Oecologia (2010) 163:461–469
DOI 10.1007/s00442-009-1529-0COMMUNITY ECOLOGY - ORIGINAL PAPER
Ecosystem-phase interactions: aquatic eutrophication decreases terrestrial plant diversity in California vernal pools
Jamie M. Kneitel · Carrie L. Lessin
Received: 3 May 2009 / Accepted: 25 November 2009 / Published online: 11 December 2009© Springer-Verlag 2009
Abstract Eutrophication has long been known to nega-tively aVect aquatic and terrestrial ecosystems worldwide.In freshwater ecosystems, excessive nutrient input results ina shift from vascular plant dominance to algal dominance,while the nutrient-species richness relationship is found tobe unimodal. Eutrophication studies are usually conductedin continuously aquatic or terrestrial habitats, but it isunclear how these patterns may be altered by temporal het-erogeneity driven by precipitation and temperature varia-tion. The California vernal pool (CVP) ecosystem consistsof three distinct phases (aquatic, terrestrial, and dry) causedby variation in climatic conditions. The purpose of thisstudy was to test the hypothesis that resource addition dur-ing the aquatic phase results in increased algal abundance,which reduces vascular plant cover and richness of the ter-restrial phase upon desiccation. We used mesocosms lay-ered with CVP soil, in which treatments consisted of Wvelevels of nitrogen and phosphorous added every 2 weeks.Resource addition increased available phosphorus levelsand algae cover during the aquatic phase. Increased algalcrusts resulted in decreased vascular plant percent coverand species richness. Few signiWcant patterns wereobserved with individual plant species and total biomass.The phosphorus-plant richness relationship was not signiW-cant, but species composition was signiWcantly diVerentamong the low and high treatment comparisons. Theseresults highlight a neglected eVect of eutrophication inseasonal habitats. Interactions among ecosystem phasesclearly require more attention empirically and theoretically.
Management and restoration of temporally heterogeneoushabitat, such as the endemic-rich CVP, need to consider theextensive eVects of increased nutrient input.
Keywords Eutrophication · Mesocosm experiment · Nutrient addition · Plant composition · Seasonal wetlands
Introduction
Eutrophication, the excessive input of nitrogen and phos-phorus into ecosystems that results from human activities,is one of the leading threats to terrestrial, freshwater, andmarine ecosystems worldwide (Schindler 2006; Conleyet al. 2009; Smith and Schindler 2009). In particular, fresh-water nutrient pollution continues to increase globally,while the concerns for freshwater conservation of humanand non-human systems also increase (Vitousek et al. 1997;Conley et al. 2009; Smith and Schindler 2009; WorldWater Assessment Programme 2009). The negative eVectsof eutrophication include major compositional and func-tional shifts in ecosystems (ScheVer et al. 2001; Schindler2006), losses of trophic levels (Smith and Schindler 2009),increases in species invasions (Chase and Knight 2006),and increased emerging diseases (Johnson et al. 2007).Recent reviews have indicated that an understanding of thedirect and indirect eVects of eutrophication in freshwatersystems is still incomplete; however, consistent patternshave been observed over the past decades (Schindler 2006;Smith and Schindler 2009).
Empirical and theoretical studies of eutrophication haveidentiWed several patterns related to vascular plant and algalgrowth in shallow lakes and ponds (ScheVer 1990; ScheVerand Carpenter 2003; Schindler 2006). Submersed vascularplants typically dominate the biomass at low nutrient levels
Communicated by Joel Trexler.
J. M. Kneitel (&) · C. L. LessinDepartment of Biological Sciences, California State University, Sacramento, 6000 J Street, Sacramento, CA 95819-6077, USAe-mail: [email protected]
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(e.g., Sand-Jensen and Borum 1991; ScheVer et al. 1997;Jones et al. 2002; Phillips et al. 2005). As nutrientsincrease, algal growth increases and species compositionchanges (e.g., ScheVer et al. 1997; Leibold 1999), whichcan produce thick algal mats (e.g., Power 1990; ScheVeret al. 1997); this occurs concurrently with a decline in vas-cular plant growth and biomass. Vascular plant-algae com-petition for phosphorus, dissolved inorganic carbon (Joneset al. 2002), or light (ScheVer et al. 1997), as well as otherchanges to water chemistry and trophic structure, can leadto these shifts in dominance.
