Advances in Algal Biology: A Commemoration of the Work of Rex Lowe (Developments in Hydrobiology)

Advances in Algal Biology: A Commemoration of the Work of Rex Lowe

Developments in Hydrobiology 185

Series editor

K. Martens

Advances in Algal Biology: A Commemoration of the Work of Rex Lowe

Edited by

R. Jan Stevenson1, Yangdong Pan2, J. Patrick Kociolek3 and John C. Kingston4 1 Department of Zoology, Michigan State University, East Lansing, Michigan 48824, USA Environmental Science and Resources, Portland State University, Portland, Oregon 97207, USA

2

3

California Academy of Sciences, Golden Gate Park, San Francisco, California 94118, USA 4

Natural Resources Research Institute, 1900 E. Camp St., Ely, Minnesota 55731, USA

Reprinted from Hydrobiologia, Volume 561 (2006)

123

Library of Congress Cataloging-in-Publication Data

A C.I.P. Catalogue record for this book is available from the Library of Congress.

ISBN 1-4020-4782-7 Published by Springer, P.O. Box 17, 3300 AA Dordrecht, The Netherlands

Cover illustration: A species of Draparnaldia from the Great Smoky Mountains. Draparnaldia is a morphologically elaborate and beautiful genus of filamentous green algae found mainly in aquatic habitats with low human disturbance. Photo credit: Rex Lowe

Printed on acid-free paper All Rights reserved  2006 Springer No part of this material protected by this copyright notice may be reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording or by any information storage and retrieval system, without written permission from the copyright owner. Printed in the Netherlands

TABLE OF CONTENTS

Preface Algology and algologists at Bowling Green, a short history R.L. Lowe

vii–viii 1–11

Rexia erecta gen. et sp. nov. and Capsosira lowei sp. nov., two newly described cyanobacterial taxa from the Great Smoky Mountains National Park (USA) D.A. Casamatta, S.R. Gomez, J.R. Johansen

13–26

Large-scale regional variation in diatom-water chemistry relationships: rivers of the eastern United States D.F. Charles, F.W. Acker, D.D. Hart, C.W. Reimer, P.B. Cotter

27–57

Short-term effects of elevated velocity and sediment abrasion on benthic algal communities S.N. Francoeur, B.J.F. Biggs

59–69

The effects of pH on a periphyton community in an acidic wetland, USA J.L. Greenwood, R.L. Lowe

71–82

Food limitation affects algivory and grazer performance for New Zealand stream macroinvertebrates J.R. Holomuzki, B.J.F. Biggs

83–94

Benthic diatom communities in subalpine pools in New Zealand: relationships to environmental variables C. Kilroy, B.J.F. Biggs, W. Vyverman, P.A. Broady

95–110

The relationships among disturbance, substratum size and periphyton community structure M.R. Luttenton, C. Baisden

111–117

Relationships between environmental variables and benthic diatom assemblages in California Central Valley streams (USA) Y. Pan, B.H. Hill, P. Husby, R.K. Hall, P.R. Kaufmann

119–130

Response of periphytic algae to gradients in nitrogen and phosphorus in streamside mesocosms S.T. Rier, R.J. Stevenson

131–147

Comparing effects of nutrients on algal biomass in streams in two regions with different disturbance regimes and with applications for developing nutrient criteria R.J. Stevenson, S.T. Rier, C.M. Riseng, R.E. Schultz, M.J. Wiley

149–165

Differential heterotrophic utilization of organic compounds by diatoms and bacteria under light and dark conditions N.C. Tuchman, M.A. Schollett, S.T. Rier, P. Geddes

167–177

Using diatom assemblages to assess urban stream conditions C.E. Walker, Y. Pan

179–189

vi Developing and testing diatom indicators for wetlands in the Casco Bay watershed, Maine, USA Y.-K. Wang, R.J. Stevenson, P.R. Sweets, J. DiFranco

191–206

Diatom assemblages and their associations with environmental variables in Oregon Coast Range streams, USA C.L. Weilhoefer, Y. Pan

207–219

Algal assemblages in multiple habitats of restored and extant wetlands L. Zheng, R.J. Stevenson

221–238

Ecology and assessment of the benthic diatom communities of four Lake Erie estuaries using Lange-Bertalot tolerance values G.V. Sgro, M.E. Ketterer, J.R. Johansen

239–249

Hydrobiologia (2006) 561:vii–viii  Springer 2006 R.J. Stevenson, Y. Pan, J.P. Kociolek & J.C. Kingston (eds), Advances in Algal Biology: A Commemoration of the Work of Rex Lowe DOI 10.1007/s10750-005-1600-8

Preface The authors of papers in this special issue of Hydrobiologia want to express their respect and gratitude for the inspiration that Dr Rex Lowe has provided. Rex has had extraordinary effects on his students and colleagues with his engaging personality, sometimes dangerous senses of humor and fun, and infectious fascination with the biodiversity and ecology of algae. The occasion for this special issue has been the coincidence of Rex’s 60th birthday, having 60 graduate students, and having taught a field phycology course at the University of Michigan Biological Station for 30 years, where many of us met Rex. The authors include colleagues and graduate students as well as academic grandchildren and great grandchildren from his graduate students that are professors at universities throughout the US. Rex got his Ph.D. from Iowa State University in 1970 studying with Dr John Dodd, who had a great influence on Rex’s commitment to students. Immediately afterward, Rex joined the faculty in the Department of Biological Sciences at Bowling Green State University (BGSU). Throughout his career at BGSU, Rex has maintained an active research program with his graduate students. He has published more than 80 papers, books, and book chapters. He has also been recognized with 4 distinguished teaching awards from 1974 to 1996 at BGSU, which demonstrates that Rex achieves his goal of providing students with ‘‘one of the best and most memorable experiences of their lives.’’ The field of algal biology in the United States has benefited greatly from Rex’s efforts. Through his pioneering leadership in the North American Benthological Society during the 1970s, benthic algal ecology has become a wholly integrated element of research conducted by stream ecologists. His review of diatom ecological tolerances provided a key reference for researchers in environmental assessment. Rex and his students have explored algal flora, described new species, and documented regional biodiversity throughout the US for the last 30 years. This special issue of Hydrobiologia exemplifies these contributions to algal biology. The issue is

introduced by Rex himself, with a description of his career, students, and their research contributions. Papers were contributed in three broad areas of algal biology: aquatic ecology, environmental assessment, and systematics. Effects of disturbance (flow and herbivory), substrates, sediments, light, and organic compounds on benthic algae in streams, lakes, wetlands, and the Great Lakes are explored in aquatic ecology. Algal biodiversity is related to human alterations of streams and wetlands in environmental assessment. Several regional studies document changes in algal species composition and their relation to human disturbances; plus they are used to develop algal indicators and multimetric indices of biological condition. Three ‘‘systematics’’ papers were submitted to a different journal for publication. These included a paper on the development of a diatom flora for freshwater ecosystems in the continental United States and new species of diatoms and cyanobacteria described from Michigan and the Great Smoky National Park. These contributions to algal biology are a tribute to Rex’s inspiration of his students and colleagues. Rex and his wife Sheryn create a special environment for learning and intellectual debate at their home in Bowling Green and their summer retreat at the University of Michigan Biological Station. The warm and friendly atmosphere fosters open dialogue, creativity, and collegiality that attracts fellow scientists and students and produces interactions that have grown into extensive advances in the fields of ecology, biodiversity, systematics, and environmental assessment as well as algal biology. Rex has inspired us to study, teach, and live our lives with more enthusiasm and satisfaction in a way that helps us understand and protect the wonder and diversity in the world around us. Thank you Professor Lowe. R. Jan Stevenson Yangdong Pan Pat Kociolek John Kingston and all other authors of these papers.

viii

List of Reviewers Reviewer

Reviewer institution

Eugene Stoermer Liz Bergey Steve Kohler Christopher Peterson Paul McCormick Jennifer Winter Scott Hagerthey Marina Potapova Robert Sinsabaugh Dean DeNicola Rhonda McDougal Harry Leland Alan Steinman Rex Lowe Walter Dodds Christine Weilhoefer Russel Kreis Don Charles Evelyn Gaiser R. Jan Stevenson Yangdong Pan J. Pat Kociolek

The University of Michigan The University of Oklahoma Western Michigan University Loyola University of Chicago United States Geological Survey Ontario Ministry for the Environment South Florida Water Management District The Academy of Natural Sciences of Philadelphia University of New Mexico Slippery Rock University Ducks Unlimited Canada United States Geological Survey Grand Valley State University Bowling Green State University Kansas State University Portland State University US Environmental Protection Agency The Academy of Natural Sciences of Philadelphia Florida International University Michigan State University Portland State University California Academy of Sciences

Hydrobiologia (2006) 561:1–11  Springer 2006 R.J. Stevenson, Y. Pan, J.P. Kociolek & J.C. Kingston (eds), Advances in Algal Biology: A Commemoration of the Work of Rex Lowe DOI 10.1007/s10750-005-1601-7

Algology and algologists at Bowling Green, a short history Rex L. Lowe1,2,* 1

Department of Biological Sciences, Bowling Green State University, Bowling Green, Ohio, 43403, USA University of Michigan Biological Station, Pellston, Michigan, 49762, USA (*Author for correspondence: E-mail: [email protected]) 2

Key words: algae, periphyton, ecology, environment, assessment, systematics

Abstract This paper summarizes the past 34 years of studies of algae by Rex Lowe and his students and collaborators at Bowling Green State University, Ohio, USA. Sixty-two students have received graduate degrees in this academic program focusing on systematics, ecology and environmental assessment. The taxonomic/ floristic research initially focused on northern Ohio streams but is now continental to international in scope focusing on the algal flora of the Great Smoky Mountains National Park and on the South Island of New Zealand. Ecological research has focused on factors that regulate the structure and function of benthic algae. Variables that have been examined include abiotic resources (nutrients and light), grazers and physical disturbance. Studies on environmental assessment have focused primarily on the impact of pointsource loads of chemicals into water bodies.

