A Prospectus for Periphyton

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A prospectus for periphyton: recent and future ecological research

Author(s): Scott T. Larned

Source: Journal of the North American Benthological Society, 29(1):182-206.

Published By: The Society for Freshwater Science

DOI: http://dx.doi.org/10.1899/08-063.1

URL: http://www.bioone.org/doi/full/10.1899/08-063.1

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A prospectus for periphyton: recent and future ecological research

Scott T. Larned1

National Institute of Water and Atmospheric Research, P.O. Box 8602, Riccarton,Christchurch, New Zealand

Abstract. The presence, abundance, composition, and growth of periphyton are controlled or influencedby 5 broad classes of environmental variation: disturbances, stressors, resources, hydraulic conditions, andbiotic interactions. In turn, periphyton communities affect water chemistry, hydraulic conditions, habitatavailability, and foodweb dynamics. This review focuses on responses of periphyton communities toenvironmental variation. A specific objective of the review is to identify robust periphytonenvironmentrelationships and insightful concepts. Contributors to J-NABS have led the field in testing and expandingconcepts in periphyton ecology. J-NABS papers about periphyton patch dynamics, light- and nutrient-limited periphyton growth, and the effects of disturbances on periphyton structure and function have beenparticularly influential. However, many topics in periphyton ecology remain unexplored and under-

explored. These topics include resource colimitation, physiological responses to stressors, allelopathy,competitive inhibition and exclusion, and the effects of drag forces and turbulence. Periphyton ecologystudies inJ-NABStend to be multivariable, phenomenological, and nonmechanistic. Such studies provideinformation about temporal and spatial patterns, but rarely provide evidence for the causes of thosepatterns. These studies are often impaired by low statistical power and insufficient experimental control.Periphyton ecology needs more rigorous manipulative experiments, particularly experiments that generateclear relationships between environmental drivers and ecological responses.

Key words: periphyton, physical disturbance, stressors, resource limitation, competitive interactions,hydraulic ecology.

Periphyton communities are solar-powered biogeo-

chemical reactors, biogenic habitats, hydraulic rough-ness elements, early warning systems for environ-mental degradation, and troves of biodiversity. Thisabridged list gives some indication of the ecologicaland cultural importance of periphyton. The roles ofperiphyton in freshwater ecosystems and society havewarranted several book-length reviews (Stevensonet al. 1996 [Fig. 1], Wehr and Sheath 2003, Azim et al.2005). My review focuses on the responses ofperiphyton communities to variation in the chemical,solar, thermal, and hydraulic environment, and tocompetitive interactions. By advancing our knowl-edge of these responses, freshwater ecologists cancontribute to the growth of ecological theory and toimprovements in ecosystem management. Contribu-tions of periphyton ecology to theory and manage-ment are partly based on the availability of robustmechanistic relationships, such as those linkingdiversity to flood frequency (Biggs and Smith 2002),and photosynthesis to light (Graham et al. 1995).

Further contributions from periphyton ecology will

require a more diverse set of periphytonenvironmentrelationships.

The term periphyton refers to assemblages offreshwater benthic photoautotrophic algae and pro-karyotes. Heterotrophic and chemoautotrophic bacte-ria, fungi, protozoans, metazoans, and viruses inhabitperiphytic communities, but are not included in thisreview. Symbiotic and endophytic algae and cyano-

bacteria also are excluded because they are partiallyisolated from the external environment by their hosts.The taxa that are included comprise a diverse group,represented by thousands of taxa, with a size rangespanning 6 orders of magnitude (mmm).

About 150 papers with periphyton ecology as aprimary focus have been published in J-NABS(basedon searches of Web of Science, Google Scholar,Biological Abstracts, and J-NABS bibliographies).Most of these papers can be classified into 7 broadtopics: 1) effects of physical disturbances, 2) effects ofexposure to stressors, 3) limiting abiotic factors, 4)competitive interactions, 5) effects of herbivores, 6)periphytic algae as environmental indicators, and 7)1 E-mail address: [email protected]

J. N. Am. Benthol. Soc., 2010, 29(1):182206 2010 by The North American Benthological SocietyDOI: 10.1899/08-063.1Published online: 5 February 2010

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the roles of periphyton in nutrient cycling in foodwebs and between abiotic pools. The last 3 topics arecovered in companion reviews on interspecific inter-actions (Holomuzki et al. 20101), biomonitoring(Doledec and Statzner 2010), and nutrient dynamics(Mulholland and Webster 2010), and are not dis-cussed here. An additional topic in this review is theinfluence of hydraulic conditions (e.g., drag forcesand turbulence) on periphyton. Despite an encourag-

ing review in J-NABS(Statzner et al. 1988), studies ofperiphytonhydraulic interactions are uncommon.Because J-NABS is one of the principal journals inperiphyton ecology, the specific contributions of J-NABS articles to the topics in this review arehighlighted at the end of each topic section.

A Brief History

My review is focused on research in periphytonecology over the last 25 y (since the start ofJ-NABSin1986), but biologists have studied periphyton for farlonger. The origins of periphyton ecology are difficultto identify precisely because benthic algae have beenused for centuries as model systems for studies ofphototropism, light limitation, and other problems inecophysiology (e.g., Blackman and Smith 1910, Alli-son and Morris 1930; Fig. 1). Two of the earliestreports from periphyton field studies (Fritsch 1906,Brown 1908 [Fig. 1]) concern seasonal variation in thegrowth and composition of stream and pond algae.Similar descriptive studies dominated the field forseveral decades (e.g., Transeau 1916, Eddy 1925[Fig. 1], Butcher 1932). In the 1940s, 2 new researchareas emerged: the effects of abiotic factors onperiphyton composition and abundance, and the use1 Boldface indicates paper was published in J-NABS

FIG. 1. Selected publications in periphyton ecology from the early 20th

century to the present. This timeline illustrates thediversity of research topics, not the original, most important, or most highly-cited publications. Bold font indicates paper waspublished in J-NABS.

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of periphyton communities as indicators of streamhealth. Ruth Patrick (Academy of Natural Sciences,Philadelphia) and R. W. Butcher (British Ministry ofAgriculture and Fisheries) were pioneers of both areas(Butcher 1940 [Fig. 1], 1947, Patrick 1948 [Fig. 1],1949). Periphyton ecology in the modern sense (e.g.,

manipulative experiments and multiple response andexplanatory variables) began in the 1950s andexpanded rapidly. This period coincided with thedevelopment of radiotracers and other technologies, agrowing awareness of human impacts on the envi-ronment, and a focus on freshwater ecosystems bysystems ecologists (e.g., Odum 1956; Fig. 1). The newtechnologies facilitated research in stream metabolismand organic matter budgets (Odum 1956, 1957, Teal1957, McIntire 1966 [Fig. 1]), light-limited primaryproduction (McConnell and Sigler 1959; Fig. 1), andnutrient uptake by periphyton (Whitford and Schu-macher 1961; Fig. 1). Some of the seminal field studies

of lotic periphyton and grazing, succession, andnutrient cycling were published between the late1950s and the early 1970s (e.g., Douglas 1958, Tippett1970, Elwood and Nelson 1972 [Fig. 1], Horne andCarmiggelt 1975). During this period, the HubbardBrook Ecosystem Study, the Walker Branch Water-shed Project, and other ecosystems research programsprovided logistical support for a large cohort ofstream ecologists, including periphyton specialists.The mid-1970s to late 1990s were characterized byrapid growth in studies of natural disturbances andlight and nutrient limitation. A remarkable number ofthese studies were published in J-NABS; among the

most frequently cited are Lowe et al. (1986), Pringle etal. (1988; Fig. 1), Grimm and Fisher (1989), Mulhol-land et al. (1991), McCormick et al. (1996), and Biggset al. (1999a). Since the late 1990s, the number ofdisturbance and resource-limitation studies in J-NABSand other aquatic ecology journals has declined,presumably because of shifts in research agendasand funding.

The last decade has seen continued growth inperiphyton ecology and new conceptual models aboutthe development of periphyton communities andtheir responses to the external environment. One ofthe most intriguing new models is the microbial (orperiphyton) landscape, which views periphyton com-munities as dynamic structures with spatially distrib-uted populations, shifting zones of biogeochemicalactivity, and continual communityenvironment feed-

back (Battin et al. 2003, 2007, Arnon et al. 2007,Besemer et al. 2007, Kuhl and Polerecky 2008). Acorollary of the periphyton landscape perspective isthat processes traditionally associated with large-scalelandscape ecology, such as metapopulation dynamics

and taxonomic turnover, can also be applied toperiphyton landscapes at mm- or mm-scales (Battinet al. 2007).

Many of the advances in periphyton ecology inthe last decade were made possible by paralleladvances in technology. Microelectrodes and op-

todes allow researchers to make detailed biogeo-chemical profiles within periphyton mats (Kuhl andPolerecky 2008). Acoustic and optical velocimetersare used to characterize hydraulic conditions nearand within periphyton communities, and boundary-layer transport to and from periphyton (Hart andFinelli 1999 [Fig. 1], Larned et al. 2004). Confocallaser scanning microscopy has influenced the pe-riphytonlandscape perspective by making fine-scaled studies of intact periphyton structures possi-

ble (Larson and Passy 2005). The development ofpulse-amplitude modulated (PAM) fluorometers inthe 1980s allowed ecologists to measure photosyn-

thetic performance in periphyton communities insitu and without instrument interference. Applica-tions of PAM fluorometry in periphyton ecologyquickly diversified and now range from toxicologyto light and nutrient limitation (Vopel and Hawes2006, Muller et al. 2008).

