Zooplankton invasion on a grand scale: insights from a 20 ......Zooplankton invasion on a grand scale: insights from a 20-yr time series across 38 Northeast Paciﬁc estuaries ERIC

Zooplankton invasion on a grand scale: insights from a 20-yr timeseries across 38 Northeast Pacific estuaries

ERIC DEXTER ,1,2,� STEPHEN M. BOLLENS ,1,3 JEFFERY CORDELL ,4 ANDGRETCHEN ROLLWAGEN-BOLLENS 1,3

1School of the Environment, Washington State University, 14204 NE Salmon Creek Avenue, Vancouver, Washington 98686-9600 USA2Department of Environmental Sciences, The University of Basel, Vesalgasse 1, Basel, 4051 Switzerland

3School of Biological Sciences, Washington State University, 14204 NE Salmon Creek Avenue, Vancouver, Washington 98686-9600 USA4School of Aquatic and Fishery Sciences, University of Washington, Box 355020, Seattle, Washington 98195-5020 USA

Citation: Dexter, E., S. M. Bollens, J. Cordell, and G. Rollwagen-Bollens. 2020. Zooplankton invasion on a grand scale:insights from a 20-yr time series across 38 Northeast Pacific estuaries. Ecosphere 11(5):e03040. 10.1002/ecs2.3040

Abstract. We present the first comprehensive analysis of the Pacific Northwest estuaries (PNWE)zooplankton time series, which encompasses 38 estuaries distributed across more than 1000 km of theNorth American Pacific Coast. With observations spanning more than 20 yr, we here examine biogeo-graphic trends among zooplankton communities, patterns of biological invasion across the region, andenvironmental correlates with dominant native and invasive taxa. Our results show that some estuar-ies across the region are invaded by multiple zooplankton species and that the geographic extent ofinvasion is far greater than previously reported for at least five species of copepods: Pseudodiaptomusinopinus, Pseudodiaptomus forbesi, Oithona davisae, Limnoithona sinensis, Sinocalanus doerrii, and the clado-ceran Bosmina coregoni. Some of these species appear to be rapidly spreading across the region, whileothers have occupied a relatively static geographic range for decades. The copepod, P. inopinus, is byfar the most abundant and geographically widespread of these invaders, comprising more than 90%of all zooplankton abundance at some sites. We propose that the geographic distribution of these inva-ders is strongly constrained by geomorphic characteristics that define the salinity and mixing regimesin these estuaries, reflecting the strong role that physical forces play in structuring estuarine zooplank-ton communities.

Key words: biogeography; ecological niche; geomorphology; habitat; Oithona davisae; Pacific Northwest;Pseudodiaptomus forbesi; Pseudodiaptomus inopinus;.

Received 23 November 2019; accepted 3 December 2019; final version received 7 January 2020. Corresponding Editor:D. P. C. Peters.Copyright: © 2020 The Authors. This is an open access article under the terms of the Creative Commons AttributionLicense, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.� E-mail: [email protected]

INTRODUCTION

Estuarine zooplankton invasionsZooplankton are a taxonomically diverse

assemblage of predominantly microscopicorganisms that play a crucial role in freshwater,estuarine, and marine ecosystems. Freshwaterand estuarine zooplankton populations tend tobe structured across landscapes in a mannerdetermined by the hydrological connectivity of

the water bodies that they inhabit. Some spe-cies of zooplankton achieve long-range disper-sal via stress-resistant eggs carried byfloodwaters, aquatic birds, or air currents(C�aceres and Soluk 2002, Frisch et al. 2007),but varied anthropogenic activities now facili-tate the long-range transport of many zoo-plankton species. Of the numerouszooplankton invasions that have been docu-mented in recent decades (Bollens et al. 2002,

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https://orcid.org/0000-0003-2296-9923https://orcid.org/0000-0003-2296-9923https://orcid.org/0000-0003-2296-9923https://orcid.org/0000-0001-9214-9037https://orcid.org/0000-0001-9214-9037https://orcid.org/0000-0001-9214-9037https://orcid.org/0000-0002-7566-7083https://orcid.org/0000-0002-7566-7083https://orcid.org/0000-0002-7566-7083https://orcid.org/0000-0002-5127-5720https://orcid.org/0000-0002-5127-5720https://orcid.org/0000-0002-5127-5720info:doi/10.1002/ecs2.3040http://creativecommons.org/licenses/by/4.0/http://crossmark.crossref.org/dialog/?doi=10.1002%2Fecs2.3040&domain=pdf&date_stamp=2020-05-15

Dexter and Bollens 2019), most have been asso-ciated with the discharge of ballast water fromcommercial shipping vessels (Carlton and Gel-ler 1993, Ruiz et al. 2000, Grosholz 2002).

