spatial segregation of periphyton communities in a desert stream: causes and consequences for n...

Spatial segregation of periphyton communities in a desert stream: causes and consequencesfor N cyclingAuthor(s): Julia C. Henry and Stuart G. FisherSource: Journal of the North American Benthological Society, Vol. 22, No. 4 (December 2003),pp. 511-527Published by: Society for Freshwater ScienceStable URL: http://www.jstor.org/stable/1468349 .

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511

J. N. Am. Benthol. Soc., 2003, 22(4):511–527q 2003 by The North American Benthological Society

Spatial segregation of periphyton communities in a desert stream:causes and consequences for N cycling

JULIA C. HENRY1 AND STUART G. FISHER

Department of Biology, Arizona State University, Tempe, Arizona 85287-1501 USA

Abstract. The goal of this research was to understand the underlying causes of patterns of distri-bution and abundance of N-fixing periphyton and non N-fixing periphyton in a desert stream, andto evaluate potential consequences of these patterns for stream N cycling. Sampling of periphytoncommunities at sandbar edges in Sycamore Creek, Arizona, revealed community differences relatedto direction of hydrologic exchange with the subsurface. N-fixing cyanobacteria were abundant atsandbar inwelling edges. Non N-fixing taxa predominated at outwelling edges. We evaluated severalpredictions of the hypothesis that this difference was attributable to differences in N availability atsandbar edges. NO3-N at outwelling edges was 3.5 times higher than at inwelling edges, consistentwith past work showing microbial nitrification to characterize sandbars. Non N-fixing and N-fixingperiphyton biovolume were related to NO3-N concentration at edges. Reciprocal transplants of pe-riphyton from original edges to edges with the opposite direction of hydrologic exchange revealedsignificant declines in periphyton relative to controls. Experiments using NO3-N diffusing substratesrevealed non N-fixing taxa to be more abundant where NO3-N was elevated. N-fixing periphytonwas, in contrast, more abundant at naturally low NO3-N or unenriched sites. These results supportthe hypothesis that differences in N availability between inwelling and outwelling edges caused theobserved pattern of periphyton distribution at sandbar edges. Last, 80% of outwelling NO3-N wasremoved from outflowing water by periphyton at sandbar edges. This temporary retention of availableN results in a surface stream depleted of inorganic N and accentuates spatial heterogeneity of pe-riphyton communities in this ecosystem.

Key words: edge effect, sandbar, hydrologic exchange, stream, nitrogen limitation, hyporheic, pe-riphyton, algae, cyanobacteria.

Many factors influence the distribution of pe-riphyton in streams. Substrate conditions (Pe-terson and Stevenson 1989), hydrology (Peter-son and Stevenson 1989, Biggs and Hickey 1994,Biggs and Stokseth 1996), desiccation (Peterson1987), grazing (Hill and Knight 1988), distur-bance (Grimm and Fisher 1989, Peterson et al.1990), and nutrient concentration and ratios(Pringle 1987, Peterson and Grimm 1992) haveall been implicated. In many desert streams, in-organic N may be a particularly important fac-tor influencing periphyton type and distributionbecause N often limits rates of in situ primaryproduction in these streams (Grimm and Fisher1986a, b).

Streamwater dissolved inorganic N (DIN)concentration can be highly variable in space.For example, surface and subsurface zones maydiffer in concentration of different forms of in-organic N (Triska et al. 1989, 1990, Coleman andDahm 1990, Hill 1990, McDowell et al. 1992,Claret et al. 1997). Inorganic N in SycamoreCreek, Arizona, surface water is typically low

1 E-mail address: [email protected]

and limiting (Grimm and Fisher 1986a), butDIN is often elevated in subsurface hyporheicand parafluvial zones relative to the main chan-nel (Valett et al. 1990, Holmes et al. 1994).

Localized sources of NO3-N may exist at lo-cations of hydrologic exchange between surfaceand subsurface zones. Differences in DIN be-tween surface and subsurface zones in Syca-more Creek result from microbial transforma-tions (ammonification and/or nitrification) oforganic N to inorganic forms. Depending on re-dox conditions and availability of organic C, de-nitrification may also occur, resulting in a per-manent loss of N from the stream (Holmes etal. 1996, Hedin et al. 1998). Alternatively, DINmay follow subsurface pathways and later re-enter surface flow where it again becomes avail-able to periphyton (Triska et al. 1990, Holmes etal. 1994, Valett et al. 1994, Claret et al. 1997).

Localized sources of NO3-N in locations of hy-drologic exchange with the subsurface can in-fluence periphyton communities in the surfacestream. Some studies report algal blooms at up-welling or outwelling locations (Coleman andDahm 1990, Valett et al. 1994). These studies



512 [Volume 22J. C. HENRY AND S. G. FISHER

linked emerging subsurface inorganic N and to-tal periphyton standing crop. However, taxo-nomic differentiation of periphyton communi-ties, particularly between periphyton that arecapable of fixing N ( fixers) and those that arenot (nonfixers), may reveal additional patternsthat are important. Fixers and nonfixers are of-ten abundant in Sycamore Creek (Fisher et al.1982), and the distribution and abundance ofthese two kinds of organisms may be influencedby surface–subsurface exchange occurring alongsandbar edges.

