Fresh water Ben thic Ecosystems docx

Foremost was the realization that benthic algae are primary producers in food webs and are the fundamental components in biogeochemical cycles of aquatic ecosystems.. The Taxonomic and M

Alga,1 Ecology

Freshwater Benthic Ecosystems

AQUATIC ECOLOGY Series

Fresh water Ben thic Ecosystems

Edited by

R Jan Stevenson

Department of Biology University of Louisville Louisville, Kentucky

Max L Both well

Environmental Sciences National Hydrological Research Institute Saskatoon, Saskatchewan, Canada

Rex L Lowe

Department of Biological Sciences Bowling Green State University Bowling Green, Ohio

ACADEMIC PRESS

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Front cover photograph: The filamentous diatom Aulacoseira

entangled among the stalked diatoms Cymbella and Gomphonema

(See Chapter 1, Figure 1 for more details.)

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Copyright 1996, Elsevier (USA)

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Library of Congress Cataloging-in-Publication Data

Algal ecology: freshwater benthic ecosystems/edited by R Jan

Stevenson, Max I Bothwell, Rex L Lowe

p cm.-(Aquatic ecology series)

Includes bibliographical references and index

ISBN 0-12-668450-2 (alk paper)

1 Freshwater algae Ecology 2 Freshwater ecology

I Stevenson, R Jan II Bothwell, M.L (Max L.) III Lowe, Rex

IV Series

QK570.25.A43 1996

CIP PRINTED IN THE UNITED STATES OF AMERICA

wife Carol R Bothwell (deceased November 5, 1994) in remembrance of the selfless dedication she gave to me over the years so that my career might prosper In this, she was not unlike many other wives, including Mariellyn Stevenson and Sheryn Lowe, who spend their lives nurturing their husbands and children so that they might grow and fulfill their own dreams

Max L Bothwell

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B The Habitats of Freshwater Benthic Algae 8

II The Niche of Freshwater Benthic Algae 10

A The Role of Benthic Algae in Ecosystems 10

B How Are Algae in Benthos and Plankton Different? 11 III Methods for Characterizing Freshwater Benthic Algae 12

A Population and Community Structure 12

B Population and Community Function 18

W Conceptual Frameworks for Benthic Algal Community Ecology 23

B Typical Biomass Values for Streams 34

II Temporal Patterns 36

A Short Term 36

B LongTerm 38 III Spatial Patterns 42

A Microscale: Substratum Patterns 42

B Mesoscale- Within Catchment Patterns 43

C Broadscale: Intercatchment Patterns 44

IV Benthic Algal Proliferations 46

V Concluding Remarks 51 References 51

II Algal Assemblages in Wetlands 78

III The Role of Algae in Wetlands 81

IV Species Composition of Wetland Algae 87

V Algal Production in Wetlands 89

VI Factors Affecting Algal Production 90

A Dry State 103

B Open State 105

C Sheltered State 107

D Lake State 108 VIII Conclusion 109

F Estimating in Situ Primary Production

V Ecological Effects of Light Intensity 135

A Biomass and Productivity 135

B Taxonomic Responses 138

VI Ecological Effects of Light Quality 141 VII Ultraviolet Radiation 142

VIII Summary 143 References 144

II Autecological Responses 153

A Photosynthesis and Respiration 154

B Cell Composition 156

C Heat Shock Proteins 157

D Life Cycles 157 III Population Responses 158

A Temperature and Maximum Growth Rates 158

B Temperature Tolerance Ranges and Optima for Growth 159

C Interactive Effects of Temperature and Nutrient Limitation on Growth Rates 162

IV Community Structure 163

A Lotic Periphyton 163

B Lentic Periphyton 166

D Temperature and Light Interactions 190

E Steady-State versus

III Conceptual Framework:

A Boundary Layer and Sublayer 193

B Molecular and Eddy Diffusion 194

C Diffusion Limitation 195

D Boundary Layer Instability 196

IV Nutrient Limitation of Benthic Algae 196

D Nutrients and Species Composition 207

V Nutrient Kinetics of Benthic Algae 208

VI Effects of Water Motion on Benthic Algal NutrientUptake and Nutrient-Limited Growth 212

