Changes in Community Structure and Ecosystem Function...

23

One of the most pervasive human impacts to salt marshes around the world is theintroduction of nonnative species. Plant introductions to salt marsh systems haveresulted in significant changes ranging from species replacement to broad-scalealteration of ecosystem properties. In this chapter, we examine the changes producedby the invasive Atlantic smooth cordgrass Spartina alterniflora in two wetlandecosystems, one in San Francisco Bay, California, and one in Willapa Bay,Washington. We compare and contrast the impacts of Spartina invasion on a rangeof processes, focusing primarily on benthic invertebrate communities and thesediment environment. Our work shows that the structure of the plant itself and the changes it produces in the physical and chemical environment strongly influencebenthic communities. The aboveground structure shades the substrate, reducingphotosynthesis of benthic microalgae and restricts water flow, which contributes todecreased recruitment and slower growth of benthic suspension feeders. At the sametime, the plant structure increases sedimentation of fine-grained particles and leadsto the accumulation of detritus and low-quality organic matter. These changes,together with increased belowground plant biomass and peat production, influencesediment chemistry and metabolism. In addition, belowground plant biomass canpreempt substantial amounts of belowground habitat, directly reducing benthicabundance and diversity. These physical and chemical changes can result in dramaticshifts in benthic communities including substantial reductions in larger, surface-feeding taxa concurrent with increases in smaller, subsurface detritivores. Such shiftsin the functional identity of benthic species may negatively affect feeding of bothinvertebrate and vertebrate predators. The magnitude and direction of these variouschanges depend on the habitat invaded and are generally more substantial whereSpartina has invaded open mudflat and less where Spartina invades areas of nativevegetation. We discuss the consequences of these changes in the context of planteffects in other coastal systems in order to develop a set of predictions regarding futureplant invasions. The ultimate consequences of plant invasion on benthiccommunities involve a dynamic balance of positive and negative effects.

2

Changes in Community Structure andEcosystem Function Following Spartinaalterniflora Invasion of Pacific Estuaries

Edwin D. Grosholz, Lisa A. Levin, Anna C. Tyler, and Carlos Neira

Silliman_ch02.qxd 12/3/08 4:00 PM Page 23

Salt marshes are among the many habitatsworldwide experiencing rapid change as the re-sult of human-mediated stressors (Vitouseket al. 1997; Chapin et al. 2000; Mooney andHobbs 2000). Among the most importantchanges experienced by salt marshes is the in-troduction of nonnative plants. Wetlands gener-ally are susceptible to invasion, and introducedplants can foster changes acting broadly acrossmultiple spatial and temporal scales, producinglong-lasting and system-wide effects (Zedlerand Kercher 2004). These changes may includea host of physical and chemical alterations thatcan influence populations and communities ofplants and animals as well as alter the storageand recycling of nutrients (Mack et al. 2000).Introduced plants can also directly affect theabundance, diversity, and functional identity ofcommunities via the provision or preemption ofphysical habitat and as well as changes in thebasis of trophic support.

The invasion of Spartina alterniflora in U.S.West Coast estuaries provides an excellentdemonstration of the extent to which plant inva-sions can rapidly and extensively alter commu-nity and ecosystem dynamics in salt marshsystems. In this chapter, we will compare andcontrast the invasions of the Atlantic smoothcordgrass Spartina alterniflora in two estuariesin western North America. The first is SanFrancisco Bay, California, where S. alterniflorahybridized with the native Spartina foliosa, andthe resulting hybrid has spread rapidly through-out the central and southern portions of SanFrancisco Bay. The second is Willapa Bay,Washington, where in the absence of any nativeSpartina, S. alterniflora has colonized habitatsthroughout most of this bay.

We will address the impacts of Spartina onbenthic systems in these two regions with a par-

ticular focus on infaunal and epifaunal commu-nities and the changes in physical and chemicalprocesses in the sediment environment. Thechanges brought about by Spartina are ulti-mately the result of the extensive above- and be-lowground growth of the plant. But the overalleffects on community and ecosystem processesdepend on the magnitude of change in a rangeof properties, including above- and below-ground vascular plant biomass, production anddecomposition of detritus, microalgal produc-tivity, and sediment physicochemistry, all ofwhich can have variable effects on the nativeplants and animals. The consequences ofSpartina invasion strongly depend on the age ofthe invasion, the habitat being invaded, thepresence or absence of native vegetation, andmany site-specific characteristics including ele-vation, sediment grain size, and hydrodynamicregime.

The primary goal of this chapter is to synthe-size recent studies of Spartina invasions inWashington and California to better understandand predict the impacts of Spartina and othermarsh plants in the future. We do this by com-paring our results with other studies of invasiveSpartina in this western region and other re-gions, as well as with systems where Spartina isnative.

An additional goal is to use this under-standing to assist ongoing, eradication pro-grams in California and Washington that aimto eliminate invasive Spartina from this re-gion. By quantifying the full extent of thechanges being brought about by the Spartinainvasion, as well as knowing the mechanismsunderlying the changes, we hope to assist re-source managers in determining when, where,and how eradication of Spartina will be mosteffective.

24 i n v a s i o n s i n n o r t h a m e r i c a n s a l t m a r s h e s

By understanding the mechanisms that determine the magnitude and direction ofthese effects, scientists and managers will be better able to understand theconsequences of human-induced plant invasions in salt marsh systems and to predictthe impacts of future introductions.

Silliman_ch02.qxd 12/3/08 4:00 PM 4

CONTRASTING INVASIONS

The invasion of Spartina alterniflora in SanFrancisco Bay, henceforth “SFB,” began in 1975with its intentional introduction from theAtlantic Coast of the United States. by the ArmyCorp of Engineers for salt marsh restoration(Ayres, Strong, and Baye 2003; Ayres, Strong,et al. 2004). Following the initial introduction,a hybrid developed from S. alterniflora and thenative S. foliosa (hereafter referred to as hybridSpartina) (Daehler and Strong 1997). This hy-brid grows more vigorously than either parentplant and has a higher and lower tidal rangethan native plants (Ayres et al. 2003; Ayres,Smith, et al. 2004; Ayres, Zaremba, and Strong2004). The hybrid has successfully colonizednearly eight hundred hectares of the central andsouthern portions of SFB, where it has invadedopen mudflat at the lower end of its tidal distri-bution. Although three other species ofSpartina have been introduced into SFB (S. den-siflora, S. anglica, and S. patens), and another hy-brid (S. densiflora � S. foliosa) has been found(D. Ayers, personal communication), none havespread significantly (California CoastalConservancy 2006). The hybrid has displacedthe native S. foliosa as well as the original parentS. alterniflora in central SFB through hybridiza-tion and overgrowth (Ayres et al. 2003; Ayres,Smith, et al. 2004; Ayres, Zaremba, and Strong2004) and competes with native plants such asSalicornia virginica, Distichlis spicata, andJaumea carnosa.

The invasion of Willapa Bay, henceforth“WB,” began with the accidental introduction ofS. alterniflora around 1890 (Feist and Simenstad2000; Davis et al. 2004; Civille et al. 2005).Throughout most of the century since its initialintroduction, the spread of Spartina has beenfairly gradual. However, from 1995 to 2005, itrapidly spread to cover 1,600 hectares in WB forunknown reasons. Because there are no nativeSpartina species in the Pacific Northwest withwhich to hybridize, this invasion is entirely theresult of the spread of S. alterniflora. As in SFB,S. alterniflora has rapidly colonized open mud-

flat and has been found among native plants inthe upper intertidal zone, where it has the po-tential to compete with and even excludespecies such as Salicornia virginica, Distichlis spi-cata, and Deschampsia caespitosa, although thishas not so far been demonstrated.