Introduction I was surprised, humbled and greatly honored upon learning of my students’ plans to organize a celebration in 2003 to recognize, summarize and reflect on studies of algae undertaken at Bowling Green State University during the past 34 years. When asked to write the introductory chapter to a collection of scientific papers contributed by former academic advisees and research collaborators I decided instead to write about the former students themselves and how their ambitions and interests helped shape my own. Sixty-two graduate students matriculating through the Algal Ecology Laboratory at Bowling Green State University coinciding with my 60th birthday seems an appropriate time for retrospection. The theme of this special volume is ‘‘Benthic algae: Their Roles in Aquatic Ecology, Systematics, and Environmental Assessment.’’ Although these subdisciplines encompass an expansive continuum of questions of scientific interest it has become

increasingly clear that ecology and systematics are inseparable (Kociolek & Stoermer, 2001). One cannot accurately describe species interactions and environmental relationships if the species are unknown. This issue is particularly critical when attempting to extrapolate insights gained from research to other algal communities separated by time (paleolimnolgy) or space (biogeography). In addition, the biological species concept has been difficult to apply to algae given their cryptic sexual behavior. Indeed, most algal ‘‘species’’ have not been observed reproducing sexually. Thus, morphology and increasingly ecology are being employed in algal species concepts. The inseparability of ecology and systematics has been extended to the application of algal communities in environmental assessment (Bahls, 1973, 1974; Descy, 1979; Stevenson & Lowe, 1986; Morgan, 1987; Biggs, 1989; Dixit et al., 1992; Lowe & Pan, 1996; Stevenson & Pan, 1999). Accurate species identification is essential for accurate environmental assessment whether the algal communities are modern or fossil.

2 Students in the algal graduate program over the past three decades pursued a continuum of interests in the three sub disciplines (systematics, ecology and environmental assessment). This research continuum led to close and fertile interstudent collaborations that continue today. Many of the students that matriculated through the program are at the forefront of the field today. I am extremely proud of them. I will divide my summary of these research pursuits into the three sub disciplines, while recognizing their interrelatedness.

Systematics and morphology Our initial interest in the algae laboratory was documenting the local flora of northwest Ohio, USA. Bowling Green rests in an area formerly known as ‘‘The Great Black Swamp,’’ a glacial remnant of Lake Erie (Kaatz, 1955). Streams in northwest Ohio are all low-gradient in nature and strongly influenced by agricultural practices. The Portage River system was studied by McCullough (1971), Jackson (1975) and Rohr (1977). Stevenson (1976), Kline (1975) and Pryfogle (1976) investigated algal communities in the Sandusky River. Acker (1977), Fisher (1980) and Lamb (1983) researched the algae of the Maumee River. The algal flora of these rivers is typical of sluggish, nutrient-rich water. Phytoplankton was typically dominated by small centric diatoms in the genera Cyclotella, Stephanodiscus and Thalassiosira (Lowe & Crang, 1972; Busch, 1974; Lowe, 1975; Lowe & Busch, 1975; Lowe & Kline, 1976; Kline & Lowe, 1976). The benthic algal flora of these sediment-rich rivers was dominated by epipelic species typical of low-gradient streams (Jackson & Lowe, 1978; Kociolek et al., 1983). Following extensive research on northwestern Ohio streams we initiated studied in the southeastern United States in the late 1970s. Camburn (1977) wrote a thesis on the diatom flora of Long Branch Creek in South Carolina that led to his substantial and profusely-illustrated manuscript (Camburn et al., 1978) in which he described eleven new diatom taxa form a flora of 268 total taxa. The appearance of so many undescribed taxa provided incentive for continued taxonomic and floristic research in the southeast. Kociolek (1982) and Keithan (1983) both conducted their graduate research in the

Great Smoky Mountains National Park. While Kociolek focused on taxonomic issues documenting the diatom flora of selected streams including the description of five new taxa (Kociolek & Lowe, 1983; Lowe & Kociolek 1984), Keithan was ecologically focused examining the role of current in structuring benthic algal communities (Keithan & Lowe, 1985). This initial research in the Great Smoky Mountains National Park made our current large-scale algal biodiversity project which is part of a larger all-taxa biodiversity inventory possible (Sharkey, 2001; Gomez et al., 2003; Potapova et al., 2003; Johansen et al., 2004). Taxonomic and floristic research in our laboratory took a more international approach in the 1990s. In collaboration with Barry Biggs at The National Institute for Water and Atmospheric Research while on a sabbatical leave in New Zealand, we observed that diatoms from many local habitats were not easily identified using taxonomic literature from the northern hemisphere. This led to a more intensive investigation into endemic New Zealand diatom species (Sabbe et al., 2001; Kilroy et al., 2003) that is still in progress. In addition to our New Zealand algal floristic work, the arrival of Sophia Passy in Bowling Green enabled us to pursue taxonomic/floristic work on diatoms from Bulgaria (Passy & Lowe, 1994) and from South Africa (Passy-Tolar et al., 1997). Taxonomy and floristics continue to one of the central areas of research interest in the Bowling Green algae laboratory.

Ecology The major focus of research activities of students matriculating through the graduate program in the algology laboratory at Bowling Green has, not surprisingly, centered on ecology. Because algal assemblages are spatially compact and respond to environmental variables relatively quickly, they are ideal subjects for students wanting to pursue a research question addressing community ecology in a limited period of time. Also, algae stand at the interface of the abiotic and biotic components of the ecosystem converting inorganic minerals to organic compounds. Thus, algal community structure, function and dynamics are potentially

3 strongly regulated by abiotic resources and/or consumers and/or disturbance. This complexity is increased when one considers that algal assemblages are composed of a large numbers of species, with species richness often exceeding 100, providing an incredibly complex system for investigation. Initial investigations were descriptive in nature, generating correlative data sets (Lamb & Lowe, 1981; Lowe et al., 1982; Millie & Lowe, 1983; Belanger et al., 1985). Bruno (1978) and Kingston (1980) researching benthic algal assemblages in an Ohio bog lake and Grand Traverse Bay, Lake Michigan were among the early researchers applying multivariate techniques in the analysis of algal communities (Bruno & Lowe, 1980; Kingston et al., 1983). Kingston’s research documented a benthic diatom assemblage living below the maximum penetration of the summer thermocline in Lake Michigan that was highly diverse and structurally stable through seasons. In contrast, he found that shallower benthic assemblages displayed strong seasonal variability in structure. Kingston’s is one of the few data sets detailing this important deep benthic community in Lake Michigan. Passy (1997) applied multivariate analyses to seasonal benthic algal community structure in the Mesta River, Bulgaria. From detailed collections of epilithon, epiphyton, epipelon, epipsammon and plocon across nutrient gradients she was able to define subsets of taxa based on both nutrient and microhabitat preferences (Passy-Tolar et al., 1999). Miller (1983) and Krejci (1985) examined algal distribution patterns at a much finer scale than had been customary in algal ecology. Both students focused on epipsammic diatom communities. Miller investigated the role of micro-topography of sand grains and its influence on diatom distribution (Miller et al., 1987). Her investigation demonstrated habitat partitioning among diatoms on sand grains with prostrate diatoms normally occupying depressions while the ridges were occupied by diatom taxa with relatively short and stout flexible stalks that enabled these forms to better resist crushing during sand drifting events. Krejci examined seasonal phenology of epipsammon in a stable spring-fed brook (Krejci & Lowe, 1987a) documenting, among other findings a preferred temperature range for the spring Meridion bloom

(Krejci & Lowe, 1987b). Krejci also documented the role of sand grain mineralogy using scanning electron microscopy (SEM) and x-ray energy dispersive spectroscopy technology for sand grain elemental analysis as an influence on diatom colonization. Krejci determined that stalked diatoms preferred quartz sand grains, which comprised 65% of the grains he examined. In contrast, motile prostrate diatoms showed no preference between quartz and feldspar sand grains (Krejci & Lowe, 1986). Krejci and Miller’s research was a strong confirmation that algae significantly exploited habitat variability at microscopic scales. Insights into microalgal ecology must focus at the appropriate scale. Greenwood et al. (1999) also employed SEM to examine the distribution and behavior of diatoms moving through sediments (endopelic). This littleexplored microhabitat still holds many interesting mysteries on algal behavior and the interface with endopelic consumers.