A Positive Effects of Water Motion 212

B Negative Effects of Water Motion 213

C Interaction of Flow Velocity and

Nutrient Concentration 214

xii Contents

VII Nutrient Competition 214

A Characterizing Nutrient Competitive Ability 214

B Predicting Competition with Optimum Ratios 216

C Effects of Water Motion on Nutrient Competition 217

D Nutrient Competition among Benthic Algae 218

References 218

in Freshwater Benthic Algal Assemblages

D Are Trade-offs Absolute? 245

V Summary and Recommendations for Future Research 247

IV Known Influences of Substratum Composition 263

A Rock Substrata and Epilithic/

Endolithic Algae 263

B The Edaphic Habit: Epipsammic and Epipelic Algae among Sands and Other Sediments 264

C Plant Substrata and Epiphytic Algae 267

D Animal Substrata and Epizoic Algae 275

E Advanced Chemical Interdependence:

I Defining Autotrophy and Heterotrophy 299

A Illustrations and Evidence of Facultative

Heterotrophy in Algae 303

B Discerning the Difference between

Heterotrophic and Dormant Algae 306

C Mechanisms of Organic Substrate Uptake and Relative Efficiency of Heterotrophic Metabolism

B The Role of Algal Heterotrophy in Benthic Microbial Carbon Cycling 314

II Direct Effects 323

A Nutrient Transport and Algal Physiology

B Drag Affects Immigration, Export,

and Morphology 326 III Indirect Effects 329

323

xiv Contents

IV Manifestations of Current Effects

A Filamentous Algae and Great Algal Biomasses 331

B Community Development and Flow Regime 331

C Lakes 333

D Streams 333

V Conclusions 3 3 5 References 336

Natural Physical Disturbance

Christopher G Peterson

I Introduction 375

II Factors Influencing Resistance to Scour 378

A Influence of Substratum Size and Surface Irregularity 378

B Community-RelatedFactors 379 III Factors Influencing Resilience

C Model for Temporal Change in Resilience Based

on Change in Community Condition 391

IV Factors Influencing Response to Emersion 392

V Factors Influencing Response to Light Deprivation and Burial 395

VI Concluding Remarks 397 References 398

14 Ecotoxicology of Inorganic Chemical Stress

to Algae

Robert Brian Genter

I Introduction 404

II Adsorption and Uptake 404

A Two Phases of Uptake 405

B Sites of Accumulation 406

C General Factors Affecting Uptake 407

D Applied Phycology 408

III Effects of Inorganic Chemical Stress on Algae

A Effects to the Cell 417

B Relative Toxicity of Inorganic Stressors 420

IV Mechanisms of Tolerance 420

A CellSurfaces 421

B Organelles and Subcellular Components 430

C Acclimation and Cotolerance

E Importance to Higher-Level Consumers 454

F A Schematic Model of Metal Fate

in Periphyton 456

VIII Algal Bioassay of Inorganic Stressors 457

A Static and Flow-Through Methods 457

B Assessing Toxicity of Sediments 458

References 458

409

XV[ Contents

15

16

Effects of Organic Toxic Substances ,

Kyle D Hoaglund, Justin P Carder, and Rebecca L Spawn

IV Indirect Effects 489

V Conclusions and Future Directions 490 References 491

II Structure of "Macroscopic" Benthic

Food Webs 535

III Periphyton in Aquatic Energy Budgets 536

IV Periphyton in Benthic Food Webs 539

A Fate and Utilization 539

B Are Benthic Grazers Food-Limited? 545

C Other Associations between Benthic Plants and Animals 546

D Interplay of Production and Consumption 547

V Top-down and Bottom-up Regulation of Benthic Food Webs 548

VI The Case for "Intermediate Regulation" 560

A Herbivores and Omnivores 560

B The Disturbance Template 561

VII General Conclusions and Directions for

II Algal-Bacterial Interaction 576

III Detection of Microbial Feeding Relationships 576

E Oligochaetes and Chironomid Larvae 5 9 4

V Use of Other Food Resources, Intraguild Predation, and Links to Higher Organisms 595