While both systems involve invasion ofmudflats at the lower tidal range, noteworthydifferences may further influence the impact ofSpartina. In WB, the invasion is much older, theaerial cover is much greater, and other ecosys-tems, such as oyster reefs, are at risk of dis-placement. In addition, the invasive Spartinadoes not resemble any native marsh plantforms, and since there were no native Spartinaspecies present prior to the invasion, none ofthe native plants or animals have coevolved withthis genus. In contrast, the SFB invasion is rela-tively recent and involves a hybrid that became asuperior competitor that threatens to eliminatethe pure native S. foliosa (Ayres et al. 2003). Thesystem that is adapting to the invasion in SFB isreplete with birds, fish, and invertebrates thathave evolved with native Spartina in upper in-tertidal elevations. SFB is also heavily invaded,and because many of these introductions camefrom the Atlantic Coast, these invaders have along evolutionary history with the presence ofSpartina across a broad tidal range (Cohen andCarlton 1998). These include bivalves such asGeukensia demissa, Mya arenaria, and Gemmagemma as well as gastropods such as Urosalpinxcinerea and Ilyanassa obsoleta; these are amongthe most common species in areas of SFB withinvasive Spartina.

CONSEQUENCES OF INVASION

VASCULAR PLANT PRODUCTION

The productivity of Spartina, both above- andbelowground, was greater than that of nativevascular plants at both the WB and SFB sites.The magnitude of the differences between na-tive and nonnative habitats varied depending onthe initial conditions (vegetation type and sub-strate) and the age of the invasion. In SFB, the

s p a r t i n a a l t e r n i f l o r a i n p a c i f i c e s t u a r i e s 25


aboveground biomass of invasive Spartina wassignificantly higher than the biomass of nativeS. foliosa and Salicornia sp. (see table 2.1; Brusatiand Grosholz 2006; Tyler, Lambrinos, andGrosholz 2007). The belowground biomass ofinvasive Spartina was also generally higher thannative plants including S. foliosa, although thedifference was not as great as for abovegroundbiomass (table 2.1; Brusati and Grosholz 2006,Tyler et al. 2007). Also, the biomass of invasiveSpartina was obviously much greater than themicro- and macroalgae on historically “unvege-tated” mudflats. The belowground biomass ofhybrid Spartina in SFB (top six to ten centime-ters) changes with invasion stage. For example,at one site it increased from unvegetated tidalflats (less than one hundred grams per squaremeter) to 348 grams per square meter onthe “growing edge” (about one meter insidevegetation—i.e., young invasion), to over 720grams per square meters in the central area(thirty-year-old invasion) (Neira et al. 2007).

In WB, the introduced eelgrass Zostera japon-ica overlaps considerably in the tidal zone colo-nized by S. alterniflora (fig. 2.1). This eelgrassapparently produces only about a third of thebiomass produced by S. alterniflora (Ruesinket al. 2005). The long history of invasion in WB

has allowed us to determine the dynamics ofSpartina production by using the different-agedmeadows as a chronosequence to represent thetrends in biomass through time. Based on a se-ries of eighteen S. alterniflora meadows rangingfrom less than one year to more than thirty yearsold (age was determined based on the date whenthe areal extent of cordgrass in each region wasgreater than 50 percent), we found that above-ground biomass reached a peak within five toten years and then declined as the meadow aged.In contrast, the buildup of a dense mat of rootsand rhizomes required a longer time (ten to


TABLE 2.1 Summary of studies to date examining changes in primary production, sediment respiration, and sediment

organic C and N in invaded western salt marshes

san francisco bay willapa bay

Mudflat Spartina Mudflat Spartina

(mean � SE) (mean � SE) (mean � SE) (mean � SE)AG biomass (g m�2)1,2 ——— 1823 � 283 3 � 1 1695 � 245

BG biomass (g m�2)1,2 ——— 4197 � 773 55 � 8 878 � 91

Benthic Chl a (mg m�2)3 184 � 51 97 � 15 117 � 9 247 � 23

GPP (mg Cm�2 d�1)3 459 � 92 258 � 52 ——— ———Respiration (mg Cm�2 d�1)3 179 � 34 752 � 91 ——— ———%N4 0.10 � 0.03 0.17 � 0.02 0.12 � 0.00 0.23 � 0.02%C4 1.22 � 0.30 2.70 � 0.29 1.35 � 0.04 3.36 � 0.34C:N4 14.8 � 2.1 21.8 � 2.2 12.9 � 0.1 16.0 � 0.6

NOTE: Aboveground (AG) and belowground (BG) biomass were measured at the end of the growing season (September–October).

SOURCES: 1Tyler et al. 2007 (Spartina values); 2mudflat biomass values are for the invasive intertidal seagrass Zostera japonica from A. C. Tyler, unpublished data, 2002; 3Tyler and Grosholz (n.d.), except for Willapa Bay chlorophyll a values, which are from A. C. Tyler,unpublished data, 2003); 4A. C. Tyler, unpublished data, fall 2002.

FIGURE 2.1 Introduced Spartina alterniflora seedlingscompeting for space with introduced eelgrass Zosterajaponica in Willapa Bay, Washington.


fifteen years) but then remained relatively con-stant (A. C, Tyler, unpublished data). This above-ground biomass of S. alterniflora in WB wassimilar to that of hybrid Spartina in SFB; how-ever, the belowground biomass in WB was con-siderably less than in SFB (table 2.1).

PHYSICAL PROCESSES

The large amount of aboveground biomass pro-duced by invasive Spartina necessarily results inchanges in the physical regime of the invadedmudflats. The plant reduces both the lightreaching the mudflat surface and tidal energy.In both SFB and WB, the aboveground canopyof invasive Spartina significantly reduced lightpenetration to the sediment surface by up to 83percent (Neira, Levin, and Grosholz 2005; Neiraet al. 2006; Tyler and Grosholz, forthcoming).Also, the plant canopy significantly restrictedwater flow and reduced velocity by up to 76 per-cent and bed stress relative to unvegetated areas(Neira et al. 2005, 2006). These reductions inlight and flow produced by the invasive Spartinacanopy were greater than those of native S. fo-liosa (Brusati and Grosholz 2006; Tyler andGrosholz, forthcoming), but they were compa-rable to those produced by Salicornia virginica,which can result in more substantial reductionin light than Spartina (Neira et al. 2005; Tylerand Grosholz, forthcoming).

The aboveground structure of Spartina inva-sion also led to increased sediment accretionrates and reduced sediment grain size (Neiraet al. 2006). Together with the buildup of be-lowground biomass and peat, this has resultedin increased tidal elevation of invaded areas.These changes are common to both SFB andWB. In areas of even moderate flow, unvege-tated mudflats experience rapid changes in ele-vation of up to four centimeters over periods asshort as a few weeks in comparison withchanges usually much less than one centimeterin vegetated areas. By reducing flow, Spartina at-tenuated these short-term changes in elevationresulting in a pattern of gradual increase in ele-vation relative to the adjacent unvegetated areas(E. D. Grosholz, unpublished data).

MICROALGAL PRODUCTION

The Spartina invasion has a substantial impacton benthic microalgal photosynthesis. In manyintertidal habitats, benthic microalgal produc-tion comprises a substantial proportion of over-all system primary production and is animportant contributor to local food webs(Zedler 1980, 1984; Page 1995; Deegan andGarritt 1997; Kwak and Zedler 1997; Page1997). This is especially true on Pacific Coastmudflats and in Salicornia-dominated marshes,where microalgae are the primary carbonsource for many secondary consumers (Kwakand Zedler 1997; Moseman et al. 2004). Theimpact of Spartina invasion on benthic microal-gae was variable across sites and is dependent tosome extent on the nature of the uninvadedhabitat. Where Spartina had invaded mudflatsin both SFB and WB, benthic chlorophyll a con-centration (a proxy for microalgal biomass) wasoften, but not always, higher in Spartina mead-ows than in the adjacent uninvaded mudflats(table 2.1; Neira et al. 2005, 2006; Tyler andGrosholz, forthcoming; A. C. Tyler et al., un-published data). However, microalgal produc-tion was consistently higher on the mudflats ofSFB than in the adjacent Spartina marshes.Factors such as light availability and grazing(see “Food Web Structure”) may create a dispar-ity between chlorophyll a–based standing stockand overall productivity. Overall, the Spartinainvasion had a negative impact on microalgalproductivity with important ramifications foroverall food web support.