Physical Disturbances

Ecologists generally define physical disturbances asepisodic events that remove organisms at rates fasterthan rates of accrual or recruitment (Peterson 1996,Biggs et al. 1999a, Stanley et al. 2010). In earlier

studies, including a widely cited J-NABS review(Resh et al. 1988), disturbances were defined asunpredictable events, and were distinguished frompredictable events, such as spring snowmelt. Therationale for this restricted definition was that motileaquatic organisms might be genetically programmedto avoid deleterious predictable events (Townsendand Hildrew 1994). For immobile periphyton, no clearthresholds separate predictable and unpredictabledisturbances, and the restricted definition is unnec-essary.

In broad terms, physical disturbances that affectperiphyton include desiccation, anoxia, freezing,rapid changes in osmotic potential, acute contaminantexposure, substrate movement, and rapid increases inhydraulic forces, heat, and light. Hydraulic forces,substrate movement, and desiccation are frequentlystudied by periphyton ecologists, and their effects arethe focus of this section. Periphyton responses to long-term, sublethal exposure to contaminants and otherstressors are discussed in the following section.Separating stresses and disturbances on the basis of

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duration is artificial, but it highlights the need toconsider disturbances in the context of periphytongeneration times and rates of community succession.Taxa with generation times shorter than disturbancerecurrence intervals are likely to be more resilient tothose disturbances than taxa with longer generation

times (Steinman and McIntire 1990). Similarly, pe-riphyton communities characterized by rapid succes-sion are likely to be more resilient than thosecharacterized by slow succession or many seral stages(Fisher et al. 1982, Poff and Ward 1990).

Periphyton responses to physical disturbances aretypically assessed in 2 phases, responses to the onsetand duration of disturbance, and responses to thecessation of disturbance. Responses to the onset ofdisturbance are related to susceptibility or resistance(e.g., periphyton biomass loss and changes in metab-olism and taxonomic composition). Responses to thecessation of disturbance are related to recovery and

resilience (e.g., regrowth, recolonization, and thedegree to which similar communities develop duringeach recovery phase).

Responses to the onset of disturbances

Field and laboratory investigations indicate thatsusceptibility to hydraulic disturbances (e.g., elevatedshear stress) is influenced by periphyton growth formand age, magnitude of disturbance, rate of onset, andthe hydraulic conditions under which periphytoncommunities develop (Peterson and Stevenson 1992,Biggs and Thomsen 1995). For a given community, a

hydraulic threshold exists beyond which structuralfailure occurs. Biomass loss is rarely a linear functionof disturbance intensity or duration; most biomassloss occurs immediately after the threshold is exceed-ed (Biggs and Thomsen 1995, Francoeur and Biggs2006). Highly susceptible growth forms include chain-forming diatoms, uniseriate filaments, and loosely-attached cyanobacterial mats, and highly resistantforms include prostrate diatoms, and chlorophyte

basal cells and rhizoids (Grimm and Fisher 1989,Biggs et al. 1998a, Benenati et al. 2000, Passy 2007).Susceptibility of periphyton to hydraulic disturbancegenerally increases as intervals between disturbancesincrease. When disturbances are infrequent, thickmats develop with weak attachment to substrata

because of basal cell senescence; these mats can beremoved by small increases in shear stress (Power1990, Peterson 1996). Information about thresholds forperiphyton removal is important for designing envi-ronmental flows intended to remove periphytonproliferations in regulated rivers (Biggs 2000 [Fig. 1],Osmundson et al. 2002).

In addition to the direct effects of increased shearstress, elevated flows affect periphyton by increasingsediment mobility, which leads to abrasion bysuspended sediment and substrate tumbling (Grimmand Fisher 1989, Uehlinger 1991, Biggs et al. 1999a).In field studies, the direct effects of shear stress are

rarely distinguished from the effects of sedimentmovement. However, Biggs et al. (1999a) identifiednatural conditions in which these factors varysomewhat independently. In armored stream reaches,sediment mobility at a given bed shear level is lowerthan in depositional reaches, and both reach typesoccur over a wide range of flood regimes. Biggs et al.(1999a) used 12 streams to create a natural factorialexperiment with sites with high or low sedimentmobility and high or low flood frequencies (a proxyfor bed shear stress). Sediment mobility stronglyaffected periphyton biomass in their study, but floodfrequency had no detectable effect. Subsequent field

and flume studies with varied sediment and velocitylevels support the view that sediment abrasion andtumbling dominate the negative effects of floods onperiphyton (Francoeur and Biggs 2006, Lepori andMalmqvist 2007).

Periphyton responses to the onset of desiccationvary with mat or biofilm thickness, physiognomy,taxonomic composition, and production of extracel-lular mucilage, among other factors (Hawes et al.1992,Blinn et al. 1995, Stanley et al. 2004, McKnight etal. 2007, Ledger et al. 2008). In some taxa, the onset ofdesiccation triggers protective physiological respons-es, such as encystment, cell-wall thickening, andsynthesis of osmolytes that increase resistance tochanges in osmotic potential. Broad taxonomic differ-ences in desiccation resistance are clearly seen in damtailwaters, which are alternately exposed and sub-merged by operating flows. Shallow tailwaters withfrequent exposure often are dominated by sheathedcyanobacteria and deep, rarely exposed areas bysusceptible taxa, such as Cladophora (Blinn et al.1995, Benenati et al. 1998). In general, desiccationresistance is high in mucilaginous cyanobacteria anddiatoms, and low in chlorophytes, rhodophytes, andnonmucilaginous diatoms. Exceptions include desic-

cation-tolerant chlorophytes that occur in both terres-trial and aquatic habitats, such as Chlorella,Klebsormi-dium, and Trebouxia (Morison and Sheath 1985, Grayet al. 2007).

Responses to the cessation of disturbances

Periphyton communities recover from hydrody-namic disturbances by recolonization or by regrowthfrom persistent cells. The relative importance of these



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pathways has been partially evaluated by comparingperiphyton biomass accrual on newly exposed sub-strata (colonization only) with that on substratacontaining persistent tissue (colonization plus re-growth) (Hoagland et al. 1986, Dodds et al. 1996,Downes and Street 2005). Colonization dominates

recovery when substrata are overturned duringfloods, exposing previously buried surfaces. Re-growth might dominate when substrata are abraded,

but not overturned. Community succession on newlyexposed substrata depends on the composition of thepropagule pool (Peterson 1996). Succession on sub-strata with persistent cells depends on the rate ofregrowth and interactions between resident taxa andpropagules. In the latter case, macroalgae withpersistent basal crusts (e.g., Stigeoclonium) oftendominate early successional stages (Power andStewart 1987).

Recolonization and regrowth are also the pathways

by which periphyton recover from emersion anddesiccation. Stanley et al. (2004) predicted thatrecolonization is the main recovery pathway follow-ing rapid drying (e.g., downstream of hydroelectricdams), because resident periphyton have insufficienttime for protective physiological responses. Recovery

by regrowth might be more important at sites withgradual water loss caused by seepage or evaporation.

Physiological recovery from desiccation has beenmeasured in many environments and periphytontaxa. The premier examples are cyanobacterial matsin Antarctic and Mediterranean streams. Upon rewet-ting, these mats reach pre-emersion photosyntheticrates in minutes (Vincent and Howard-Williams 1986,Hawes et al. 1992, Roman and Sabater 1997,McKnight et al. 2007). Mechanisms that promote suchrapid recovery include osmotic changes that reducemembrane and organelle damage and antioxidantproduction (Potts 1999, Gray et al. 2007).

Interactions between disturbances and resource availability

Several field surveys and laboratory stream studieshave been motivated by observations of elevatednutrient concentrations during floods (Grimm andFisher 1989, Mulholland et al. 1991, Humphrey andStevenson 1992, Peterson et al. 1994, Biggs et al.1999b, Biggs and Smith 2002, Riseng et al. 2004). Inthese cases, periphyton experiences both the negativeeffects of sediment movement and the positive effectsof nutrient enrichment. Two general hypotheses have

been tested: 1) that nutrient limitation increasesperiphyton susceptibility to disturbances, and 2) thatnutrient enrichment hastens recovery followingfloods. In field surveys, the direct effects of flood

disturbances and nutrient levels have been confound-ed by variation in bed armoring and herbivory (Biggsand Smith 2002, Riseng et al. 2004). In laboratoryexperiments, the direct effects of increased flow orscour were significant, but the effects of nutrientconcentrations on biomass loss during disturbances

and on subsequent recovery were generally small orundetectable, particularly when concentration differ-ences among treatments were relatively small (Mul-holland et al. 1991, Humphrey and Stevenson 1992,Peterson et al. 1994). The study by Biggs et al. (1999b)was an exception; a 10-fold increase in NO3

2

concentration and a 4-fold increase in dissolvedreactive P (DRP) concentration 10 d before and 2 to9 d after a scouring flood significantly reducedperiphyton biomass loss in experimental streamsand reduced the time required for biomass to returnto predisturbance levels. Most disturbance 3 resourcestudies have addressed periphyton responses to

floods and nutrient availability, but Wellnitz andRader (2003) combined floods with variation in lightlevel and grazing intensity and reported several 3-way (flood 3light 3 grazing) interactions.