Abiotic resources Fairchild’s (Fairchild & Lowe, 1984) development of a means of manipulating nutrients in-situ using clay flower pots stimulated many students to manipulate abiotic variables while investigating interspecific interactions among benthic algal populations (Carrick, 1985; Luttenton, 1989; Marks, 1990; Pillsbury, 1993; Pan, 1993). Nitrogen or phosphorus were found to be a limiting nutrient for periphyton populations in most of the lotic and lentic habitats investigated (Fairchild et al., 1985; Lowe et al., 1986). Although Carrick & Lowe (1988) found some benthic algal populations to be silicon limited when not allowed contact with quartz sand substrate by supplying nitrogen and phosphorus in a silicon-free medium. Carrick’s major contribution resulted from research he conducted in northern Lake Michigan demonstrating that different benthic algal populations are limited by different resources and that it is incorrect to assume that algae are limited by a single resource as if they were a population rather than an assemblage of many populations (Carrick et al., 1988). DeYoe et al. (1992) demonstrated the sensitivity of some taxa to nitrogen/phosphorus ratios in the environment demonstrating that the numbers of endosymbiotic nitrogen-fixing

4 cyanobacteria within the diatom Rhopalodia is partially a function of the external N/P ratio. Fairchild’s nutrient diffusing substrate technique was also employed to understand how pH differences in aquatic ecosystems can impact nutrient limitation. Keithan et al. (1988) investigated periphyton species response to nitrogen and phosphorus manipulation in a culturally acidified stream while Carrick manipulated nutrients along a natural pH gradient in a northern Michigan lake (Carrick & Lowe, 1989). Pillsbury (1993) investigated light resources examining both quantity and quality of light with the application of tannic acid light filters in four acid lakes in northern Michigan, USA (Pillsbury & Lowe, 1999). He found that light accounted for most of the variation in biomass and community structure with high light environment favoring filamentous green algae (Zygnematales) and low light favoring desmids and diatoms. Marks (1990) manipulated light and nutrients simultaneously in a three-way factorial design in oligotrophic Flathead Lake, Montana, USA. While nitrogen and phosphorus together significantly increased algal biomass, light had little effect in this system (Marks & Lowe, 1993). Disturbance The influence of physical flow-mediated disturbance on benthic algal community structure was recently reviewed by Peterson (1996). Although not addressing this topic directly, a few students at Bowling Green did pursue aspects of this phenomenon. Lamb (1983) employed scanning electron microscopy to investigate the role of current in shaping algal community physiognomy. The publication resulting from his thesis (Lamb & Lowe, 1987) was awarded the best paper of the year in the Ohio Journal of Science. Barnese (1989) examined diel patterns of algal drift in the Maple River, Michigan, USA and found that disturbance caused by benthic insect activity partially explained patterns of algal drift (Barnese & Lowe, 1992). Francoeur (1997) studied mechanisms of periphyton disturbance-resistance in a disturbance-prone river in New Zealand. He found that imbricated microform bed clusters of stones served as refugia for disturbance-vulnerable species (Francoeur et al., 1998). These refugia serve

as epicenters for post-disturbance re-colonization of the stream by both periphyton and invertebrates. It is important to remember that nutrient resources and disturbance do not operate in isolation from each other and there may be interactive effects. Resource stress can alter the impact of hydrological disturbance on periphyton communities (Biggs et al., 1999). Biggs et al. (1998b) developed a habitat matrix model that considered the simultaneous impacts of nutrient abundance and disturbance intensity/ frequency. The model predicted responses of several common stream periphyton species and was later successfully tested on three valley segments of a New Zealand grassland river (Biggs et al., 1998a). Grazers Grazers can strongly influence the structure, density and physiology of periphytic algal communities (Steinman, 1996). Grazer-periphyton interactions have been the focus of several research investigations by students and collaborators at Bowling Green. The impact of grazing snails was a focus in of Lowe and Hunter (1988) who examined the impact of Physa integra on periphyton communities in Spring Lake, Michigan and by Barnese et al. (1990) who examined radular ultrastructure and grazing efficiency of six sympatric snails in Douglas Lake, Michigan. Barnese’s investigation demonstrated the capability of the prostrate green alga Coleochaete orbicularis to resist grazing by snails. The thallus often lost erect colorless setae to snails but the prostrate chlorophyll-bearing cells remained largely intact. Further, benthic diatoms associated with the thallus of Coleochaete also often escaped predation. In further research in Douglas Lake, Marks and Lowe (1989) investigated the independent and interactive effects of snail grazing (Elimia livescens) and nutrient enrichment on structuring periphyton communities. Grazing had a more pronounced effect on algal community composition on the nutrientenriched substrates than on the controls. Grazing caused a decrease in periphyton diversity and an increase in the relative proportion of green algae, especially Stigeoclonium tenue. Gresens and Lowe (1994) also working in Douglas Lake manipulated periphyton patches with nutrient-diffusing substrates to examine patch preference by the grazing larva of the chironomid Paratanytarsus dubius. As with Marks & Lowe (1989), addition of nitrogen and

5 phosphorus resulted in a Stigeoclonium-dominated community, which was negatively correlated with Paratanytarsus grazing. Grazing preference was correlated positively, however, with algal diversity. Two stream studies in which nutrients and grazers were manipulated illustrated the impact that grazers can exert on periphyton communities often greatly dampening the expected biomass increase of periphyton from nutrient stimulation. In the Maple River in northern Michigan Pan & Lowe (1995) found that colonization of benthic substrates by hydropsychid caddisflies can have a stronger impact on periphyton accrual than nutrients. Biggs & Lowe (1994) described the same phenomenon in the Kakanui River in New Zealand when the grazing snail Potamopyrgus antipodarum negated the effects of expected biomass accrual from nutrient addition. Environmental assessment The recent literature is rife with examples of the application of algae as tools for monitoring environmental quality both present (Lowe & Gale, 1980; Lowe, 1981; Shubert, 1984; Stevenson & Lowe, 1986; Whitton et al., 1991; Whitton & Rott, 1995; Lowe & Pan, 1996; Stevenson & Pan, 1999) and past (Battarbee et al., 1999; Bradbury, 1999; Fritz et al., 1999). The value of algae as integrators of fluctuating environmental variables is well established and documented. This application has been a continuing interest to students in the algae laboratory at Bowling Green (McCullough, 1971; Rohr, 1977; Maurice, 1982; Karl, 1983; Blake, 1987; Passy, 1997; Gooden, 2002). Algae are excellent integrators of fluctuating abiotic variables but these variables must be measured at correct temporal and spatial scales. Initial studies at Bowling Green were focused on local systems. For example, impact of treated domestic sewage on the Portage River, Ohio was the first research initiative using algae as environmental indicators at Bowling Green (Lowe & McCullough, 1974). Our research group initially focused on aquatic environments near Bowling Green. Pryfogle and Lowe (1979) authored a methodology manuscript based on some of the initial findings and experiences with periphyton monitoring. In the 1970s, Stevenson (1976), Pryfogle (1976), Kline (1975) and others were focused on research projects in the Sandusky River

watershed (Ohio). This was a particularly fertile time in this research group and led to Stevenson developing some of his early thought on environmental monitoring (Stevenson & Pryfogle, 1976; Stevenson, 1984). Stevenson has now become a leading authority on the application of algae for water quality monitoring. In the 1990s the laboratory established research collaboration with Procter and Gamble Experimental Stream Facility near Cincinnati, Ohio. In this controlled environment many synthetic chemicals and particularly surfactants were tested for their potential impact on benthic algal communities (Belanger et al., 1994). This collaboration provided us with the opportunity not for only bioassay research (Belanger et al., 1996), but also facilitated periphyton research not directly related to the bioassays (Lowe et al. 1996; Greenwood et al., 1999). These integrated research activities continue with a new cadre’ of graduate advisees researching and learning the roles of systematics, ecology and environmental assessment.