NUTRIENTS AND ORGANIC MATTER

The invasion of Spartina resulted in a shift inthe overall cycling of organic matter and nutri-ents because of the refractory nature (highercarbon:nitrogen) of its tissues (A. C. Tyler et al.,unpublished data). Following the invasion ofWB, we observed an extensive accumulation ofdetritus associated with S. alterniflora litter thatoccurs primarily at the end of the growing sea-son when the aboveground portion died back.This detritus accumulated in massive heaps inthe high intertidal, where it slowly decomposed



and had detrimental effects on native vegetationplant biomass, aboveground productivity, andspecies richness (A. C. Tyler et al., unpublisheddata; Lambrinos, forthcoming).1 In SFB, be-cause hybrid Spartina decomposes more slowlythan native S. foliosa, more wrack build-up canbe attributed to the hybrid (A. C. Tyler et al., un-published data).

In addition to the high aboveground litterproduction, belowground production generateslarge volumes of roots, rhizomes, and peat,leading to an increase in belowground organicmatter and particulate organic carbon and nitro-gen relative to the native systems in both SFBand WB (table 2.1; Neira et al. 2006; Levin,Neira, and Grosholz 2006; A. C. Tyler et al., un-published data). We observed a subsequent in-crease in meadow sediment respiration ratesrelative to mudflats in SFB that fostered a shiftfrom a net autotrophic system, dominated bymicroalgal production, to a new heterotrophicsystem, dominated by belowground microbialdecomposition (table 2.1; Tyler and Grosholz,forthcoming). However, we found higher sedi-ment respiration rates in native vegetation thanin hybrid Spartina, most likely as a result of themore refractory nature of the Spartina detritusthat is a less desirable substrate for microbialdecomposers (Tyler and Grosholz, forthcom-ing). In all cases, the turnover of carbon and nu-trients is slowed down, resulting in theaccumulation of massive quantities of highly re-fractory organic matter.

In contrast to the dramatic increase in sedi-ment particulate nitrogen upon invasion of un-vegetated mudflats, we found a significantdecrease in available porewater ammonium ininvaded meadows compared to native mudflatsin both SFB and WB (A. C. Tyler, unpublisheddata). Possible causes for this decrease are plantuptake, increased microbial immobilization, orincreased coupling of nitrification-denitrifica-tion in the oxidized root zone of Spartina. Onthe Atlantic coast, the invasion of Phragmitesaustralis also caused distinct changes in nitro-gen cycling in sediments depending on the in-vaded community (Windham and Meyerson


2003). Even though hybrid Spartina is able toincrease the redox potential in the vicinity of itsroots, we observed an overall decrease in redoxpotential (Neira et al. 2005). Accordingly, ourresults from SFB also show that porewater sul-fide concentrations are nearly one hundredtimes greater in Spartina meadows relative touninvaded mudflats (meadow, 1,016 � 121 �

M; mudflat, 12 � 1 � M; mean � SE; A. C.Tyler, unpublished data; Neira et al. 2007),which is likely due to the increased organic mat-ter pool and subsequent increase in both micro-bial oxygen demand and sulfate reduction.

BENTHIC COMMUNITIES

The altered physical and chemical environ-ments can also strongly influence the recruit-ment, survival, growth, and reproduction ofbenthic invertebrates in the invaded areas. Bothepifaunal and infaunal organisms respond tothe changing light, flow, and sediment condi-tions in ways that affect not only the biomassand diversity of these organisms, but also thefunctional identity of many groups (Neira et al.2006).

Our work has shown significant changes inthe recruitment and growth of common taxa inthe hybrid Spartina meadows relative to unin-vaded areas. Measurements of barnacle(Balanus glandula) recruitment on standard-ized recruitment substrata (mussel shells)placed in the growing edge of hybrid Spartinameadow and on adjacent mudflat areasshowed recruitment was ninefold higher onthe mudflats (Neira et al. 2006). Experimentsusing marked Macoma petalum transplantedinto hybrid Spartina meadows, and adjacentmudflat areas showed growth was significantlyreduced by up to twofold in the hybrid Spartinatreatments (Brusati and Grosholz 2007). Ourresults suggest reductions in flow; thus, re-duced delivery of propagules (recruitment)and seston (for growth) likely contribute tothese patterns.

Our work has also shown that both biomassand diversity of infauna can decline stronglyin invaded areas relative to the previously

1 AddLambrinosto Refs.


unvegetated control areas (Neira et al. 2005,2007; Levin et al. 2006; Grosholz et al., forth-coming).2 In SFB, invertebrate densities declineby as much 75 percent relative to unvegetatedmudflat (Neira et al. 2005), although densitiesat some sites are not significantly different fromthose in native Salicornia virginica areas.Species richness also showed a significant 25percent decline in Spartina invaded areas com-pared with unvegetated controls, but it was ele-vated relative to Salicornia-vegetated habitat(Neira et al. 2005).

Similar patterns were measured in WB,where invertebrate species richness was signifi-cantly higher in mudflat/Zostera areas than inS. alterniflora areas (mudflat, 11.75 � 2.62;Spartina, 6.0 � 3.12; mean � 1 SE; per 19.6square centimeter). Species diversity was alsohigher in the mudflat/Zostera areas relative tothe Spartina meadow (Shannon-Wiener H�

[log2] � 3.92, mudflat; 2.79, Spartina), and thedensity of invertebrates was slightly greater inmudflat/Zostera areas, although not signifi-cantly so.

In SFB, we experimentally investigated themechanisms underlying these changes in a se-ries of transplant experiments, plant manipula-tions, predator inclusion and exclusion studies,and trophic investigations. This work demon-strated that the changes in the density and di-versity of infauna were due to the combinedeffects of preemption of belowground habitat bySpartina, changes in the food supply and preda-tion pressure, as well as the physical and chem-ical changes to sediments and porewater (Neiraet al. 2006; Levin et al. 2006). For these rea-sons, the effects of Spartina on benthic abun-dance and diversity are less dramatic in areaspreviously occupied by native marsh plants(Neira et al. 2005).

FACILITATING OTHER INVASIVE SPECIES

The aboveground structure of Spartina can haveother positive effects, including facilitatinghigher densities of other invasive species. InSFB, our data suggest that the invasive hybridhas facilitated several nonindigenous inverte-

brate species, creating invasive hot spots (areasof greater abundance) in the recently colonizedSpartina edge areas not present on the openmudflat. At one site in SFB, we found that den-sities of several clams introduced from theAtlantic (Macoma petalum, Mya arenaria,Geukensia demissa) were two to ten times higherin the growing edge of the hybrid Spartinameadow than on the adjacent open mudflat (E.D. Grosholz et al., unpublished data). Althoughhigh Geukensia densities were largely due to therequirement of structure for attachment pro-vided by Spartina (similar structure is virtuallyabsent on open mudflats), densities of Mya andMacoma may be higher as the result of refugefrom predation by bat rays (Myliobatus califor-nica). At one site where greater than 40 percentof the substrate was disturbed by bat rays, den-sities of Mya and Macoma were two to threetimes greater in the growing edge of Spartinacompared with adjacent mudflats. At a secondsite with less than 1 percent of the area dis-turbed by bat rays, there was no difference inclam densities between Spartina and mudflats(E. D. Grosholz et al., unpublished data).

In SFB, we also found high abundances of introduced Atlantic gastropods Urosalpinxcinerea and Ilyanassa obsoleta along the leadingedge of the hybrid Spartina. In experimentswhere we simulated the aboveground structureof Spartina by adding wooden dowels to mud-flat areas, we found twenty- to fiftyfold increasesin the density of both Urosalpinx and Ilyanassain dowel addition treatments compared withadjacent mudflat control areas (E. D. Grosholzet al., unpublished data). Data documentingsediment temperatures in dowel addition areassuggest that lower sediment temperatures maystrongly influence these patterns.

