invaders in a given year and

environmental and trade variables using a zero-inflated Poisson (ZIP)

model (Lambert 1992) because there were no invasions in most years

(79%), as described in Appendix S1. We considered a ZIP model in

which both the probability of invasion and the number of invaders in

each year were functions of the five covariates, which were: (1) X2,

(2) commercial export as a surrogate for increasing propagule pressure

as a result of expanding international commerce, (3) chlorophyll a,

(4) clam abundance (C. amurensis + M. arenaria) and (5) cumulative

number of invasions. Given that temporal autocorrelation of invasion

numbers is possible, a 1-year lag autocorrelation term was included for

both the probability of invasion and for the number of invaders. We

considered two models: current-year covariates and 3-year trailing

averages of covariates (i.e., current and preceding 2 years). The latter

model was motivated by the hypothesis that persistent drought lasting

several years was required to facilitate the success of invaders,

suggesting a 3-year trailing average X2 as a covariate. We applied the

same transformation to all covariates to avoid giving X2 a possible

spurious advantage due to a change in autocorrelation structure.

Long-term trend estimates were calculated as the linear slope and

statistical significance of the slope determined using the Mann–

Kendall test (Hensel & Hirsch 1992). Slopes were expressed as

percent per year by dividing the long-term mean of the variable.

RESULTS AND DISCUSSION

Variation in freshwater flow

Freshwater flow to the San Francisco Estuary has considerable

seasonal and annual variation, reflecting wet winters and dry summers

(Fig. 2a). The estuary has experienced extended drought periods with

unusual dry winters or short-lived winter ⁄ spring flow peaks since the

mid 1950s, including low-flow years from 1959 to 1961, 1976 to 1977,

1985 to 1994, 2001 to 2002 and 2007 to 2009. River flow in this

ecosystem drives large fluctuations of the salinity field (Monismith et al.

2002). Drought periods have been characterised by persistent intrusion

of X2 into the upper estuary beyond 75 km, a critical distance

separating Suisun Bay, an important benthic and pelagic nursery area,

from the Delta (Figs 1 and 2b). In years when X2 extended beyond

75 km, average salinity during the growing season of the aquatic biota

increased considerably in both the downstream low-salinity �suisun�and the upstream more freshwater �delta� subregions (Fig. 2c).

Chronology of invasive zooplankton establishment

Since the 1970s, the upper San Francisco Estuary has been invaded by

eight exotic copepod species and two mysid species (Fig. 3). The

establishment of all zooplankton species occurred during extended

drought periods, when salinity intrusion extended beyond 75 km

distance from the Golden Gate (Fig. 2d). Sinocalanus doerrii, a

carnivorous freshwater species endemic to rivers in mainland China

(Hada & Uye 1991) was first detected in 1978 (Orsi et al. 1983) and

had high abundances between 1979 and 1989 (Fig. 3a). The brackish

water species Oithona davisae, native to East Asia, appeared after the

short-term drought of 1976–1977 in the upper part of the estuary

(Ferrari & Orsi 1984) and remained at low abundance until the

extended drought of 1985–1994 (Fig. 3b). Similarly, Limnoithona

sinensis, native to China, was detected the first time in 1979 (Ferrari

& Orsi 1984) and remained abundant until 1992 (Fig. 3c).