After an initial period of establishment, newlyarrived estuarine species may undergo sec-ondary spread to upstream locations (e.g., fresh-water-tolerant species such as the copepodPseudodiaptomus forbesi) or downstream to coastalwaters (e.g., salt-tolerant species such as thecopepod Oithona davisae; Svetlichny and Hubar-eva 2014, Emerson et al. 2015). However, themechanisms and patterns of secondary spreadacross estuarine systems are not well-under-stood, because regular monitoring of zooplank-ton has occurred at only a small number ofestuaries, making it difficult to understand inva-sion processes across regional scales.

For more than two decades, our group has sur-veyed zooplankton communities across the Paci-fic Northwest coast of North America, fromsouthern British Columbia, Canada, to northernCalifornia, USA, with recent expansion into cen-tral and southern California. These surveys havebeen conducted every four years (1996–2016) bysampling along the upstream salinity gradient at20–30 estuaries. The surveyed estuaries span awide range of environmental conditions andland use, from small rural watersheds to largeurbanized water bodies (Lee and Brown 2009).

A least 12 nonindigenous zooplankton specieshave been documented across this region, butmost observations have been from two-wellstudied bodies of water: the San Francisco Estu-ary and the lower Columbia River. Note that weemploy the term “nonindigenous” in reference toany nonnative species, but reserve the term “in-vasive” for species that have been associatedwith negative ecological impacts or rapid popu-lation expansion (see Davis and Thompson 2000for a discussion of this terminology). This list ofnonindigenous species includes nine copepods(e.g., Acartiella sinensis, Limnoithona sinensis, Lim-noithona tetraspina, Oithona davisae, Pseudodiapto-mus forbesi, Pseudodiaptomus inopinus,Pseudodiaptomus marinus, Sinocalanus doerrii, andTortanus dextrilobatus), the cladoceran Bosminacoregoni, and larvae of the clams Corbicula flu-minea and Potamocorbula (Carlton et al. 1990, Orsiand Walter 1991, Cohen and Carlton 1998, Orsiand Ohtsuka 1999, Gifford et al. 2007, Winder

and Jassby 2011, Bollens et al. 2012, Smits et al.2013, Hassett et al. 2017). Among these species,50% occur at both locations. Zebra mussels(Dreissena polymorpha) and quagga mussels(Dreissena bugensis) are not yet present at eithersite, but quagga mussels have recently arrived inthe western United States and may be poised forrapid spread across the region (Wong and Ger-stenberger 2011).We present the first detailed analysis of the

PNWE zooplankton time series, in which weexamine biogeographic trends among PacificNorthwest zooplankton communities, patternsof biological invasion across the region, and envi-ronmental correlates of dominant native andinvasive taxa. We also examine the salinity andstratification conditions occupied by a widerange of native and nonnative taxa, based on apreviously developed habitat occupancy modelfor the regionally widespread invader P. inopinus(Cordell et al. 2010). We also examine whetherzooplankton communities exhibit sharp biogeo-graphic breaks or slowly intergrade across broaddistances, and whether we can identify geo-graphic hotspots of introduction across theregion.

METHODS

Sample collectionThe Pacific Northwest estuaries (PNWE) zoo-

plankton time series comprises estuarine zoo-plankton community surveys conducted acrossthe Pacific Northwest coast of North America.This program includes 38 estuaries and tributaryrivers across more than 1000 km of coastline,with several recent sites extending into southernCalifornia (Fig. 1). We here present data from sixsurveys undertaken from 1996 to 2016. Thesesurveys were conducted in collaboration with avariety of regional agencies and stakeholdersevery four years, with some interannual varia-tion in the geographic extent of sampling(Table 1). This variation arises from sampledesign trade-offs between greater spatial cover-age and reduced temporal resolution at theperiphery of our study region, as well as theevolving research objectives of our regional col-laborators.In each survey year, we collected samples

across an approximately 6-week window


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centered on the month of September. Zooplank-ton samples were collected from each water bodyalong a longitudinal transect spanning a salinitygradient from 0 to 15 practical salinity units(PSU). Samples were collected from a small (4 m)boat at approximately mid-channel for each sta-tion via vertical net tows from just above the bot-tom to the surface using a 0.5 m diameter net.Zooplankton were collected using a 250-lmmesh net in 1996–2004, but a 75-lm mesh netwas deployed from 2008 onwards to more effec-tively sample smaller taxa. Samples were pre-served in the field in a 10% buffered formalinsolution for later taxonomic processing.