Plant species richness and composition can also beaVected by nutrient addition (Leibold 1999; Dodson et al.2000; Mittelbach et al. 2001; Hautier et al. 2009). Theubiquitously predicted and well-supported pattern is theunimodal relationship between nutrient levels and vascularplant species richness (Dodson et al. 2000; Mittelbach et al.2001). Within a continuously aquatic environment, lownutrient levels are expected to support low diversitybecause of nutrient limitation to plants. Plants will over-come this with nutrient addition, resulting in increased spe-cies richness. At higher nutrient levels, algae is expected toout-compete vascular plants, and therefore, we expectdecreased levels of vascular plant richness. Along thisnutrient gradient, species turnover is expected based ontraits associated with competitive ability, herbivore edibil-ity, and light tolerance (Abrams 1995; Leibold 1999;Dodson et al. 2000; Kneitel and Chase 2004). While theaforementioned eVects of eutrophication have garneredempirical support, it is unclear whether they are upheld inheterogeneous environments that produce interactionsamong aquatic and terrestrial habitat.
The movement of materials and organisms in spatiallyheterogeneous ecosystems can be important for structuringcommunities and altering ecosystem functioning (Poliset al. 1997; Loreau et al. 2003; Baxter et al. 2005; McCannet al. 2005); indeed eutrophication is itself a form of spa-tially subsidized resources. Recent reviews and theoreticalstudies have highlighted the coupling among ecosystems bythe movement of organisms between aquatic and terrestrialhabitats (Baxter et al. 2005; Attayde and Ripa 2008;Schreiber and Rudolf 2008; Nowlin et al. 2008; McCoyet al. 2009). Most empirical studies Wnd positive bottom-upeVects of the movement of prey from an aquatic communityto an adjacent terrestrial community (e.g., Nakano andMurakami 2001; Power et al. 2004; Nowlin et al. 2008).Other recent studies, however, have identiWed the potentialfor negative eVects of predation and increased competitionresulting from this exchange of organisms (Huxel et al.2004; Knight et al. 2005). These types of interactions mayalso occur in the same location when temporal heterogene-ity in climate conditions creates aquatic and terrestrialcommunities.
Seasonal Xuctuations, whether regular or irregular, are aubiquitous occurrence that can greatly alter ecosystemcharacteristics and functioning (e.g., Sanders et al. 1989;Fahrig 1992; Oksanen 1990; Schmidt et al. 2000; Mehneret al. 2005). While most studies focus on a single commu-nity (i.e. terrestrial or aquatic community), climatic varia-tion in precipitation and temperature can generate diVerentcommunities in a particular location: precipitation produc-ing an aquatic community and desiccation producing a ter-restrial community. Examples of these ecosystems includeseasonal wetlands and temporary ponds, which are com-mon worldwide in arid, temperate, and tropical regions(Williams 1996; Euliss et al. 2004; De Meester et al. 2005).Few theoretical or empirical studies have addressed thepotential for interactions among these communities by themovement of resources or organisms as it has been for spa-tially heterogeneous systems (e.g., McCann et al. 2005;McCoy et al. 2009). One possibility is that they respondlike continuously aquatic or terrestrial systems (Fig. 1). Forexample, nutrient deposits (eutrophication) in grasslandsincrease biomass and thatch layers which inhibit the fol-lowing year’s plant percent cover and richness (e.g., Heady1956; Huenneke et al. 1990; Foster and Gross 1998; Levineand Rees 2004); an aquatic community may provide asimilar inhibitory layer with thick algal mats.