We have also documented that the hybrid fa-cilitates the European green crab Carcinus mae-nas in SFB. Our data show that this species isthree to five times more abundant, particularlyfor smaller size classes, in hybrid in compari-son with the adjacent mudflat (E. D. Grosholzet al., unpublished data; Neira et al. 2006). Thispredator, in turn, appears to have a significant


2 Add thelast work toRefs.


impact on the invertebrate taxa that are nega-tively affected by Spartina invasion and so mayreinforce the changes brought about by thisplant invasion (Neira et al. 2006). The extent towhich Spartina facilitates other invasive speciesin WB is less certain. However, evidence sug-gests that Spartina fills a similar role facilitatingyounger size classes of green crabs (Yamada2001).

We summarize the generalized effects ofabove- and belowground portions of Spartinaon invertebrate diversity and abundance intable 2.2. The growing edge of the hybridSpartina meadow that had been colonizedwithin approximately five years functions simi-larly to the native S. foliosa and has a similar in-fluence on invertebrate abundance anddiversity. In this growing margin, the above-ground structure has the same generally posi-tive effects on invertebrates, but thebelowground portion of the hybrid has not de-veloped sufficiently to reduce infaunal densi-ties. In areas farther back from the growingedge, which are approximately five to ten yearsold, changes in sediment biogeochemistry andbelowground biomass have progressed to thepoint of significantly depressing densities anddiversity of infauna (Neira et al. 2005).Therefore, we suggest that the influence of hy-brid Spartina on benthic communities varieswith the successional stage of the invasion(table 2.2; Neira et al. 2007).

FOOD WEB STRUCTURE

The structure of benthic food webs was also af-fected by the changes in vascular plant and litter

availability relative to other food sources. Weused stable isotope enrichment experiments tofollow consumption of Spartina detritus andmicroalgae by invertebrates and to determinethe broader effects of Spartina invasion on ben-thic food web structure. Using 15N-labeledSpartina detritus and 13C-labeled microalgae si-multaneously, we found that the Spartina inva-sion in SFB has dramatically shifted the tidalflat infaunal invertebrate community from onedominated by surface feeders that primarilyconsume microalgae (amphipods, bivalves) toone dominated by belowground feeders thatprimarily consume plant detritus (oligochaetes,capitellid polychaetes) (Levin et al. 2006).Using two- and three-end-member mixingmodels, we determined that a significant por-tion of the diet of these belowground detriti-vores was the detritus produced by hybridSpartina. Therefore, this invasion has resultedin a qualitative shift of the entire food web fromone based on fresh primary production to onebased on detritus. We summarize these overallresults of these changes on invertebrate func-tional groups in table 2.3.

When we compare these results with thosefrom native Spartina areas that have not beeninvaded, we note some important differences.Natural abundance stable isotope studies con-ducted in native versus hybrid Spartina areasshow little incorporation of the added detritusinto the food web. Larger epifauna in hybridareas did not show � 13C values consistent withthe added detrital input of Spartina when com-pared with organisms collected from openmudflat habitats, though there was a slight


TABLE 2.2 A comparison of the effects of both above- and belowground structure for invasive versus native Spartina on

overall abundance and diversity of benthic invertebrates relative to unvegetated mudflats

invasive spartina native spartina

Growing Edge Developed Meadow Growing Edge Developed Meadow

Aboveground Increase Increase Increase IncreaseBelowground Slightly decrease Decrease Minimal Slightly decrease

NOTE: The growing edge areas for both are areas colonized within the last five years approximately and the developed meadows areasthat have had vegetation for at least ten years (from Brusati and Grosholz 2006; Neira et al. 2007).


isotopic shift toward Spartina in invertebratescollected in native S. foliosa meadows com-pared with those on the open mudflat (Brusatiand Grosholz 2007). This is also consistentwith the idea that the detritus of S. foliosa is lessrefractory than that of the hybrid Spartina detri-tus, and benthic invertebrates may consumemore detritus of the native than invasiveSpartina. However, a comparison of ingestionof 15N-labeled S. foliosa and 15N-labeled hybridSpartina in SFB indicated mostly similar infau-nal uptake (oligochaetes and capitellid poly-chaetes) or avoidance patterns (Levin et al.2006).

We investigated food web changes in WBusing similar isotopic enrichment experiments.We found that the taxonomic range of benthicspecies that consumed detritus of Spartina al-terniflora was similar to SFB (E. D. Grosholzet al., unpublished data). We found that tanaids,bivalves, spionid and cirratulid polychaetes, andchironomid larvae all showed enriched signalsin treatments with Spartina detritus in theSpartina zone (E. D. Grosholz et al., unpub-lished data). Based on elevated � 15N values (30to 80 per mille), we found significantly moreSpartina detritus was consumed in the Spartinazone than in mudflat/Zostera zone treatments.As in the SFB study, we found that � 13C values(15 to 50 per mille) were higher for surfacefeeders including amphipods, tanaids, andcirratulid polychaetes, with values similar inboth Spartina and mudflat/Zostera zone treat-ments. Although we see some differences be-tween food web impacts in SFB and WB, thesedo not appear to be due to differences in

palatability since the carbon:nitrogen ratios ofS. alterniflora relative to the hybrid are similar(WB � 46.0 � 1.9; SFB � 48.4 � 1.8, and therewas no difference in percent nitrogen; A. C.Tyler, unpublished data). Instead, the differ-ences may reflect the much longer history of in-vasion in WB (nearly one hundred years) or thepresence of extensive Zostera cover and detritusinput in what was historically an unvegetatedmudflat. We found that the detritus of the intro-duced Z. japonica was consumed to a muchgreater extent than Spartina in the WB experi-ments based on enriched � 15N signatures. Awide range of surface-feeding consumers in-cluding several bivalves and terebellid poly-chaetes showed elevated � 15N values with muchgreater values (100 to 500 per mille), support-ing the higher edibility of Zostera relative toSpartina based on the lower carbon:nitrogenratio (Z. japonica carbon:nitrogen 17.3 � 0.7;A. C. Tyler, unpublished data).

VERTEBRATE CONSUMERS

The expansion of hybrid Spartina has also influ-enced grazing of cordgrasses by Western Canadageese (Branta canadensis moffitti) in SFB. Ourstudies have shown that the geese can distin-guish differences in blade toughness betweenthe native and hybrid forms of Spartina and com-pletely avoid the hybrid while readily consumingthe native S. foliosa. Data from both field studiesand feeding trials using captive geese haveshown that geese will graze more than 90 per-cent of the S. foliosa biomass at some sites whilegrazing less than 1 percent of the hybrid (E. D.Grosholz et al., unpublished data).


TABLE 2.3 A summary of predicted effects of aboveground and belowground invasive

Spartina on densities of different functional groups of benthic invertebrates

Aboveground Belowground

Mobile epifauna Positive NoneSurface-feeding infauna Negative NegativeDetrital-feeding infauna Positive NegativeBivalves Positive/negative Negative

SOURCES: From Neira et al. (2005, 2006); Levin et al. (2006); Brusati and Grosholz (2006, 2007); E. D. Grosholz, unpublished data.


The Spartina invasion may also have impor-tant implications for wintering populations ofmigratory shorebirds. Most shorebirds will notforage in vegetated areas (Page, Stenzel, andKjelmyr 1999; Stenzel et al. 2002), so the colo-nization of naturally unvegetated mudflats byinvasive Spartina is a de facto loss of foraginghabitat (fig. 2.2). Also, our data show that thebiomass of invertebrates is greater in tidal flatareas at higher tidal elevations (Christiansenet al., forthcoming). Therefore, as the Spartinainvasion expands to occupy a greater portion ofthese higher-elevation areas, shorebirds will beincreasingly forced to forage at lower tidal eleva-tions, which are not only exposed for shorter pe-riods of time, but also contain lower densities ofinvertebrate prey.