In order to sample across a range of salinityconditions, target salinities at each station wereset at 0, 1, 3, 5, and 15 PSU (measured at the bot-tom). In rare instances, we were unable to sampleall target stations due to issues of channel depthor abruptness of the salinity gradient. Surveys of

freshwater tributaries were conducted at 5equally spaced stations along a ~10-km transect.In all statistical analyses, we used measuredsalinity values rather than target salinity values.Surface and bottom salinity and temperature,

as well as water depth, were recorded at eachstation. Salinity and temperature values weremeasured using a YSI probe (Yellow SpringsInstruments), and water depth was recordedusing either an electronic depth finder or amarked and weighted line (depending on theyear and boat). We calculated a simple stratifica-tion index as the difference between surface andbottom values at each station for salinity andtemperature. This index serves as a rough indica-tor of mixing, but not an estimate of rate changeacross depth, or a measurement of the depth orshape of the thermocline or halocline. At themajority of our sites, however, the differencebetween surface and bottom salinity was

taxa present in

for each cluster, and clusters were visualized asan interpretive overlay on the NMDS ordination.Environmental factors (e.g., salinity, temperature,and stratification) were plotted as vectors on theNMDS ordination using the envfit function in thevegan package for R, which produces a good-ness-of-fit statistic (r2) for each environmental fac-tor across the ordination space. The significanceof each association was assessed using a MonteCarlo randomization test with 1000 permutations.

Finally, we characterized the salinity andstratification conditions under which the most

abundant native and invasive taxa wereobserved. Pairwise comparisons were con-ducted for areas of overlap between all invasivetaxa, as well as between the 10 most abundantnative taxa and the regionally significant inva-der, P. inopinus. We delineated areas in this 2-dimensional salinity-stratification space as theconditions under which at least one samplewas at least 50% comprised of the given taxon.This high threshold was employed to excludemarginal habitats from the analysis. Unlessotherwise specified, all species abundanceswere standardized to relative abundances (0–1scale) within each sample. This standardizationwas performed to reduce the effects of variationin sampling gear (e.g., net mesh size) and per-sonnel across years, and to more readily com-pare community composition across sites withmarkedly different levels of overall abundance(Field et al. 1982, Clarke 1993). All statisticalanalyses were conducted in R (version 3.5.1, RCore Team 2016) with figures generated usingthe colorblind-safe palette Viridis in ggplot(Wickham 2016). The complete R-code is pro-vided in Data S1.

RESULTS

OverviewA total of 584 samples were collected from 38

estuaries and associated tributary rivers(Table 1). Most of the estuaries were connecteddirectly to the Pacific Ocean or the Salish Sea, butfour tributary rivers draining into the ColumbiaRiver estuary were also surveyed (Grays, Cowl-itz, Youngs, and Willamette rivers). Zooplanktontaxa richness varied widely across samples, rang-ing from 1 to 18 taxa collected per station. Thecopepods Oithona davisae, Acartia spp., and Eury-temora affinis, and the larvae of bivalves and Cir-ripedia were the most abundant taxa overall(Fig. 2). For some of these taxa, high abundanceswere observed across a relatively small numberof sites. When considered in terms of relativeabundance across sites, the copepods Pseudodiap-tomus inopinus, Pseudodiaptomus forbesi, Pseudo-bradya sp., and Eurytemora spp., and variousHarpacticoida were the most abundant taxa(Fig. 3).Bottom and surface salinity ranged from 0 to

34 PSU across the entire dataset, with sites

Table 2. Inventory of taxonomic groups used at alllevels of analysis.

Group Taxon

Cladocerans Bosmina sp.ChydoridaeDaphnia sp.

Bosmina coregoniPodon sp.

Cladocera misc.Calanoid Copepods Acartia californiensis

Acartia tonsaAcartia spp.Calanus spp.Calanoida

Calocalanus sp.Diaptomidae

Eurytemora affinisEurytemora americana

Eurytemora spp.Paracalanus spp.

Pseudocalanus spp.Pseudodiaptomus inopinusPseudodiaptomus forbesi

Sinocalanus doerriiCyclopoid Copepods Corycaeus anglicus

CyclopidaeHalicyclops sp.

Limnoithona sinensisOithona davisaeOithona similisOithona spp.Oncaea spp.

Harpacticoid Copepods Coullana canadensisPseudobradya sp.Harpacticoida

Other taxa BivalviaCirripediaGastropodaSpionidaePolychaeta

Note: Nonindigenous taxa are shown in bold.


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ranging from unstratified (no difference betweentop and bottom salinity) to strongly stratified (34PSU difference from top to bottom). Bottom tem-peratures ranged from 5.5° to 22.4°C and tendedto be strongly correlated with surface tempera-tures, which ranged from 5.6° to 22.7°C. Acrossthe entire dataset, differences between top andbottom temperatures ranged from 0° to 7.5°C.