Fig. 1 Conceptual framework for eutrophication along habitat types(aquatic and terrestrial) and temporal heterogeneity of climate (low andhigh). Arrows indicate the process of eutrophication, with a brief list ofits eVects. Oligotrophic states of the system (Olig), eutrophic state(Eu), vascular plants (Plant), dead aboveground plant material(Thatch), dissolved oxygen (DO), and algal growth (Algae), whichproduces an algal crust upon desiccation, are indicated. Asteriskindicates the focus of the present study. Note that this diagram does notinclude a comprehensive list of all eVects, including trophic interac-tions within a habitat
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Eutrophication studies can provide the basis for under-standing the potential for interactions in a seasonal ecosys-tem. For example, increases in phosphorus input are wellknown to increase algal abundance in aquatic habitats(Dillon and Rigler 1974; ScheVer 1990; Correll 1998; Smithand Schindler 2009), but it is unclear whether desiccationcan result in the formation of algal crusts that decreaseterrestrial plant germination, growth, and consequentlyspecies richness. The goal of the present study is to test thishypothesis using the California vernal pool ecosystem.
Study system: California vernal pools
California vernal pools (CVP) are ephemeral wetland eco-systems found in shallow depressions over an underlyingimpermeable substrate, which prevents water from percolat-ing through the soil (Holland and Jain 1981; Witham et al.1998). The habitat between CVPs are usually grasslandscomposed of annual grasses and forbs, dominated by non-native species. The term “phase” is commonly used for theaquatic and terrestrial communities of CVP (Witham et al.1998) and will be employed here. The variation in tempera-ture and precipitation creates the three phases of CVP:aquatic phase, terrestrial phase, and a dry phase. Californiahas a Mediterranean climate with cool wet winters and hotdry summer and fall months. The aquatic phase is usuallypresent between November and April, the terrestrial phasebetween April and May, and the dry phase between Mayand November. Precipitation occurs from approximatelyNovember to April (Sacramento, California, receiving460 mm annually), with most of the rainfall occurring inJanuary (Sacramento, mean = 93.7 mm). Temperatures arealso lowest in January (Sacramento, mean = 8.0°C) andreach a maximum in July (Sacramento, mean = 24.1°C).The timing and amount of rainfall are quite variable amongyears (Bliss and Zedler 1998; Bauder 2000) and these, inturn, determine the length and timing of the diVerent phases,as well as species composition within each phase (Bliss andZedler 1998; Bauder 2000; Gerhardt and Collinge 2003).
During the dry phase period, few species are presentaboveground, but organisms of the aquatic and terrestrialphases lie dormant as cysts and seeds in the soil awaitingthe return of rains (Holland and Jain 1981). The aquaticphase develops with inundation during California’s winterrains. Aquatic community composition is typical of mosttemporary ponds (Wilbur 1997; Williams 1996; Blausteinand Schwartz 2001), dominated by aquatic microbes, algae,invertebrates, vertebrates, and vascular plants (Williams1996; King et al. 1996; Witham et al. 1998; Angeler et al.2008). As rainfall ceases and temperatures increase in latespring, the pools desiccate and are replaced by a terrestrialphase (Holland and Jain 1981; Gerhardt and Collinge2003). A vascular-plant community, consisting of annual
native forbs and grasses, dominates the terrestrial phase(Holland and Jain 1981; Stone 1990). These plant speciesexhibit great variation in their germination and growth phe-nology (Keeley 1990; Bliss and Zedler 1998). The strate-gies include species that germinate, grow, and emerge instanding water, as well as species that do not germinate andgrow until the Wnal stages of the aquatic phase. However,most species will germinate at some point after inundationand not grow and Xower until the Wnal stages of the aquaticphase or after complete desiccation (Bliss and Zedler 1998;Bauder 2000).
The vernal pool ecosystem is the focus of extensive con-servation eVorts in California for two reasons. First, vernalpool habitat has been greatly reduced to 3–10% of its origi-nal density because of habitat conversion to agriculture andurbanization (Holland and Jain 1988; Keeley and Zedler1998). The remaining habitat is embedded in an urban andagricultural matrix, leaving it especially vulnerable toeutrophication (Carpenter et al. 1998). We know of nostudy that has examined the potential impact of increasednitrogen and phosphorus in CVP. Second, both aquatic andterrestrial phases have high levels of endemism and speciesthat are of concern, threatened, or endangered (Holland andJain 1981; King et al. 1996; Federal Register 2003). Seveninvertebrate species and 11 plant species are federally listedendangered species (Federal Register 2003). Over 200 vas-cular plants species are found in this system and approxi-mately 55% are endemic (Stone 1990; Keeler-Wolf et al.1998; Gerhardt and Collinge 2003); the aquatic invertebratecommunity is similarly characterized by high richness andendemism. Few studies have examined the role of nutrientaddition on these organisms.