VI Impact on Production and Standing Crops 597

xviii Contents

19

20

21

VII Nutrient Regeneration 599

VIII Conclusions, Implications, and Research Needs 599

A Formation of Boundary Zones 621

B Effects of Algal-Herbivore Interactions 627

IV Nutrient Turnover Rates and Comparison with Other Ecosystems 630

V Summary and Conclusions 632 References 633

Benthic Algae and Nutrient Cycling in Lentic Freshwater Ecosystems

B Examples of Benthic Algal Models from

Stream Ecology 670

C Objectives 671

II A Modeling Approach 671

III The McIntire and Colby Stream Model 672

IV An Updated Herbivory Subsystem Model 673

V Behavior of the Herbivory Subsystem Model

A Standard Run 677

B Algal Refuge 680

C Food Consumption and Demand 682

VI Behavior of the Updated M & C Model 685

A Irradiance and Algal Refuge 685

B Allochthonous Inputs 689

C Food Quality and Nutrients 690

VII Hypothesis Generation 694

VIII Discussion and Conclusions 698

B Collection of Benthic Algal Samples 710

C Bioassays and Artificial Stream Systems 714

D Analysis of the Benthic Algal Community 714

E Quality Assurance, Quality Control, and

Standard Operating Procedure 720

E Data Analysis and Statistical Procedures 722

IV Summary and Conclusions 732

References 733

Taxonomic Index 741

Subject Index 749

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Contributors

Numbers in parentheses indicate the pages on which the authors" contributions begin

Barry J E Biggs (31), National Institute of Water and Atmospheric Research, Christchurch, New Zealand

Mark A Borchardt (183), Marshfield Medical Research Foundation, Marshfield, Wisconsin 54449

Thomas L Bott (573), Stroud Water Research Center, Academy of Natural Sciences, Avondale, Pennsylvania 19311

JoAnn M Burkholder (253), Department of Botany, North Carolina State University, Raleigh, North Carolina27695

Justin P Carder (469), Department of Forestry, Fisheries, and Wildlife, University of Nebraska, Lincoln, Nebraska 68583

Dean M DeNicola (149), Department of Biology, Slippery Rock Univer- sity, Slippery Rock, Pennsylvania 16057

xxi

Paul V McCormick (229), Everglades Systems Research Division, South Florida Water Management District, West Palm Beach, Florida 33416

C David Mclntire (669), Department of Botany and Plant Pathology, Ore- gon State University, Corvallis, Oregon 97331

Patrick J Mulholland (609), Environmental Sciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831

Yangdong Pan (705), Water Resources Laboratory, University of Louis- ville, Louisville, Kentucky 40292

Christopher G Peterson (375), Department of Natural Sciences, Loyola University of Chicago, Chicago, Illinois 60626

D Planas (497), D6partement des Sciences Biologiques, Universit~ du Qu6bec ~ Montreal, Montr6al, Quebec, Canada H3C 3P8

Gordon G C Robinson (77), Department of Botany, University of Mani- toba, Winnipeg, Manitoba, Canada R3T 2N2

Rebecca L Spawn (469), Department of Forestry, Fisheries, and Wildlife, University of Nebraska, Lincoln, Nebraska 68583

Alan D Steinman (341,669), Department of Ecosystem Restoration, South Florida Water Management District, West Palm Beach, Florida 33416

R ]an Stevenson (3, 321), Department of Biology, University of Louisville, Louisville, Kentucky 40292

Nancy C Tuchman (299), Department of Biology, Loyola University of Chicago, Chicago, Illinois 60626

Robert G Wetzel (641), Department of Biological Sciences, University of Alabama, Tuscaloosa, Alabama 35487

Preface

Benthic algae have been intensively studied, especially over the past two decades This intensity has been stimulated by the widespread recog- nition that benthic algae are ideal indicators of the health of many, if not most, aquatic ecosystems With this book we hope to synthesize this vital area of research and share its essence with our colleagues and students We started with an outline of the myriad abiotic and biotic determinants of benthic algal ecology Foremost was the realization that benthic algae are primary producers in food webs and are the fundamental components in biogeochemical cycles of aquatic ecosystems We then chose experts to write and review chapters and most eagerly agreed to participate These contributions are a tribute to the authors and to the reviewers

Some necessary limitations had to be placed on the breadth of cover- age of the book Thus, these reviews are not encyclopedic, but are repre- sentative of the excitement we all share for our discipline Of course, cov- erage was limited to freshwater benthic algal research, but often important

xxiii

xxiv Preface

observations and experimental results from planktonic and marine research were included to round out a chapter We feel sure that many of the conceptual developments derived from studies of benthic algal ecology will also be interesting to our colleagues who concentrate on other aspects

of algal and aquatic ecology

Early research on energy sources in food webs of aquatic ecosystems focused on phytoplankton in lentic habitats, leaf litter in streams, and plants in wetlands More recently, attention has focused on the algae on substrata The cycle of science has taken benthic algal ecology from obser- vation and experimentation to synthesis We hope this book will generate

a new wave of conceptual innovation for students and researchers of algal ecology