N-fixing cyanobacteria have a competitive ad-vantage over other periphyton under N-limitingconditions because they can fix N while otherprimary producers must obtain it as dissolvedNO3-N or NH4-N (Vitousek and Howarth 1991).Cyanobacteria dominate in some freshwater en-vironments with low inorganic N concentration.Examples include Castle Lake, California (Reu-ter and Axler 1992) and Kennedy Lake, BritishColumbia, where blooms of cyanobacteria de-pend on low N:P ratios (Stockner and Shortreed1988). Furthermore, nutrient concentration influ-ences cyanobacterial endosymbiont loads in cer-tain diatom species. In both lab and field exper-iments involving N enrichment, numbers of en-dosymbiont cells in the diatoms Epithemia tur-gida and Rhopalodia gibba were inversely relatedto N levels when P was not limiting (DeYoe etal. 1992). However, N fixation is energeticallyexpensive (Gutschick 1981), so the advantage offixers is lost where DIN is plentiful. For exam-ple, in a fertilization study of Arctic lakes, Nfixation was lower in lakes fertilized with Nthan in those fertilized with P (Bergman andWelch 1990).

Periphyton is often abundant and spatiallyvariable in Sycamore Creek, forming largeblooms of certain taxa of cyanobacteria, dia-toms, and other algae that are easy to identifyby eye based on their color, texture, and form(Busch 1979). In particular, workers at SycamoreCreek have noted for years that filamentous al-gae, such as Cladophora glomerata and membersof the family Zygnematales, appear to be moreabundant at downstream than upstream terminiof sandbars. Workers have also noticed the op-posite pattern of distribution for cyanobacteria,such as Nostoc spp., Anabaena spp., and Oscilla-toria spp. This observation has neither been doc-umented rigorously nor tested statistically. The

1st goal of our study was to determine the ro-bustness of this observation.

Our 2nd objective was to determine what pro-cess caused this pattern of periphyton distribu-tion. We tested several predictions of the hy-pothesis that periphyton segregation at sandbarinwelling (where water moves into sandbarsfrom surface flow) and outwelling (where waterflows out of sandbars into the surface stream)edges was caused by differences in N availabil-ity. The hypothesis would be supported if DINwas significantly higher at outwelling edgesthan at inwelling edges, and inwelling edges ex-hibited concentrations known to be limiting toperiphyton growth. Further, abundance of non-fixers, but not fixers, would be significantly pos-itively correlated with DIN. In addition, recip-rocal transplant experiments would reveal thatperiphyton grows better in its original hydro-logic environment (inwelling or outwelling)than in a local environment where flow direc-tion was the reverse. We also predicted thatmore nonfixers would grow on artificial sub-strates placed in environments where NO3-Nconcentration was elevated (outwelling edges orenriched inwelling edges) than on control sub-strates placed in environments where NO3-Nwas low (unenriched inwelling edges). The re-verse was expected for N-fixing taxa.

Our 3rd objective was to evaluate the conse-quences of algal growth at sandbar edges fornutrient retention by the larger ecosystem. Weexamined this objective by measuring the rateof movement of N across sandbar edges withintact algal communities and across edges fromwhich algae were removed experimentally, anddeduced the effect of periphyton on rate of re-turn of N to the surface stream.

Methods

Study site

Sycamore Creek is a spatially intermittentSonoran Desert stream ecosystem located ;35km northeast of Phoenix. The watershed area of505 km2 ranges in elevation from 427 to 2164 masl. An average of 39 cm of rain falls on thelower watershed annually. The stream is char-acterized by frequent flash flooding, resulting ina wide, active channel through which the wettedsurface stream meanders, often across deep,coarse alluvial sediments. The channel exhibits



2003] 513PERIPHYTON SEGREGATION AND N CYCLING

FIG. 1. Configuration of sandbars that is typical in a sandy run of Sycamore Creek.

a pattern of alternating riffles and runs; rifflesare steeper and composed of coarse material,and runs are of shallower slope and are com-posed primarily of sand (Wertz 1963). Runs con-tain sandbars that are highly porous such thatwater flows through them at a rate of ;1 m/h(Fisher et al. 1998). Surface water flows intosandbars at inwelling edges and out of sandbarsat outwelling edges (Fig. 1) that are identifiableusing small dye injections and measurements ofvertical hydraulic gradient (Fisher et al. 1998).Flash flooding often removes all biota from thechannel and initiates a rapid periphyton succes-sional sequence, starting with diatoms rapidlycolonizing bare sand and followed by filamen-tous algae and cyanobacteria (Fisher et al. 1982).Periphyton is spatially variable in SycamoreCreek and often accumulates at stream edges.High primary production in Sycamore Creekrelative to other ecosystems has been attributedto high light intensity, elevated water tempera-ture, and moderate current velocity (Busch andFisher 1981). Our study sites included severalsandy runs ranging from 100 to 400 m long lo-cated at ;650 m asl. Sandbar inwelling and out-welling edges were distributed among manydifferent sandbars in the different runs, andwere located on flowpaths that were indepen-

dent from one another, as confirmed with flo-rescent dye. Our study lasted from summer1998 through summer 2001.

Hydrology and water chemistry at sandbar edges

Vertical hydraulic gradient (VHG) betweensandbar edge and surface stream was measuredat 21 sandbar edge locations, each on an inde-pendent flowpath, on 18 January 2000 and on asubset of 12 of those edges on 28 March, 10April, and 18 April 2000, using a manometer(Lee and Cherry 1978, Valett et al. 1994). A ma-nometer is used to measure the difference inwater-table elevation between 2 locations. In thiscase, we measured the difference between wa-ter-table elevation in the surface stream and wa-ter-table elevation in small holes dug in sandbarsediments 20 cm away from the main channel–sandbar edge. Outwelling edges have positivevalues and inwelling edges have negative val-ues. Direction of flow was confirmed at eachedge by injecting fluorescent dye into sandbarsediments near the sandbar edge and recordingits appearance in the surface stream, or its ap-pearance in interstitial water farther into thesandbar.