Most CVP studies have examined spatial diversity pat-terns (Holland and Jain 1981; King et al. 1996; Kneitel andCutler, in preparation), species composition within a phase(Gerhardt and Collinge 2003; Marty 2005) and morerecently, aquatic productivity-diversity relationships (Lessinand Kneitel, in preparation). Like other seasonal ecosys-tems, studies have focused on a single phase and have nottested the potential for interactions among the phases. TheeVects of nutrient addition and its mediation of phase inter-actions is the focus of the present study with special con-cern for management implications in the California vernalpool ecosystem. SpeciWcally, we used mesocosms to testthe predictions that: (1) nutrient addition during the aquaticphase increases algal abundance (Dillon and Rigler 1974;Correll 1998), which creates greater algal crust layers as thepools desiccate; (2) the nutrient-addition treatments alsoreduce vascular plant cover and richness in the terrestrialphase because of increases in the algal crust layer; and (3)there is a quadratic relationship between vascular plantrichness and nutrients accompanied by a shift in speciescomposition (Dodson et al. 2000; Mittelbach et al. 2001) .
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Materials and methods
Soil from a vernal pool complex in the Elder Creek Watershedin Sacramento County, California, was collected from randompoints and used for the mesocosm experiment. The top 6 cmof soil was collected to ensure the presence of the eggbanks (Brendonck and De Meester 2003). Soil was homog-enized with a cement mixer to intersperse the cyst and seedbank. All emergent plant species came from the seed bank.
In the fall 2007, thirty experimental mesocosms (con-tainers held 38 l, diameter = 0.6 m, height = 0.18 m, area =0.28 m2) were established in the California State University,Sacramento Arboretum. Five centimeters of soil (7.5 l) wasdistributed to each mesocosm, which were then allowed toWll by natural rain events. Mesocosms were Wlled with rain-fall from December until May; water levels Xuctuatedthroughout this period, but the mesocosms did not dry outcompletely. Each mesocosm received one of Wve nutrient-addition treatments, and each was replicated 6 times. Thetreatments were randomly assigned to mesocosms in arandomized block design.
The treatments consisted of nitrogen and phosphorusaddition via an aqueous solution of NH4Cl, NaNO3, andKH2PO4 (Jardillier et al. 2005). A control treatmentreceived no added nutrients while the next three levels reX-ected the natural gradient of nitrogen and phosphorus levelsfound in local pristine vernal pools (Yolo County Planningand Public Works Department and ESA 2005). A low nutri-ent treatment consisted of 0.25 mg/l each of phosphate andnitrate, a medium treatment consisted of 1.0 mg/l phosphateand 0.5 mg/l nitrate and a high treatment consisted of2.0 mg/l phosphates and 1.0 mg/l nitrate (Yolo CountyPlanning and Public Works Department and ESA 2005).The Wfth nutrient-addition level (very high) had an exagger-ated amount of nutrients designed to mimic urban runoVand it consisted of 4.0 mg/l phosphate and 2.0 mg/l nitrateadded. The nutrients were added twice a month fromDecember 2007 (2 weeks after inundation) up to andincluding April 2008 (once the water level began todecrease). In early May, the mesocosms began to dry andno standing water was present by late May. Total phospho-rus and nitrate were measured throughout the course of theaquatic phase with Hach DREL/2800 Complete WaterQuality Lab (Hach). For the purposes of this study, we ana-lyzed the data from the last aquatic sampling period.