Another influx of invasive zooplankton species occurred during the

long drought of 1985–1994 (Fig. 2). Pseudodiaptomus marinus and

P. forbesi, endemic to the Indo-Pacific region, were first observed at a

few sites in 1986 and 1987, respectively (Orsi & Walter 1991), and

spread throughout the upper estuary in 1988 (Fig. 3d). Towards the

end of the drought period, the upper San Francisco Estuary was

invaded by three other copepod species: L. tretaspina, originally

described in the Yangtze River in China, was detected in 1993 (Orsi &

Ohtsuka 1999) and experienced an explosive population growth and

Letter Synergistic effects on biotic invasions 751


spread, dominating copepod abundances since its establishment

(Fig. 3e) (Winder & Jassby 2010). Tortanus dextrilobatus and Acartiella

sinensis, both from East Asia, were observed in 1993 (Orsi & Ohtsuka

1999) and became successfully established thereafter (Fig. 3f–g). Two

Chinese mysid species (Hyperacanthomysis longirostris and Acanthomysis

aspera) were found in the estuary in 1992 (Modlin & Orsi 1997) and

developed persistent populations (Fig. 3i). These copepods and

mysids, all of them native to East Asia, proliferated in the upper San

Francisco Estuary and displaced native copepods and the native mysid

shrimp N. mercedis (Fig. 3h,j,l). Thus, the zooplankton community

shifted to a system more characteristic of East-Asian estuaries

compared with estuarine communities typical along the west coast of

North America (Cordell et al. 2008).

Unprecedented conditions during the last decades

The San Francisco Estuary has experienced prolonged droughts in the

past (Malamud-Roam et al. 2007), and propagules of non-native

species have been arriving over the last two centuries (Carlton 1979).

However, apparently none of the invasive zooplankton became

established in the upper low-salinity section until the 1970s when

unusual conditions coincided. First, as a result of increasing global

commerce and shipping traffic from East Asia with the opening of

new ports since the 1970s (Carlton et al. 1990; Carlton 1996),

inoculum frequency and invasion risk of East-Asian organisms to

ports in the San Francisco Estuary increased (Figs 4a,b). Second,

natural climate extremes have been exacerbated by hydrological

management of flow increasingly since the 1940s, with diversions

upstream of the estuary and exports from the Delta (Arthur et al.

1996). The major dam structures on the Sacramento River and its

tributaries were completed between 1945 and 1968. These modifi-

cations have caused more extreme salinity conditions during drought

periods in the upper part of the estuary, as indicated by the salinity

positioning calculated for actual and unimpaired flow (Fig. 4c).

Drought periods since the mid-20th century would not have been as

extensive and severe without anthropogenic hydrological perturba-

tions, indicated by the increasing difference between X2 for actual

and unimpaired flow (slope = 1.4% year)1; P < 0.001), and salinity

would have been within the historical range of salinity fluctuations.

Managed hydrological effects also exceeded the magnitude of the

Dust Bowl drought of the 1930s (Fig. 4c). Anomalous drought

conditions caused by hydrological modifications were the most likely

stressors for native fauna not adapted to these unusual environ-

mental conditions. In comparison, the majority of East-Asian

Sal

inity 0

2

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0.00.10.20.30.40.50.60.7

1955 1960 1965 1970 1975 1980 1985 1990 1995 2000 2005 2010

X2

(km

)

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1955 1960 1965 1970 1975 1980 1985 1990 1995 2000 2005 2010

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w (

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–1)

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1955 1960 1965 1970 1975 1980 1985 1990 1995 2000 2005 2010

Year

suisundelta

1987–88:Pseudodiaptomus

marinusP. forbesi

1992–94:Limnoithona tetraspinaTortanus dextrilobatus Acartiella sinensis Hyperacanthomysis longirostris Acanthomysis aspera

1978–79:Sinocalanus doerrii

Oithona davisaeLimnoithona sinensis

(a)

Data not available

Data not available

(b)

(c)

(d)

500

1000

1500

Figure 2 Chronology of zooplankton species invasion in the upper San Francisco estuary related to long-term flow and salinity patterns. (a) Freshwater inflow and timing of

first appearance of invasive zooplankton (arrows). (b) Extension of the salinity field indexed by the positioning of 2 & salinity distance from the Golden Gate (X2, red) and

freshwater flow (blue). A 3-year backward moving average of monthly values was applied to emphasise persistent long-term conditions. Shaded areas highlight invasion periods.