Acknowledgements and concluding remarks This manuscript is dedicated to Dr. John C. Kingston my first doctoral advisee who succumbed to a brain tumor in 2004. John will forever stand as a shining example of a productive scientist who maintained balance in his life between science, his family, music and nature. I thank all of my graduate advisees, current and future without whom most of this research would never have happened. I thank especially R. Jan Stevenson and Yangdong Pan for supplying the inertia necessary for this event to happen. I thank my collaborators who have enriched my career. Finally, I thank John Dodd, who served as an important role model for teaching and advising students. Dodd wrote an article on this topic that strongly influenced me, ‘‘Science, a Modern Fountain for Youth’’ (Dodd, 1953). This little two-page paper is of a sort that is often undervalued by readers expecting ‘‘hard science’’ from science writers, but the manuscript outlined Dodd’s approach to teaching and training students. I have tried to incorporate Dodd’s ideas in my teaching

6 approach. Dodd asks the following questions in equating teaching of science as a ‘‘fountain for youth.’’ ‘‘1. Is the water in your fountain always clear and sparkling? Do students become thirsty just watching it? 2. Is it free from any taint of bias, boredom or bunk? 3. Is the pressure adjustable, so students can drink their fill without choking or without becoming disgusted because it flows too slowly? 4. Do you shut the fountain off at four o’clock sharp? 5. Can you accept the fact that most of the water goes down the drain, and console yourself with the thought that the little which is imbibed has important metabolic implications? 6. Do you have enough well-springs of information so the fountain never runs dry? 7. Are you patient with the eager ones who always manage to fall into the fountain? 8. Can you recognize the timid ones who are desperately thirsty but are unable to crowd around a busy fountain? 9. And, finally, do you ever take a little drink yourself, just to see if the stuff is as advertised?’’ Thanks again, John.

References Acker, F., 1977. The phytoplankton of the Maumee River between Grand Rapids, Ohio and Maumee, Ohio. Masters Thesis, Bowling Green State University, Bowling Green, Ohio, USA, 90 pp. Bahls, L. L., 1973. Diatom community response to primary wastewater effluent. Journal of the Water Pollution Control Federation 45: 134–144. Bahls, P. A. & L. L. Bahls, 1974. Trophic response to a hatchery effluent. Proceedings of the Montana Academy of Science 34: 5–11. Barnese, L. E., 1989. A survey and experimental study of algal drift in the Maple River, Pellston, Michigan. Doctoral Dissertation, Bowling Green State University, Bowling Green, Ohio, USA, 124 pp. Barnese, L. E. & R. L. Lowe, 1992. Effects of substrate, light and benthic invertebrates on algal drift in small streams. Journal of the North American Benthological Society 11: 49–59. Barnese, L. E., R. L. Lowe & R. D. Hunter, 1990. Comparative grazing efficiency of six species of sympatric snails in Douglas Lake, Michigan. Journal of the North American Benthological Society 9: 35–44. Battarbee, R. W., D. F. Charles, S. S. Dixit & I. Renberg, 1999. Diatoms as indicators of surface water acidity. In Stoermer, E. F. & J. P. Smol (eds), The Diatoms: applications for the Environmental and Earth Sciences. Cambridge University Press, 85–127. Belanger, S. E., J. B. Barnum, D. M. Woltering, J. W. Bowling, R. M. Ventullo, S. D. Schermerhorn & R. L. Lowe, 1994.

Algal periphyton structure and function in response to consumer chemicals in stream mesocosms. In Graney, R. L., J. H. Kennedy & J. H. Rogers (eds), Aquatic Mesocosm Studies in Ecological Risk Assessment. SETAC Special Publication Series Lewis Publishers, Boca Ratan, FL: 535–567. Belanger, S. E., R. L. Lowe & B. H. Rosen, 1985. Epiphytism of Synedra parasitica on Surirella robusta: observations of populations and associations in a Virginia pond. Transactions of the American Microscopical Society 104: 378–386. Belanger, S. E., K. L. Rupe, R. L. Lowe, D. W. Johnson & Y. Pan, 1996. A flow through laboratory microcosm for assessing effects of surfactants on natural periphyton. Environmental Toxicology and Water Quality 11: 65–76. Biggs, B. J. F., 1989. Biomonitoring of organic pollution using periphyton, South Branch, Canterbury, New Zealand. New Zealand Journal of Marine and Freshwater Research 23: 263–274. Biggs, B. J. F. & R. L. Lowe, 1994. Responses of two trophic levels to patch enrichment along a New Zealand stream continuum. New Zealand. New Zealand Journal of Marine and Freshwater Research 28: 119–134. Biggs, B. J. F., C. Kilroy & R. L. Lowe, 1998a. Periphyton development in three valley segments of a New Zealand grassland river: test of a habitat matrix conceptual model within a catchment. Archive fu¨r Hydrobiologie 143: 147–177. Biggs, B. J. F., R. J. Stevenson & R. L. Lowe, 1998b. A habitat matrix conceptual model for stream periphyton. Archive fu¨r Hydrobiologie 143: 21–56. Biggs, B. J. F., N. Tuchman, R. L. Lowe & R. J. Stevenson, 1999. Resource stress alters hydrological disturbance effects in a stream periphyton community. Oikos 85: 95–108. Blake, G., 1987. The effects of the agricultural herbicide alachlor on total biomass and community structure of algal periphyton in artificial streams. Masters Thesis, Bowling Green State University, Bowling Green, Ohio, USA, 97 pp. Bradbury, J. P., 1999. Continental diatoms as indicators of long-term environmental change. In Stoermer, E. F. & J. P. Smol (eds), The Diatoms: applications for the environmental and Earth Sciences. Cambridge University Press, 169–182. Bruno, M. G., 1978. Distribution and periodicity of desmids and diatoms in a Northwestern Ohio bog lake. Masters Thesis, Bowling Green State University, Bowling Green, Ohio, USA, 64 pp. Bruno, M. G. & R. L. Lowe, 1980. Differences in the distribution of some bog diatoms: a cluster analysis. American Midland Naturalist 104: 70–79. Busch, D. E., 1974. Ultrastructure of the filamentous habit in the diatom Navicula confervacea (Ku¨tz.) Grun. Journal of Phycology 10: 241–243. Camburn, K. E., 1977. The haptobenthic diatom flora of Long Branch Creek, South Carolina. Masters Thesis, Bowling Green State University, Bowling Green, Ohio, USA, 266 pp. Camburn, K. E., R. L. Lowe & D. E. Stoneburner, 1978. The haptobenthic diatom flora of Long Branch, South Carolina. Nova Hedwigia 37: 149–279. Carrick, H. J., 1985. The response of Lake Michigan benthic algae to an in situ nutrient manipulation. Masters Thesis,

7 Bowling Green State University, Bowling Green, Ohio, USA, 86 pp. Carrick, H. J. & R. L. Lowe, 1988. Response of Lake Michigan benthic algae to in situ enrichment with Si, N and P. Canadian Journal of Fisheries and Aquatic Science 45: 271–279. Carrick, H. J., R. L. Lowe & J. T. Rotenberry, 1988. Functional associations of benthic algae along experimentally manipulated nutrient-gradients: Relationships with algal community diversity. Journal of the North American Benthological Society 7: 117–128. Carrick, H. J. & R. L. Lowe, 1989. Benthic algal response to N and P enrichment along a pH gradient. Hydrobiologia 179: 119–127. Descy, J. P., 1979. A new approach to water quality estimation using diatoms. Nova Hedwigia Beihefte 64: 305–323. DeYoe, H. R., R. L. Lowe & J. C. Marks, 1992. The effect of nitrogen and phosphorus on the endosymbiont load of Rhopalodia gibba and Epithemia turgida (Bacillariophyceae). Journal of Phycology 28: 773–777. Dixit, S. S., B. F. Cumming, J. P. Smol & J. C. Kingston, 1992. Monitoring environmental changes in lakes using algal microfossils. In McKenzie, D. H., D. E. Hyatt & V. J. MacDonald (eds), Ecological Indicators. Elsevier Applied Sciences, Amsterdam: 1135–1155. Dodd, J. D., 1953. Science, a modern fountain for youth. American Biology Teacher 15: 1–2. Fairchild, F. W. & R. L. Lowe, 1984. Algal substrates which release nutrients: effects on periphyton and invertebrate succession. Hydrobiologia 114: 29–37. Fairchild, G. W., R. L. Lowe & W. B. Richardson, 1985. Nutrient-diffusing substrates as an in situ bioassay using periphyton: Algal growth responses to combinations of N and P. Ecology 66: 465–472. Fisher, D. Z., 1980. Autumn periphyton and phytoplankton diatom communities in relation to depth and current velocity in the Maumee River, Ohio. Masters Thesis, Bowling Green State University, Bowling Green, Ohio, USA, 86 pp. Francoeur, S. N., 1997. Microform bed clusters as refugia for periphyton in a flood-prone headwater stream. Masters Thesis, Bowling Green State University, Bowling Green, Ohio, USA, 34 pp. Francoeur, S. N., B. J. F. Biggs & R. L. Lowe, 1998. Microform bed clusters as refugia for periphyton in a flood-prone headwater stream. New Zealand Journal of Marine and Freshwater Research 32: 363–374. Fritz, S. C., B. F. Cumming, F. Gassee & K. R. Laird, 1999. Diatoms as indicators of hydrologic and climate change in saline lakes. In Stoermer, E. F. & J. P. Smol (eds), The Diatoms: Applications for the Environmental and Earth Sciences. Cambridge University Press, 41–72. Gomez, S. R., J. R. Johansen & R. L. Lowe, 2003. Epilithic aerial algae of Great Smoky Mountains National Park. Biologia Bratislavia 58: 603–615. Gooden, W., 2002. Periphyton responses to surfactants: Community structure and mat architecture. Doctoral Dissertation, Bowling Green State University, Bowling Green, Ohio, USA, 220 pp. Greenwood, J. L., T. A. Clason, R. L. Lowe & S. E. Belanger, 1999. Examination of endopelic and epilithic algal commu-