Terrestrial plants began to dominate as the mesocosmsdried, as is found in natural vernal pools. The timing ofcomplete desiccation (wet soil, but no standing water)occurred within a week among all replicates. Cladophorasp. was the dominant green algae sampled; it attaches tosubstrates initially and accumulates as Xoating mats whenabundance increases (Bellis and McLarty 1967; Power1990); these developed into an algal crust as the pools
dried. Following desiccation, algae and each plant species’percent cover were estimated to the nearest 5%; total per-cent cover was the summation of each of the plants’ percentcover, and species richness (numbers of species) was mea-sured. In this study, all of the vascular plants were annuals,which die once the reproductive cycle is complete. Aftereach vascular plant completed its life cycle, all above-ground plant parts were clipped, dried in a drying oven for48 h, and total biomass (grams) of all plants combined wasmeasured. This included the dried algae that were entangledand diYcult to separate from the plants. Therefore, totalbiomass included algae and all terrestrial plant species.Species were identiWed using Hickman (1993) and werecategorized as endemic (distribution limited to vernalpools) or widespread (distributed in vernal pools as well asother habitats, including wetlands and grasslands).
Total biomass, algal crust percent cover, and plant per-cent cover of the six most common species (species withmean percent cover >1%) were analyzed using randomizedblock ANOVA. Total plant percent cover, total plant rich-ness and richness of endemic and widespread species wereanalyzed using analysis of covariance (ANCOVA) withtreatment as the Wxed factor and algal percent cover as thecovariate. We conducted regression analysis to test whetherthere was a linear or quadratic relationship between speciesrichness and total phosphorus. To examine vascular plantcompositional diVerences among treatments, we conductedanalysis of similarity (ANOSIM), a non-parametric permu-tation procedure based on a similarity matrix. Our matrixwas based on species abundances in treatment replicates;we used Bray-Curtis distances and ran 1,000 permutations.We conducted Bonferroni-corrected pairwise comparisonsamong treatments following a signiWcant result of theGlobal model. When necessary, data were arcsine (percentcover) or square-root (richness, phosphorus) transformed tomeet normality and homogeneity of variances assumptions.We used PAST, version 1.94b (Hammer et al. 2001) to con-duct ANOSIM, and all other analyses were conducted usingSPSS version 16.0.1 for Mac.
Results
Total aquatic phosphorus signiWcantly increased with nutri-ent-addition treatments, but nitrates did not diVer amongtreatments (Table 1). Phosphorus in the very high treatmentlevel was signiWcantly greater than all of the other treat-ments (Fig. 2a). Algal crust cover also signiWcantlyincreased with nutrient addition (Table 1; Fig. 2b). Insteadof a continuous increase in algae, there was an abrupt shiftbetween the low and medium nutrient-addition levels. Thecontrol and low levels were not signiWcantly diVerent thanone another and the medium to very high treatment levels
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were also not signiWcantly diVerent from one another, butthere were diVerences between these two groups (Fig. 2b).Total aboveground biomass, including the plants and algae,was not signiWcantly aVected by the treatments (Table 1).
Total plant percent cover decreased with the nutrient-addition treatments with no signiWcant eVect of the covari-ate [ANCOVA: Treatment, F(4,24) = 4.71, P = 0.006; Algae(covariate), F(1,24) = 1.81, P = 0.19; Fig. 3a]. Plant percentcover signiWcantly decreased with nutrient addition; thehigh and very high treatments did not signiWcantly diVer.Total plant species richness signiWcantly decreased withnutrient addition and the algal cover contributed to thisdecrease [ANCOVA: Treatment, F(4,24) = 5.62, P = 0.026;Algae (covariate), F(1,24) = 3.54, P = 0.021; Fig. 3b]. Therewas no change among the Wrst three nutrient treatments fol-lowed by a gradual decline among the medium, high andvery high treatments. When species richness was catego-rized into endemic or widespread groups, no signiWcantdiVerences among treatments and the covariate (algae)resulted [Endemic—Treatment, F(4,24) = 2.44, P = 0.074;Algae (covariate), F(1,24) = 3.05, P = 0.094; Widespread—Treatment, F(4,24) = 2.1, P = 0.11; Algae (covariate), F(1,24) =1.14, P = 0.30].