R Jan Stevenson Max L Bothwell Rex L Lowe

Ackno wledgm.en ts

The development of this book was made possible by support for R Jan Stevenson when on sabbatical at the Institute of Ecosystem Studies with funds from the Mellon Foundation to Gene Likens In addition, the College of Arts and Sciences, through the Water Resources Laboratory at the University of Louisville, provided substantial support Support from the National Hydrology Research Institute for Max Bothwell and from Bowling Green State University and the University of Michigan Biological Station for Rex Lowe is also acknowledged

The following scientists contributed as reviewers: N Aumen (South Florida Water Management District), B Biggs (National Institute of Water and Atmospheric Research, New Zealand), D Blinn (Northern Arizona University), R Carlton (University of Notre Dame), W Clements (Col- orado State University), H Carrick (State University of New York at Buf- falo), A Cattaneo (Universit~ de Montreal), E Cox (University of Sheffield), D D'Angelo (Proctor and Gamble), J Feminella (Auburn Uni-

x x v i Acknowledgments

versity), G Goldsborough (Brandon University), S Jensen (University of Nebraska), S Kohler (Illinois Natural History Survey), M Lewis (U.S Environmental Protection Agency), P Montagna (University of Texas Marine Science Institute), Y Pan (University of Louisville), R Pillsbury (Bowling Green State University), S Porter (U.S Geological Survey), A Steinman (South Florida Water Management District), M Sullivan (Miss- issippi State University), and M Turner (Fisheries and Oceans, Canada) Finally, all of us would like to thank our families In particular, the edi- tors would like to acknowledge the time that our families gave us to review manuscripts and consult with the authors So thank you Mariellyn, Philip, and Virginia; Carol, Julie, and Peter; and Sheryn, Chris, and Terry

R Jan Stevenson Max L Bothwell Rex L Lowe

PATTERNS OF BENTHIC ALGAE

tX AOUATIC

ECOSYSTEMS

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An Introduction to Algal Ecology in Fresh water Ben thic Habitats

R Jan Stevenson

Department of Biology University of Louisville Louisville, Kentucky 40292

I The Diversity of Benthic Algae and Their Habitats in Fresh Waters

A The Taxonomic and Morphological Diversity of Benthic Algae

B The Habitats of Freshwater Benthic Algae

II The Niche of Freshwater Benthic Algae

A The Role of Benthic Algae in Ecosystems

B How Are Algae in Benthos and Plankton Different?

III Methods for Characterizing Freshwater Benthic Algae

A Population and Community Structure

B Population and Community Function

IV Conceptual Frameworks for Benthic Algal Community Ecology References

I THE DIVERSITY OF BENTHIC ALGAE AND THEIR HABITATS

IN FRESH WATERS

A The Taxonomic and Morphological Diversity of Benthic Algae

Algae are a highly diverse group of organisms that have important functions in aquatic habitats Algae are an evolutionarily diverse group of photoautotrophic organisms with chlorophyll a and unicellular reproduc- tive structures By various taxonomic schemes, the number of algal divi- sions ranges from 4 to 13, with as many as 24 classes, and about 26,000 species (see Bold and Wynne, 1985; Raven and Johnson, 1992) The num- ber of recognized species probably greatly underestimates the actual num- ber of species because many habitats and regions have not been extensively sampled and many algae are very small and hard to distinguish from each

Algal Ecology

4 R Jan Stevenson

other Benthic algae are those that live on or in association with substrata Phytoplankton are algae suspended in the water column An individual alga may be benthic or planktonic at one time or another, but many species are characteristically found in just one habitat

Most benthic algae in freshwater ~ habitats are blue-green algae (Cyanophyta), green algae (Chlorophyta), diatoms (Bacillariophyta), or red algae (Rhodophyta) However, most other divisions of algae can occur

in freshwater benthic habitats The Chrysophyta, Xanthophyta, Crypto- phyta, and Pyrrophyta have many species that usually occur in the phyto- plankton, but they may also occur in physiologically active forms in some benthic habitats In addition, resting cells of many algae can be found in the benthos, which may have originated there or may have settled from the water column (Sicko-Goad et al., 1989) The latter divisions seldom con- stitute more algal biomass in a benthic habitat than blue-green algae, green algae, diatoms, or red algae