nity structure employing scanning electron microscopy. Freshwater Biology 41: 821–828. Gresens, S. E. & R. L. Lowe, 1994. Periphyton patch preference in grazing chironomid larvae. Journal of the North American Benthological Society 13: 89–99. Jackson, D. C., 1975. Distribution and morphology of members of the diatom genera Gyrosigma Hassal and Pleurosigma W. Smith in the Portage River Drainage System. Masters Thesis, Bowling Green State University, Bowling Green, Ohio, USA, 75 pp. Jackson, D. C. & R. L. Lowe, 1978. Valve ultrastructure of species of the diatom genera Gyrosigma Hassal and Pleurosigma W. Sm. from the Portage River Drainage system, Ohio. Transactions of the American Microscopical Society 97: 569–581. Johansen, J. R., R. L. Lowe, S. R. Gomez, J. P. Kociolek & S. A. Makosky, 2004. New algal species records for the Great Smoky Mountains National Park, U.S.A., with an annotated checklist of all reported algal species for the park. Algological Studies. Kaatz, M. R., 1955. The black swamp: a study in historical geography. Annals of the Association of American Geographers 45: 1–35. Karl, K. A., 1983. The effects of fly ash extract on periphyton community structure in field enclosures. Masters Thesis, Bowling Green State University, Bowling Green, Ohio, USA, 97 pp. Keithan, E. D., 1983. Primary productivity and structure of phytolithic communities in streams in the Great Smoky Mountains National Park. Doctoral Dissertation, Bowling Green State University, Bowling Green, Ohio, USA, 83 pp. Keithan, E. D. & R. L. Lowe, 1985. Primary productivity and structure of phytolithic communities in streams in the Great Smoky Mountains National Park. Hydrobiologia 123: 59–67. Keithan, E. D., R. L. Lowe & H. DeYoe, 1988. Benthic diatom distribution in a Pennsylvania stream: the role of pH and nutrients. Journal of Phycology 24: 581–585. Kilroy, C., K. Sabbe, E. Bergy, W. Vyverman & R. Lowe, 2003. New species of Fragilariforma (Bacillariophyceae) from New Zealand and Austrailia. New Zealand Journal of Botany 41: 535–554. Kingston, J. C., 1980. Characterization of benthic diatom communities in Grand Traverse Bay, Lake Michigan. Doctoral Dissertation, Bowling Green State University, Bowling Green, Ohio, USA. Kingston, J. C., R. L. Lowe, E. F. Stoermer & T. Ladewski, 1983. Spatial and temporal distribution of benthic diatoms in northern Lake Michigan. Ecology 64: 1566–1580. Kline, P. A., 1975. Survey of the phytoplankton of the Sandusky River at Fremont, Sandusky Co., Ohio. Masters Thesis, Bowling Green State University, Bowling Green, Ohio, USA. Kline, P. E. & R. L. Lowe, 1976. Phytoplankton of the Sandusky River near Fremont, Ohio. In Baker, D. & B. Prater (eds), Proceedings of the Sandusky River Basin Symposium . United States Environmental Protection Agency, 175–208. Kociolek, J. P., 1982. Diatoms from two streams in Great Smoky Mountains National Park. Masters Thesis, Bowling Green State University, Bowling Green, Ohio, USA, 175 pp.

8 Kociolek, J. P., M. A. Lamb & R. L. Lowe, 1983. Notes on the growth and ultrastructure of Biddulphia laevis Ehr. (Bacillariophyceae) in the Maumee River, Ohio. Ohio Journal of Science 8: 125–130. Kociolek, J. P. & R. L. Lowe, 1983. Scanning electron microscopic observations on the frustular morphology and filamentous growth habit of Diatoma hiemale v. mesodon. Transactions of the American Microscopical Society 102: 281–287. Kociolek, J. P. & E. F. Stoermer, 2001. Taxonomy and ecology: a marriage of necessity. Diatom Research 16: 433–442. Krejci, M., 1985. Spatial patterns of epipsammic diatoms in a spring-fed brook with emphasis on the effect of sand grain mineralogy on diatom occurrence. Doctoral Dissertation, Bowling Green State University, Bowling Green, Ohio, USA. Krejci, M. E. & R. L. Lowe, 1986. The importance of sand grain mineralogy and topography in determining microspatial distribution of epipsammic diatoms. Journal of the North American Benthological Society 5: 221–229. Krejci, M. E. & R. L. Lowe, 1987a. Spatial and temporal variation of epipsammic diatoms in a spring-fed brook. Journal of Phycology 23: 585–590. Krejci, M. E. & R. L. Lowe, 1987b. The seasonal occurrence of macroscopic colonies of Meridion circulare (Bacillariophyceae) in a spring-fed brook. Transactions of the American Microscopical Society 106: 173–178. Lamb, M. E., 1983. The effects of current velocity on the structuring of diatom communities. Masters Thesis, Bowling Green State University, Bowling Green, Ohio, USA, 94 pp. Lamb, M. A. & R. L. Lowe, 1987. Effects of current velocity on the physical structuring of diatom (Bacillariophyceae) communities. Ohio Journal of Science 87: 72–78. Lamb, M. A. & R. L. Lowe, 1981. A preliminary investigation of the effect of current speed on periphyton community structure. Micron 12: 211–212. Lowe, R. L., 1975. Comparative ultrastructure of the valves of some species of Cyclotella (Bacillariophyceae). Journal of Phycology 11: 415–424. Lowe, R. L., 1981. The utility of diatoms for hazard assessment of chemicals in ecosystems . Special Publication of the National Academy of Science, Washington, DC, pp 133–136. Lowe, R. L. & D. E. Busch, 1975. Morphological observations on two species of the diatom genus Thalassiosira from freshwater habitats in Ohio. Transactions of the American Microscopical Society 94: 118–123. Lowe, R. L. & R. E. Crang, 1972. The ultrastructure and morphological variability of the frustule of Stephanodiscus invisitatus Hohn and Hellerman. Journal of Phycology 8: 256–259. Lowe, R. L. & W. F. Gale, 1980. Monitoring periphyton with artificial benthic substrates. Hydrobiologia 69: 235–244. Lowe, R. L. & R. D. Hunter, 1988. The effect of grazing by Physa integra on periphyton community structure. Journal of the North American Benthological Society 7: 29–36. Lowe, R. L. & P. E. Kline, 1976. Planktonic centric diatoms of the Sandusky River near Fremont, Ohio. In Baker, D. B. Prater (eds), Proceedings of the Sandusky River Basin Symposium. United States Environmental Protection Agency : 143–152.