Contributions of J-NABS

The roles of physical disturbances in periphytoncommunity structure and succession have been majorthemes inJ-NABSfor most of its history. This research

began beforeJ-NABS(e.g., Douglas 1958), but many ofthe subsequent experiments and syntheses werereported in J-NABS (e.g., Pringle et al. 1988, Grimm

and Fisher 1989, Townsend 1989, Sinsabaugh et al.1991,Cooper et al. 1997,Stevenson 1997a,Lake 2000).The patch dynamics concept was used in some ofthese papers to help explain complex community-level responses to disturbances (Winemiller et al.2010). This concept has been the basis of severalinfluential hypotheses in periphyton ecology, includ-ing: 1) spatial patchiness increases diversity atinterpatch scales (Lake 2000, Hagerthey and Kerfoot2005); 2) fine-scaled patchiness increases variability inlarger-scale processes, such as nutrient spiraling(Pringle et al. 1988); 3) sizes and configurations ofperiphyton patches are determined by processesoperating at multiple scales, including turbulent flowand sediment movement (Sinsabaugh et al. 1991).One limitation of the patch dynamics concept is that itis viewed from a planar perspective. Stream channelsand lake basins are concave, and vertical gradientsexist in the durations and frequencies of emersion andother disturbances. These gradients should producevertical zonation in periphyton communities alongchannel and basin cross-sections. Vertical zonation



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has been reported in dammed rivers, where operatingflows for power generation cause frequent depthchanges (Benetati et al. 1998, Burns and Walker 2000),and in lakes subject to wave disturbances (Hoaglandand Peterson 1990). No comparable cases of flow-driven vertical zonation have been reported for

natural streams and rivers.Among the notable contributions ofJ-NABSpapersto disturbance ecology are studies of simultaneousnegative and positive effects of hydrological distur-

bances on periphyton (e.g., Humphrey and Steven-son 1992, Biggs et al. 1999a, Riseng et al. 2004). Thesedisturbances remove organisms, but they also gener-ate resources (e.g., nutrients and bare substrate),alleviate competition, and transport propagules. Theresponses of periphyton populations and communi-ties to disturbances reflect the balance betweenincreased mortality and emigration, and increasedgrowth, reproduction, and immigration (Stevenson

1990). The J-NABS papers have contributed to themodern view of hydrological disturbances as complexphenomena with pervasive ecological effects in all butthe most stable streams.

The intermediate disturbance hypothesis has alsobeen used as a working model in periphyton studiespublished in J-NABS (McCormick and Stevenson1989, Suren and Duncan 1999) and other journals(Fayolle et al. 1998, Biggs and Smith 2002). Thesestudies focused on patterns of diversity-disturbancerelationships, and whether those patterns confirmedthe prediction of peak diversity at intermediatedisturbance levels. Most of the studies were correla-

tive, and the proximate causes of diversitydistur-bance patterns could not be confirmed. As Lake (2000)noted, biodiversity is not controlled by disturbancealone, but by combinations of disturbance, resourcesupply, reproduction, and other processes. Howdisturbances interact with other biological and eco-logical processes, and how these interactions controlspecies coexistence are central questions in commu-nity ecology (Agrawal et al. 2007). The high diversityand ease of manipulation of periphyton communitiesmake them ideal systems for addressing thosequestions experimentally (Steinman 1993).

Exposure to Stressors

Ultraviolet radiation

Ultraviolet radiation (UVR) is a frequently studiedstressor in phytoplankton ecology, but is less fre-quently studied in periphyton ecology. Currentknowledge of UVR effects on aquatic autotrophscomes primarily from phytoplankton studies. Forperiphyton, UVR exposure varies with riparian

shading, water depth, and dissolved and particulatesuspended matter (Vinebrooke and Leavitt 1998,Kelly et al. 2001, 2003, Frost et al. 2005, Weidmanet al. 2005 [Fig. 1]). UVR exposure also varies duringsuccession in periphyton communities because of self-shading (Kelly et al. 2001, Tank and Schindler 2004).

Variable exposure makes measuring UVR at realisticscales challenging. In most field studies, UVRmeasurements are made above periphyton surfaceswith large (.50-cm tall) spectrophotometers. Morerealistic measurements at periphyton surfaces andwithin periphyton matrices will require microprobes(Garcia-Pichel 1995).

Molecular and physiological studies of the effectsof UVR on aquatic photoautotrophs have focused ondamage to deoxyribonucleic acid (DNA) and D1, themain structural protein of photosystem-2. DNAdamage delays mitosis, and damage to D1 reduceselectron transport and slows the generation of

reducing power for C fixation (Grzymski et al.2001, Helbling and Zagarese 2003). Collectively,these changes can reduce growth rates, but studiesof UVR-effects on periphyton growth have hadmixed results. Growth in UVR-exposed periphytonwas suppressed in some laboratory and field studies(Bothwell et al. 1993, Kiffney et al. 1997, Frost et al.2007 [Fig. 1]), but no effects were detected in otherfield studies (DeNicola and Hoagland 1996, Hill etal. 1997, Hodoki 2005, Weidman et al. 2005). Thegenerally weak effects of UVR on periphytongrowth have been attributed to protective UVR-absorbing compounds, rapid repair of UVR-induced

damage, self-shading, attenuation by tree canopiesand water, and solar trophic cascades (Bothwell etal. 1994, Francoeur and Lowe 1998, Frost et al. 2007).Solar trophic cascades occur when the negativeeffects of UVR on herbivores reduce grazing lossesin periphyton, compensating for direct negativeeffects of UVR on periphyton (Bothwell et al.1994). As with periphyton growth, UVR exposureat natural levels appears to have moderate toundetectable effects on periphyton taxonomic com-position (DeNicola and Hoagland 1996, Vinebrookeand Leavitt 1996, Tank and Schindler 2004). Long-term exposure to elevated UVR leads to shifts inperiphyton communities to a predominance of UVR-tolerant taxa (Vinebrooke and Leavitt 1996, Navarroet al. 2008). A comparison of the responses of UVR-tolerant and UVR-sensitive periphyton to Cd expo-sure indicated that UVR-tolerant periphyton werealso relatively Cd-tolerant (Navarro et al. 2008).UVR exposure and metal exposure both inducereactive O2 in algal cells, and UVRCd cotolerancemight be caused by similar physiological responses



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to both stressors, including enhanced antioxidantactivity (Prasad and Zeeshan 2005).

Thermal stress

Optimal temperatures for growth of hot-springalgae can be .50uC (Ciniglia et al. 2004, Liao et al.

2006), but optimal temperatures for most periphytonrange from 10 to 30uC, and higher temperaturesinduce heat stress and reduce growth (DeNicola1996). Direct physiological effects of high tempera-tures include protein and nucleic acid denaturation,photosystem degradation, and respiration in excess ofC fixation (Davison 1991, Wahid et al. 2007).

Optimal growth temperatures and maximum tem-peratures for survival bracket the high-temperaturetolerance ranges of periphyton. Some evidence indi-cates that heat tolerance varies among major taxa.Cyanobacteria generally tolerate higher temperatures(.30uC) than do chlorophytes, which tolerate highertemperatures than do diatoms and rhodophytes(DeNicola 1996). Variation in tolerance suggests thatthermal regimes influence spatial patterns in periph-yton communities. Surveys along thermal gradientscreated by coolant water outfalls and geothermalsprings provide some support for this proposition,with cyanobacteria dominant near thermal sourcesand diatoms dominant in cooler distal reaches(Squires et al. 1979, Bonny and Jones 2003). Additionalsupport comes from heated artificial streams, inwhich rhodophytes were eliminated at temperatures12.5uC above ambient, and cyanobacteria dominated

at temperatures.

30uC (Wilde and Tilly 1981). Last,the effect of water temperature is often significant in

multivariate analyses of geographic or seasonalvariation in periphyton composition (e.g., Wehr1981, Griffith et al. 2002). However, other environ-mental factors covary with temperature, and con-trolled experiments are the best means of assessingdirect thermal effects.

pH stress

Studies of stream and lake acidification generallyfocus on the effects of anthropogenic acidification

caused by mine drainage and fallout from smeltersand power plants. Many sources of natural acidifica-tion exist (e.g., wetland outflows, volcanic ashfall,pyrite weathering), but these have received lessattention as stressors (for exceptions, see Sheath etal. 1982, Sabater et al. 2003, Baffico et al. 2004).Naturally acidic freshwater environments are inhab-ited by acidophilic periphyton (DeNicola 2000, Gross2000). The taxa that make up these communities tendto share some physiological traits, including efficient

C uptake (to cope with low inorganic C concentra-tions), and tolerance or resistance to proton influxthrough cell membranesa necessity in H+-richenvironments (Gross 2000). At sites of recent, anthro-pogenic acidification, the original periphyton com-munities are often replaced by depauperate commu-

nities of acidophilic chlorophytes and diatoms(Turner et al. 1991, Verb and Vis 2000, Greenwoodand Lowe 2006). Recovery of algal diversity andreduction in acidophile dominance are indicators ofsuccess in remediation of acidified ecosystems (Vine-brook 1996, Vinebrooke et al. 2003).

The direct effects of acidification on algal cells arenot well known, but might include osmotic stress anddisruption of cell division (Gross 2000, Visviki andSantikul 2000). In addition to direct toxic effects,acidification increases exposure to other stressors.Stream acidification often is accompanied by metaldissolution and subsequent deposition of metal

hydroxides downstream of the acid source. Acidicfreshwater typically is enriched in dissolved Fe, Zn,Ni, Hg, Al, and other metals. Potential negative effectsof dissolved metal exposure include alterations inmembrane permeability, inhibition of photosyntheticelectron transport, and metalphosphate coprecipita-tion, which can reduce P availability (Pettersson et al.1985, Genter 1996, Kinross et al. 2000). Deposition ofoxidized metals in moderately acidic streams elimi-nates many periphyton taxa and favors a smallnumber of tolerant taxa (e.g., Ulothrix, Mougeotia,andZygogonium) (Niyogi et al. 1999, 2002, Kleeberg etal. 2006). The properties of these algae that confertolerance to oxidized metal deposition are unknown,

but might include growth rates that exceed the rate ofdeposition, or mucilaginous sheaths that preventdeposition.