Water samples were taken for chemical anal-




ysis at each edge on the latter 3 sample dates.At inwelling edges, duplicate water sampleswere taken from the surface stream 10 cm fromthe sandbar edge. At outwelling edges, intersti-tial water was sampled using a 60-mL syringefrom small holes dug in sandbar sediments, 10cm laterally from the surface stream–sandbaredge. Water in these holes was allowed to re-charge for $30 min prior to sampling. Watersamples were stored on ice, returned to the laband filtered (Whatman pre-combusted GF-Fglass fiber filters). Concentrations of NO3-Nwere determined using a Lachat QC8000 au-toanalyzer within 24 h of sampling. NH4-N wasnot analyzed because it is low in SycamoreCreek, often below detection level (5 mg/L) inboth surface and interstitial water. Temperaturewas measured using a glass thermometer ateach edge in the surface stream, 10 cm from thesandbar–surface stream interface.

Periphyton distribution in relation to flow direction

Periphyton communities were qualitativelymeasured at 21 sandbar edges on 18 January2000 and then quantitatively measured on asubset of 12 of those edges throughout the fol-lowing spring to determine whether periphytoncommunities differed at inwelling and outwell-ing edges of sandbars. The initial, qualitativetest used color, shape, and texture to determinethe dominant periphyton patch type at eachsandbar edge. Edges were assigned to either analgal-dominated group, meaning that the domi-nant patch type at the edge was a filamentousalgal taxon (Vaucheria spp.: dark green withshort carpet-like filaments, dense mat; Cladopho-ra glomerata: medium green with tangled, mat-ted, hair-like, branched filaments; Spirogyra spp.:coarse, slippery, dark green filaments; Zygnemaspp.: less coarse, medium green, slippery fila-ments; Mougeotia spp.: very fine, fluffy, and slip-pery filaments), or to a cyanobacteria-dominatedgroup, meaning that the dominant patch typewas a cyanobacterial taxon (Oscillatoria spp.:brownish green, dense mats, tangled, but notbranched; Lyngbya spp.: brownish green, lessdense, smooth; Nostoc spp.: brown or blue-greenballs, slippery; or Anabaena spp.: blue-green,slippery, falls apart when touched). A smallsample of periphyton was taken at each site toverify patch type microscopically.

Periphyton abundance, community composi-

tion, and chlorophyll a concentration were thenquantitatively determined at a subset of 12sandbar edges on 28 March, 10 April, and 18April 2000. The same 12 edges were sampled oneach date in a location slightly upstream ordownstream from previous samplings. Seven ofthese edges were inwelling edges and 5 wereoutwelling edges on 28 March 2000. Two of theoutwelling edges changed to inwelling edgesprior to 10 April. Percent cover of different pe-riphyton patches was estimated with a 25 3 50cm PVC grid strung with thin wire to make 36intersections over each sandbar edge such thatone of the 50-cm edges was aligned with andtouching the sandbar edge. The periphyton typeoccurring directly below each of the 36 wire in-tersections was identified based on color, shape,and texture and belonged to one of the follow-ing patch types: Anabaena spp., Nostoc spp., Os-cillatoria spp., C. glomerata, Spirogyra spp., Mou-geotia spp., Zygnema spp., Vaucheria spp., diatoms(golden brown, no visible filaments), othergreen algae (any green algae not in the abovegroups), or flocculent material. Percent cover ofdifferent patch types was calculated. Predomi-nant patch types were sampled with a 12-cmdiameter plexiglass corer to a depth of 5 cm.Periphyton cores (containing periphyton andsediments) were transported to the lab in whirl-packs. Periphyton was separated from sedi-ments by elutriation. The sample containingsediments and periphyton was placed in a largebeaker, water was added to cover sediments,and the mixture was stirred vigorously. The wa-ter and associated periphyton were poured offand saved. This process was repeated until noperiphyton was visible on the sediments. Sedi-ments were then discarded. This technique as-sumes that all periphyton is successfully re-moved from sediments. This assumption wastested by analyzing chlorophyll a in both theelutriant slurry and remaining sediment fromsamples taken during early succession, a timewhen diatoms affixed to sediments are likely tomake up a high % of total chlorophyll a in Syc-amore Creek. Results from this test revealedthat between 90 and 96% of periphyton was re-moved from sediments by our elutriation tech-nique. The periphyton slurry was then homog-enized in a blender for 0.5 to1 min. Subsampleswere preserved in Lugol’s solution for prepara-tion of permanent slides. A separate 5- to 20-mLsubsample of homogenate was filtered onto GF-




F filters for spectrophotometric chlorophyll aanalysis following methanol extraction (Tett etal. 1975). Permanent slides for algal counts weremade using Taft’s syrup medium solution (Ste-venson 1984).