Lowe, R. L. & J. P. Kociolek, 1984. New and rare diatoms from Great Smoky Mountains National Park. Nova Hedwigia 39: 465–276. Lowe, R. L., S. Golladay & J. Webster, 1986. Periphyton response to nutrient manipulation in a clear-cut and forested watershed. Journal of the North American Benthological Society 5: 211–220. Lowe, R. L., J. B. Guckert, S. E. Belanger, D. H. Davidson & D. W. Johnson, 1996. An Evaluation of Periphyton Community Structure and Function on Tile and Cobble Substrata in Experimental Stream Mesocosms. Hydrobiologia 328: 135–146. Lowe, R. L. & J. M. McCullough, 1974. The effect of sewage treatment plant effluent on diatom communities in the Portage River, Wood Co., Ohio. Ohio Journal of Science 74: 154–161. Lowe, R. L. & Y. Pan, 1996. Use of Benthic Algae in Water Quality Monitoring. In Stevenson, R. J., M. L. Bothwell & R. L. Lowe (eds), Benthic Algal Ecology in Freshwater Ecosystems. Academic Press, San Diego, CA, USA: 705–739. Lowe, R. L., B. H. Rosen & J. C. Kingston, 1982. A comparison of epiphytes on Bangia atropurpurea (Rhodophyta) and Cladophora glomerata (Chlorophyta) from Northern Michigan. Journal of Great Lakes Research 8: 164–168. Luttenton, M. R., 1989. In situ manipulation of factors affecting periphyton community structure. Doctoral Dissertation, Bowling Green State University, Bowling Green, Ohio, USA. Marks, J. C., 1990. The independent and interactive effects of nitrogen, phosphorus and light on structuring periphyton in Flathead Lake, Montana. Masters Thesis, Bowling Green State University, Bowling Green, Ohio, USA, 92 pp. Marks, J. C. & R. L. Lowe, 1989. The independent and interactive effects of snail grazing and nutrient enrichment on structuring periphyton communities. Hydrobiologia 185: 9–17. Marks, J. C. & R. L. Lowe, 1993. Interactive effects of nutrient availability and light levels on the periphyton composition of a large oligotrophic lake. Canadian Journal of Fisheries and Aquatic Science 50: 1270–1278. Maurice, C. G., 1982. Effects of acidification on the periphyton of an artificial stream. Masters Thesis, Bowling Green State University, Bowling Green, Ohio, USA, 92 pp. McCullough, J. M., 1971. The effect of sewage-treatment-plant effluent on diatom communities in the North Branch of the Portage River, Wood County, Ohio. Masters Thesis, Bowling Green State University, Bowling Green, Ohio, USA, 75 pp. Miller, A. R., 1983. Temporal and spatial relationships in the epipsammic diatom community. Masters Thesis, Bowling Green State University, Bowling Green, Ohio, USA, 87 pp. Miller, A. R., R. L. Lowe & J. T. Rotenberry, 1987. Microsuccession of diatoms on sand grains. Journal of Ecology 75: 693–709. Millie, D. F. & R. L. Lowe, 1983. Studies on Lake Erie’s littoral algae; host specificity and temporal periodicity of epiphytic diatoms. Hydrobiologia 99: 7–18. Morgan, M. D., 1987. Impact of nutrient enrichment and alkalinization on periphyton communities in the New Jersey Pine Barrens. Hydrobiologia 144: 233–241.

9 Pan Y., 1993. The effects of nutrients on periphyton. Doctoral Dissertation, Bowling Green State University, Bowling Green, Ohio, USA, 98 pp. Pan, Y. & R. L. Lowe, 1995. The effects of hydropsychid colonization on algal response to nutrient enrichment in a small Michigan stream, U.S.A. Freshwater Biology 33: 393–400. Passy, S. I., 1997. Ecology and systematics of the periphytic diatoms from the Mesta River system, Bulgaria. Doctoral Dissertation, Bowling Green State University, Bowling Green, Ohio, USA, 241 pp. Passy, S. I. & R. L. Lowe, 1994. Taxonomy and ultrastructure of Gomphoneis mesta sp. nov. (Bacillariophyta), a new epilithic diatom from the Mesta River, Bulgaria. Journal of Phycology 30: 885–891. Passy-Tolar, S. I., J. P. Kociolek & R. L. Lowe, 1997. New Gomphonema species (Bacillariophyta) from South African rivers. Journal of Phycology 33: 455–474. Passy-Tolar, S. I., Y. Pan & R. L. Lowe, 1999. Ecology of the major periphytic diatom communities from the Mesta River, Bulgaria. International Review der Gesempten Hydrobiologie 84: 129–174. Peterson, C. G., 1996. Response of benthic algal communities to natural physical disturbance. In Stevenson, R. J., M. L. Bothwell & R. L. Lowe (eds), Benthic Algal Ecology in Freshwater Ecosystems. Academic Press, San Diego, CA, USA: 375–402. Pillsbury, R. W., 1993. Factors influencing the structure of benthic algal communities in acid lakes. Doctoral Dissertation, Bowling Green State University, Bowling Green, Ohio, USA, 142 pp. Pillsbury, R. W. & R. L. Lowe, 1999. The response of benthic algae to manipulations of light resources in four acidic lakes in northern Michigan. Hydrobiologia 394: 69–81. Potapova, M. G., K. C. Ponader, R. L. Lowe, T. A. Clason & L. A. Bahls, 2003. Small-celled Nupela species from U.S.A. rivers. Diatom Research. 18: 293–306. Pryfogle, P. A., 1976. Seasonal distribution of periphytic diatoms on natural substrates in Tymochtee Creek. Masters Thesis, Bowling Green State University, Bowling Green, Ohio, USA, 79 pp. Pryfogle, P. A. & R. L. Lowe, 1979. Sampling and interpretation of epilithic lotic diatom communities. In Weitzel, R. (ed.), Methods and Measurements of Attached Microcommunities: A Review. American Society for Testing and Materials, Philadelphia, PA, USA: 77–89. Rohr, J. L., 1977. Changes in diatom community structure due to environmental stress. Masters Thesis, Bowling Green State University, Bowling Green, Ohio, USA, 157 pp. Sabbe, K., K. Vanhoutte, R. L. Lowe, E. A. Bergey B. J. F. Biggs, S. Francoeur, D. Hodgson & W. Vyverman, 2001. Six new Actinella (Bacillariophyta) species from Papua New Guinea, Australia and New Zealand: further evidence for widespread diatom endemism in the Australasian region. European Journal of Phycology 36: 321–340. Sharkey, M. J., 2001. The all taxa biological inventory of the Great Smoky Mountains National Park. Florida Entomologist 84: 556–564. Shubert, L. E., 1984. Algae as Ecological Indicators . Academic Press, London, England 434.

Steinman, A. D., 1996. Effects of grazers on freshwater benthic algae. In Stevenson, R. J., M. L. Bothwell & R. L. Lowe (eds), Benthic Algal Ecology in Freshwater Ecosystems. Academic Press, San Diego, CA, USA: 341–373. Stevenson, R. J., 1976. The periphytic diatoms of the Sandusky River. Masters Thesis, Bowling Green State University, Bowling Green, Ohio, USA, 114 pp. Stevenson, R. J., 1984. Epilithic and epipelic diatoms in the Sandusky River, with emphasis on species diversity and water quality. Hydrobiologia 114: 161–175. Stevenson, R. J. & R. L. Lowe, 1986. Sampling and interpretation of algal patterns for water quality assessments. In Isom, B. G. (ed.), Rationale for Sampling and Interpretation of Ecological Data in the Assessment of Freshwater Ecosystems American Society for Testing and Materials. Philadelphia, PA, USA: 118–149. Stevenson, R. J. & Y. Pan, 1999. Assesing environmental conditions in rivers and streams with diatoms. In Stoermer, E. F. & J. P. Smol (eds), The Diatoms: Applications for the Environmental and Earth Sciences. Cambridge University Press, 11–40. Stevenson, R. J. & P. A. Pryfogle, 1976. A comparison of the winter diatom flora of the Sandusky River and Tymochtee Creek. In Baker, D. & B. Prater (eds), Proceedings of the Sandusky River Basin Symposium. United States Environmental Protection Agency, 209–231. Whitton, B. A., E. Rott & G. Friedrich, 1991. Use of Algae for Monitoring Rivers. E. Rott, Publisher, Institut fu¨r Botanik, AG Hydrobotanik, Universita¨t Innsbruck, A-6020 Innsbruck, Austria, 193 pp. Whitton, B. A. & E. Rott, 1995. Use of algae for monitoring rivers II. E. Rott, Publisher, Institut fu¨r Botanik, AG Hydrobotanik, Universita¨t Innsbruck, A-6020 Innsbruck, Austria. 196 pp.

Appendix 1 Graduate theses and dissertations from the Bowling Green State University Algae Laboratory, 1971–2003. 1. J. Michael McCullough, M. A., 1971. The effect of sewage-treatment-plant effluent on diatom communities in the North Branch of the Portage River, Wood County, Ohio. 2. Robert Reitz, M. S., 1973. Phytoplankton periodicity in two Northwestern Ohio ponds. 3. Bill Brower, M. S., 1973. Phytoplankton and periphyton diatom relationships in two highly eutrophic lakes. 4. David E. Busch, M. S., 1974. Vertical and seasonal distribution of the Bacillariophyta in the Miller Blue Hole, Sandusky Co., Ohio.