In nature, individual vernal pools tend to have 15–25plant species (Keeler-Wolf et al. 1998); 11 vernal poolplant species were found in our experimental mesocosms.Two species (Ranunculus aquatilis and Eleocharis macro-stachya) emerged and Xowered before the end of theaquatic phase. Neither of these species had signiWcant treat-ment eVects. All other species germinated, but did not growuntil the Wnal stages of the aquatic phase. Individual speciescover was quite variable, and few signiWcant eVects werefound, although Deschampsia danthonioides signiWcantly
decreased with resource addition (Table 1). Two species,E. macrostachya and Downingia bicornuta, were ubiqui-tous and their cover was almost invariable across treat-ments. Five of the 11 species were absent in the highestnutrient-addition treatments.
Total phosphorus was not signiWcantly related (linear orquadratic) to species richness (P > 0.05). However, vascu-lar plant composition was signiWcantly diVerent amongtreatments, but these diVerences were weak (ANOSIMGlobal: R = 0.115, P = 0.048). Pairwise comparisons oftreatments resulted in a signiWcant diVerences between thelow and high treatments (R = 0.49, P = 0.04) and the lowand very high treatments (R = 0.40, P = 0.02).
Discussion
Nutrient addition during the “aquatic phase” of the Califor-nia vernal pool ecosystem increased available aquatic
Table 1 ANOVA results for nutrient-addition treatments (Wxed) andblock eVects (random). Only species with mean percent cover >1% arepresented
a Endemic to California vernal pools
Dependent variable Nutrient addition Block
F(4,20) P F(5,20) P
Total water phosphorus (mg/l) 3.63 0.022 1.02 0.44
Total nitrate (mg/l) 1.25 0.32 2.42 0.07
Algal percent cover 3.41 0.028 2.22 0.09
Total plant/algal biomass (g) 1.6 0.21 1.76 0.67
Eleocharis macrostachya cover 0.61 0.66 11.0 <0.001
Deschampsia danthonioidescover
4.2 0.01 1.6 0.20
Centaurium muehlenbergii cover 1.9 0.15 0.86 0.52
Plagiobothrys stipitatus covera 0.7 0.60 1.04 0.42
Eryngium vaseyi covera 1.2 0.33 0.58 0.72
Gratiola ebracteata cover 1.2 0.34 0.57 0.72
Fig. 2 EVects of Wve nutrient treatments on a total phosphorus (mg/l)and b percent of algal cover (arcsine-transformed) in mesocosmsin aquatic phase (mean § SE). Treatment eVects were signiWcant(ANOVA, P < 0.05) with both dependent variables (see Table 1 forstatistics). Letters above treatments represent the results of Bonferroni-adjusted post hoc tests: treatments with the same letters are not signiW-cantly diVerent (P > 0.05)
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phosphorus, and as the mesocosms dried, we measuredincreased algal-crust cover and decreased vascular plantpercent cover and species richness (Fig. 3). Species compo-sition diVered between the low and higher nutrient treat-ments, but we did not Wnd a signiWcant relationshipbetween phosphorus and vascular plant species richness.Several dependent variables did not respond signiWcantly tothe nutrient-addition treatments, including biomass, mostspecies’ percent cover, and the richness of endemic andwidespread species.
These results augment our understanding of the range ofeutrophication eVects in ecosystems, especially seasonalwetlands and ponds (Williams 1996; De Meester et al.2005). Eutrophication commonly occurs as spatially subsi-dized resources, which leads to the suppression of vascularplants by algae in freshwater systems (ScheVer 1990; Jones
et al. 2002; Fig. 1). We found that increased nutrient addi-tion had signiWcant negative eVects on the richness andcover of the terrestrial plants following desiccation of sea-sonal ponds. A few of the plant species were submersed,but most species delay germination and growth until desic-cation of the pools because of the stressful aquatic environ-ment (Stone 1990; Bliss and Zedler 1998). Despite thevariation in germination and growth phenology, we foundnegative eVects of aquatic eutrophication on terrestrialplant richness and cover, which was most likely mediatedby the inhibitory eVects of algal mats (Fig. 3).