Mixing index values of the sampled estuariesbroadly reflected the coastal geomorphology ofthe study area (Emmett et al. 2000, Hickey andBanas 2003, Lee and Brown 2009). Sites locatedin northern Oregon and southern Washington(approximately 43°–47°N) tended to exhibit longand well-mixed zones of transition from fresh to

marine waters, consistent with their origins aslow-elevation drowned river valleys (e.g., the Til-lamook River; Table 1). In contrast, sites at thenorthern and southern end of our study regiontended to show stronger vertical stratificationand short salt wedges at the mouth of the estuary(e.g., the Chetco River; Table 1). This patternreflects the steep elevation gradient of the south-ern Oregon and northern California coast, andthe glacial fjord origins of our northernmost estu-aries (Emmett et al. 2000, Hickey and Banas2003). These hydrological differences wereapparent in the field, where sharp gradients ofsalinity prevented us from precisely samplingthe target maximum salinity of ~15 PSU at most

Fig. 2. Total abundance by taxon (summed across all samples).


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northern and southern estuaries, but not estuar-ies in the central region (Fig. 4A). Hereafter, werefer to the central latitudinal range between 43°and 47°N (southern Washington and northernOregon) as the “Central Coast” subregion, withsites located above 47°N (northern Washingtonand British Columbia) as the “North Coast” sub-region, and with sites located below 43°N (south-ern Oregon and California) as the “South Coast”subregion.

Community-level patternsNMDS ordination of the community data

yielded an evenly distributed cloud of points

without obvious breakpoints in communitystructure (Fig. 5). Higher-dimensional NMDSsolutions (not shown) showed little change in therelative position of samples along the first twoaxes. Visual inspection of the associated Shep-herd plot for outlying points (Field et al. 1982,Clarke 1993) did not show specific regions ofpoor fit on the ordination space. Results from theDexter et al. (2018a) NMDS stress test (1-sampleZ-test; P < 0.05) based on 1000 constrained per-mutations of the data matrix indicated that thestress value of 0.25 achieved by the 2-dimen-sional ordination remained within acceptablelimits for interpretation.

Fig. 3. Mean relative abundance by taxon (when present in a sample).


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Hierarchical agglomerative clustering of com-munity samples yielded three groups whichcould be distinguished by several biological andphysical characteristics (Fig. 6). Division of thedata into a greater number of clusters yieldedgroups that were difficult to distinguish fromeach other. Group 1 samples typically originatedfrom higher salinity stations, with a mean salin-ity of 13.4 PSU compared with 4.0 and 2.6 PSUfor groups 2 and 3, respectively. Group 1 encom-passed samples from across the entire geo-graphic range of the study, while groups 2 and 3were predominantly found in Oregon and Wash-ington. Samples from group 3 were associatedwith slightly warmer waters than groups 1 and2, although all groups spanned a wide range oftemperatures (Fig. 6). The three community

groups are visualized on the NMDS ordination,with the associated environmental factors shownas vectors (Fig. 5). Note that samples are contin-uously distributed across ordination space andthat samples positioned at group borders arelikely intermediate in values.Salinity, temperature, and stratification

showed strong patterns of correlation across theNMDS ordination (Fig. 5; Table 3). These associ-ations are plotted as vectors on the NMDS ordi-nation with vector length scaled to the r2 value ofthe environmental variable. For clarity, only vec-tors for bottom values are shown on the ordina-tion figure, because vectors pertaining to thesurface values were largely redundant. This fig-ure shows that points in the upper right regionof the ordination space (i.e., the axis which

Fig. 4. (A) The bottom salinity and site latitude of each sample in the PNWE data series. (B) The proportionof P. inopinus in each sample relative to all other zooplankton taxa.


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divides groups 2 and 3) are associated with war-mer water temperatures. In contrast, salinity andstratification both increase toward the lowerright of this ordination space (i.e., the axis whichdivides group 1 from groups 2 and 3). Depthwas uncorrelated with community structure inour analysis, likely because most samples werecollected from small and shallow estuaries wheredepth could rapidly fluctuate with tidal stageand rainfall.

Community groups were also clearly differen-tiated based on their taxonomic composition.Although some taxa were common across allsamples, each group could be readily character-ized by its most abundant members (Table 4).Group 1 contained a high proportion of moremarine-oriented taxa (e.g., Acartia spp., Cirri-pedia, polychaetes), reflecting the higher salini-ties typical of this group. Groups 2 and 3 werenumerically dominated by brackish and freshwa-ter copepods, but showed striking differences inspecies composition. Samples in group 3 were

numerically dominated by the invasive copepodP. inopinus, comprising 83% of the average abun-dance. P. inopinus comprised only 4.3% of aver-age abundance in group 2, with the harpacticoidcopepod Pseudobradya sp. being the most abun-dant member of this group.