Studies of abiotic stressors published in J-NABStend to focus on multivariable problems, rather thandirect effects of single stressors. For example, Fair-child and Sherman (1993) used nutrient-diffusingsubstrata in 12 lakes representing a broad aciditygradient (pH 4.48.8) to explore the combined effectsof acidification and nutrient limitation on periphytongrowth and composition. Their results suggested thatC enrichment enhanced periphyton growth, whichlends support to the hypothesis that acidificationcauses C limitation. Several J-NABS papers thataddressed periphyton responses to multiple stressors(e.g., acidity, herbivory, and nutrient limitation) usedexploratory multivariate analyses (Vinebrook 1996,Naymik et al. 2005, Cao et al. 2007, Stevenson et al.



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2008). Responses to individual stressors were notidentified or quantified in these studies because ofcovariance or because ordination axis scores were theonly dependent variables reported. Vinebrook (1996)used reciprocal periphyton transplants and herbivoreexclosures to study periphyton responses to a lake

acidity gradient. This approach controlled for effectsof herbivory and colonization sources, but the directeffect of acidity could not be separated from otherabiotic factors that varied among lakes or fromenclosure artifacts. Complex periphyton responses tomultiple stressor gradients are important in environ-mental monitoring programs and indicator analyses,

but it is also important to identify and quantifyunivariate periphytonstressor relationships. The lat-ter are needed to predict the effects of stressorexposure, detect trends, and identify mechanisms bywhich stressors affect periphyton.

Limiting Abiotic Factors

Periphytic organisms vary in their minimumresource requirements for survival because of differ-ences in physiology and morphology, e.g., diatomshave high Si requirements and N2-fixing cyanobacte-ria have high Mo requirements compared with othermajor taxonomic groups (Stal 1995). These differencesare well established for many planktonic algae, forwhich minimum cell quotas for nutrients and com-pensation light intensities have been defined inculture (Reynolds 2006). Minimum resource require-ments are unknown for most periphyton taxa, but

these requirements are certain to vary as they do forphytoplankton (Hill 1996).

Transient changes in physiological condition andgrowth form lead to short-term variation in periph-yton resource requirements (Graham et al. 1995,Hillebrand and Sommer 1999). For example, nutri-ent-replete periphyton might have higher light-satu-rated photosynthetic rates and higher photosyntheticefficiencies than nutrient-deficient periphyton (Taul-

bee et al. 2005, Hill and Fanta 2008). However, thescarcity of autecological studies of periphyton makespredicting changes in resource requirements difficult.Resource-limitation studies generally address re-sponses of whole periphyton communities, notindividual taxa. It is implicit in community studiesthat aggregate responses of multiple taxa are beingmeasured, and these responses might include changesin taxonomic composition and relative abundance(e.g., Lohman et al. 1991, Hill and Fanta 2008).Specific responses depend on the time scale ofresource variation. Responses to short-term (,1 d)variation in resources are primarily physiological

(e.g., Wellnitz and Rinne 1999). Responses to long-term variation, such as month-long nutrient additions,are dominated by biomass and taxonomic changes(e.g., Harvey et al. 1998). Responses to very long-term(moy) variation include secondary effects, such asspecies turnover and changes in foodweb structure

(Blumenshine et al. 1997, Slavik et al. 2004). Thefollowing discussion considers the main effects oflight-, temperature- and nutrient-limitation on pe-riphyton communities, and pairwise interactions

between these factors.

Light limitation

Most periphytic organisms are obligate photoauto-trophs that use sunlight to generate reducing powerand dissolved inorganic C to produce carbohydrates.Some periphyton taxa are facultative photohetero-trophs (sunlight + organic C substrates) or chemoor-

ganoheterotrophs (organic compounds for reducingpower + organic C substrates). Nutrient assimilationin photoautotrophs is catalyzed by chemical energy inC compounds, and light energy is required to producethose compounds. Consequently, nutrient limitationis detected frequently under high-light conditions andrarely under low-light conditions (Hill and Knight1988, Bourassa and Cattaneo 2000, Larned and Santos2000, Greenwood and Rosemond 2005).

Facultative heterotrophy has been proposed as amechanism that allows periphyton communities topersist under severe light limitation (Tuchman 1996,Tuchman et al. 2006). Heterotrophy is energetically

favored only at high dissolved organic C (DOC)concentrations, so facultative heterotrophy should berestricted to dark, DOC-rich environments, such as lakesediments and the interiors of dense periphyton mats.

The influence of riparian tree canopies on lighttransmission to stream periphyton has been a prom-inent research topic since the 1950s (e.g., McConnelland Sigler 1959, Hansmann and Phinney 1973, Hilland Knight 1988, DeNicola et al. 1992, Larned andSantos 2000, Hill and Dimick 2002, Ambrose et al.2004). Most of these studies were categorical compar-isons of periphyton under canopy gaps (high light) ordense canopies (low light). Studies that use continu-ous gradients in riparian light transmission providemore information about complex responses to lightinput. For example, Hill and Dimick (2002) measuredin situ periphyton photosynthesis over the wideirradiance range created by a heterogeneous forestcanopy and reported nonlinear effects of irradianceon photosynthetic efficiency, photosaturation, lightutilization efficiency, and pigment concentrations.Heavily shaded photoautotrophs undergo a physio-



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logical process of photoacclimation that increasesphotosynthetic efficiency at low light levels andreduces the irradiance required for maximum photo-synthesis (Hill 1996).

At finer spatial scales, the 3-dimensional structureof periphyton communities causes variation in light

transmission to cells within the community matrix.Vertical light attenuation increases with increasingperiphyton density and thickness (Meulemans 1987,Dodds 1992, Johnson et al. 1997). Presumably, algaeat the bases of periphyton mats are shade-acclimated.Supporting evidence for this assumption includesreports of increased photopigment concentrations atmat bases (Tuchman 1996) and a positive relationship

between photosynthetic efficiency and depth in afilamentous periphyton mat (Dodds 1992).

Temperature limitation

Thermal energy is not a resource in the strictsense; it is not consumed and is not an object ofcompetition. However, periphyton (like all organ-isms) requires thermal energy for enzyme-catalyzedreactions, and thermal energy deficits can limitgrowth and other physiological processes. Algalphotosynthesis and growth respond unimodally totemperature variation, as they do to light variation(Graham et al. 1995, ONeal and Lembi 1995).Temperatures corresponding to maximum photosyn-thesis and growth in freshwater algae (excludingextremophiles such as hot-spring algae) range from10 to 30uC (Butterwick et al. 2005). This range

suggests that thermal energy could be a limiting orcolimiting factor in cold climates. Empirical modelsfor periphyton indicate that photosynthetic ratesincrease with temperature over a 5 to 25uC range(Morin et al. 1999), and experimental resultsindicate positive relationships between light-saturat-ed photosynthesis and temperature, with a rate ofchange caused by a 10uC increase in temperature(Q10) 2 (DeNicola 1996). Temperature acclimationcan reduce the severity of temperature limitation.Algae that are acclimated to low temperature havehigher maximum photosynthetic rates, lower tem-perature optima for photosynthesis, and higherconcentrations of C-fixing enzymes than nonaccli-mated algae (Davison 1991).

Thermal energy is unlikely to be the sole limitingfactor for periphyton under natural light and nutrientlevels. Temperature acclimation incurs nutrient costsfor increased enzyme synthesis, and low tempera-tures might lead to nutrient limitation rather thantemperature limitation per se. Thermal energy could

be the sole limiting factor under light- and nutrient-

replete conditions (DeNicola 1996), but these condi-tions are rare in natural aquatic systems.

Nutrient limitation

Nutrient limitation is one of the best-studied topicsin periphyton ecology. The high level of interest in

nutrient limitation reflects concern about eutrophica-tion and recognition of the role of nutrient limitationin community and ecosystem processes (Rosemond1993, Smith et al. 1999, Hillebrand 2002 [Fig. 1],Holomuzki et al. 2010). Studies of nutrient limitationin periphyton generally focus on macronutrients (e.g.,N, P, Fe, Si), and rarely on micronutrients (e.g., Mo, B,Zn) (but see Pringle et al. 1986). Nutrients that are inlow demand relative to availability (e.g., K, Mg) arerarely limiting. Other nutrients (e.g., N, P, Si) arefrequently limiting because demand is high relative toavailability. For a 3rd class of nutrients (e.g., Fe, Ca),

great taxonomic and geographical variation in de-mand and availability suggests that limitation rangesfrom negligible to severe.

A common goal in nutrient limitation studies is toidentify a single nutrient that controls periphytongrowth because its availability relative to demand islower than any other nutrient. The concept of single-nutrient limitation is enshrined in Liebigs Law of theMinimum, which states that plant yield declines asthe scarcest nutrient is depleted (De Baar 1994). Theexpectation that periphyton growth will be limited bya single nutrient might have originated with influen-tial studies of single-nutrient limitation in phyto-

plankton cultures (Droop 1974). Comparable resultsare not always observed in periphyton studies, inwhich N, P, or other nutrients can be colimiting(Francoeur et al. 1999, Dodds and Welch 2000,Francoeur 2001[Fig. 1]).