10 5. Terrance L. Breyman, M. S., 1974. Bangia in Western Lake Erie. 6. David C. Jackson, M. S., 1975. Distribution and morphology of members of the diatom genera Gyrosigma Hassal and Pleurosigma W. Smith in the Portage River Drainage System. 7. Phillip A. Kline, M. S., 1975. Survey of the phytoplankton of the Sandusky River at Fremont, Sandusky Co., Ohio. BGSU. 8. Ronald J. Bockelman, M. S., 1975. The seasonal productivity of zooplankton and benthic macroinvertebrate populations in six northwest Ohio ponds. 9. R. Jan Stevenson, M. S., 1976. The periphytic diatoms of the Sandusky River. 10. P.A. Pryfogle, M. S., 1976. Seasonal distribution of periphytic diatoms on natural substrates in Tymochtee Creek. 11. Keith Camburn, M. S., 1977. The haptobenthic diatom flora of Long Branch Creek, South Carolina. 12. Frank Acker, M. S., 1977. The phytoplankton of the Maumee River between Grand Rapids, Ohio and Maumee, Ohio. 13. J. L. Rohr, M. S., 1977. Changes in diatom community structure due to environmental stress. 14. R. F. Andritsch, M. S., 1977. Seasonal photosynthetic rates of Chara globularis in Steidtmann Pond. 15. Mary Bruno, M. S., 1978. Distribution and periodicity of desmids and diatoms in a Northwestern Ohio bog lake. 16. David F. Millie, M. S., 1979. An analysis of epiphytic diatom assemblages of three species of aquatic vascular plants in three Lake Erie marshes. 17. Robert Foster, M. S., 1980. Selected toxic metal concentrations in several species of western Lake Erie fish with respect to age. 18. Daniel Z. Fisher, M. S., 1980. Autumn periphyton and phytoplankton diatom communities in relation to depth and current velocity in the Maumee River, Ohio. 19. John C. Kingston, Ph.D., 1980. Characterization of benthic diatom communities in Grand Traverse Bay, Lake Michigan. 20. Earl Chilton, M. S., 1982. A comparison of macroscopic invertebrates living in Bangia

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atropurpurea and Cladophora glomerata beds in Lake Erie. John P. Kociolek, M. S., 1982. Diatoms from two streams in Great Smoky Mountains National Park. Charles G. Maurice, M. S., 1982. Effects of acidification on the periphyton of an artificial stream. David R. Beeson, M. S., 1982. Epiphytic diatom (Bacillariophyceae) community structure in a wetland continuum, Sugar Island, Michigan. Barry H. Rosen, Ph.D., 1982. Physiological and ultrastructural responses to light intensity and nutrient limitation in the planktonic diatom Cyclotella meneghiniana. Mark E. Lamb, M. S., 1983. The effects of current velocity on the structuring of diatom communities. Ann R. Miller, M. S., 1983. Temporal and spatial relationships in the epipsammic diatom community. Robert Genter, M. S., 1983. The effects of different initial colonists on the outcome of periphyton succession in a small stream. Kevin A. Karl, M. S., 1983. The effects of fly ash extract on periphyton community structure in field enclosures. Elaine D. Keithan, Ph.D., 1983. Primary productivity and structure of phytolithic communities in streams in the Great Smoky Mountains National Park. Norlida Anis, M. S., 1985. Effects of water chemistry on the distribution of diatom communities. Mark Krejci, Ph.D., 1985. Spatial patterns of epipsammic diatoms in a spring-fed brook with emphasis on the effect of sand grain mineralogy on diatom occurrence. Hunter J. Carrick, M. S., 1985. The response of Lake Michigan benthic algae to an in situ nutrient manipulation. Gail Blake, M. S., 1987. The effects of the agricultural herbicide alachlor on total biomass and community structure of algal periphyton in artificial streams. Mark R. Luttenton, Ph.D., 1989. In situ manipulation of factors affecting periphyton community structure.

11 35. Lisa E. Barnese, Ph.D., 1989. A survey and experimental study of algal drift in the Maple River, Pellston, Michigan. 36. Douglas Deutschman, M. S., 1990. Response of an algal community to temporal variability of resources. 37. Jane C. Marks, M. S., 1990. The independent and interactive effects of nitrogen, phosphorus and light on structuring periphyton in Flathead Lake, Montana. 38. Craig D. Layne, M. S., 1990. The algal mat of Douglas Lake, Michigan: Its composition, role in lake ecology, and response to chemical perturbations. 39. Hudson DeYoe, Ph.D., 1991. Preliminary characterization of the relationship between Rhopalodia gibba (Bacillariophyceae) and its cyanobacterial endosymbiont. 40. Susan Hardman, Ph.D., 1992. Environmental components influential in epipelic algal community structure. 41. James C. Sferra, M. S., 1992 Potential effects of the zebra mussel, Dreissena polymorpha (Pallas) on the Western Basin of Lake Erie. 42. Carmen Pedraza-Silva, M. S., 1992. A description of the algal floras of Guzmania berteroniana and Vriesia sintenisii (Bromeliaceae) and preliminary investigation of bromeliad-algal interactions. 43. Robert W. Pillsbury, Ph.D., 1993. Factors influencing the structure of benthic algal communities in acid lakes. 44. Diane Longanbach M. A. T., 1993. Survey of aquaria educational curricula across the United States. 45. Yangdong Pan, Ph.D., 1993. The effects of nutrients on periphyton. 46. LouAnne Reich, M. S., 1994. An examination of Douglas Lake, Cheboygan County, Michigan as suitable habitat for the zebra mussel (Dreissena polymorpha): food quality and attachment site preference. 47. Bret Gargasz, M. S., 1994. Non-thesis, plan II. 48. Steven Francoeur, M. S., 1997. The effect of in-stream flow refugia on the recovery of

stream periphyton communities following flooding disturbance. 49. Sophia Passy, Ph.D., 1997. Ecology and systematics of the periphytic diatoms from the Mesta River system, Bulgaria. 50. Joanne Rhoers, M. S., 1997. The Impact of the Crayfish Orconectes propinquis on Benthic Algae and Zebra Mussels. 51. Rebecca Visnyai, M. S., 1997. Wetland restoration: the need to base restoration on function and landscape-level processes. 52. Randy Litteral, 1998. Benthic algal community structure and the compensation point. 53. Jennifer L. Greenwood, M. S., 1998. The effects of pH light on periphyton communities in a Michigan Wetland. 54. Todd A. Clason, M. S., 1999. Diurnal migration and community ultrastructure of benthic algae in Douglas Lake. 55. Timothy Stewart, Ph.D., 1999. Evidence and mechanisms for Dreissena effects on other benthic macroinvertebrates in western Lake Erie. 56. Julianne Heinlein, M. S., 2000. Flood disturbance mechanisms in stream periphyton: individual and interactive effects of shear stress perterbations and suspended sediment concentration. 57. Agnieszka Pinowska, Ph.D., 2001. Indirect effect of sediment nutrient enrichment on epiphytic algal communities. 58. Amy Kireta, M. S., 2001. Benthic algal shifts in response to the round goby. 59. Wanda Gooden, Ph.D., 2002. Periphyton responses to surfactants: Community structure and mat architecture. 60. Jennifer Ress, M. S., 2003. Comparative grazing efficiencies of three aquatic grazers and their impact on periphyton recovery. 61. Jennifer Wearly, M. S., 2004. Changes in algal communities due to zebra mussel invasion of an oligotrophic inland lake. 62. Sarah Zeiler, M. S., 2004. The ratio of periphyton to plankton under variable nutrient regimens in a fen peatland.

Hydrobiologia (2006) 561:13–26  Springer 2006 R.J. Stevenson, Y. Pan, J.P. Kociolek & J.C. Kingston (eds), Advances in Algal Biology: A Commemoration of the Work of Rex Lowe DOI 10.1007/s10750-005-1602-6

Rexia erecta gen. et sp. nov. and Capsosira lowei sp. nov., two newly described cyanobacterial taxa from the Great Smoky Mountains National Park (USA) Dale A. Casamatta, Shannon R. Gomez & Jeffrey R. Johansen* Department of Biology, John Carroll University, University Heights, Ohio, 44118, USA (*Author for correspondence: Tel.: +1-216-397-4487; Fax: +1-216-397-4482; E-mail: [email protected])

Key words: ATBI, Capsosira, Cyanobacteria, endophytic, epilithic, Nostocales, Rexia, Stigonematales

Abstract Two newly discovered taxa of Cyanobacteria from the Great Smoky Mountain National Park (USA) are presented. The first is the newly described species Capsosira lowei (Capsosiraceae), differing from the only other previously described species C. brebissonii Ku¨tz. ex Born. et Flah. in regard to cell size and filament morphology. In addition, C. brebissonii is described as an aquatic or subaerophytic taxon, while our isolate was obtained as a phycobiont from the lichen Hydrothyria venosa J. L. Russell. Capsosira is currently placed in the Capsosiraceae of the Stigonematales due to its ability to have division in two planes. However, molecular evidence gathered in this study indicates closest affinity with Aulosira and Nostoc commune Vaucher, both in the Nostocaceae, Nostocales. Rexia erecta was isolated from concurrently collected aerophytic, epilithic sites. The hormogonia production, near absence of heterocysts and division in two planes are all typical of the Stigonematales, but it fits none of the currently circumscribed families in that order. This genus in other ways appears morphologically similar to members of the Scytonemataceae and Microchaetaceae. Molecular evidence (nearly complete 16S rRNA sequence data and 16S–23S internal transcribed spacer ITS region) places Rexia in the Microchaetaceae. These taxa are both problematic as they indicate that cell division in two planes has likely arisen more than once in the Nostocales, and thus the Stigonematales as currently circumscribed is not a monophyletic group. The Nostocales and Stigonematales are, in our opinion, in need of revision at the family and order level of classification.