Periphyton cells were counted at 10003 mag-nification under oil immersion. At least 500 cellswere identified on $3 transects across differentparts of the slide. Diatoms other than the pre-sumed N-fixing taxa Epithemia spp. and Rhopa-lodia spp. were not identified, but rather countedin groups of similar shapes and sizes so thattheir biovolume could be estimated. Biovolumeof a cell was estimated with BIOVOL (D. B. Kir-schtel. 1996. BIOVOL version 2.1, www.uvm.edu/;dkirscht/biovol.html) using the equationfor volume that best fit the geometry of the tax-on. The dimensions of 10 to 20 cells of each tax-on were measured from at least 3 slides. Bio-volume of each microscopically identified taxonat each sandbar edge was calculated based onthe biovolume of each taxon or diatom shapeclass in each sample and % cover of the patchrepresented by that sample. Nonfixer biovolumeincluded the algal taxa: C. glomerata, Vaucheriaspp., Spirogyra spp., Mougeotia spp., Zygnemaspp., Ulothrix subtilissima, Stigeclonium spp., Pe-diastrum spp., Closterium spp., and other smallunicellular green algae as well as non N-fixingdiatoms and nonheterocystous cyanobacteria forwhich N fixation is not known to occur: Oscil-latoria spp., Lyngbya spp., and Chorococcus spp.N-fixer biovolume included the presumed N-fix-ing diatoms Rhopalodia spp. and Epithemia spp.,and heterocystous cyanobacteria including An-abaena spp., Nostoc spp., and Calothrix spp. Rel-ative abundance of fixers and nonfixers at eachedge was calculated based on these biovolumeestimates for the 3 sample dates.

Transplant experiment

On 18 January 2000, we selected 4 outwellingedges dominated by algae, meaning that theedge was visually dominated by filamentous al-gae of the taxa: Vaucheria spp., C. glomerata, Spi-rogyra spp., Mougeotia spp., and Zygnema spp.,and 3 inwelling edges dominated by cyanobac-teria, meaning that the dominant patch typewas one of the cyanobacterial taxa: Oscillatoriaspp., Lyngbya spp., Nostoc spp., and Anabaenaspp. for a transplant experiment. VHG and NO3-N concentration were measured at each edge.

Small cylindrical baskets (6 cm diameter 3 6 cmheight) were created using 2-mm mesh alumi-num screen. Controls consisted of 3 basketsfilled with resident cyanobacteria (at inwellingedges) or algae (at outwelling edges) to cover100% of the bottom of the basket, and replacedat their original edge. In addition, 3 identicalbaskets were made for transplant to an edgewith the opposite hydrologic type for a total of6 baskets at each edge. The 6 baskets wereplaced 15 cm from the sand edge in randomorder. One set of transplants at an inwellingedge was restarted after 1 wk because of dis-turbance by cattle. Percent cover by algae andcyanobacteria in each of the 6 baskets at eachedge (total of 42) were visually estimated after2 wk incubation at sandbar edges, and respons-es of transplanted periphyton were compared tocontrols that remained at their original edge.

Nutrient-diffusing substrates

A NO3-N diffusing experiment was begun on12 June 2001 at 5 sandbar inwelling edges and5 sandbar outwelling edges that occurred on 5independent flowpaths. NO3-N concentrationwas determined, as described above, prior to theexperiment at each edge. Using a method simi-lar to Fairchild and Lowe (1984), 3 control claysaucers (9.5-cm diameter) containing a 2% agarsolution, and 3 NO3-N diffusing saucers with2% agar and 0.5 M NO3-N solution were placedat each edge. The 6 saucers were placed alongeach of the 10 sandbar edges in single rows withcontrols upstream of NO3-N diffusing saucers.The saucers were retrieved after 8 d of incuba-tion at the sandbar edges. A longer incubationtime was not possible during this experimentbecause of vandalism. Although 8 d is a shortincubation time, periphyton growth was visibleon the substrates by this time, and a treatmenteffect was apparent. The surface of the sub-strates was scrubbed with a toothbrush andrinsed with deionized water until no periphytonwas visible. The periphyton slurry from eachsaucer was then homogenized and treated, asdescribed above, for measurements of chloro-phyll a and periphyton community composition.

NO3-N retention at outwelling edges

Outwelling NO3-N concentration was mea-sured at 10 sandbar outwelling edges before




and after removing resident periphyton fromthe edge during the summer of 1998 (30 June,16 July, and 4 August). Outwelling flow wasconfirmed at each outwelling edge using flores-cent dye injected into sandbar sediments. Dyewas seen flowing out of sandbar sediments,through periphyton mats, and into the mainchannel in all cases. Open-topped clear plasticboxes (30 3 20 3 15 cm) with one end panelremoved were fitted with a 2-cm diameter rub-ber tube in a hole made in the other end panelof the box. Sandbar outwelling edges were iden-tified using fluorescent dye and the boxes werepushed into the sand, disturbing periphyton aslittle as possible. Outwelling discharge wasmeasured after letting the boxes equilibrate fora few minutes by affixing a small plastic bagover the rubber tube with an elastic band. Afterwaiting for one residence time (0.5–2 h, depend-ing on discharge at each location), a water sam-ple was taken with a 60-mL syringe from thecenter of the box for NO3-N determination. Pe-riphyton mats in the box were then removed us-ing a goldfish net and, after waiting for anotherresidence time, the experiment was repeated.Percent retention was calculated for each boxand retention measurements were averaged for2 replicate boxes at each of the 10 sandbar edg-es.