Discrepancies between Liebigs Law of the Mini-mum and experimental results for periphyton haveseveral causes. In some studies, multiple-nutrientenrichment causes switching between single limitingnutrients. A more fundamental discrepancy iscommunity colimitation, which occurs when periphy-ton communities contain taxa that are limited bydifferent nutrients, and multiple-nutrient enrichmentenhances growth in more taxa than single-nutrientenrichment. Community colimitation often occurs innatural phytoplankton communities, as indicated bydifferential nutrient limitation assays (Arrigo 2005,Danger et al. 2008, Saito et al. 2008). Communitycolimitation appears to be common in periphyton(Francoeur 2001), but differential nutrient limitationin periphyton is rarely tested (Fairchild and Sher-man 1993).



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Nutrient limitation has been assessed in manyperiphyton studies, using several different methods.Differences in methods can affect the outcomes ofthese studies, and obscure general patterns (Fran-coeur 2001). Examination of ambient nutrient concen-trations is the most economical method for assessing

nutrient limitation, but it has some short-comings.Periphyton growth rates are not always positivelycorrelated with ambient nutrient concentrations. Infact, growthnutrient relationships can be inverse

because of ambient nutrient depletion by fast-growingperiphyton (Welch et al. 1988, Stevenson et al. 2006).Different molecular forms of a given nutrient vary in

bioavailability, which increases uncertainty in con-centrationgrowth relationships (Saito et al. 2008).Ratios of 2 or 3 ambient nutrient concentrations (e.g.,N:P:Si) provide information about their relativeavailability, but not about the nutrient requirementsfor periphyton growth (Francoeur et al. 1999, Stelzer

and Lamberti 2001). Cellular nutrient concentrationsand ratios may be used in lieu of ambient nutrients toassess nutrient limitation (e.g., Hillebrand and Som-mer 1999), but these measures can also be unreliable.Periphyton taxa and communities vary in nutrientstorage capacity, and it is rarely clear whether cellularnutrient levels reflect nutrient storage capacities ornutrient requirements for growth.

Experimental nutrient addition is generally a morereliable method for assessing nutrient limitation thanexaminations of nutrient concentrations. Nutrientadditions have been used in periphyton studies for60 y, starting with Huntsman (1948; Fig. 1). Most of

these studies used nutrient diffusing substrata (NDS)that release dissolved nutrients from enriched mediainto porous substrata on which periphyton attachesand grows (e.g.,Coleman and Dahm 1990,Francoeuret al. 1999). Limiting nutrients are then identified bycomparing the biomass on substrata enriched withdifferent nutrients. Other studies have used whole-stream nutrient enrichment (Peterson et al. 1993,Greenwood and Rosemond 2005). Two general issuesare addressed in nutrient addition studies: whetherperiphyton growth is nutrient-limited (and by whichnutrients), and the effects of nutrient limitation onperiphyton community composition and succession.The 1st issue is usually addressed with NDS deploy-ments that are brief enough to prevent switching

between limiting nutrients, generally ,1 mo.The 2nd issue, concerning nutrient-limited commu-

nity development, is addressed with long NDSdeployments or whole-stream enrichment. The resultsof these studies indicate that nutrient availabilityinfluences periphyton succession and mediates inter-specific interactions. One of the clearest examples of

these effects comes from a comparison of NO32-

enriched and unenriched substrata in SycamoreCreek, Arizona (Peterson and Grimm 1992). In thatstudy, unenriched substrata were dominated bydiatoms with N2-fixing endosymbiontic cyanobacteriaduring early successional stages, and by N2-fixing

cyanobacteria during later stages. NO32

-enrichedsubstrata were initially colonized by non-N2-fixingdiatoms and filamentous chlorophytes and later, bycyanobacteria. Seral stages were more apparent, anddiversity higher, on NO3

2-enriched substrata than onunenriched substrata. General relationships betweenperiphyton diversity and the availability of limitingnutrients are still elusive; enrichment experimentshave resulted in increased, decreased, and unchangeddiversity (Carrick et al. 1988, Pringle 1990, Miller et al.1992, Peterson and Grimm 1992, Greenwood andRosemond 2005).

To sustain long-term growth, periphyton commu-

nities require nutrients from external sources to offsetlosses. The major pathways for external nutrientsupplies are advection from the overlying watercolumn and diffusion or upwelling from underlyingsubstrata (Pringle 1987, Henry and Fisher 2003).Nutrient recycling within dense periphyton matsand biofilms can temporarily uncouple periphytonfrom external nutrient sources (Mulholland 1996,Mulholland and Webster 2010). Internal recyclingcannot sustain periphyton indefinitely, but it can besurprisingly efficient over short time scales. Inlaboratory periphyton communities, recycling ac-counted for 10 to 70% of the P uptake, and daily P

turnover was ,15%/d (Mulholland et al. 1995,Steinman et al. 1995). Periphyton communities arelikely to acquire nutrients from multiple sourcessimultaneously. Observations of vertical gradients innutrient concentrations and enzyme activities withinperiphyton communities suggest that surface cellsrely on water-column nutrient sources, whereas cellsin the matrix rely on sediment-derived nutrients andrecycling (Wetzel 1993, Mulholland 1996).

Calcareous periphyton mats have a unique mech-anism for P recycling (Noe et al. 2003). Daytimephotosynthesis raises pH levels within mats, whichpromotes rapid P precipitation with and adsorption tocalcium carbonate. Respiration at night reduces pHlevels within mats, which promotes calcium carbonatedissolution and P desorption. In a P tracer study, Noeet al. (2003) estimated that 80% of P uptake byperiphyton was initially bound to Ca, and thisfraction dropped to 15% after 1 d because of bioticuptake. P enrichment can lead to the replacement ofcalcareous cyanobacterial mats by filamentous chlor-ophytes, which lack the P adsorptiondesorption



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mechanism, but have higher growth potential(McCormick and ODell 1996).

Light 3 nutrient interactions

Tests of nutrient 3 light interactions have beenmade in natural streams with nutrient diffusing

substrata and water-column enrichment beneathriparian canopy gaps and closed canopies (Lowe etal. 1986, Hill and Knight 1988, Larned and Santos2000, Von Schiller et al. 2007) and in artificial streamswith water-column enrichment and shade screens(Rosemond 1993, Bourassa and Cattaneo 2000, Hilland Fanta 2008). In the field studies, increasedirradiance generally enhanced periphyton growth,nutrient enrichment had little or no detectable effect,and the nutrient 3 light interaction terms (whentested) were rarely significant. Possible explanationsfor the lack of detectable effects of nutrient enrich-

ment included consumption of periphyton in en-riched treatments by grazers and competitive inhibi-tion by benthic heterotrophs. In contrast, Rosemond(1993), Hill and Fanta (2008), and Hill et al. (2009)reported significant main effects of both light andnutrient levels in artificial streams. Hill et al. (2009)used simultaneous gradients in DRP concentrationand irradiance to quantify nutrient 3 light interac-tions. In that study, the positive effects of DRPenrichment on periphyton growth increased withincreasing irradiance. Photoinhibition was apparentat high irradiance and low DRP concentrations, andDRP enrichment alleviated photoinhibition, presum-

ably through increased synthesis of protective pig-ments. Colimitation at low light and DRP levels inthese studies was less apparent, although a residualanalysis in the study by Hill and Fanta (2008)indicated that P-enrichment enhanced growth at lowlight levels.

One of the predicted outcomes of nutrient-lightcolimitation is an increase in cellular nutrient levelswith decreasing irradiance caused by the nutrientrequirements of shade acclimation (Sterner et al. 1997,Hessen et al. 2002). Sterner et al. (1997) developed thelight:nutrient hypothesis to explain how the balanceof light energy and nutrient supplies controls algalproductivity and stoichiometry in lakes. In its originalformulation, the hypothesis was based on qualitativecomparisons of low and high light:P ratios. Highratios were predicted to cause P limitation and lowratios to cause C limitation. The light:nutrienthypothesis was subsequently tested with periphyton

by Frost and Elser (2002), Hill and Fanta (2008), andHill et al. (2009). In these latter studies, variation inlight intensity did not affect periphyton C:P ratios or

cellular P concentrations as predicted, although P-enrichment clearly increased productivity. However,Hill et al. (2009) reported a negative relationship

between cellular N and light intensity, a result thatsuggested that Nlight colimitation was in effect, notPlight colimitation. Support for the light:nutrient

hypothesis as it applies to periphyton is equivocal atpresent, but further testing could be done by varyingthe concentrations of nutrients other than P.

Temperature interactions with light and nutrients

Temperature 3 light interactions in periphytonhave been tested in several experiments (Graham etal. 1985, 1995, ONeal and Lembi 1995). Graham et al.(1995) used a high-resolution design (58 temperature3 light combinations) and reported that optimal andcompensation irradiances for photosynthesis in-creased with temperature up to ,30uC. At highertemperatures, net photosynthesis decreased across thelight gradient. Reduced photosynthesis at high tem-peratures is partly caused by photorespiration, ascellular CO2 concentrations decrease with increasingtemperature more rapidly than O2 concentrations(Davison 1991).

The effects of temperature 3 nutrient interactionson periphyton communities have not been studiedunder controlled conditions. However, seasonal NDSdeployments indicate that the frequency and severityof nutrient limitation increase during warm seasons(Allen and Hershey 1996,Francoeur et al. 1999). Themost likely physiological basis for temperature-

dependent nutrient limitation is that respiration andphotosynthesis rates increase with temperature,which increases nutrient demand for C fixation,

biomolecule synthesis, and other growth-relatedprocesses (Falkowski and Raven 2007).