The consequences of Spartina invasion forshorebirds apply to WB as well. Although SFBis a more important area for wintering shore-birds, WB and adjacent Gray’s Harbor repre-sent important winter grounds in that regionfor shorebirds (Page et al. 1999). Nonetheless,the same overall consequences of habitat lossapply, although we do not have similar data onthe abundances of benthic invertebrates at dif-ferent tidal elevations. The Spartina influence

in WB is also complicated by the extensive inva-sion of lower tidal elevations by the Japaneseeelgrass Z. japonica, which during the summermonths covers virtually the entire tidal rangefrom the lower border of Spartina to the upperborder of the native Zostera marina.

In contrast to shorebirds that forage on tidalflats at low tide, estuarine fish forage in thesesame areas at high tide. Fish such as Chinooksalmon, California halibut, rainwater killifish,striped bass, and Tule perch could potentiallyexperience the same habitat losses and densityeffects in SFB and WB as the shorebirds.

PREDICTING IMPACTS OF INVASION

We can identify three distinct invasion scenar-ios where Spartina effects appear to differ. Thefirst is the invasion of unvegetated, higher-en-ergy sand flats, which results in the largestchanges in flow rates, sediment accumulation,elevation increase, and litter buildup, as well asthe largest changes in plant and animal com-munities. This type of invasion has occurred inportions of both SFB and WB. A second type in-volves invasion of existing vegetation in highmarsh habitats, which results in less alteration


FIGURE 2.2 Hybrid Spartina colonizing open mudflat and preempting foraging habitatused by wintering populations of migratory shorebirds in San Francisco Bay.


of benthos and in some cases leads to enhanceddiversity of associated fauna (which are often in-vasives as well) (Neira et al. 2005). Under thesecircumstances, displacement of native plantsmay occur through light/space or nutrient com-petition (Tyler et al. 2007). A third mode of in-vasion involves hybridization with nativeSpartina, threatening the integrity of nativeSpartina species (Ayers et al. 2003) and alteringthe above- and belowground habitat structure.Understanding that Spartina invasions canyield different consequences under differentcircumstances can help identify the most ur-gent conservation needs (Thompson 1991;Hacker et al. 2001; Hacker and Dethier 2006).

The changes caused by Spartina invasioncan be viewed within the broader context ofubiquitous plant effects on wetland benthos.Plants have been recognized as ecosystem engi-neers (or foundation species) with major influ-ence on the structure of marine communities,independent of invasion status (Levin andTalley 2000;3 Crooks 2002). The generalized in-

fluences of introduced plants on the benthoscan be partitioned into two major pathways. Weidentify the details of these pathways and thetargets in figure 2.3 and illustrate these pointsusing the changes produced by Spartina.

The first pathway involves the indirect ef-fects of plants on benthic organisms mediatedthrough several changes in abiotic processes.First, reduced flow due to increased above-ground biomass generally reduces systemenergy; increases sediment stability, sedimen-tation rates, and organic matter accumulation;and reduces fluxes of reproductive propagulesand food particles for consumers. Second,reduced light, also due to increased above-ground biomass, results in reduced evapora-tion and lower levels of sediment porewatersalinity, sediment temperature, and higherwater content. Third, plant belowground struc-tures influence soil geochemical conditions(via root transport of oxygen, litter buildup anddegradation), exploit space, and mechanicallyanchor sediments.


FIGURE 2.3 Conceptual model of changes following Spartina invasion. The many changes broughtabout by the Spartina invasion are illustrated in this diagram showing positive (�) and negative (�)effects on a range of physical, chemical, and biological processes. Spartina reduces light and tidalwater flow and increases deposition of fine sediments and sediment organic matter. The increasedbelowground biomass together with changes in the sediments results in increased levels of sulfideand decreased ammonium levels, which can negatively affect other plants and animals. These changesresult in increasing detrital loads and decreasing productivity of benthic microalgae, which favorsubsurface deposit feeders and detritivores at the expense of grazers, suspension feeders, and surfacedeposit feeders. The shift toward smaller, subsurface species may reduce invertebrate food resourcesfor larger consumers such as crabs, birds, and fishes.

3 Please addLevin &Talley to the Refs.


The second pathway involves direct effectson benthic invertebrates mediated by thestructural habitat they provide. Introducedplants can provide substrate for sessileepibionts, both plant and animal, simply bytheir presence in benthic habitats such asmudflats with limited emergent structure.Plants can also provide refugia for mobilepredator and prey species, both infaunal andepifaunal, as well as provide living plant tissuefor herbivores or litter for detritivores (Levinet al. 2006; Neira et al. 2006).

COMPARISONS WITHIN THE PACIFIC REGION

To understand the overall effects of Spartina onbenthic communities, we first compare our re-sults with recent work on the benthic impacts ofnative S. foliosa. Studies comparing invertebratecommunities in native versus invasive Spartinameadows in SFB showed that the nativeSpartina positively affects invertebrate abun-dance and, to a lesser extent, diversity in com-parison to the largely negative effects ofthe hybrid (Brusati and Grosholz 2006).Invertebrate densities were up to five timesgreater in S. foliosa at some sites, although themagnitude of the effect was variable. This islargely the result of positive effects of above-ground structure but much lower belowgroundbiomass. The density of roots and rhizomes ap-parently was not sufficient to reduce infaunalabundance as the hybrid does (see table 2.1).Recent removal and shading experiments con-ducted in southern California (Whitcraft andLevin 2007) suggest S. foliosa controls mac-robenthic abundance and composition throughlight effects, which moderate soil temperatureand salinity, enhance water retention, and pro-mote microalgal growth.

This positive effect of S. foliosa on benthicfauna parallels what we see in the initial stagesof the hybrid Spartina invasion along the grow-ing edge. Within the first few meters of a hybridclone, plant densities and belowground bio-mass are similar to S. foliosa areas resulting in

the same facilitation of species abundance. This“edge effect” is similar to the increases in ben-thic abundance documented at the edges of sea-grass meadows relative to the center (Bolognaand Heck 2002). However, within five to tenyears, the increasingly large above- and below-ground biomass of the hybrid starts to reducethe benthic diversity and abundance throughhabitat changes at the surface and preemptionof habitat space belowground.

Our results from SFB and WB showingstrong effects of Spartina invasion on benthicanimal communities are broadly consistentwith other studies of Spartina in the westernUnited States. Other studies in WB have shownreduced infaunal diversity and abundance inthe middle of Spartina meadows (Zipperer19964; Dumbauld et al. 1994; O’Connell2002). and negative effects on bivalve growth(Ratchford 1995). Interestingly, other WB stud-ies have also documented an “edge effect” withincreased diversity and abundance of some taxain the growing edge of the Spartina marsh.Dumbauld et al. (1994) found increased abun-dances of introduced clams (Mya) withinSpartina meadows in WB. Zipperer (2002),also working in the same area, found increasedabundances of infaunal invertebrates in thenewly growing Spartina border. The facilitativeeffects of S. alterniflora in WB are again similarto what we find for both S. foliosa and for thegrowing edge of the hybrid Spartina invasion inSFB.

Our results showing dramatic shifts in thetrophic mode of infaunal invertebrates follow-ing Spartina invasion are also in agreementwith results from other studies in the U.S. WestCoast region. In WB, Cordell et al. (1998)found a shift from surface-feeding bivalves andamphipods to deposit feeders and insect preda-tors within the Spartina meadows. Also in WB,trophic shifts were documented by O’Connell(2002), who found increases in belowgrounddetritivores in S. alterniflora marshes, consis-tent with our findings. Also, both Zipperer(1996) and Dumbauld et al. (1994) found re-duced densities of bivalves and other surface


4 AddZipperer‘96 to Refs.


feeders within Spartina clones and increasingnumbers of larval insects in areas with highertidal elevation as the community moved towarda more terrestrial assemblage.