The increased thatch layer deposited by the aquaticphase is similar to what has been well established in manyplant communities: thatch build up inhibits plant germina-tion, growth, and community composition (e.g., Heady1956; Foster and Gross 1998; Levine and Rees 2004;Hamilton 2008). For example, Huenneke et al. (1990) foundbiomass increased with fertilization (nitrogen and phosphorus)addition in California serpentine grasslands. This increasedbiomass resulted in an increased thatch layer, which alteredspecies composition (decreased diversity and increasedinvasive species). Recently, Hautier et al. (2009) identiWedlight (aboveground competition) as the key limiting resourcewith increased nutrient addition (eutrophication). Increasedfertilization resulted in increased aboveground biomass thatlowered light availability, and reduced plant richness as aconsequence.
The algal crust may have directly aVected plant richnessand composition, but we could not completely excludeother explanations for these negative eVects. The eVects ofnutrient addition could have altered the competitive interac-tions among plants directly. We did not consider the role ofdissolved inorganic carbon, which has been found to inXu-ence the outcome of competitive interactions among vascu-lar plants and algae (Jones et al. 2002). The present studyalso did not consider the eVects of aquatic herbivores inregulating algal abundance during the aquatic phase, whichcan have indirect eVects on vascular plant growth (e.g.,ScheVer 1990; Leibold 1999; Jeppesen et al. 2000; Joneset al. 2002). Future work will have to determine howaquatic trophic structure and the presence of diVerent nutri-ents interact to regulate eutrophication in this system(ScheVer 1990).
Total and Deschampsia danthonoides percent coverdecreased signiWcantly with nutrient addition. Several otherspecies exhibited negative trends that were not signiWcant,but Wve of the 11 species were absent from highest nutrienttreatments. Endemics and widespread species richness didnot diVer in their responses to treatments. Further, indirectevidence has suggested that reduced vascular plant cover isassociated with increased thatch layers in vernal pools(Linhart 1988; Marty 2005; Hamilton 2008). Species traits(trade-oVs) associated with competition for nutrients and
Fig. 3 EVects of Wve nutrient-addition treatments on a arcsine-trans-formed vascular plant cover [analysis of covariance (ANCOVA): treat-ment, F(4,24) = 4.71, P = 0.006; algae (covariate), F(1,24) = 1.81,P = 0.19] and b square-root-transformed vascular plant species rich-ness [ANCOVA: treatment, F(4,24) = 5.62, P = 0.026; algae (covariate)F(1,24) = 3.54, P = 0.021] in mesocosms during Xower phase(mean § SE). Letters above treatments represent the results of Bonfer-roni-adjusted post hoc tests: treatments with the same letters are notsigniWcantly diVerent (P > 0.05)
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light are commonly identiWed as important factors inXuenc-ing patterns of plant diversity and composition (Kneitel andChase 2004).
Total aboveground plant biomass did not diVer amongnutrient-addition treatments. While we found no eVects onbiomass, previous work has shown that the length of inun-dation can have strong negative eVects on plant biomass(Bliss and Zedler 1998). Since all mesocosms were inun-dated for approximately the same length of time, it ispossible that this contributed to the lack of a nutrienteVect. Further, the changes in species composition couldhave oVset any biomass increases (Engelhardt and Ritchie2001).
Plant species richness patterns in this study were notconsistent with classic nutrient-diversity predictions(Abrams 1995; Dodson et al. 2000; Mittelbach et al. 2001).The unimodal relationship is commonly found for bothaquatic macrophytes (Dodson et al. 2000) and terrestrialplants (Mittelbach et al. 2001). We found no quadratic rela-tionship between aquatic phosphorus and species richness.Determining the relative importance of competition fornutrients and light availability may allow us to decipherthese results. Further, the plant composition of these com-munities could have aVected the availability of phosphorus,and thereby altered this relationship (Engelhardt andRitchie 2001). Species composition diVerences between thelow and the higher nutrient levels were consistent with pre-vious empirical and theoretical studies (e.g., Abrams 1995;Leibold 1999; Dodson et al. 2000). Species turnover wasexhibited along the nutrient gradient, which is likely theresult of reduced recruitment or increased loss of speciesthat are less tolerant of low light conditions (e.g., Fosterand Gross 1998; Hautier et al. 2009) caused by increasedalgal mat cover.