Nonindigenous zooplankton taxaWe observed a large increase in the number of

nonindigenous zooplankton species across the20-yr period of study, with most taxa foundexclusively in the central coast subregion (Fig. 7).At the outset of the PNWE program, weobserved only the invasive copepod P. inopinusamong our surveyed sites. We then detected anincreasing number of nonindigenous species atnearly every subsequent survey, such that by2016, six nonindigenous species were detectedacross multiple sites: the copepods Pseudodiapto-mus forbesi, Pseudodiaptomus inopinus, Oithonadavisae, Sinocalanus doerrii, Limnoithona sinensis,and the cladoceran Bosmina coregoni (Fig. 8).

Fig. 5. NMDS ordination of all samples with points colored according to hierarchical clustering group mem-bership. Salinity (r2 = 0.42), stratification (r2 = 0.22), and temperature (r2 = 0.18) are plotted as vectors on theNMDS ordination with arrow length scaled to the r2 value of the environmental variable.


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With the exception of the copepod O. davisae,these species were found only in the centralcoast. This increase in the number of detectedspecies does not appear to be driven by the 2008-onwards deployment of a finer (75-lm) meshnet, as the small-bodied O. davisae were collectedin large numbers prior to 2008, and our firstdetection of B. coregoni (which are large enoughto be captured in both sizes of net) occurred 8 yrafter the switch to a finer mesh.

The copepods P. forbesi, P. inopinus, and O. davi-sae have been previously characterized as invasiveon the U.S. West Coast (Cordell and Morrison1996, Cordell et al. 2008, Emerson et al. 2015),and each comprised a major fraction of total zoo-plankton abundance across multiple estuaries thatwe sampled. P. inopinuswas the single most abun-dant taxon in terms of relative abundance withinindividual samples (Fig. 3) and was observed in200 samples across 14 estuaries. When present, P.inopinus typically comprised more than 50% oftotal zooplankton abundance, and in some casesmore than 90% (Fig. 4B). We observed P. inopinuspredominantly within the central coast subregion(Fig. 4B) although a small number of P. inopinusindividuals were occasionally observed at moredistant sites.The congeneric copepod P. forbesi was detected

in 12 samples collected across 3 sites: the Wil-lamette River, the Youngs River, and the GraysRiver. Each of these rivers is a tributary of thelower Columbia River, where large populationsof P. forbesi are established (Cordell et al. 2008,

Fig. 6. Boxplots of selected biological and environmental variables across each of the three identified commu-nity groups.

Table 3. Environmental vector correlation scoresacross NMDS ordination space.

Environmental variable R2 value P-value

Salinity (bottom) 0.42 0.001Salinity (stratification) 0.32 0.001Temperature (stratification) 0.24 0.001Temperature (surface) 0.23 0.001Temperature (bottom) 0.18 0.001Salinity (surface) 0.12 0.001Latitude 0.05 0.001Depth 0.01 0.115


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Bollens et al. 2012, Breckenridge et al. 2015, Dex-ter et al. 2015, Emerson et al. 2015). In all cases,P. forbesi were collected across a narrow range ofsalinities (0–7.3 PSU), with most specimensobserved at

tended to dominate in freshwater conditions.With respect to native zooplankton, we foundthat nearly all examined taxa occurred under thesalinity-stratification conditions in which P. inopi-nus typically dominated, although some occupieda much wider range of conditions (Fig. 11).

We identified several presently uninvadedestuaries which may, in terms of this salinity-

stratification niche, be viable habitat for P. inopi-nus (Fig. 9). Most of these estuaries lie in thePuget Sound region of Washington state(Duwamish, Dungeness, Samish, Skagit, andSnohomish rivers) and have previously beencharacterized as potentially viable habitat for P.inopinus (Cordell et al. 2010). However, we foundthat the Russian River and the Eureka Slough

Fig. 7. The total number of nonindigenous zooplankton species detected across time. Values are shown for theentire PNWE series and three geographic regions: the northern coast (northern Washington and Vancouver, BC),the central coast (southern Washington and northern Oregon), and the southern coast (southern Oregon and Cal-ifornia). This figure excludes six cases of uncertain detection (out of 584 samples) where only a single individualwas collected from an estuary.

Fig. 8. The total number of sites occupied by each of the six nonindigenous species across the duration of thestudy. Oithona davisae was initially detected at 7 sites in 2004, but subsequently absent from many of those sitesuntil recent years. Bosmina coregoni and Sinocalanus doerrii were not reliably sampled and/or identified prior to2008.