Finally, many of the changes we have mea-sured in the sediment ecosystem have alsobeen documented following the invasion ofSpartina anglica in Australia, England, and thePuget Sound region of Washington State. InAustralia, Hedge and Kriwoken (2000) foundthat both the diversity and abundance of inver-tebrates were not significantly different be-tween S. anglica–invaded areas and naturallyvegetated marsh, but there was reduced diver-sity and abundance of invertebrates on nearbymudflats. In England, S. anglica has lowereddensities of bivalves and Corophium and en-hanced densities of tubificid oligochaetes rela-tive to mudflat settings (Jackson 1985), with anoverall effect of reduced species richness (Fridand James 1989). Studies of S. anglica invasionin Washington by Reeder and Hacker (2004)and Hacker and Dethier (2006) at sites withvarying substrate and salinity found above- andbelowground biomass varied substantially withhabitat type, as did sediment accretion rates,sediment water content, salinity, and redox po-tential. In their mudflat and high-salinitymarshes (most similar to our studies), sedi-ment salinity was lower and water content washigher in the presence of invasive S. anglica.However, they found a predictable increased inredox potential in areas invaded by S. anglica,in contrast to our data showing lower redox inareas with hybrid Spartina. This difference isexpected based on studies by Maricle and Lee(2001), who showed that S. anglica transportsoxygen to their roots much more effectivelythan S. alterniflora.

COMPARISONS WITH OTHER REGIONS

Studies from the native range of S. alterniflorahave also shown that Spartina strongly influ-ences the diversity and abundance of benthicspecies. Several studies from the Atlantic andGulf coasts of the United States have generally

shown a positive effect of S. alterniflora on theabundance of invertebrates relative to unvege-tated sediments (Rader 1984; LaSalle, Landin,and Simms 1991; West and Williams 1986).Similar results have been shown in studies ofnative Spartina alterniflora effects on infaunamarshes in Brazil (Lana and Guiss 1991; Nettoand Lana 1991).

Shifts in trophic modes have also been mea-sured in studies from the native range of S. al-terniflora. Declines in the abundance ofsurface-feeding bivalves has been demonstratedin the native range of Spartina alterniflora in theeastern United States (Capehart and Hackney1989), as have changes in trophic modes of in-fauna with successional stage of Spartina areas(Kneib 1984). Declines in suspension feeders inSpartina areas in comparison with open mud-flats have also been documented in the nativeSouth American range of S. alterniflora (Lanaand Guiss 1991).

Finally, other studies have also shownimpacts at higher trophic levels involvingvertebrate consumers. In perhaps the best-documented study of impacts of invasiveSpartina on shorebirds, Goss-Custard andMoser (1988) showed significant declines in thenumbers of Dunlin (Calidris alpina) in estuariesin the United Kingdom that had been invadedby S. anglica.

Overall, the conclusions from studies ofSpartina in its native range suggest that it gen-erally has a positive effect on the diversity andabundance of native benthos. This provides aninteresting contrast with the largely negative ef-fects of Spartina in the introduced range. Onetheory for opposing effects of Spartina on thetwo coasts is that predation pressure is consid-ered much greater in Atlantic coastal systems(e.g., due to the presence of blue crabs, horse-shoe crabs); thus, Spartina stands are morelikely to function as refugia on the Atlanticcoast. The much higher animals densities onPacific than Atlantic mudflats supports thishypothesis (Levin, Talley, and Hewitt 1998).These findings are broadly consistent with ourfinding that Spartina tends to facilitate many



species that have evolved within its native rangeand thrive in the microenvironment producedby this plant, but it negatively affects manyspecies that have evolved in systems devoid oflarge vascular plants like Spartina and that gen-erally do not tolerate the changed conditions.

PROSPECTS FOR ERADICATION AND RECOVERY

Extensive Spartina eradication programs arecurrently being carried out in SFB and WB(fig. 2.4). In both bays, the primary means oferadication is aerial and boat-based spraying ofthe commonly used herbicide Imazypyr(known as “Arsenal”). The expectation is thatcomplete eradication is a reality with sufficienteffort invested over a long enough period oftime. The goal in each case is restoration to thepreinvasion condition. It is clear that some ofthe changes can be rapidly reversed. By remov-ing the aboveground portion of the plant withherbicide, eradication efforts will be able to lo-cally reverse the immediate physical modifica-tion of flow, light, and sedimentation. Our datasuggest the aboveground contribution to addeddetrital buildup following eradication will berelatively short-lived. In areas that were previ-ously vegetated by native plants, there is the ex-pectation that native species will recolonizesuccessfully, although additional efforts may beneeded to jump-start this process in some

areas. The short-lived seed bank of the invasiveSpartina provides hope that once eradicationfrom large areas has occurred, it will be main-tained notwithstanding dispersal from otherareas. However, this will take vigilance in re-moving Spartina seedlings.

Our work in areas that have undergone trialeradication or natural dieback suggests thatthere are more lasting effects of the roots andrhizomes that may require several years to de-compose (Neira et al. 2007; A. C. Tyler and E. D.Grosholz, unpublished data). The rate of break-down appears to be dependent on rates of flush-ing, sediment grain size, and other local habitatvariables. The decay of belowground biomassand the sulfide and anoxia that result can slowthe return of sediment conditions that wouldpermit reestablishment of native plants and an-imals. Also, the increased tidal elevation createdby enhanced accretion in invasive Spartinastands may not be quickly reversed. Because theincreased elevation reduces tidal inundation,the mat of roots and rhizomes may continue tomaintain the increased tidal elevation and sub-stantially delay recovery. In some areas, if nativeplants colonize prior to the return of sedimentto its preinvasion elevation, there may be a per-manent shift from intertidal mudflat to vege-tated tidal marsh, as has been documentedfollowing eradication of S. anglica in PugetSound, Washington (Reeder and Hacker 2004;Hacker and Dethier 2006).


FIGURE 2.4 Ongoing eradication of Spartina alterniflora at a higher tidal elevation site in Willapa Bay, Washington.


However, there is room for optimism basedon our monitoring of sites in WB that had beentreated with herbicide seven years earlier. Ourdata indicate that recovery of sediment charac-teristics and porewater chemistry as well as in-vertebrate community indices can be achievedwithin six years and possibly faster (E. D.Grosholz and A. C. Tyler, unpublished data).However, these treated areas were small, iso-lated clones in relatively sandy sediments. Inlarge continuous meadows or in muddier sedi-ments, we predict that the recovery rate for na-tive plants will be similar to that following S.anglica eradication (Reeder and Hacker 2004).

OVERALL CONCLUSIONS

Introductions of nonnative species are clearlyamong the most pervasive anthropogenicchanges in salt marsh systems and threaten toalter their structure and function on a broadscale. Our work has documented that Spartinainvasions in two major estuaries in westernNorth America are rapidly changing a widerange of physical, chemical, and biologicalprocesses. First, there are immediate changes torates of light penetration, water flow, and sedi-mentation that then more gradually influencesediment physicochemistry as well as recruit-ment, growth, and survival of benthic organ-isms. The Spartina invasion has shifted thedominant primary producers from short-stature native plants and benthic microalgae toa tall, dense plants that create approximatelytwo kilograms per square meter of refractoryaboveground detritus annually. This change re-sults in a less “available” food source and slowsdown carbon and nutrient recycling. Thesechanges in turn result in dramatic shifts in ben-thic communities and food web structure.

In San Francisco Bay, our studies support theidea that this changing resource base appears tohave contributed to a shift in benthic communi-ties from surface feeders to subsurface feeders.The shifts in benthic communities may alsohave consequences for higher trophic levels(fig. 2.5). Within the Spartina meadow, the

reduced densities of larger, surface-feeding in-vertebrates and increase in smaller infaunal de-tritivores may reduce the food base available tobirds, fishes, and crabs. The presence of the in-vasive grass itself may also negatively affect win-tering shorebirds by reducing the quality andavailability of foraging areas on open tidal flats.