Resource-limited periphyton metabolism andgrowth have been the topics of many J-NABSpapers.Several of the papers are from multivariable studiesthat tested for interactions between resource avail-ability and physical disturbances or herbivory (Mul-

holland et al. 1991, Humphrey and Stevenson 1992,Gafner and Robinson 2007). These latter paperscontributed to an emerging picture of the relativeimportance of processes that control periphytongrowth and composition. Resource limitation isunlikely to have a strong influence if disturbances orgrazing pressure maintain periphyton at low-biomasslevels and early successional stages (Biggs 1996,Steinman 1996). In turn, light limitation is often moresevere than nutrient limitation, as indicated by the



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general lack of response to nutrient enrichment atvery low light levels (e.g., Lowe et al. 1986,Ambroseet al. 2004). However, it should be noted that theprimacy of light limitation in periphyton field studiesmight reflect the limited range of environmentsstudied, not a strict physiological hierarchy of limiting

factors. The most common environments used forcomparisons of light and nutrient limitation in J-NABS papers were densely shaded, mesotrophicstreams. Comparisons made over broader gradients(from ultraoligotrophic to hypereutrophic and fromdensely-shaded to full sun) might provide a moreaccurate view of resource limitation.

Nutrient limitation studies in J-NABShave focusedon N, P, or both. In species-rich periphyton commu-nities, community colimitation might involve .2nutrients, simultaneously or sequentially (Passy2008). Enrichment studies with multiple nutrientsand tests of differential nutrient limitation among the

populations in mixed-species communities haveadvanced our understanding of phytoplankton co-limitation (Arrigo 2005). Similar studies are needed toadvance periphyton ecology, although these studiescould be challenging to design and interpret becauseof spatial variation in the forms and severity ofnutrient limitation within periphyton communities(Burkholder et al. 1990, Johnson et al. 1997).

The NDS periphyton assay has been a popular toolfor J-NABS contributors; NDS results appear in 15 J-NABSpapers, and the results of 237 NDS assays werecompared in a meta-analysis published in J-NABS(Francoeur 2001). InJ-NABSpapers, NDS assays werecombined with a range of environmental variables,including riparian canopy removal (Lowe et al. 1986),lake acidification (Fairchild and Sherman 1993),salmon carcass addition (Ambrose et al. 2004), andzebra mussel invasion (Pillsbury et al. 2002). TheNDS approach has been productive, but it has manylimitations, including uncertainty about nutrientdiffusion rates and whether the nutrient sourcesimulated by NDS is the natural substrate or theoverlying water (Pringle 1987, Coleman and Dahm1990, Hillebrand 2002, Rugenski et al. 2008).

Hydraulic Conditions

The pervasive effects of flow on benthic organismsare evident to most aquatic ecologists. The paper thatpopularized the idea of flow as the master variable inlotic ecosystems has been cited .300 times (Poff et al.1997). Experiments and field surveys have generatedrelationships between stream flow and periphyton for,100 y (e.g., Brown 1908). However, it is not alwaysclear in these studies which components of stream

flow directly affected periphyton or whether theresearchers were measuring the most relevant vari-ables. Two explanatory variables, volumetric dis-charge and velocity in the downstream direction, areused in most flowbiota studies. Velocity is usuallymeasured at the water surface or at a depth thought to

correspond to vertically-averaged velocity (e.g., 60%

of total depth). In many cases, the measurement depthis in the outer or logarithmic portion of the benthic

boundary layer (the region of water column influ-enced by friction at the benthos). These velocitymeasurements are referred to as free-stream velocities(e.g., Poff et al. 1990, Francoeur and Biggs 2006).Discharge and free-stream velocity might be correlat-ed with hydraulic processes that affect benthicorganisms, but they are rarely direct causes of

biological changes (Biggs et al. 1998a, Hart and Finelli1999). For example, periphyton detachment duringperiods of elevated discharge is not caused by free-

stream velocity per se (e.g., Horner et al. 1990), but bydrag and lift acting on periphyton. Spatially andtemporally averaged metrics, such as discharge andfree-stream velocity, do not accurately describe thehydraulic conditions that benthic organisms experi-ence. Metrics that describe near-bed flow at spatialand temporal scales relevant to periphyton include

bed shear stress and near-bed turbulence intensity(Statzner et al. 1988, Nikora et al. 1998a, Stone andHotchkiss 2007).

The focus of this section is the influence ofhydraulic conditions on periphyton communities.The term hydraulic conditions is used here to refer tothe near-bed water movements that impinge onperiphyton communities and is distinguished fromhydrological conditions, which refer to stream flowregimes (Stevenson 1997a).

Solute transport

Studies of hydraulic effects on solute transport to orfrom periphyton have focused on N, P, and C uptakeand O2 release (Riber and Wetzel 1987, Borchardt1994, Larned et al. 2004). These solutes move betweenthe water column and periphyton in several steps:rapid, turbulent transport to and from the near-bedregion, slower transport near and within periphytonmatrices, mass-transfer through the viscous sublayers(VSLs) of benthic boundary layers, and transportthrough cell membranes. These steps can be viewedas resistors in series; the slowest step poses thegreatest transport resistance and will control nutrientuptake rates (Larned et al. 2004). Transport throughouter benthic boundary layers is mediated by turbu-lent diffusion and is rarely rate-limiting; either mass-



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transfer through VSLs (by molecular diffusion) ormembrane transport (by diffusion or carrier-mediatedtransport) limits uptake rates under most conditions.Nutrient mass-transfer rates increase as concentrationgradients steepen and VSL thickness decreases.Membrane transport increases as concentration gra-

dients steepen and carrier densities increase. Flowexperiments indicate that mass-transfer can controluptake by benthic and epiphytic algae over a widevelocity range (Cornelisen and Thomas 2002, Larnedet al. 2004). At low velocities, transport resistance iscaused by thick VSLs that cover the benthos. At highvelocities, most of the transport resistance is caused

by individual VSLs that surround filaments and otherstructures that protrude into regions of turbulent flow(Ry et al. 2002, Larned et al. 2004).

Variation in uptake rate-limiting steps and theircontrols suggests that some periphyton taxa havemorphological or physiological traits that maximize

nutrient acquisition. For example, long filamentousand stalked algae with high surfacevolume ratios(e.g., Ulothrix, Audouinella, Didymosphenia, Rhizoclo-nium) often occur in nutrient-poor streams (Biggs etal. 1998b, Shea et al. 2007). This pattern might beunexpected because large algae presumably havegreater nutrient requirements than small algae.However, elongate algae often protrude from thenear-bed region into the overlying turbulent flow,where mass-transfer resistance is lower (Steinman etal. 1992, Larned et al. 2004). In nutrient-rich water,light limitation, disturbances, and herbivory might bemore important than nutrient acquisition, and elon-gate growth forms might not be optimal. In theseenvironments, adaptive traits include rapid growth,shade tolerance, high reproductive output, and anti-herbivore defenses (Steinman et al. 1992, Biggs et al.1998b).

Drag forces

Hydrodynamic drag affects periphyton coloniza-tion, growth, survival, and morphology. Some obser-vational studies of periphyton have linked broadmorphological classes (e.g., crustose, mucilaginous,densely-branched, and filamentous algae) to variationin free-stream or near-bed velocities (e.g., Parodi andCaceres 1991, Biggs et al. 1998a). The results of thesestudies suggest that compact, prostrate forms repre-sent adaptations to high-drag environments com-pared with filamentous and upright forms. A morerigorous approach for assessing morphologydragrelationships is to manipulate flows or transplantperiphyton between hydraulic environments andobserve subsequent changes in morphology and drag

forces. Such experiments are common in seaweedecology (e.g., Koehl et al. 2008), but rare in periphytonecology. Ironically, the sole J-NABS paper abouteffects of hydrodynamic drag on autotroph morphol-ogy concerned a terrestrial plant (Vogel 2006).

The drag force acting on periphyton has 2 compo-

nents, both originating from fluid viscosity. Skinfriction (or viscous drag) is caused by localized fluidshear across organism surfaces; form drag is caused

by large-scale pressure variations over whole com-munities. Form drag is primarily influenced by thefrontal area of periphyton patches, and skin friction

by total surface area. Flexible periphyton reducesfrontal area by bending downstream, and crusts,mats, and diatom films minimize frontal area by theirlow stature (Nikora et al. 1998b). Skin friction isreduced when filaments or other flexible appendages

become compacted into streamlined bundles (Vogel1994). Optimal morphologies for drag reduction (e.g.,

prostrate, low surfacevolume ratio, compact branch-ing, flexibility) might be different from morphologiesoptimized for nutrient acquisition and sun exposure(e.g., elongate, high surfacevolume ratio, expansive

branching, rigidity). Clearly, morphological tradeoffsare required to survive in high-velocity, resource-limited environments (Sheath and Hambrook 1988,Raven 1992). These tradeoffs can be analyzed incomparative morphology studies along resource andhydraulic gradients. Again, such comparative studiesare common in seaweed and terrestrial plant ecology(e.g., Read and Stokes 2006, Haring and Carpenter2007), but rare in periphyton ecology. The rarity ofcomparative studies of periphyton might be theresult, in part, of the difficulties posed by manipulat-ing small, freshwater algae, compared with largeseaweeds and plants. Recent advances in instrumen-tation should improve the situation for periphytonecologists (Callaghan et al. 2007).