(c) Three-year backward moving average of annual salinity during the growing season (May–November) in the downstream �suisun� and upstream �delta� subregions (for

subregions see Fig. 1 in Winder & Jassby 2010). Years when long-term X2 averages extend above 75 km are highlighted, corresponding to < 300 m3 s)1 outflow from the

Delta into Suisun Bay. (d) Boxplots of the 2 & isohaline distance, X2, in years when an invasion occurred (+invasion) compared with years without zooplankton invasions

()invasion). The shaded areas are approximate 95% confidence limits for the median of the 3-year moving X2 average. The shadings of the two plots do not overlap, which is

�strong evidence� that the two medians differ (Chambers et al. 1983).



brackish water copepods have high potential for adapting to new

habitats (Ohtsuka et al. 1995; Orsi & Ohtsuka 1999), which probably

contributed to their initial success and increased the likelihood of

establishing self-sustaining populations in the upper San Francisco

Estuary.

Quantitative support for a relation between invasion and drought

We used a 3-year backward moving average of X2 > 75 km to

define years representing persistent dry conditions, implying that

there were 16 dry and 22 non-dry years from 1972 to 2009. There

were 8 years in which invasions took place, of which seven were dry

years. The number of ways in which at least seven of eight

randomly chosen years could be dry years, given that invasions into

the San Francisco Estuary are independent among years (Cohen &

Carlton 1998), is 0.54% of the total possible outcomes for choosing

8 years from the 38 years total. The high prevalence of invasions

during dry years therefore appears to be more than a coincidence

(P = 0.0054). If the timing of invasive zooplankton proliferation

were simply a function of introduction or arrival to the estuary, we

would expect that colonisation would be uniform over time and

would not be clustered with periods of low freshwater flow, as

reported here. The combinatoric analysis does not account for

autocorrelation or alternative variables. Results from the ZIP models

showed that the model that included 3-year covariate averaging for

both the probability of invasion and number of invaders was much

superior to the model based on current-year covariate values (for

details see Appendix S1). The probability of new invasions, although

not the number of invader species per se, recorded in a year

appeared to be associated strongly with drought indexed by three-

year averaged X2 (Table 1). The result is evident even when the

influence of the previous year�s invasion value is taken into account

(Table 1). None of clam abundance, concentration of chlorophyll a,

increasing international commerce or cumulative number of invaders

(a surrogate for decreased �niche� availability) appeared to be an

important additional source of explained variability in probability of

invasion. Furthermore, although ship arrivals from mainland China

apparently increased steadily in the 1980s (Carlton et al. 1990),

arrivals from East Asia and other foreign sources combined showed

no steep increase prior to the invasive species proliferation of the

1980s or 1990s. Total ship arrivals also showed no abrupt increase

before the invasion period of the late 1970s (Fig. 4b), supporting

that invasion was more linked to drought than frequency of ship

arrivals.

NI

(a)

(b)

(c)

(d)

(e)

(f)

(g)

(h)

(i)

(j)

(k)

(l)

Figure 3 Historical abundances of introduced and native species in the upper San Francisco Estuary between 1972 and 2009. (a–h) Abundance of adult invasive copepod

species and total native copepod species. Adult stages are shown because immature stages were not continuously identified. Pseudodiamptous spp. is dominated by P. forbesi,

whereas P. marinus contributes in small numbers. (i–j) Introduced and native mysid species. Introduced mysids are dominated by Hyperacanthomysis longirostris (formerly

Acanthomysis bowmani) and to a lesser extent by Acanthomysis aspera. (k) Clam Mya arenaria and Corbula amurensis. M. arenaria was replaced by C. amurensis introduction after 1986.

Years in which continuous sampling occurred are indicated by triangles along the x axis in a–k. (l) Total biomass of native and introduced copepod species. Native copepod

biomass significantly decreased (slope = )4.9% year)1; P < 0.001) and invasive copepod biomass increased (slope = 4.5% year)1; P < 0.001).