The divisions of algae are distinguished by a variety of chemical and morphological differences (Bold and Wynne, 1985; Lee, 1989) All divi- sions have chlorophyll a, but different divisions can also have either chlorophylls b, c, or d Distinctive accessory pigments, such as phycobilins and fucoxanthin, also are characteristic of different algal divisions Acces- sory pigments may color the algae red, blue, or golden-brown, if they are not green with chlorophyll as the dominant pigment The different divi- sions also have chemically different cell walls and storage products, or they have distinctive forms of motility or numbers of flagella Ultrastructural features, such as the number of membranes around chloroplasts, also dis- tinguish the different divisions and indicate that the algae have many ancestors and are an evolutionarily diverse group (Stewart and Mattox, 1980; Gibbs, 1981; Cavalier-Smith, 1986)

Even though these groups have great evolutionary, genetic, and chem- ical differences, they share many of the same growth forms (Table I) The blue-green algae, green algae, and diatoms have the greatest morphological diversity with unicellular, ~ colonial, and filamentous forms Many of the green algal filaments are individually macroscopic, whereas most of the other algae (except Vaucberia, a xanthophyte) are only macroscopically evident in multicellular masses Each of the growth forms has a motile and nonmotile stage in one division or another Blue-green algal filaments are motile because trichomes (a series of cells) can move through sheaths of mucilage Unicellular green algae, chrysophytes, cryptomonads, and dinoflagellates are commonly found in benthic habitats, where they move

by means of flagella A few benthic algae, particularly chrysophytes, may

be amoeboid Few species of colonial green algae with flagella actually occur in motile form in benthic habitats, but Gonium, Pandorina, Eudo- rina, and even Volvox may occur incidentally in some benthic algal sam- ples Desmids, a family of green algae characteristic of acidic habitats, can

TABLE I Morphological Variability in the Divisions of Benthic Algae a

Morphology

Unicellular Colonial Filamentous

Taxon Mot N-M Mot N-M Mot N-M Means of motility

the cell wall) But one genus of diatom, Bacillaria, is filamentous and

motile and can occur in benthic habitats, even though it is characteristi- cally planktonic

Nonmotile forms of unicellular, colonial, and filamentous algae may

be attached to substrata or entangled in the matrix of other organisms that are attached (Fig 1) These organisms attach by specially adapted cells and

mucilaginous secretions Some taxa, such as the green filamentous alga Sti- geoclonium, are heterotrichous, which means they have morphologically

distinct basal and filamentous cells The basal cells form broad horizontal expanses of cells across the substratum surface, and filaments develop ver- tically from the basal cells Mucilaginous secretions can be amorphous for unicellular blue-green and green algae or organized into special pads, stalks, or tubes for diatoms (Fig 1)

Benthic algal growth forms are hypothesized to confer competitive advantages during different stages of benthic algal community develop-

6 R Jan Stevenson

FIGURE I Growth forms of benthic algae Upper left, adnate Navicula (x2400); upper right, apically attached Synedra (x2000); lower left, the filamentous diatom Aulacoseira

entangled among the stalked diatoms Cymbella and Gomphonema (x600); lower right, the filamentous green alga Stigeoclonium (x285) (Reprinted with permission from Hoagland et al., 1982.)

B The Habitats of Freshwater Benthic Algae

Freshwater benthic algae are found in the photic zones of streams and rivers, lakes, and wetlands Many terms are used to distinguish the groups

of benthic organisms that live in different aquatic habitats In the follow- ing discussion, terms for benthic algae and associated organisms are defined according to common modern usage and to the widely read and respected limnology text by Robert Wetzel (1983a) My definition of terms

is not meant to be a final definition of terms, because permanent definition impedes creativity New definitions are required when new information is developed and new ideas evolve about how systems are organized, what their parts are, and how the parts are linked We (M L Bothwell, R L Lowe, and I) have tried to standardize use of most terms in the chapters because consistency does facilitate communication