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(both in central California) fall within this salin-ity-stratification niche as well.

DISCUSSION

Biogeographic patternsEstuaries are highly dynamic environments in

which physical and chemical conditions rapidly

shift across time and space. Salinity and tempera-ture are typically considered the primary envi-ronmental factors that determine estuarinezooplankton community structure (Collins andWilliams 1982, Soetaert and Van Rijswijk 1993,Tackx et al. 2004, Marques et al. 2006, Grahamand Bollens 2010, Bollens et al. 2011, 2014, Breck-enridge et al. 2015), with water column stratifica-tion, eutrophication, and other anthropogenicdisturbances exerting further influence (Lapriseand Dodson 1994, Marques et al. 2006). Ourstudy confirms that salinity is a primary correlateof community differentiation within and acrossestuaries of the U.S. Pacific Northwest. We foundthat moderate-to-high salinity stations hundredsof kilometers apart tended to be far more similarto each other than to fresher stations situatedslightly upstream in the same estuary and viceversa.In contrast, temperature was a poor predictor

of structure among the zooplankton communi-ties that we studied, with most species beingfound across a wide range of temperatures. Weobserved that sites highly invaded by P. inopinustended to be slightly warmer than uninvadedsites, but it is unclear whether this associationreflects a causal relationship, or whether temper-ature merely serves as a proxy for other traitsthat differentiate invaded from non-invaded sites(e.g., flushing rates). A strong temporal correla-tion has been observed between water tempera-ture and the seasonal abundance of the closelyrelated P. forbesi in the Columbia River (Dexteret al. 2015), and it is interesting to see a similar(but weaker) correlation across space with P.inopinus.Like salinity (but unlike temperature), stratifi-

cation appears to be a primary factor differentiat-ing the zooplankton communities that wesurveyed. We found highly invaded estuaries toshow low average salinity and little vertical strat-ification of the water column (i.e., well-mixedwaters). These mixing regimes reflect localcoastal geomorphology, with the low-elevationdrowned river valleys of northern Oregon andsouthern Washington showing much higher ratesof invasion than other regions of the coast. Wealso found that average salinity and stratificationconditions across the entire estuary were a farbetter predictor of occupancy for P. inopinus thanconditions at individual sampling stations. These

Fig. 9. Mean salinity and degree of thermal stratifi-cation (averaged across stations) for each study site.Sites with similar conditions to invaded estuaries butwhich remain uninvaded (shown inside circle) are pre-dominantly situated in the Puget Sound area.

Fig. 10. Visualization of the salinity and stratifica-tion conditions under which the three highly abundantzooplankton invaders (Pseudodiaptomus inopinus, Pseu-dodiaptomus forbesi, and Oithona davisae) comprise morethan 50% of total zooplankton abundance.


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findings accord with studies of rocky intertidalcommunities along the U.S. West Coast, whichshowed that local coastal features tended todelineate biogeographic breaks, and that latitudi-nal gradients in temperature explained biogeo-graphic patterns only at continental scales(Blanchette et al. 2008).

Accumulation of nonindigenous speciesDuring our two-decade period of study, we

observed a steady increase in the number of non-indigenous zooplankton among the estuariesthat we surveyed. In 1996, we detected only asingle invader, the copepod P. inopinus. Duringthe next two decades, a new species was docu-mented approximately every four years. We donot attribute this increase to the gradual inclu-sion of new sites across survey years, becausenew arrivals were primarily detected at consis-tently monitored sites in the central study region,not at peripheral sites.

This pattern of increase raises several ques-tions. Should we expect this relatively constantincrease in the number of nonindigenous speciesto continue in the coming years, or is the system

nearing a saturation point? Why have new spe-cies arrived as a steady stream and not a singlewave of introductions? What effect do thesenewly arrived species have on the establishmentand persistence of other previously observedspecies? Are nonindigenous species facilitatingthe further introduction of new species (i.e., inva-sional meltdown; Simberloff and Holle 1999) ordoes competition limit establishment and coexis-tence among new arrivals?Although our data do not allow us to directly

examine ecological interactions, we observe sev-eral lines of evidence pointing toward strongcompetition among some invaders. For example,we can identify several instances in which anewly arrived invasive species appears to havedisplaced a previously established (and highlyabundant) invader. The invasive copepod P.inopinus was one of the most abundant species ofzooplankton in the Columbia River Estuary forat least a decade, but disappeared from the sys-tem shortly after the establishment of P. forbesi(Cordell et al. 1992, 2008, Sytsma et al. 2004). Itis also noteworthy that despite the fact that theinvasive copepods O. davisae, P. forbesi, and P.