Statistical analyses

Transformations of some of our data were re-quired to meet statistical requirements of nor-mality before analysis. Chlorophyll a measure-ments were natural log transformed, biovolumemeasurements were log transformed, and rela-tive abundance measurements were arcsine andsquare root transformed. Percent cover mea-surements from the transplant experiment andmeasurements of NO3-N retention were nor-mally distributed and needed no transforma-tion.

Differences in NO3-N concentration, chloro-phyll a concentration, relative abundance, andbiovolume of nonfixers and fixers between in-welling and outwelling edges were evaluatedusing t-tests done for the 2 edge types on eachof the 3 sample dates. NO3-N concentrations arereported as mean values averaged for all in-welling edges and all outwelling edges over the3 sample dates. Regression analysis was used todetermine whether chlorophyll a concentration,

total periphyton biovolume, and biovolume orrelative abundance of nonfixers or fixers wererelated to NO3-N concentration at sandbar edg-es. Regression analyses were done on the meanof the 3 biovolume or relative abundance mea-surements for each edge taken over the studyperiod (n 512 independent edges).

A t-test was done on mean % cover of algaein baskets transplanted to inwelling edges ascompared to % cover of algae in control basketsleft at outwelling edges after a 2-wk incubationto determine whether transplanting periphytonfrom original edges caused a change in abun-dance compared to controls. Percent cover of cy-anobacteria in baskets transplanted to outwell-ing edges was compared to % cover of cyano-bacteria in control baskets left at inwelling edg-es using a t-test.

The nutrient-diffusing-substrate experimentwas evaluated using 2-way ANOVA, with sitetype (inwelling vs outwelling) and treatment(control or NO3-N diffusing) as factors to deter-mine whether the location, NO3-N amendment,or some interaction between the 2 factors influ-enced chlorophyll a accrual, total periphytonbiovolume, nonfixer and fixer biovolume, or rel-ative abundance of nonfixers on substrates. Therelationship between NO3-N retention and rateof outwelling discharge was evaluated using lin-ear regression. All statistical analyses were per-formed using Systat 5.02 for Windows (1993.Systat Inc., Evanston, Illinois).

Results

Periphyton differences at inwelling and outwellingedges

Each of the 21 sandbar edges examined inJanuary 2000 was classified as either algal dom-inated (10 sandbar edges) or cyanobacteriadominated (11 sandbar edges). Nine of the 10algal-dominated sandbar edges were outwellingedges (average VHG 5 0.05). All 11 cyanobac-teria-dominated sandbar edges were inwellingedges (average VHG 5 20.20). Quantitativemeasurements of periphyton biovolume at 12sandbar edges on 28 March, 10 April, and 18April 2000 confirmed this pattern. Specifically,inwelling edges were characterized by a N-fix-ing community, whereas outwelling edges weredominated by non N-fixing organisms (Fig. 2).The relative abundance of nonfixers was greater




FIG. 2. Periphyton community composition at sandbar edges averaged over 3 sample dates. Non N-fixingtaxa are represented by the bottom 3 bars and N-fixing taxa are represented by the top 2 bars.

at outwelling edges than inwelling edges on all3 sample dates (t-test; p 5 0.001, 0.028, and0.006 in order of date). Biovolume of nonfixerswas significantly higher at outwelling edgesthan at inwelling edges on all 3 dates. (t-test; p5 0.037, 0.045, and 0.043 in order of date) (Fig.3A). Biovolume of N-fixing organisms was notstatistically different between inwelling and out-welling edges on any sampling date (t-test; p 50.099, 0.306, and 0.260 in order of date) (Fig. 3B).Chlorophyll a was not significantly different be-tween inwelling and outwelling edges on any ofthe 3 sample dates (t-test; p 5 0.512, 0.252, and0.738 in order of date).

Tests of predictions from nutrient hypothesis

When averaged across 3 sample dates, NO3-N was significantly higher at outwelling edges(25 6 3 SE mg/L, n 5 5) than at inwelling edges(7 6 1 mg/L, n 5 9), (t-test; p 5 0.002). NO3-Nconcentration was also significantly higher atoutwelling edges than inwelling edges on eachsample date treated separately (t-test; p , 0.001,p 5 0.002, and p 5 0.040 in order of date). Nei-ther temperature nor chlorophyll a concentrationwas significantly different among edge types.Chlorophyll a concentration along sandbar edg-es showed no relationship with NO3-N concen-

tration at those edges (r2 5 0.068, p 5 0.165);however, total periphyton biovolume was posi-tively correlated with NO3-N concentration (r2 50.141, p 5 0.035). The biovolume of nonfixerswas positively correlated with NO3-N concen-tration at sandbar edges (r2 5 0.468, p 5 0.014)(Fig. 4A). The relative abundance of nonfixerbiovolume in the community was also positivelyrelated to NO3-N concentration at sandbar edg-es (r2 5 0.582, p 5 0.004). In contrast, biovolumeof fixers was negatively related to NO3-N con-centration at sandbar edges (r2 5 0.391, p 50.030) (Fig. 4B).

Transplant experiment. Algae transplantedfrom outwelling to inwelling edges showed asignificant decline in % cover relative to controlalgae that remained at their original edges (t-test; p 5 0.003) (Fig. 5). Cyanobacteria trans-planted from inwelling edges to outwellingedges declined significantly when compared tocontrols (t-test; p 5 0.010) (Fig. 5).