Benthos refers to organisms living on the "bottom" or associated with substrata Wetzel (1983a) considers benthos to be the animals associated with any solid-liquid substratum Common use of the term benthos includes most organisms associated with substrata in aquatic habitats: fish, macroscopic invertebrates and meiofauna, fungi, bacteria, and even hypo- rheic (below substratum surface) organisms Periphyton and aufwuchs are also terms that are more or less synonymous with the term benthic algae

Aufwuchs is a German word that means "to grow upon" and is not often used in the modern literature Periphyton is a commonly used term that refers to all the microflora on substrata (Wetzel, 1983a) Therefore, peri-

phyton includes all the microscopic algae, bacteria, and fungi on (or asso- ciated with) substrata According to this definition, macroscopic benthic algae would not be considered periphyton Using this distinction between periphyton and benthic algae enables the use of periphyton to refer to the biofilms and thicker matrices of microscopic organisms in which flow, eddy diffusivity of nutrients, and exposure to other organisms are very dif- ferent than among the filaments of macroscopic algae, such as Cladopbora, Spirogyra, Cbara, and Vaucberia

The nature of the habitat in which these organisms are found depends

on the habitat diversity of aquatic ecosystems and on the size of the organ- ism For example, macroalgae on substrata are in very different habitats than microalgae on the same substratum type, because they extend farther into the water column However, one common criterion for habitat is the substratum type (see Burkholder, Chapter 9) Epilitbic algae grow on hard, relatively inert substrata, such as gravel, pebble, cobble, and boulder, that are bigger than most algae (see Hynes, 1970, for substratum size defini- tions) Epipbytic algae grow on plants and larger algae, which provide rel- atively firm substrata that are bigger than the epiphytic algae, but can be highly active metabolically and can be a great source of nutrients (see Burkholder, Chapter 9) Epipsammic algae grow on sand, which is hard, relatively inert, and smaller than all but the smallest diatoms Algae grow- ing on inorganic or organic sediments that are smaller than most unicellu- lar algae are called epipelic Few large algae live among sand grains, because the sand is too unstable and may crush them; however, epipelic algae are characteristically large motile diatoms, motile filamentous blue- green algae, or larger motile flagellates like Euglena

Metapbyton are the algae of the photic zone that are not directly attached to substrata, nor are they freely suspended in the water column Metaphyton come in many forms and may have many origins Metaphy- ton are usually clouds of filamentous green algae, like Spirogyra, Mougeo- tia, or Zygnema, that commonly do not attach directly to substrata, but become loosely aggregated and associated with substrata in areas that are protected from current or waves They may become trapped between sur- face and substrata near shorelines or actually entangled with plants or other substrata Denser assemblages of filamentous blue-green algae~ diatoms, bacteria, and fungi can also form floating surface assemblages at the water surface that are usually entangled among or attached to sub- strata The origin of metaphyton is usually algae from other substrata, typ- ically epiphyton (see Goldsborough and Robinson, Chapter 4), but epipelon and epilithon can also form floating mats of microscopic organ- isms when they slough from submerged substrata The persistence of these communities is highly dependent on their ability to withstand rain, mild currents, or animal disturbances In the Everglades, metaphyton forms floating mats that are dominated by blue-green algae laden with calcareous

10 R Jan Stevenson

depositions and that cover the surface of sloughs (Browder et al 1994)

My observations (unpublished) indicate that the calcareous deposition within the Everglades metaphyton increases its resistance to disturbance by winds and heavy rains

Some algal ecologists would argue that edapbic (soil) algal communi- ties are benthic in the sense that they are attached to substrata Many of the same habitat characteristics apply to edaphic algae and periphytic algae (Metting, 1981; Starks et al., 1981; Bell, 1993; Johansen, 1993): cells are packed closely on a substratum, provide habitat and nutrition for other organisms, stabilize substrata, and create their own microenvironment Expanding the definition of periphyton to include edaphic microbial com- munities is an example of how definitions of terms can be revised to accommodate new information and conceptual approaches

II THE NICHE OF FRESHWATER BENTHIC ALGAE

A The Role of Benthic Algae in Ecosystems

Benthic algae are important primary producers in streams, lakes, and wetlands The main source of energy in streams was once thought to be detritus from terrestrial origin before Minshall's seminal paper (1978) that showed primary production by algae was important in many streams Ben- thic algae are now predicted to be the primary energy source in many mid- sized (third to sixth order) streams (Vannote et al., 1980) Benthic algae are also known to be important sources of energy for invertebrates in some headwater streams (Mayer and Likens, 1987) Wetzel (1964) has argued that benthic algae are important, and even dominant, primary producers in many shallow lakes and ponds In wetlands, Goldsborough and Robinson (Chapter 4) have reported that algae may be significant primary producers because of their high turnover rate, even though macrophytes are the dom- inant photosynthetic biomass