Mechanisms linking colonisation of invasive species and

environmental conditions

The precise mechanisms that allowed successful establishment of

diverse zooplankton invaders in the low-salinity section of the San

Francisco Estuary during prolonged droughts probably differ among

species because these organisms differ in life history, feeding mode,

salinity preference and predation susceptibility (Orsi & Ohtsuka

1999; Rollwagen Bollens & Penry 2003; Bouley & Kimmerer 2006).

Effects of droughts on invasions are expected to act both directly in

a salinity-related manner and indirectly by changing environmental

conditions associated with droughts. Unusually high salinity during

drought periods probably contracted the available habitat range for

native copepods and other zooplankton species adapted to low-

salinity or freshwater conditions. For example, the native copepod

E. affinis has a narrow range of salinity (Kimmerer 2002) and

cladocerans, important copepod competitors in the upstream region,

are freshwater species and therefore became reduced in abundance

following saltwater intrusion. Thus, reduced interspecific competition

may have facilitated establishment of some exotic copepods and

invasive mysids that are more euryhaline (Orsi & Knutson 1979)

during drought periods.

Moreover, prolonged droughts created temporary shifts in the

benthic community from low densities dominated by deposit feeders

during normal flow years to high abundances of suspension-feeding

clams (Nichols 1985; Nichols et al. 1990). Increasing benthic densities

were associated with the upstream migration along the salinity

gradient of the clam M. arenaria during the 1976–1977 drought and

expansion of C. amurensis after its introduction in 1986 (Fig. 3k).

Abundances of these clams increased significantly during periods of

low river flow (Fig. 5) and affected resident zooplankton by

competition for food and predation on early life stages. Immediately

X2

(km

)

65

70

75

80

1920 1930 1940 1950 1960 1970 1980 1990 2000 2010

# sh

ip a

rriv

als

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US

$ b

illio

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(b)

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Unimpaired

(c)

Imports

Exports

(a)

3000

4000Other foreign countries

East Asia

Total

# s

hip

arri

vals

(to

tal)

Year

Figure 4 Patterns of international trade and salinity intrusion in

the San Francisco Estuary. (a) Foreign trade through all California

ports from 1970 to 2009. Commercial export (slope = 6.03%

year)1; P < 0.001) and import (slope = 6.84% year)1; P < 0.001)

rates increased significantly. (b) Total foreign ship arrivals to ports

in the San Francisco Estuary (dots) and arrivals by their last port

of call (bars). Ships arriving from East Asia contributed on

average 50% of total foreign ships arrivals, as highlighted.

(c) Distance of X2, the 2 & bottom isohaline along the axis

from the Golden Gate, for actual and unimpaired flow conditions.

Shaded areas in (a) and (c) indicate zooplankton and the Asian

shrimp invasion periods.

Table 1 Parameter estimates for a zero-inflated Poisson invasion model based on the number of invaders and probability of invasion in the upper San Francisco estuary from

1972 to 2009 for the model with 3-year trailing averages of covariates (current year plus the two previous years). This model was much superior compared with the model based

on current-year covariate values (see Appendix S1)

Quantity A X2 Clam abundance Exports Chl a Cum. Inv. Auto-correlation

Numbers of invaders in year –0.41 ± 0.44 0.50 ± 0.47 –0.22 ± 0.50 –0.16 ± 0.57 –0.10 ± 0.45 0.06 ± 0.54 0.18 ± 0.41

Odds-ratios 4.6 6.0 2.0 1.6 1.5 1.2 2.2

Probability of invasion in year –1.45 ± 0.39 1.10 ± 0.47 –0.13 ± 0.50 –0.48 ± 0.56 0.06 ± 0.47 –0.15 ± 0.55 0.68 ± 0.48

Odds-ratios Infinite 102.1 1.5 4.0 1.2 1.6 11.8

Values are parameter estimates ± SD and corresponding odds-ratios, which are measures of whether a parameter differs from 0; values ‡ 10 (bold) are deemed important