The decrease in terrestrial plant cover and richnessmay also have cascading eVects during the terrestrialphase. For example, Haddad et al. (2009) recentlyshowed that arthropod richness and trophic structurecould be suppressed by decreased plant richness. Thesame is true for the arthropod pollinators, which can benegatively aVected by resource reduction that accompa-nies reduced plant richness (e.g., Kearns and Inouye1997). The California vernal pool system supports manyspecialist pollinators, speciWcally bees (Thorp and Leong1998), and these may be especially vulnerable to reducedspecies richness or changing species composition witheutrophication.
While our study focused on the unidirectional eVects ofthe aquatic on the terrestrial phase, it is very likely that theterrestrial phase also contributes to the functioning of theaquatic phase (Nakano and Murakami 2001; Fig. 1). Forexample, the terrestrial litter layer will provide the resourcebase for decomposers and hence the rest of the aquatic food
web (Fisher and Likens 1973; Polis et al. 1997; Baxter et al.2005). Recently, Attayde and Ripa (2008) showed in a the-oretical study that herbivores can reduce detritus pathwaysdependent on leaf litter, and the presence of carnivores cancreate trophic cascades that alleviate these negative eVects.In seasonal wetlands or ponds, this eVect could also occuracross the terrestrial-aquatic phases. Further, the eVects ofaquatic algae may be similar to terrestrial herbivores, whichwill ultimately reduce leaf litter available for decomposi-tion during the return of the aquatic phase. Indeed, there isgreat potential for complex interactions among phases,including positive or negative feedback loops that can alterecosystem dynamics temporally (Fig. 1), as is found in spa-tially connected ecosystems (Polis et al. 1997; Nakano andMurakami 2001; Baxter et al. 2005).
Most vernal pool habitats lie adjacent to agricultural andurban development, and therefore, the potential forincreased phosphorus and nitrogen input to the system ispresent (Carpenter et al. 1998). This input can create otherproblems for the management of CVP: increased nutrientavailability can also increase the potential for invasive spe-cies to inWltrate vernal pools from the surrounding grass-land. Gerhardt and Collinge (2003) found increasedabundance of several exotic plant species with increasedphosphorus and organic matter in vernal pools. Manage-ment strategies and reserve design need to consider thedirect and indirect eVects of nutrient input on both phasesof CVP.
Eutrophication continues to be a major problem interrestrial, freshwater, and marine ecosystems worldwide(Carpenter et al. 1998; Schindler 2006; Conley et al.2009) by producing major shifts in community composi-tion and function (ScheVer et al. 2001). The results of thisstudy highlight the potential for eutrophication (spatialnutrient subsidies) to cross aquatic and terrestrial phasesin temporally heterogeneous environments (Fig. 1; e.g.,seasonal wetlands, seasonally Xooded forests). This inter-action between the movement of organisms and resourcesin time (across phase) and space (eutrophication) under-scores the complexities of seasonal ecosystems thatneed to be further considered. Future theoretical andempirical work should consider examining the role ofresource dynamics and pulses (e.g., Yang et al. 2008),spatial dynamics (e.g., Loreau et al. 2003; Angeler et al.2008), and ecosystem regime shifts and alternativestable states (sensu ScheVer 1990; ScheVer and Carpenter2003) in temporally heterogeneous environments (e.g.,Bayley et al. 2007). Since seasonal ecosystems are com-mon worldwide and support high levels of endemism(Williams 1996; De Meester et al. 2005), this comprehen-sive approach to these ecosystems will enhance ourunderstanding of ecosystem dynamics and the eVects ofeutrophication.
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Acknowledgments We thank L. Cabral, B. Love, and M. Memeo forhelp with various aspects of this study. J. Alford, R. Croel, W. Hamilton,E. Kachorek, J. Trexler, and two anonymous reviewers kindly provideduseful comments on earlier drafts. We are grateful to C. Collison,E. Schwab, and S. Beachley from Caltrans for access to the soil and toM. Baad for his hospitality at the CSUS Arboretum. This study was sup-ported by the California State University, Sacramento, Department ofBiological Sciences and College of Natural Sciences and Mathematics.
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