In addition to primary producers, benthic algae are chemical modula- tors in aquatic ecosystems (e.g., Lock et al., 1984) They transform many inorganic chemicals into organic forms The conversion of atmospheric N2

to NH3 and amino acids by blue-green algae and diatoms with endosym- bionic blue-green algae may enable high primary productivity in low-nitro- gen habitats (Fairchild et al., 1985; Peterson and Grimm, 1992; DeYoe et al., 1992) Benthic algae are primary harvesters of inorganic phosphorus and nitrogen in stream spiraling (see Mulholland, Chapter 19), in lake lit- toral modulation of influxes (see Wetzel, Chapter 20) and in wetlands (see Goldsborough and Robinson, Chapter 4) Effects of active nutrient uptake during the day explain the diurnal variation in nitrate concentrations in streams (Triska et al., 1989) Benthic algae on surface sediments and plants

are considered to be important sinks for nutrients before release into the water column (see Wetzel, Chapter 20) The uptake of nutrients in wet- lands is often attributed to macrophytes, however, recent research shows that macrophytes actually pump nutrients out of the sediments The ben- thic algal covering over macrophytes, however, traps nutrients before they reach the water column and returns them to the sediments when epiphytic algae settle to the bottom (Moeller et al., 1988; Burkholder et al., 1990; Wetzel, Chapter 20)

Benthic algae stabilize substrata in many aquatic habitats Diatoms, fil- amentous blue-green algae, and Vaucheria can overgrow sands and sedi- ments so that the substrata are less likely to move when current increases (see Biggs, Chapter 2) Many filamentous algae, particularly Vaucheria and

Cbara, can trap sediments Cbara can trap enough sand to form hum- mocks more than a meter in length in the sandy streams of many north- central states of the United States

Benthic algae can also be important habitats for many other organ- isms Cbara hummocks can support a great diversity and density of aquatic invertebrates in streams where sand provides a poor habitat for most invertebrates Cladophora and other filamentous algae that support epiphytes often also support great numbers of smaller invertebrates, such

as chironomids, amphipods, and many smaller meiofauna (e.g., Chilton et al., 1986; Holomuzki and Short, 1988; Power, 1990; see review by Dodds and Gudder, 1992) Even thicker periphyton matrices dominated by diatoms can shelter substantial numbers of chironomids and meiofauna

B How Are Algae in Benthos and Plankton Different?

Many species of algae are distinctly more common in benthic than in planktonic habitats Some major taxonomic groups of algae can be char- acterized as "benthic" or "planktonic," such as orders of filamentous green algae and pennate diatoms that are generally benthic and the Volvo- cales and centric diatoms that tend to be planktonic Other groups have been poorly characterized or have species that are found in either the ben- thos or plankton, such as many orders of blue-green algae and the diatom genera Fragilaria, Synedra, and even Nitzschia

Obvious morphological characteristics, such as the diatom raphe, mucilage pads and stalks, or the holdfast mechanisms of filamentous algae, seem to confer a selective advantage for many algae to attach to substrata and remain there when disturbed by current However, the same alga may utilize a morphological adaptation for attachment to substrata in the ben- thos and for attachment to other cells to form buoyant colonial growth forms in the plankton The apically attached diatoms Synedra form hemi- spherical rosettes of cells on substrata and spherical colonies of radially arranged cells in plankton that are attached to each other at their apices

12 R Jan Stevenson

The same habitat-specific growth forms are evident for blue-green algae with tapered trichomes in hemispherical rosettes of Rivularia on substrata and in spheres of Gloeotrichia in the plankton

Many algal ecologists would hypothesize that algae characteristically found in benthic habitats may settle faster than algae usually found in plankton, because they have greater specific gravity Few data are available

to test that hypothesis Stevenson and Peterson (1989) compared relative abundances of diatom species in the plankton and after settling on sub- strata, which should identify species with relatively high specific gravity, but most data were for pennate diatoms that are commonly found in the ben- thos Cyclotella meneghiniana, a common diatom in stream plankton, was characterized in several studies and was found to be relatively more abun- dant in plankton than in immigration assemblages in two of the three stud- ies (Stevenson and Peterson, 1989) Peterson and Hoagland (1990) found much higher relative abundances of planktonic taxa (Asterionella and two