Effects of hydraulic conditions on periphyton development

The relationship between periphyton species com-position and prevailing hydraulic conditions is one ofthe original research problems in periphyton ecology(Butcher 1940, Patrick 1948). Hydraulic conditionsaffect many components of periphyton communities,not only composition. For simplicity, 2 general stagesof community development are discussed here,immigration (including propagule dispersal andsettlement), and post-immigration (including biomassaccrual and changes in physiognomy).

The initial stages of periphyton community devel-opment are influenced by the composition andabundance of propagules in the water column, and



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rates of propagule settlement (Peterson 1996). Celldivision and sloughing create a constant flow ofpropagules to the water column (Hamilton andDuthie 1987, Barnese and Lowe 1992, Peterson1996). Floods can substantially alter propagule com-position and abundance in streams through increased

sloughing and fragmentation and propagule dilution(Hamilton and Duthie 1987). Studies of flow-depen-dent periphyton dispersal are rare, and generalrelationships linking flow levels to propagule abun-dance, diversity, and settlement rates are lacking.

Negative relationships between periphyton coloni-zation rates and free-stream or near-bed velocitieshave been reported in several studies, but whetherthese relationships reflect low rates of propaguleattachment under high shear, or high rates ofdetachment following settlement is unclear (DeNicolaand McIntire 1991, Stevenson 1996, Besemer et al.2007). Another open question for periphyton ecolo-

gists is the importance of hydraulic conditions vssubstrate suitability as determinants of colonization.Many benthic algae have motile, chemotactic, orphototactic propagules, which suggests that directed,reversible settlement interacts with hydraulic forces todeliver propagules to the benthos. Directed settlementhas been observed in many marine algae (e.g., Callowand Callow 2000), but directed settlement also mightoccur in freshwater taxa with motile propagules, suchasOedogoniumand Vaucheria.

Once a community has been established, relation-ships between periphyton biomass and free-streamvelocity are highly variable; biomass increases with

increasing velocity in some cases and decreases inothers (McIntire 1968 [Fig 1.], Stevenson 1996). Posi-tive biomassvelocity relationships have been attri-

buted to velocity-dependent nutrient advection toperiphyton (Horner and Welch 1981 [Fig. 1], Stein-man and McIntire 1986, Stevenson and Glover 1993).Negative biomassvelocity relationships have beenattributed to sloughing. Over wide velocity ranges,

biomassvelocity relationships are likely to be mono-tonic; biomass initially increases with velocity becauseof increased nutrient supplies, then decreases becauseof sloughing (Biggs et al. 2005).

Periphyton communities and their hydraulic envi-ronments interact continually. As communitieschange in structure (i.e., size, density, and flexibility),they modify bed roughness and near-bed watervelocity and turbulence (Nikora et al. 2002). In turn,the drag imposed by flowing water leads to changesin community structure, as discussed above. Contin-ual feedback might lead to an equilibrium state withthe maximum height and roughness of periphytoncommunities determined by local hydraulic condi-

tions. For communities that exceed these maxima,drag forces will exceed attachment strength andinitiate sloughing. Circumstantial evidence for suchequilibrium states come from comparisons of devel-oping periphyton communities in which differentstarting values of shear stress and hydraulic rough-

ness converge over time as the communities mature(Reiter 1989).


Periphyton studies published in J-NABS that usedhydraulic conditions as independent or dependentvariables include studies of algal drift (Barnese andLowe 1992), flow attenuation by periphyton (Doddsand Biggs 2002), and colonization and successionunder varied free-stream velocities and turbulencelevels (Peterson 1986, Poff et al. 1990, DeNicola andMcIntire 1991,Humphrey and Stevenson 1992). Most

of these studies used artificial streams where hydrau-lic conditions could be controlled by adjusting slopesand pump speeds and adding roughness elements.The experimental control and replication provided byartificial streams should be weighed against hydraulicartifacts and size constraints; these trade-offs arediscussed in detail in a J-NABS special series onartificial streams (Lamberti and Steinman 1993).

The hydraulic data in most studies of periphytonflow interactions, including those in J-NABS, are free-stream velocities (Poff et al. 1990, Bourassa andCattaneo 1998). Free-stream velocities are not neces-sarily the appropriate hydraulic measurements for the

research objectives, which include predicting periph-yton biomass and prescribing flows that prevent orremove periphyton proliferations. The hydraulicforces that periphyton experience should be measuredin the near-bed zones that periphyton occupy and atspatial scales that correspond to the ecologicalproperties being studied. For example, if periphyton

biomass or species composition vary at cm scales,hydraulic measurements intended to explain the

biological patterns should be made at correspondingscales. In a special issue of J-NABS Heterogeneity inStreams (Volume 16, issue 1) focused on environ-mental heterogeneity in streams, Cooper et al. (1997)reviewed techniques for identifying the dominantscales of spatial variability. Matching scales in

biological and hydraulic measurements should in-crease the precision and accuracy of periphytonflowrelationships. Stream ecologists were encouraged toadopt more relevant hydraulic variables than dis-charge and velocity in an early J-NABS review(Statzner et al. 1988). Useful guides for understand-ing and measuring near-bed hydraulic conditions in



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periphyton studies include Statzner et al. (1988),Carling (1992), Nikora et al. (1998a), Hart and Finelli(1999), and Stone and Hotchkiss (2007).

Competitive Interactions

Close packing among organisms and steep gradi-

ents in resources within periphyton communitiescreate suitable conditions for interspecific and intra-specific competition. However, McCormick (1996)reported a near-absence of direct evidence forcompetitive inhibition or exclusion in periphytonstudies. The situation has changed little in the decadesince McCormicks review. Direct evidence of com-petition requires measurements of density- or bio-mass-dependent responses (Manoylov and Stevenson2006). In one of the rare studies with such evidence,McCormick and Stevenson (1991) reported negativerelationships between growth rates of some benthic

diatom taxa and biovolumes of other taxa.Studies of competitive interactions generally dis-tinguish between exploitation (indirect inhibitioncaused by depletion of a resource pool) and interfer-ence (direct inhibition of access to resources). Thedistinction is not always clear, but overgrowth andpre-emption of space are usually considered forms ofinterference, and shading and nutrient depletionforms of exploitation. Allelopathy is a form ofinterference in which chemicals produced by someorganisms inhibit colonization and growth of otherorganisms. Interspecific allelopathy has been docu-mented in benthic cyanobacteria, charophytes, vascu-

lar macrophytes, and terrestrial bryophytes (Smithand Doan 1999, Juttner and Wu 2000, Gross 2003,Mulderij et al. 2003). Clear evidence that allelopathicsubstances are produced by other benthic algae orfrom natural periphyton communities is rare (Lefla-ive and Ten-Hage 2009), but the diversity ofallelopathic taxa identified to date suggests thatallelopathy is a widespread competitive strategy.

Exploitative competition among autotrophs fordissolved nutrients appears to be common in closedsystems, such as ponds and lakes and laboratoryflasks (e.g., Van der Grinten et al. 2004). In closedsystems, nutrient uptake rates can exceed rates ofnutrient input or remineralization and cause nutrientdepletion. These conditions favor taxa with low half-saturation constants, high nutrient storage, andefficient conversion of nutrients to cellular material(Borchardt 1996). In streams, nutrient input rates oftenexceed uptake by orders of magnitude, so depletion isless common. Longitudinal nutrient depletion andcorresponding changes in periphyton compositionhave been observed in natural and artificial streams

with high residence time, high periphyton biomass,and low nutrient input (Mulholland and Rosemond1992,Mulholland et al. 1995, Vis et al. 2008, Mulhol-land and Webster 2010). Under these conditions,longitudinal changes in periphyton might be caused

by changing nutrient availability. However, unidirec-

tional stream flow prevents the periphyton upstreamfrom exploiting the nutrient-limited periphytondownstream, and no competitive feedback occurs.

Intense nutrient competition is unlikely at the scaleof stream reaches, but it might be prevalent withinperiphyton mats. Uptake by organisms in periphytonmats depletes dissolved nutrients as water passesthrough mats (Burkholder et al. 1990, Stevenson andGlover 1993, Wetzel 1993). Water flow through densemats is limited by low porosity (De Beer and Kuhl2001). Nutrient depletion and low flow rates reducenutrient supplies to cells deep within mat matricesand set the stage for competitive interactions. How-

ever, low nutrient supply rates alone are insufficientconditions for competition. Exploitative competitionrequires nutrient uptake rates to equal or exceedsupply rates, and this situation has not been demon-strated (Stelzer and Lamberti 2001). Nutrient uptakerates might remain lower than supply rates because ofsevere light limitation. Alternatively, cells withinperiphyton mats might be supplied with nutrientsfrom underlying sediments or from mat decomposi-tion, in addition to the overlying water (Pringle 1990).Both situations would alleviate nutrient competitionin mats.

As with nutrient competition studies, studies of

light competition are rare in periphyton ecology.Dynamic light gradients in periphyton mats makethese studies technically challenging (Dodds et al.1999). As a first step, competitive hierarchies inperiphyton could be inferred by ranking irradiancerequirements for growth in different taxonomicgroups (Steinman et al. 1989). Circumstantial evi-dence for exploitative competition between overstoryand basal-layer taxa in periphyton mats comes fromobservations of taxonomic shifts during mat develop-ment and reduced irradiance and increased alkalinephosphatase activity in basal layers (Johnson et al.1997). More compelling evidence for light competitionwould come from experiments in which periphytoncanopy layers are removed. Canopy removal exper-iments are common in marine ecology (e.g., Clark etal. 2004), but not in stream ecology (Steinman 1996).