Reversing the changes brought about by theSpartina invasion will require extensive man-agement resources over a significant period oftime. But our results provide reason for opti-mism regarding the success of recovery follow-ing eradication efforts. While completeeradication of Spartina in these systems may re-quire several years of follow-up efforts, the elim-ination of most of the aboveground biomassand the decay of belowground biomass appearto begin within just a few years of the initialtreatment. Our limited evidence suggests thatthese systems can return to something similarto the preinvasion state within approximatelyfive years and possibly sooner. However, wehave now documented that these changes arehabitat-specific and that many factors such astidal exchange, sediment grain size, elevation,and other variables will strongly affect the rateat which the system can recover (Reeder andHacker 2004).

Finally, our work provides examples of themany different kinds of effects that plants canhave in estuarine systems. By altering hydrody-namics, sediment geochemistry, productivity,


FIGURE 2.5 Federally endangered California clapper rails(Rallus longirostris obsoletus) are impacted by the hybridSpartina invasion in San Francisco Bay.


and sedimentation regimes—through food webmodification and via substrate provision, stabi-lization, and refuge—invasive cordgrasses arecertainly among the foremost agents of land-scape-scale change in the coastal zone.

Acknowledgments. We would like to thank R.Blake, U. Mahl, C. Whitcraft, N. Christiansen, N.Rayl, E. Brusati, S. Norton, C. Love, A. Carranza,G. Mendoza, C. Whitcraft, D. Chiang, M. Young,S. Maezumi, P. McMillan, and J. Gonzalez forassistance with laboratory and/or fieldwork inSan Francisco and Willapa bays. Our thanks to D.Ayres and D. Strong for verifying Spartina hybridgenotypes in San Francisco Bay. We appreciatethe timely and accurate stable isotope analysesprovided by D. Harris and the University ofCalifornia, Davis, stable isotope facility. We alsothank C. Nordby, R. Blake, and E. Brusati forproviding compliance with California clapper railpermit requirements in San Francisco Bay.Thanks also to B. Couch for providing air boatservices in Willapa Bay. We greatly appreciatethe comments of Brian Silliman and twoanonymous reviewers, which helped improvethe chapter. This work was provided by theNational Science Foundation BiocomplexityProgram (DEB 0083583) to E.D.G. and L.A.L.

REFERENCES

Ayres, D. R., D. L. Smith, K. Zaremba, S. Klohr, andD. R. Strong. 2004. Spread of exotic cordgrassesand hybrids (Spartina sp.) in the tidal marshes ofSan Francisco Bay. Biological Invasions 6: 221–231.

Ayres, D. R., D. R. Strong, and P. Baye. 2003.Spartina foliosa (Poaceae): A common species onthe road to rarity. Madroño 50: 209–213.

Ayres, D. R., K. Zaremba, and D. R. Strong. 2004.Extinction of a common native species by hy-bridization with an invasive congener. WeedTechnology 18: 1288–1291.

Bologna, P. A. X., and K. L. Heck. 2002. Impact ofhabitat edges on density and secondary produc-tion of seagrass-associated fauna. Estuaries 25:1033–1044.

Bruno, J. F., J. J. Stachowicz, and M. D. Bertness.2003. Inclusion of facilitation into ecological the-ory. Trends in Ecology and Evolution 18: 119–125.

Brusati, E. D., and E. D. Grosholz. 2006. Native and introduced ecosystem engineers produce

contrasting effects on estuarine infaunal commu-nities. Biological Invasions 8: 683–695.

———. 2007. Effect of native and invasive cordgrasson Macoma petalum density, growth, and isotopicsignatures. Estuarine, Coastal and Shelf Science 71:517–522.

California Coastal Conservancy. 2006. San Franciscoestuary invasive Spartina project. Project Website: http://www.spartina.org/about.htm.

Capehart, A. A., and C. T. Hackney. 1989. The potentialrole of roots and rhizomes in structuring salt-marsh benthic communities. Estuaries 12: 119–122.

Chapin, F. S., III, E. S. Zavaleta, V. T. Eviner, R. L.Naylor, P. M. Vitousek, H. L. Reynolds, D. U.Hooper, S. Lavorel, O. E. Sala, S. E. Hobbie, M. C.Mack, and S. Diaz. 2000. Consequences ofchanging biodiversity. Nature 405: 234–242.

Christiansen, N. C., E. D. Grosholz, and P. Rosso.Forthcoming. Quantifying the potential impact ofthe Spartina invasion on invertebrate food re-sources for foraging shorebirds in San FranciscoBay. In Proceedings of the Third Annual InvasiveSpartina Conference. Cambridge: CambridgeUniversity Press.5

Civille J. C., K. Sayce, S. D. Smith, and D. R. Strong.2005. Reconstructing a century of Spartina al-terniflora invasion with historical records and con-temporary remote sensing. Ecoscience 12:330–338.

Cohen, A. N., and J. T. Carlton. 1998. Accelerating in-vasion rate in a highly invaded estuary. Science279: 555–558.

Cordell, J. R., C. A. Simenstad, B. Feist, K. L. Fresh, R.M. Thom, D. J. Stouder, and V. Luiting. 1998.Ecological effects of Spartina alterniflora invasionof the littoral flat community in Willapa Bay,Washington. Abstracts from the Eighth Intern-ational Zebra Mussel and Other Nuisance SpeciesConference, Sacramento, California, March 16–19,http://www.sgnis.org/publicat/7307.htm.

Crooks, J. A. 2002. Characterizing ecosystem-levelconsequences of biological invasions: The role ofecosystem engineers. Oikos 97: 153–166.

Daehler, C. C., and D. R. Strong. 1997. Hybridizationbetween introduced smooth cordgrass (Spartinaalterniflora; Poaceae) and native California cord-grass (S. foliosa) in San Francisco Bay, California,USA. American Journal of Botany 84: 607–611.

Davis, H. G., C. M. Taylor, J. C. Civille, and D. R.Strong. 2004. An Allee effect at the front of aplant invasion: Spartina in a Pacific estuary.Journal of Ecology 92: 321–327.

Deegan, L. A., and R. H. Garritt. 1997. Evidence forspatial variability in estuarine food webs. MarineEcology Progress Series 147: 31–47.


5 If pub-lished now,update w/year, editors,pages, andverify pub-lisher.


Dethier, M. N., and S. D. Hacker. 2005. Physical fac-tors vs. biotic resistance in controlling the inva-sion of an estuarine marsh grass. EcologicalApplications 15: 1273–1283.

Dumbauld, B. R., M. Peoples, L. Holcomb, J. Tagart,and S. Ratchford. 1994. The potential influence ofcordgrass Spartina alterniflora on clam resourcesin Willapa Bay, Washington. Journal of ShellfishResearch 14: 228.

Feist, B. E., and C. A. Simenstad. 2000. Expansionrates and recruitment frequency of exotic smoothcordgrass, Spartina alterniflora (Loisel), coloniz-ing unvegetated littoral flats in Willapa Bay,Washington. Estuaries 23: 267–274.

Frid, C., and R. James. 1989. The marine invertebratefauna of a British coastal salt marsh. HolarcticEcology 12: 9–15.

Goss-Custard, J. D., and M. E. Moser. 1988. Rates ofchange in the numbers of dunlin, Calidris alpina,wintering in British estuaries in relation to thespread of Spartina anglica. Journal of AppliedEcology 25: 95–109.

Hacker, S. D., and Dethier, M. N. 2006. Communitymodification by a grass invader has differing im-pacts for marine habitats. Oikos 113: 279–286.

Hacker, S. D., D. Heimer, C. E. Hellquist, T. G.Reeder, B. Reeves, T. J. Riordan, and M. N.Dethier. 2001. A marine plant (Spartina anglica)invades widely varying habitats: Potential mecha-nisms of invasion and control. Biological Invasions3: 211–217.