(Jeffreys 1961). X2 = salinity positioning (see text) calculated for the water year October–September; clam abundance = abundances of Mya arenaria and Corbula amurensis;

exports = commercial exports through all ports in California; Chl a = chlorophyll a concentration; Cum. Inv. = cumulative number of invasive zooplankton; auto-

correlation = a 1-year lag of the numbers of invasive species.



after clam spread, phytoplankton biomass dropped below critical

levels for zooplankton growth (Nichols 1985; Jassby et al. 2002;

Muller-Solger et al. 2002), and the phytoplankton assemblage shifted

from a diatom-dominated community to higher proportions of

phytoflagellates and cyanobacteria after 1986 (Lehman 2000). Conse-

quently, the preferred phytoplankton prey for native Acartia spp.

(Rollwagen Bollens & Penry 2003) were significantly reduced during

droughts, and the native, less selective-feeding E. affinis probably

experienced feeding interference from nutritionally inferior phyto-

plankton and detritus (Muller-Solger et al. 2006). In contrast, the

selective-feeding mode for high-quality phytoplankton of the invasive

Pseudodiaptomus spp. is advantageous at low phytoplankton availability.

Conditions where there are low primary production and high

abundances of flagellates also are more favourable for species that

utilise alternative food sources, characteristic of many zooplankton

invaders. The invasive copepods L. tetraspina and O. davisae feed

primarily on motile prey (Cordell et al. 2008), Acartiella spp. are

omnivorous, T. dextrilobatus is carnivorous, and invasive mysids utilise

a broader food range compared with the native mysid (Orsi & Mecum

1996).

In addition to competition for food, clam predation on early

zooplankton life stages became an important source of mortality

during drought periods and after the introduction of C. amurensis

(Kimmerer et al. 1994). Native E. affinis experienced high mortality

rates from clam predation (Kimmerer et al. 1994), at least for

C. amurensis, and declines of other native copepod species may be due

to the same mechanism (Kimmerer 2004). In contrast, record high

abundances of L. tetraspina and P. forbesi are attributable to effective

escape capabilities from clam predation (Gould & Kimmerer 2010).

Therefore, resident species are probably stressed by competition and

predation from clams, the effect of which is enhanced during

droughts. Environmental tolerance, feeding preference and life history

attributes give invasive zooplankton a competitive advantage under

drought conditions associated with intensified benthic grazing.

Invasive species became well established before the recovery to

normal flow conditions and were apparently able to outcompete and

prevent the return of natives during normal flow conditions (Winder

& Jassby 2010). Experimental manipulations are required to separate

direct effects associated with climate and indirect effects associated

with species interactions to fully understand the mechanisms

facilitating the establishment of individual species.

There were no new zooplankton invasions in the upper San

Francisco Estuary from the end of the drought in the 1990s, which

can be attributed to several possible factors. Ballast treatment

regulations that have been in place since 2000 require the exchange

of ballast water with oceanic water for ships entering California ports,

resulting in a decrease in the numbers of organisms discharged into

the estuary (Choi et al. 2005), and a presumed decline in pioneering

organisms that could become successful invasions. Furthermore, these

recently arrived euryhaline species that can survive periodic high

salinity events and are unaffected by associated drought stresses may

hinder establishment of new invading species. Increase in non-native

resident diversity could also have constrained further invasions

because existing ecological niches were filled, inhibiting subsequent

invasions (biotic resistance, Mack et al. 2000), although we could

find no evidence for this factor in our quantitative analysis

(Table 1, cumulative number of invasive zooplankton). Perhaps most

important, flow anomalies in the 2000s have not been as severe as

during earlier droughts, as indicated by X2 and by salinity measure-

ments (Figs 4c and 2), and environmental conditions that favour

establishment of invasive species not as aggravated compared with

prior droughts.