Fragilaria spp.) in settling traps than on substrata after short (3 d) incuba- tions, which indicates that when planktonic taxa do have relatively high set- tling rates, they attach poorly or grow slowly when on substrata Brown and Austin (1973) correlate decreases in abundances of taxa in plankton with their increases in the benthos, but do not actually compare settling rates or immigration rates of characteristically planktonic and benthic taxa One of the most important differences in benthic and planktonic habi- tats is the mode of nutrient delivery The benthic habitats in an aquatic ecosystem probably have a greater diversity in nutrient conditions than planktonic habitats within the same habitat Algae on substrata in sub- stantial currents (which are often found in lakes and wetlands, as well as streams) may have greater supplies of nutrients than algae in the water col- umn because currents reduce nutrient-poor and waste-rich boundary layers that develop around algae in still waters (see Borchardt, Chapter 7, and Stevenson, Chapter 11) However, algae on substrata in still waters may be

in lower resource conditions than algae suspended in the water column because uptake by neighboring or overlying cells may create nutrient-poor regions within periphyton mats (see Borchardt, Chapter 7; Tuchman, Chapter 10; and Stevenson, Chapter 11) Therefore, algae on substrata in currents could have greater nutrient availability than algae in the water column, but the opposite may be the case in still waters In addition, recy- cled nutrients are probably entrained within periphyton matrices more in still waters than in open-water planktonic habitats, such that interactions among organisms within periphyton are probably more tightly coupled than among freely suspended planktonic organisms Exoenzymes secreted

by organisms used to digest organic material may be more likely to confer selective advantage on the organism that produces them in relatively closed periphyton matrices than in open plankton habitats

Since taxa characteristically found in plankton do not have specific morphological adaptations for attachment to substrata, they are not well

adapted for maintaining position in currents Therefore, planktonic taxa settling into benthic habitats would settle into still-water habitats, where nutrient availability may be lower and interactions among organisms may

be higher than in the open water column Since some benthic taxa can suc- cessfully grow in benthic habitats with slow currents and planktonic taxa generally cannot (Peterson and Hoagland, 1990), then the physiological difference between taxa may be that planktonic taxa cannot grow as fast

as benthic taxa in low-resource, still-water benthic habitats However, too little research has directly compared the physiological and morphological characteristics of algae that are more commonly found in benthic or plank- tonic habitats and determined whether those characteristics conferred effective fitness The question "How are algae in benthos and plankton dif- ferent?" remains to be answered

III METHODS FOR CHARACTERIZING FRESHWATER BENTHIC ALGAE

A Population and Community Structure

Structural characteristics are measurements of system state Algal pop- ulation and community structure can be assessed for biomass, taxonomic composition, or chemical composition

1 B i o m a s s

Benthic algal biomass is the mass of algal organic matter per unit area

of substratum Many measurements are used to estimate algal biomass (Table II) Measurements of the area-specific masses of matter (such as chl

a, C, N, or P, dry mass, and ash-flee dry mass cm -z) are relatively inex- pensive methods for estimating algal biomass, however, their accuracy (susceptibility to bias) is lower than that of cell-counting methods Chloro- phyll a and other pigments are chemicals found only in algae in most ben- thic algal samples, unless plant or moss material also occurs in samples Therefore, chl a and pigment densities more accurately indicate algal bio- mass than C, N, or P, which can be found in any living or nonliving organic matter However, chromatic adaptation to low light or nutrient deficiency may alter the ratio between these chemicals and algal organic matter, so that pigment and chemical indicators of algal biomass may be biased when light and nutrient concentrations are ecological variables in the study Dry mass (DM) and ash-free dry mass (AFDM) estimates of algal biomass (mg DM or AFDM cm -2) may be biased, respectively, by inorganic matter and nonalgal organic matter (detritus, bacteria, fungi, etc.) in samples So DM is a particularly poor indicator of benthic algal biomass when silt and inorganic deposition is great in samples, and AFDM

is poor when detritus and heterotrophic organisms compose significant proportions of communities Ash mass in samples, the portion of mass