Fig. 11. Visualization of the salinity and stratification conditions under which Pseudodiaptomus inopinus com-prises more than 50% of total zooplankton abundance (yellow polygons) relative to the same criteria for each ofthe 10 most abundant zooplankton taxa (green polygons), with areas of overlap shown in yellow-green.


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inopinus dominate zooplankton communitiesunder overlapping geographic ranges and envi-ronmental conditions, these three species rarelyco-occur. These examples suggest that competi-tion may play a strong role in constraining theestablishment and spread of nonindigenous spe-cies in the Pacific Northwest. It remains unclearwhether competition or hydrological conditionsplay the stronger role in constraining newlyarrived species, or whether a combination ofboth factors ultimately delineates the extent ofinvasion spread.

Patterns of dispersalOur surveys reveal several themes regarding

the origin and dispersal of zooplankton invadersamong Pacific Northwest estuaries. First, each ofthe six nonindigenous species that we detected isnative to southeast Asian estuaries (Orsi et al.1983, Orsi and Walter 1991, Uye and Sano 1998,Wang et al. 2007, Cordell 2012). Secondly, nearlyall of these species have been collected from theballast water of commercial cargo vessels enter-ing Pacific Northwest waters (Cordell et al. 2009,Lawrence and Cordell 2010). Finally, three ofthese species (P. forbesi, O. davisae, and S. doerrii)became established in the San Francisco Estuaryprior to their appearance elsewhere in NorthAmerica (Orsi et al. 1983, Ferrari and Orsi 1984,Orsi and Walter 1991). These patterns suggest aninvasion corridor between southeast Asian estu-aries and the Pacific coast of North America thatis primarily driven by international shippingwith secondary spread facilitated in part bydomestic shipping—and strongly corroboratesfindings from ballast water surveys of shipsentering Pacific Northwest harbors (Cordell et al.2009, Lawrence and Cordell 2010).

While ballast water is the most probable vectorfor the initial introduction and secondary spreadof nonindigenous zooplankton into larger estuar-ies, it is unlikely the cause of secondary spread tosmaller estuaries across the region, because mostof the estuaries harboring nonindigenous specieshave little or no commercial shipping (PacificMaritime Association 2019). Despite the lack of ashipping vector, P. inopinus and O. davisae haverapidly colonized smaller rivers and estuariesacross the region. O. davisae were absent from allsurveyed sites in 1996, but occurred in at least 7estuaries by 2000 (Fig. 8). We detected O. davisae

at estuaries ranging from southern Canada to theUnited States–Mexico border. Similarly, P. inopi-nus spread across more than 500 km of coastlinewithin approximately one decade (Cordell et al.1992, Cordell and Morrison 1996).Because zooplankton can disperse via varied

natural and anthropogenic means (Havel andShurin 2004), the absence of commercial shippingamong smaller estuaries suggests that othertransport vectors such as oyster aquaculture(Mckindsey et al. 2007, Minchin 2007, Dumbauldet al. 2009) or overland transport of recreationalboats (Havel and Stelzleni-Schwent 2001) mayhave facilitated the spread of nonindigenousplankton species. Tides and coastal currents mayalso be effective means of dispersal for speciesthat can tolerate marine waters (Christy andStancyk 1982), while inland or salt-intolerantspecies may be transported on the plumage ofaquatic birds (Frisch et al. 2007) or as wind-car-ried eggs (C�aceres and Soluk 2002). In a previousstudy, a genetic-based reconstruction of theNorth American invasion of P. inopinus foundthat colonization and subsequent spread likelyoccurred in an erratic manner across the westcoast, largely independent of commercial ship-ping routes (Dexter et al. 2018b).The dispersal route of the nonindigenous

cladoceran, B. coregoni, may be of particularinterest in that (unlike other recently arrived zoo-plankton) B. coregoni are native to both Europeand Asia (M€uller 1985, Demelo and Hebert 1994,Wang et al. 2007, Guijun et al. 2012). B. coregonihave been present in the North American GreatLakes since the 1960s (Deevey and Deevey 1971,Balcer et al. 1984, Lieder 1991), but it was notuntil the late 2000s that B. coregoni were detectedat several sites across the Pacific Northwest(Smits et al. 2013, Dexter et al. 2015, Lee et al.2016). Each of these sites is regularly monitored,and B. coregoni are easily distinguished fromnative Bosmina; thus, these detections likely rep-resent a reasonable estimate for the time of popu-lation establishment. This raises the question ofwhether these populations originated via west-ward expansion from the Great Lakes, or fromballast water introductions from native popula-tions in Asia. As zebra and quagga mussels con-tinue westward expansion across the NorthAmerican continent (Wong and Gerstenberger2011), any information regarding dispersal of


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other taxa from the Great Lakes region to thePacific Northwest would be invaluable in assess-ing the risk of these high-impact invaders beingintroduced to Pacific Northwest waters.