Assuming that competitive hierarchies do existamong taxa in periphyton communities, many pro-cesses could prevent competitive exclusion. Principalamong these are disturbances and herbivory, whichreduce populations of dominant taxa, and changing



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resource availability. In a meta-analysis of studies oftop-down (herbivory) and bottom-up (nutrient avail-ability) effects on periphyton, Hillebrand (2002)reported that effects of herbivory were greater onaverage than nutrient effects. Differences in experi-mental designs confounded these comparisons, but

the general pattern suggests that herbivory constrainsperiphyton growth more than nutrient availability,and presumably has a greater effect on competitiveexclusion.


Few papers in J-NABS have reported results ofdirect tests of hypotheses about resource competitionin periphyton communities, and none have providedevidence for competitive exclusion. Scott et al. (2009)used a natural P gradient in 8 streams to test thehypothesis that covariation in benthic algal and

bacterial production would decrease with decreasingP availability because of algaebacteria competition.The opposite effect was observed; covariation be-tween algal and bacterial production decreased withincreasing P availability. These results suggested thatlow P availability induced mutualism, rather thancompetition.

Henry and Fisher (2003) suggested that the domi-nance of diatoms with N2-fixing endosymbioticcyanobacteria and free-living N2-fixing cyanobacteriain DIN-poor habitats was caused by a release fromnutrient competition with chlorophytes and nonsym-

biotic diatoms. Presumably, the converse pattern

reported by Henry and Fisher (2003), a scarcity ofN2-fixing algae and abundant chlorophytes in DIN-rich habitats, was caused by superior competition forspace by the chlorophytes. The capacity for N2-fixation alone does not ensure that cyanobacteria willdominate DIN-poor habitats. Light and P availability,water temperature, and grazing pressure all can limitthe competitive prowess of benthic cyanobacteria(Marcarelli et al. 2008)

In the absence of information about competitivehierarchies at a detailed taxonomic level, authors ofseveralJ-NABSpapers used a functional-form or size-

based approach. These studies include comparisonsof nutrient uptake, C-fixation, and spatial dominanceamong morphological groups (e.g., unicellular andcolonial diatoms, branched and unbranched fila-ments) (Lowe et al. 1986, Steinman et al. 1992,DeNicola et al. 2006). The results of these studieswere inconsistent (e.g., groups with high surfacevolume ratios were not consistently associated withintense resource limitation). Some of the inconsisten-cies might have resulted from variation in functional

group definitions. A single widely accepted function-al-group classification could increase comparabilityamong studies and improve our understanding ofperiphyton competition, as the functional feedinggroup classification has for invertebrates (Mihuc1997).

One reason for the scarcity of periphyton compe-tition studies is the scarcity of conceptual models thatposit roles for competition in community develop-ment and species coexistence (McCormick 1996).Useful conceptual models would generate hypothe-ses, synthesize current understanding, and identifyresearch needs. Passy (2008) recently proposed onesuch model. The primary aim of this model was toexplain why species richness in natural periphytoncommunities decreased as the number of limitingresources increased. In contrast to the negativerelationship reported by Passy (2008), diversity inphytoplankton communities often increases with

increasing numbers of limiting resources (Interlandiand Kilham 2001). The periphyton model predicts thatsevere resource scarcity leads to thin, depauperateperiphyton communities dominated by stress-tolerantspecies. High resource supply leads to the establish-ment of thick mats, with canopies dominated bystress-sensitive, eutrophic species, and understoriesstill dominated by stress-tolerant species. Nutrientuptake and shading by canopy species create verticalgradients of decreasing nutrient concentration andlight in thick mats (Meulemans 1987, Johnson et al.1997). Stress-tolerant species can persist in theunderstory of these mats, increasing overall diversity.An earlier conceptual model (Stevenson 1997b)predicted a similar increase in species richness athigh resource levels, but did not account for thephysical structure of periphyton communities. Testsof both models have been limited to observationalstudies (Passy 2008). Much scope exists for testingthese models experimentally, refining or replacingthem with improved versions, thereby improving ourunderstanding of the roles of competition.

J-NABS and Periphyton Ecology: Strengthsand Shortcomings

Papers in J-NABS have led the field in testing andexpanding conceptual models in periphyton ecology.These models include patch dynamics (Pringle et al.1988,Grimm and Fisher 1989,Sinsabaugh et al. 1991,Cooper et al. 1997), resourcestress relationships(Stevenson 1997b, Wellnitz and Rader 2003, Steven-son et al. 2008), and disturbancebiodiversity anddisturbanceecosystem function relationships (Grimmand Fisher 1989, Uehlinger and Naegeli 1998, Biggs



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et al. 1999a). Most of the papers in the preceding listhave been cited .50 times. The continuing role of J-NABS in the expansion of ecological theory depends onthe imagination and fortitude of its contributors. Newand improved theories evolve from new discoveriesand new syntheses of research fields.

Periphyton ecology studies in J-NABS tend to bemultivariable, phenomenological, and nonmechanis-tic (Creutzberg and Hawkins 2008). They provideinformation about temporal and spatial patterns inperiphyton communities, but do not always identifythe environmental or biological causes of thosepatterns (Stevenson 1997a, Beyers 1998). Combina-tions of explanatory variables in periphyton papersin J-NABS have included disturbances 3 resources,herbivory 3 substrata, stressors 3 resources, re-sources 3 substrata, and disturbances 3 resources3 herbivory. Multivariable studies like these aremore realistic than univariable studies because

independent variables rarely act in isolation, butthe effort needed to implement multivariable studiesusually comes at the expense of statistical powerand experimental control. For example, Ambrose etal. (2004) measured periphyton responses to nutrient3 light interactions with 2 levels of nutrientenrichment (salmon carcasses present or absent)and 2 light levels (canopy closed or open). No maineffects or interaction terms were statistically signif-icant. It is likely that variation within treatments,confounding variables, and low statistical poweraffected the study outcome. This example illustratesthe need to weigh realism against information yield

when designing periphyton studies. Experiments inwhich confounding variables are controlled andsingle explanatory factors are varied over broadranges are likely to be more informative than poorlycontrolled multivariable experiments with few treat-ment levels and low replication.

The aims of most periphyton studies published in J-NABSare to describe patterns, detect correlations, orcompare treatments in natural experiments, inwhich the treatments consist of naturally-occurringcontrasts or unreplicated perturbations (Townsend1989, Creutzburg and Hawkins 2008). Few studies in

J-NABSaim to test hypotheses in a formal, deductiveway. In a survey of J-NABS articles, Creutzburg andHawkins (2008) concluded thatJ-NABSauthors couldadvance freshwater benthic science best by shiftingtheir emphasis from pattern descriptions and naturalexperiments to formal hypothesis testing and devel-opment of theory.

Many topics in periphyton ecology are unexploredor underexplored; the examples identified in thisreview (e.g., resource colimitation, competitive inhi-

bition and exclusion, effects of drag forces, andturbulence) are only a small sample. Because thefield of periphyton ecology is defined by anassemblage, its domain includes many other fieldsof ecology (e.g., physiological, community, popula-tion, and ecosystem ecology). Rather than presenting

an exhaustive list of research opportunities, Irecommend 2 general approaches that might helpintegrate the disparate field of periphyton ecologyand expand its range of inquiry. One is an increasedfocus on developing, testing, and refining conceptu-al models; the other is an increased emphasis onmultidisciplinary research.

A century of field and laboratory studies hasproduced a large and diverse knowledge base forperiphyton ecology. However, the development ofconceptual models that provide context for data,contribute to ecological theory, and guide futureresearch lags behind the empirical studies. This lag

appears to apply to freshwater benthic ecology ingeneral (Creutzburg and Hawkins 2008), not justperiphyton ecology. The recent conceptual modelsdiscussed in this review (e.g., Battin et al. 2007,Passy 2008) could herald an era of rapid progress, ifperiphyton ecologists begin testing and revisingthose models and proposing new ones. These arecritical steps if periphyton ecology is to progressfrom a largely descriptive and inductive disciplineto a deductive and theory-based discipline. One ofthe primary aims of science disciplines is theconstruction of robust theory, and conceptual mod-els are the basic units of scientific theories (Scheiner

and Willig 2005).To address increasingly complex research ques-

tions and environmental problems, ecologists needto adopt interdisciplinary approaches (Hannah et al.2007). These approaches bring data, methods,theories and perspectives from different disciplinesto bear on issues that span conventional sciencedomains. Periphyton ecology is traditionally thedomain of biologists with specializations in botanyor ecology. Relatively little research in periphytonecology has been undertaken by research teamsfrom different disciplines. In contrast, collaborationsamong geologists, hydrologists, chemists, geneticistsand ecologists have led to rapid advances in otherareas of benthic ecology (e.g., Cover et al. 2008).Similar efforts would serve periphyton ecology well.Based on the knowledge gaps identified in thisreview, some of the most valuable collaborationswould combine specialists in periphyton ecology,landscape ecology (Battin et al. 2007), fluid mechan-ics (Nikora et al. 1998a), and phytoplankton phys-iology (Saito et al. 2008).



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Acknowledgements

I thank Dean DeNicola, Cathy Kilroy, Vlad Nikora,Mary Ogdahl, Aaron Packman, Alan Steinman,Pamela Silver, and 2 anonymous referees for review-ing and editing several manuscript drafts. Fundingwas provided by the New Zealand Foundation for

Research, Science and Technology through the WaterAllocation Programme (Contract C01X0308).

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AMBROSE, H . A . , M . A . WILZBACH, AND K . W . CUMMINS. 2004.Periphyton response to increased light and salmon carcassintroduction in northern California streams. Journal of theNorth American Benthological Society 23:701712.

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A Prospectus for Periphyton