CONCLUSION

The San Francisco Estuary is one of the most invaded estuaries in the

world (Cohen & Carlton 1998) and one of the most perturbed aquatic

systems (Nichols et al. 1986). This estuary experienced extended

droughts in the past, but the impact of climate anomalies has been

amplified by hydrological changes associated with freshwater diver-

sion since the mid-twentieth century. Ecological manifestations of

flow alteration were particularly strong in the upstream low-salinity

region of the estuary. In particular, unusual dry periods caused by

hydrological modification in concert with increasing inoculum

frequency provided colonisation opportunities for exotic species

better adapted to novel environmental conditions. An increase in

benthic grazing at least partially mediated these changes. The shift in

plankton species composition fundamentally changed the estuarine

food web, which became less efficient at transferring energy to upper

trophic level (Winder & Jassby 2010), one important stressor

contributing to the recent population collapse of many pelagic fish

species in this system (Sommer et al. 2007). Moreover, the San

Francisco Estuary has become a �relay station� for further spread of

East-Asian species in estuaries on the west coast of North America

(Cordell et al. 2008).

Many estuaries have experienced reduced freshwater inflow either

due to water extraction or climate warming (Cai & Cowan 2008; Miller

et al. 2008). Exacerbation of climate anomalies by hydrological

modification and concomitant establishment of invasive species may

be a mechanism for invasion in many estuaries, but proliferations of

9489

0403

X2 (km)

0

1000

2000

Cla

m a

bund

ance

(Ind

. m–2

)

3000

4000

60 65 70 75 80 85

7581

84

77

78 798082838586

87

88

90

92

9395 96

97

98

9900

010205

06

0776

0809

91

Figure 5 Densities of the clams Mya arenaria and Corbula amurensis as a function of

the salinity field (X2, km) (regression equation is abundance = )6730 + 109(X2);

R2 = 0.35; P < 0.001; including a first order autoregressive term to account for

serial correlation). Labels indicate year of observation; average X2 is calculated for

the water year October–September.



invasive species are often not so well documented as in the upper San

Francisco Estuary. Climate change is shifting the magnitude and

duration of extreme events such as droughts or floods, which are

predicted to become more frequent (IPCC 2007). These anomalies

have direct effects on resident species and can cause temporary shifts

in species interactions that mediate establishment of invaders. Further

increases in international shipping are expected and ballast water

exchange at sea will not be enforced or enacted everywhere. Our

findings provide evidence that the climate-invasion link can go beyond

warming effects on hydrological conditions. Altered flow regimes by

human activities can modulate the ecological impact of drought

anomalies and increase the susceptibility of ecosystems to invasion.

These results have implications for biodiversity conservation and

environmental management and suggest that estuarine ecosystem

management needs to consider synergistic effects of extreme events

with habitat perturbation when assessing invasion risks to coastal

ecosystems.

ACKNOWLEDGEMENTS

We thank April Hennessey, Kathy Hieb, Helen Fuller and Scott Waller

for providing the data. We also thank Wim Kimmerer, James Cloern,

Anke Muller-Solger and three anonymous referees for their valuable

comments. Figure 1 is based on a map originally drawn by Jeanne

Dileo. Financial support by the CALFED Science Program under

Grant No. R ⁄ SF-36 (CalFed U-04-SC-005), the Interagency Ecolog-

ical Program under California DWR agreement number

4600008137T5, and the Deutsche Forschungsgemeinschoft as part

of the priority program Aquashift is gratefully acknowledged. Mac

Nally acknowledges the kind hosting by Andrew Balmford, Bill

Sutherland and Rhys Green in the Department of Zoology, The

University of Cambridge, where his contributions to this paper were

done. M.W. and A.D.J. designed research; M.W. and A.D.J. performed

research; M.W., A.D.J. and R. M. N. performed analysis and wrote the

paper.

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SUPPORTING INFORMATION

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version of this article:

Appendix S1 Detailed description of data collection and analyses.

As a service to our authors and readers, this journal provides

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peer-reviewed and may be re-organized for online delivery, but are not

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Editor, Elsa Cleland

Manuscript received 21 March 2011

First decision made 20 April 2011

Manuscript accepted 3 May 2011



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