Nitrate-diffusing substrates. Total chlorophylla accrual over the 8-d incubation period wasgreater on clay pots that were amended withNO3-N than on controls (2-way ANOVA; F 512.60, p 5 0.003) (Fig. 6). There was no effect ofedge type (F 5 0.032, p 5 0.860) and no inter-action effect between the 2 factors (2-way AN-OVA; F 5 0.280, p 5 0.604) for chlorophyll a on




FIG. 3. Abundance of non N-fixers and N-fixers at sandbar inwelling and outwelling edges over time. A.—Mean (61 SE) biovolume of non N-fixers on 3 sample dates. On 28 March, n 5 7 for inwelling edges and n 55 for outwelling edges. On 10 and 18 April, n 5 7 for inwelling edges and n 5 3 for outwelling edges. Asteriskindicates significant differences between inwelling and outwelling edges (p , 0.05). B.—Mean (61 SE) biovol-ume of N-fixers for the 3 sample dates. On 28 March, n 5 7 for inwelling edges and n 5 5 for outwellingedges. On 10 and 18 April, n 5 7 for inwelling edges and n 5 3 for outwelling edges. There were no significantdifferences between inwelling and outwelling edges on any date.




FIG. 4. Abundance of non N-fixers and N-fixers as a function of NO3-N concentration at sandbar edges.A.—Biovolume of non N-fixers at sandbar edges on 3 sample dates as a function of NO3-N concentration. B.—Biovolume of N-fixers at sandbar edges on 3 sample dates as a function of NO3-N concentration.

the substrates. No significant effects of treat-ment, edge type, or an interaction between the2 were found for total periphyton biovolume.

Analysis of the community of periphyton onsubstrates revealed additional patterns. Abso-lute biovolume of nonfixers on substrates wasnot affected by treatment (2-way ANOVA; F 51.887, p 5 0.188), site type (F 5 1.353, p 50.262), or an interaction between the 2 factors (F5 3.23, p 5 0.091) (Fig. 7). The same was truefor N-fixer biovolume (F 5 2.233, p 5 0.155; F5 1.822, p 5 0.196; and F 5 0.564, p 5 0.463,

respectively) (Fig. 7). In contrast, the relativeabundance of nonfixers on substrates was af-fected by site (2-way ANOVA; F 5 14.96, p 50.001), treatment (F 5 11.99, p 5 0.003), and aninteraction between the 2 factors (F 5 6.88, p 50.018) (Fig. 8). Relative abundance of nonfixerswas significantly lower on control substratesthan NO3-N diffusing substrates incubated atinwelling edges (post hoc pairwise compari-sons; p 5 0.003) than on either controls (p 50.002) or NO3-N diffusing (p 5 0.001) substratesincubated at outwelling edges (Fig. 8).




FIG. 5. Percent cover of periphyton in transplant and control baskets after 2 wk. Baskets originally contained100% of either algae or cyanobacteria. n 5 3 for inwelling edges and n 5 4 for outwelling edges.

FIG. 6. Mean (61 SE) chlorophyll a concentration on NO3-N diffusing and control substrates incubated atsandbar inwelling and outwelling edges for 8 d. n 5 5 for each treatment (control, NO3-N) at each sandbaredge type (inwelling, outwelling) for a total of n 5 20. A 2-way ANOVA with site type (inwelling vs outwelling)and treatment (NO3-N diffusing vs control) showed a significant main effect of treatment but not site. Nointeraction effect was found. See text for details.




FIG. 7. Mean (61 SE) biovolume of periphyton on control and NO3-N diffusing substrates incubated atsandbar inwelling and outwelling edges (n 5 5 for each treatment at each edge type for a total n 5 20). A 2-way ANOVA with site type (inwelling vs outwelling) and treatment (NO3-N diffusing vs control) showed nosignificant main effects of treatment, site type or an interaction between the 2 factors. See text for details.

FIG. 8. Mean (61 SE) relative abundance of nonfixers on control and NO3-N diffusing substrates incubatedat sandbar inwelling and outwelling edges (n 5 5 for each treatment at each edge type for a total n 5 20). A2-way ANOVA with site type (inwelling vs outwelling) and treatment (NO3-N diffusing vs control) showedsignificant main effects of treatment, site type, and an interaction between the 2 factors. See text for details.Bars marked with the same lower-case letter are not significantly different from each other (post hoc pairwisecomparisons; p , 0.005).




FIG. 9. NO3-N concentration in experimental retention boxes with periphyton present and with periphytonremoved as a function of outwelling discharge.

NO3-N retention at outwelling edges

NO3-N concentration in retention boxes in-creased after periphyton was removed from thebox by an average of 97.6 6 17.6 SE mg/L (Fig.9). Mean retention of outwelling NO3-N over thelength of the box was 80% and ranged from 65to 97%. The % of outwelling NO3-N retained byalgal mats was negatively dependent upon rateof outwelling discharge (r2 5 0.598, p 5 0.009)(Fig. 10).

Discussion

Community differences at sandbar edges

Periphyton communities differed strikinglybetween inwelling and outwelling edges ofsandbars. Algae, diatoms, and nonheterocystouscyanobacteria made up a greater proportion ofthe community at outwelling than at inwellingedges, but also a greater total biovolume of non-fixers existed at outwelling edges than inwellingedges. The opposite pattern was seen for N-fix-ing taxa. The lack of a significant difference inbiovolume of fixers between inwelling and out-welling edges was a result of high variationamong replicate edges (Fig. 3B).