Hedge, P., and L. K. Kriwoken. 2000. Evidence for ef-fects of Spartina anglica invasion on benthicmacrofauna in Little Swanport estuary, Tasmania.Austral Ecology 25: 150–159.

Jackson, D. 1985. Invertebrate populations associatedwith Spartina anglica salt-marsh and adjacent in-tertidal mud flats. Estuary and BrackishwaterScience Association Bulletin 40: 8–14.

Kneib, R. T. 1984. Patterns of invertebrate distribu-tion and abundance in the intertidal salt marsh:Causes and questions. Estuaries 7: 392–412.

Kwak, T. J., and J. B. Zedler. 1997. Food web analysisof southern California coastal wetlands usingmultiple stable isotopes. Oecologia 110: 262–277.

Lana, P. D., and C. Guiss. 1991. Influence of Spartinaalterniflora on structure and temporal variabilityof macrobenthic associations in a tidal flat ofParanagua Bay (southeastern Brazil). MarineEcology Progress Series 73: 231–244.

LaSalle, M. W., M. C. Landin, and J. G. Simms. 1991.Evaluation of the flora and fauna of a Spartina al-terniflora marsh established on dredged materialin Winyah Bay, South Carolina. Wetlands 11:191–208.

Levin, L. A., C. Neira, and E. D. Grosholz. 2006.Invasive cordgrass modifies wetland trophic func-tion. Ecology 87: 419–432.

Levin, L., T. Talley, and J. Hewitt. 1998. Macrobenthosof Spartina foliosa (Pacific cordgrass) saltmarshesin southern California: Community structure andcomparison to a Pacific mudflat and a Spartinaalterniflora (Atlantic smooth cordgrass) marsh.Estuaries 21: 129–144.

Mack, R. N., D. Simberloff, W. M. Lonsdale, H. Evans,M. Clout, and F. A. Bazzaz. 2000. Biotic inva-sions: Causes, epidemiology, global consequences,and control. Ecological Applications 10: 689–710.

Maricle, B. R., and R. W. Lee. 2002. Aerenchyma de-velopment and oxygen transport in the estuarinecordgrasses Spartina alterniflora and S. anglica.Aquatic Botany 74: 109–120.

Mooney, H. A., and R. J. Hobbs. 2000. Invasive speciesin a changing world. Washington, DC: Island.

Moseman, S., L. Levin, C. Currin, and C. Forder.2004. Infaunal colonization, succession and nu-trition in a newly restored wetland at TijuanaEstuary, California. Estuarine, Coastal and ShelfScience 60: 755–770.

Neira, C., E. D. Grosholz, L. A. Levin, and R. Blake.2006. Mechanisms generating modification ofbenthos following tidal flat invasion by a Spartina(alterniflora � foliosa) hybrid. Ecological Applica-tions 16: 1391–1404.

Neira, C., L. Levin, and E. D. Grosholz. 2005. Benthicmacrofaunal communities of three sites in SanFrancisco Bay invaded by hybrid Spartina, withcomparison to uninvaded habitats. Marine EcologyProgress Series 292: 111–126.

Neira, C., L. A. Levin, E. D. Grosholz, and G.Mendoza. 2007. The influence of invasiveSpartina growth phases on associated macrofau-nal communities. Biological Invasions 9: 975–993.

Netto, S. A., and P. C. Lana. 1999. The role of above-and below-ground components of Spartinaalterniflora (Loisel) and detritus biomass in struc-turing macrobenthic associations of ParanaguáBay (SE Brazil). Hydrobiologia 400: 167–177.

O’Connell, K. A. 2002. Effects of invasive Atlanticsmooth-cordgrass (Spartina alterniflora) on infau-nal macroinvertebrate communities in southernWillapa Bay, WA. Unpublished MS thesis,Western Washington University, Bellingham.

Page, H. M. 1995. Variation in the natural abundanceof 15N in the halophyte, Salicornia virginica, asso-ciated with groundwater subsidies of nitrogen ina southern California salt-marsh. Oecologia 104:181–188.

———. 1997. Importance of vascular plant and algalproduction to macro-invertebrate consumers in a



southern California salt marsh. Estuarine, Coastaland Shelf Science 45: 823–834.

Page, G. W., L. E. Stenzel, and J. E. Kjelmyr. 1999.Overview of shorebird abundance and distribu-tion in wetlands of the Pacific Coast of the con-tiguous United States. Condor 101:461–471.

Rader, D. N. 1984. Salt-marsh benthic invertebrates:Small-scale patterns of distribution and abun-dance. Estuaries 7: 413–420.

Ratchford, S. G. 1995. Changes in the density andsize of newly-settled clams in Willapa Bay, WA,due to the invasion of smooth cordgrass, Spartinaalterniflora Loisel. Unpublished MS thesis,University of Washington, Seattle.

Reeder, T. G., and S. D. Hacker. 2004. Factors con-tributing to the removal of a marine grass invader(Spartina anglica) and subsequent potential forhabitat restoration Estuaries 27: 244–252.

Ruesink, J. L., B. E. Feist, C. J. Harvey, J. S. Hong, A.C. Trimble, and L. M. Wisehart. 2006. Changes inproductivity associated with four introducedspecies: ecosystem transformation of a “pristine”estuary. Marine Ecology Progress Series 311:203–215.

Stenzel, L. E., C. M. Hickey, J. E. Kjelmyr, and G. W.Page. 2002. Abundance and distribution of shore-birds in the San Francisco Bay area. Western Birds33: 69–98.

Thompson, J. D. 1991. The biology of an invasiveplant: What makes Spartina anglica so successful?BioScience 41: 393–401.

Tyler, A. C., and E. D. Grosholz. Forthcoming.Spartina invasion changes intertidal ecosystemmetabolism in San Francisco Bay. In Proceedingsof the Third Annual Invasive Spartina Conference.Cambridge: Cambridge University Press.6

Tyler, A. C., J. G. Lambrinos, and E. D. Grosholz.2007. Nitrogen inputs promote the spread of aninvasive marsh grass. Ecological Applications 17:1886–1898.

Vitousek, P. M., H. A. Mooney, J. Lubchenco, and J.M. Melillo. 1997. Human domination of Earth’secosystems. Science 277: 494–499.

West, D. L., and A. H. Williams. 1986. Predation byCallinectes sapidus (Rathbun) within Spartina al-terniflora (Loisel) marshes. Journal of ExperimentalMarine Biology and Ecology 100: 75–95.

Whitcraft, C. R., and L. A. Levin. 2007. Regulation ofbenthic algal and animal communities by saltmarsh plants: Impact of shading. Ecology 88:904–917.

Windham L., and L. A. Meyerson. 2003. Effects ofcommon reed (Phragmites australis) expansionson nitrogen dynamics of tidal marshes of thenortheastern US. Estuaries 26: 452–464.

Yamada, S. Y. 2001. Global invader: The Europeangreen crab. Unpublished manuscript, Oregon SeaGrant, Oregon State University.

Zedler, J. B. 1980. Algal mat productivity: Compari-sons in a salt marsh. Estuaries 3: 122–131.

———. 1984. The Ecology of Southern CaliforniaCoastal Salt Marshes: A Community Profile.Washington, DC: U.S. Fish and Wildlife Service.

Zedler J. B., and S. Kercher. 2004. Causes and conse-quences of invasive plants in wetlands: Oppor-tunities, opportunists, and outcomes. CriticalReviews in Plant Sciences 23: 431–452.

Zipperer, V. T. 1996. Ecological effects of the intro-duced cordgrass Spartina alterniflora on benthiccommunity structure in Willapa Bay, Washington.Unpublished MS thesis, University ofWashington, Seattle.


6 Same asnote 5: up-date with all biblio-graphic dataif now published.


Changes in Community Structure and Ecosystem Function...

Documents

Transcript of Changes in Community Structure and Ecosystem Function...