Mechanisms and impacts of P. inopinus invasionAlthough multiple invasive species can domi-

nate zooplankton communities across the PacificNorthwest, P. inopinus is unique in terms ofnumerical abundance and the sharp geographicboundaries defining its range. Based on a seriesof habitat occupancy models, Cordell et al.(2010) predicted that salinity and stratificationwould be the primary factors constraining thespread of P. inopinus and that a number of unin-vaded estuaries in the Puget Sound region wereat risk of invasion. Our results support both con-clusions and furthermore identify several unin-vaded estuaries on the California coast as viablehabitat for P. inopinus.

Despite the apparent suitability of multipleuninvaded sites, the geographic range of P. inopi-nus has remained static for more than 20 yr. Thiscannot be attributed to the absence of transportvectors: P. inopinus have been detected in the bal-last water of numerous ships entering the PugetSound, which contains several estuaries appar-ently suitable for its colonization (Cordell et al.2009). Puget Sound estuaries may possess physi-cal or biological characteristics that prevent theestablishment of P. inopinus—a question whichmerits further investigation. In contrast, we haverecently detected a small number of P. inopinus atseveral of the California sites which we haveidentified as potentially viable habitat. We pro-pose that P. inopinus may yet undergo furtherrange expansion in northern California, with theRussian or the Rogue rivers serving as sourcesfor southern expansion.

It is unclear whether highly abundant invaderssuch as P. inopinus have displaced native fauna,or whether they have simply occupied openniches in Pacific Northwest estuaries. Previousauthors have noted that estuaries across theNorth American west coast tend to be relativelyspecies-poor—hypothesized to be a consequenceof the young geological age of these estuaries(Jacobs et al. 2004, Dumbauld et al. 2009). Sev-eral native taxa were consistently found in thebrackish conditions where P. inopinus occur(Fig. 11), but few of those species are known to

tolerate saline waters and their presence may beattributed to advection from upstream (fresher)reaches of the estuary. A notable exception is thebrackish-tolerant copepod Eurytemora affinis, ofwhich a unique subclade exists in the PacificNorthwest (Lee 2000), but which tended to occuronly in low abundances across our survey sites.Now that we have a clearer understanding of themagnitude of zooplankton invasion across Paci-fic Northwest estuaries, we suggest that futurestudies more closely examine the ecologicaldynamics that underlie this set of invasions—both in terms of the dynamics between nativeand invasive members of the community, and inrespect to the dynamics between different inva-ders as well.

CONCLUSIONS

Across more than 1000 km of coastline, wefound consistent patterns of zooplankton com-munity differentiation within and across estuar-ies, primarily driven along axes of salinity,temperature, and stratification. Some estuariesin the Pacific Northwest region are highlyinvaded by multiple zooplankton species, whileothers appear resistant to new taxa. Weobserved six nonindigenous species of copepodsand cladocera distributed among our sites, ofwhich three (P. inopinus, P. forbesi, O. davisae)were sufficiently widespread and abundant tobe considered invasive. In most cases, the geo-graphic extent of all nonindigenous speciesextended far beyond previous literature reports.We observed a continual accumulation of non-indigenous species across our two-decade per-iod of study. The three most widespread andabundant nonindigenous species rarely co-oc-curred and appeared to partition the environ-ment across a gradient of salinity. The copepodP. inopinus was by far the most abundant andgeographically widespread of these species,comprising more than 90% of all zooplanktonabundance at some sites. The geographic rangeoccupied by P. inopinus has remained stable formore than two decades, but some species (suchas O. davisae) appear to be rapidly spreadingacross the region and can be locally abundant.We propose that the geographic distribution ofthese nonindigenous species may be largelydetermined by geomorphic characteristics that


DEXTER ET AL.

define the salinity and mixing regimes in estuar-ies—a reflection of the dominant role that thesephysical forces play in structuring estuarine zoo-plankton communities.

ACKNOWLEDGMENTS

The funding for this research was provided by aU.S. Environmental Protection Agency STAR grant(#FP91780901-0) awarded to E. Dexter and S. Bollens,and a series of grants from Washington Sea Grant/National Oceanic and Atmospheric Administration,most recently #R/HCE/PD-5 to S. Bollens, J. Cordell,and G. Rollwagen-Bollens. We thank Ben Bolam, SeanNolan, Vanessa Rose, and Josh Emerson for assistancein the field, and Olga Kalata for assistance with sampleprocessing. Additional comments on this manuscriptwere provided by Stephanie Hampton, Stephen Katz,and S�everine Vuilleumier as members of E. Dexter’sPh.D. committee.

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