Research in streams has shown that flowthrough subsurface environments causes chang-

es in nutrient concentration relative to the sur-face stream. Patterns and directions of changediffer among streams because of differing bio-geochemical conditions in the surface and sub-surface of each stream. The subsurface is a sinkfor N in some streams (Hill 1990, Hedin et al.1998). In others, the subsurface can be a sourceof some inorganic N species, as has been re-ported for the Rhone (Claret et al. 1997), LittleLost Man Creek, California (Triska et al. 1989),and Sycamore Creek (Valett et al. 1990, Holmeset al. 1994).

Exchange of surface and subsurface waterscan influence stream periphyton. For instance, itis known that periphyton standing crops arehigher at DIN-rich upwelling zones than atdownwelling zones (Coleman and Dahm 1990,Valett et al. 1994). Our findings showed that tax-onomic differences in periphyton communitiesalso occur. Exchange-dependent variation in N-fixing and non N-fixing organisms at sandbaredges may significantly influence whole-streamN cycling relationships.

The N-availability hypothesis

Our 2nd objective was to determine the causeof periphyton community differences. We hy-pothesized that edge-related differences result-




FIG. 10. Effect of periphyton growing at sandbar edges on retention of NO3-N at sandbar outwelling edgesas a function of outwelling rate (n 5 10).

ed from N availability. We suspected that mostof the N available at inwelling edges is organicN and, therefore, unavailable to periphyton. Incontrast, DIN is available at outwelling edges. Ifthis hypothesis is correct, then several predic-tions would follow: 1) NO3-N concentration willbe greater at outwelling than inwelling edges.Mean NO3-N concentration at inwelling edgeswas only 7 mg/L, low enough to limit periph-yton growth (Grimm and Fisher 1986a), butsandbar outwelling edges showed significantlyhigher concentrations. NO3-N concentration atoutwelling edges was also low, but it is 3 to 4times greater than at inwelling edges. The NO3-N increase along sandbar flowpaths in Syca-more Creek is caused by ammonification andsubsequent nitrification of organic N (Holmes etal. 1994). This prediction is true and supportsthe N-availability hypothesis.

2) Abundance of nonfixers will be positivelycorrelated with NO3-N concentration at sandbaredges. Our data showed a strong positive rela-tionship that spanned more than an order ofmagnitude of periphyton biovolume measure-ments (Fig. 4A). Furthermore, both the biovol-ume (Fig. 4B) and relative proportion of fixersin communities at sandbar edges were nega-tively correlated with NO3-N concentration atthose edges. This prediction is, thus, correct,and also supports the N-availability hypothesis.

3) The 3rd prediction is that periphyton com-

munities transplanted to edges with the oppo-site hydrology will decline in abundance rela-tive to controls that remained at their originaledges. Transplant effects were strong. Both al-gae and cyanobacteria declined significantly rel-ative to controls when moved to an edge withthe opposite hydrology (Fig. 5). Other condi-tions such as current velocity remained constantwithin the baskets, so it seems likely that thedecline in biomass was caused by removal of theNO3-N source. Furthermore, cyanobacterialabundance declined when a NO3-N source wasprovided to cyanobacteria by transplantingthem to outwelling edges. This decline wasprobably caused by competition for space withresident algae at outwelling edges because weobserved algal filaments overtaking cyanobac-teria in transplant baskets at outwelling edges.These results also support the N-availability hy-pothesis.

4) The 4th prediction is that artificial sub-strates with no added NO3-N placed at sandbarinwelling edges will grow a community domi-nated by N-fixing taxa when compared to NO3-N amended substrates placed at the same edg-es. Furthermore, more nonfixers and fewer fixerswould be found on substrates placed whereNO3-N is elevated (controls and NO3-N diffus-ing substrates at outwelling edges) than on con-trol substrates placed at inwelling edges. AN-OVA showed no significant effect of site type




(inwelling or outwelling) or treatment (controlor NO3-N) on absolute biovolume of either fixersor nonfixers (Fig. 7). This result was probablyinfluenced by high variability in total biovolumemeasurements among replicates. Measures ofrelative abundance of fixers and nonfixers re-moved the effect of high variability in total pe-riphyton biovolume on substrates. We foundthat relative abundance of nonfixers in com-munities growing on substrates was influencedby both site type and treatment. There was alsoa significant interaction between the 2 factors,meaning that the response of nonfixers to theNO3-N amendment was dependent on site type.Pairwise comparisons of the responses of the 4combinations of treatment and site (Fig. 8)showed that substrates incubated at the lowestNO3-N concentration (controls at inwelling edg-es) grew fewer nonfixers than substrates grownat a higher NO3-N concentration. These resultssupport the N-availability hypothesis in thatthey show that nonfixing organisms dominatein environments with elevated N even if that en-vironment is an inwelling edge that has beenamended with NO3-N.

Analysis of the whole periphyton community(grouping all taxa together) suggested that thereis N limitation of primary production occurringat all edge types, despite higher ambient NO3-N at outwelling edges. We found chlorophyll awas higher on NO3-N diffusing substrates thancontrols regardless of edge type (Fig. 6). How-ever, total biovolume did not match the re-sponse of chlorophyll a, probably because ofhigh variation among total biovolume measure-ments.

Alternative hypotheses. The N-availability hy-pothesis is one of a number of possible alter-natives to explain the periphyton communitydifferences observed at sandbar inwelling andoutwelling edges. None of these hypotheses aremutually exclusive. For example, communitydifferences may be related to temperature dif-ferences at sandbar inwelling and outwellingedges. It is known that cyanobacteria and algaehave different temperature constraints (Tilmanet al. 1986). We rejected this alternative basedon measurements that showed no significantdifferences in temperature between edge types.Second, community differences could also becaused by differences in the fluvial hydrody-namic (current) environment that may exist be-tween inwelling and outwelling edges. Varia-

tions in stream current causing differences inshear stress can influence periphyton commu-nity composition (Stevenson and Peterson 1989).Carling (1992) attributed blooms of algae at thedownstream edge of a gravel bar in a large riverto sheltering from faster currents. In SycamoreCreek, downstream edges may experience lessshearing than upstream edges. However, cur-rent velocities were low during our study, bed-load transport was 0, and macroalgal drift wasnegligible. Furthermore, the periphyton trans-plant experiment equalized hydrologic condi-tions and showed the hypothesized response.Although these tests of alternatives are not ex-haustive, several predictions of the N-availabil-ity hypothesis were strongly supported.

Ecological patterns are often multivariate, andour results do not eliminate the possibility thatother factors might explain more variance.These experiments were done in spring in anecosystem that had been undisturbed by floodor drought (Fisher and Grimm 1988) for sometime. Other factors could explain variation in pe-riphyton in other seasons or successional states.

N-cycling processes occurring along sandbar edges

We measured N retention by algal mats grow-ing at 10 different sandbar outwelling edgesand found that most (60–97%) of the NO3-Navailable in outwelling water was retained overthe 30-cm length of our experimental unit. Thisretention is a product of 2 processes likely oc-curring within the algal mat. First, it seems like-ly that some of the retention at outwelling edgeswas a result of uptake by algae, especially givenwidespread N limitation in Sycamore Creek.Second, some NO3-N may have been removedfrom the system via denitrification within theperiphyton mat, a process previously reportedin Sycamore Creek (Grimm and Petrone 1997).In any case, reduction of NO3-N flux occursclose to sandbar outwelling edges because ofthe presence of algal mats. Consequently, NO3-N that is leaving sandbars is not immediatelyavailable to downstream organisms. There isvery little DIN in surface water entering sand-bars at inwelling edges and fewer nonfixing or-ganisms there; therefore, less retention occursalong inwelling than at outwelling edges.

The rate of NO3-N flux change at sandbar out-welling edges is inversely related to dischargefrom the sandbar (Fig. 10). Both NO3-N uptake




and denitrification will more efficiently removeNO3-N if velocity is low. In the case of denitri-fication, anoxic conditions may also be moreprevalent when water is moving slowly. Otherfactors may also influence NO3-N retention atsandbar outwelling edges, but it is interestingthat so much variation (60%) in retention wasexplained by a purely physical variable.

Spatial considerations

Stream ecologists are becoming aware thatsomething more can be learned about biologicalprocesses in nature by examining how they maybe separated in space (Fisher et al. 2001). Forexample, Vitousek and Howarth (1991) askedhow N limitation can occur in ecosystems giventhat N fixation can alleviate N limitation?Grimm and Petrone (1997) suggested an answerto this question: N fixation and the alleviationof N limitation may be separated in time and orspace. Our chlorophyll a data showed that Nlimitation is occurring at both inwelling edgesand outwelling edges. NO3-N is extremely lowat inwelling edges, which allows fixers to thrivethere. N fixed at inwelling edges becomes partof cyanobacterial biomass. This N cannot alle-viate N limitation locally because water thatmay carry breakdown products and leachatecontaining DIN from cyanobacteria flows fromthe cyanobacterial mat directly into the sandbar.N limitation is somewhat locally alleviated sothat nonfixers predominate at outwelling edgesbecause water flows through the bar, where mi-crobes break down organic N into inorganiccomponents, and emerges at downstream out-welling locations. Locations in the stream whereNO3-N is high enough to support nonfixerswould be rare without sandbar outwelling edg-es.

The coexistence of fixers and nonfixers in Syc-amore Creek during baseflow conditions may,therefore, partly depend on the presence ofsandbars. The coexistence of broad groups ofperiphyton in spatially separate locations maybe important for whole-stream N cycling. N fix-ation at inwelling edges, and elsewhere in thesurface stream where DIN is low, adds N to theecosystem. This N becomes available to down-stream organisms but, because DIN is elevatedat sandbar outwelling edges, some of this N isretained there temporarily in periphyton bio-

mass or permanently by denitrification in thickalgal mats.

Our study is an example of the kind of insightinto stream structure and function that can beobtained by adopting a spatially explicit view.This approach has been seldom used (but seeCooper et al. 1997, Dent and Grimm 1999), de-spite being the conceptual underpinning of thefield of landscape ecology (Turner 1989, Wuand Loucks 1995). In many ways, streams pro-vide a rich opportunity to test the predictionsof landscape ecology in that changes occur ontime scales more congruent with the life spanof research projects in a milieu that can be read-ily manipulated experimentally (Fisher et al.2001).

Acknowledgements

This research was supported by NSF grantsDEB 9727311 and 0075650. We thank J. D.Schade, R. Arrowsmith and N. B. Grimm forhelpful comments on the manuscript. The man-uscript also benefited from comments and sug-gestions made by W. Hill and 2 anonymous re-viewers. We thank members of the ArizonaState University stream team for assistance inthe field and lab. R. Gomez and E. Martı wereespecially instrumental in developing methodsand concepts leading to this work. C. Petersonhelped greatly with algal processing techniques.

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Received: 23 July 2002Accepted: 15 August 2003



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