Introduction The Great Smoky Mountain National Park (GSMNP) serves as a refuge for one of the largest, richest collections of plants, animals and crytogamic taxa in the world. Comprised of over one million acres, it is the largest contiguous preserve east of the Rocky Mountains (USA). Due to the heterogeneity of habitats afforded by the geological complexity, elevational variety, north-south park orientation and moist climate, this park has been designated an International Biosphere Preserve.

Beginning in 1997, an exhaustive effort was begun to identify every species in every phyla present in the park (Sharkey, 2001). Dubbed the All Taxa Biodiversity Inventory (ATBI), this project includes researchers from myriad academic and governmental positions throughout the Unites States. One of the most poorly characterized groups in the park includes the cryptogamic flora. Given the propensity of aquatic habitats including streams, ponds, perched bogs, drippy cliffs, swamps, and a host of other permanent and ephemeral habitats, the algal community may

14 prove to be quite vast. Park inventories of both diatoms and other algae were undertaken in the 1940s and 1980s, with a complete annotated list and review presented in Johansen et al. (2004). Recently, Gomez et al. (2003) reported on the epilithic, aerial algae from the GSMNP. In their study they noted the potential for 46 potentially new species among all algal groups. Here, we describe two new taxa from drippy walls within the GSMNP system. Both belong to the clade of heterocyte-bearing cyanobacteria, but their higher-level taxonomic status is uncertain. Capsosira lowei clearly fits the genus circumscription. However, its size, filament morphology, and habitat differ markedly from C. brebissonii Ku¨tz. ex Born. et Flah., the only other species in this genus. The newly described Rexia erecta gen. nov. et sp. nov. is problematic in that while undoubtedly a new genus, it does not clearly fit into any currently circumscribed family of cyanobacteria. Both of these taxa will be described and their phylogeny based on molecular data will be presented and discussed.

Materials and methods Sample collection and culturing Aerial algae were collected from GSMNP bedrock formations 19–24 May 2001. Organic matter was scrapped from rocks wetted by springs and splash from waterfalls. Scrapings were placed directly into whirl-paks and kept under refrigeration until culture and preservation. The pH at each site was measured using Whatman pH papers (range 4.0–7.0) while latitude, longitude and altitude were recorded using a Garmin GPS unit. Upon return to John Carroll University, samples were divided into roughly equal parts for preservation in 2% formaldehyde or further culturing. Three culture dilutions were made using Bold’s Basal Medium (BBM) agar (Bold & Wynne, 1978). Cultures were maintained in a growth chamber under 200 lE cm)1 irradiance, on a 16:8 h light:dark cycle, with temperature controlled at 18 C during the light cycle and 10 C during the dark. Cultures were grown for 4 weeks before subsequent analyses. Identifications were made employing fresh, preserved and cultured materials. Both taxa were

examined and photographed using an Olympus BH2 photomicroscope with high resolution Nomarski DIC optics. Line drawings were made from fresh material and represent meticulously measured real specimens. They were chosen in preference to photographs as the plane of focus was consistently flattened in the drawings. Taxonomic references followed Geitler (1932) and Anagnostidis and Koma´rek (1990). Molecular analyses Total genomic DNA was extracted from cultures using the CTAB method as modified by Cullings (1992) for the isolation and purification of DNA from mucilaginous organisms (Doyle & Doyle, 1987). DNA pellets were re-suspended in 50 ll of TE buffer and the resulting genomic DNA was checked using 1% agarose/ethidium bromide gels. Extracted DNA samples were stored at )20 C. PCR primers were modified from Wilmotte et al. (1993) and Nu¨bel et al. (1997) and designated as follows: Primer 1: 5¢ CTC TGT GTG CCT AGG TAT CC 3¢ (after Wilmotte et al., 1993) Primer 2: 5¢ GGG GAA TTT TCC GCA ATG GG 3¢ (after Nu¨bel et al., 1997) Primer 5: 5¢ TGT ACA CAC CGG CCC GTC 3¢ (after Wilmotte et al., 1993) Primer 6: 5¢ GAC GGG CCG GTG TGT ACA 3¢ (after Wilmotte et al., 1993) Initially, DNA samples were amplified using primers 1 and 2, which are cyanobacterial-specific primers. The resulting amplified products were analyzed on 1% agarose/ethidium bromide gels and were determined to be approximately 1600 base pairs in length (‘long PCR’). All PCR reactions were performed in a total volume of 100 ll containing 10.0 ll of 10 Taq polymerase buffer (Promega Corp., Madison, WI); 0.5 ll primer mixture (1.2 ll primer 1 or 6, 1.2 ll primer 2, 7.6 ll dH2O); 0.5 ll of a stock solution of dNTPs [(10 mM in each dNTP); dATP, dCTP, dGTP, and dTTP]; 0.5 ll (Promega) Taq polymerase; 1.0 ll of extracted genomic DNA (50 ng), and the appropriate amount of dH2O to bring the volume to 100 ll. The reactions were overlaid with mineral oil, and thermal cycling was conducted using an Thermolyne’s Amplitron and Temptronic

15 thermalcyclers (Barnstead International, Dubuque, IA) using the following parameters: 94 C for 60 s, 55 C for 45 s, and 72 C for 4 min repeated for 35 cycles (primer pair 1 and 2), and 94 C for 60 s, 55 C for 45 s, and 72 C for 2 min repeated for 20 cycles (primer pair 2 and 6). After amplification, a 7-min/72 C extension step was included for primer pair 1 and 2, whereas primer pair 2 and 6 received no such extension. PCR products were analyzed on 1% agarose/ethidium bromide gels in 1 TBE buffer. Amplified PCR products were cloned into pCR 4-TOPO plasmids containing sites for universal primers M13 forward and reverse using the TOPOTM TA cloning kit (Invitrogen Corp., Carlsbad, CA). After transformation, E. coli cells (Invitrogen) were plated onto Luria Broth plates containing 100 mg l)1 of ampicillin. Plasmids were isolated according to the instructions provided in the QIAprep Mini-prep kit (Quiagen Inc., Valencia, CA). Digests were resolved on 1% agarose/ ethidium bromide gels to detect plasmid inserts. Two replicate plasmid samples were isolated from each cloning plate and sequenced by Cleveland Genomics (Cleveland, OH). Automated sequencing was performed using universal infrared (IR) primers M13IR forward and reverse. Data analysis Forward and reverse sequences were aligned using the CLUSTAL W Multiple Sequence Alignment Program (Thompson et al., 1994). The resulting sequence alignments were checked by eye for ambiguities and PCR errors by the examination of chromatograms, with corrections made where appropriate. Ingroup and outgroup taxa were obtained from Genbank (www.ncbi.nlm.nih.gov) and other sequenced taxa. Parsimony trees were generated using a heuristic search constrained by random sequence addition (1000), steepest descent, and tree-bisection branch swapping using PAUP v.4.02b (Swofford, 1998). Bootstrap values were obtained from 1000 replicates with one random sequence addition to jumble the data using PAUP software. A neighbor joining tree was constructed employing the General Time Reversible model with corrected invariable sites (I) and Gamma distribution shape parameters (G) obtained using Modeltest v3.06 (Posada & Crandall, 1998) and

bootstrap resampled (1000) using PAUP. Maximum likelihood analysis using the HKY85 distance method and assuming a ti:tv ratio of 2 was also performed. Secondary structure of the 16S–23S ITS was determined using Mfold version 3.1 (http:// www.bioinfo.rpi.edu/applications/mfold/old/rna, Zuker, 2003). Structures were determined by folding and identifying each conserved helix separately first, and then constraining the sequence to produce the entire structure. Default conditions were in all cases used.

Results and discussion We observed the phycobiont in Hydrothyria venosa J. R. Russell through the use of epifluorescence microscopy. The specimens resembled Nostoc (kinked, uniserate trichomes with diffluent sheaths), which is reportedly the phycobiont from this unusual and rare aquatic lichen (Fink, 1935). However, it appeared that the cyanobacterium had true branching (Fig. 1f), a feature that would exclude it from Nostoc. We isolated the phycobiont by fragmenting the lichen thallus and culturing on media prepared from nutrient-enriched site water from Hen Wallow Falls, where the lichen was growing. The phycobiont exhibited a very different morphology when grown on agar plates free of H. venosa, an observation also noted by other researchers studying lichen symbioses (e.g. Bubrick, 1988; Ahmadjian, 1989; Davis & Rands, 1993). Examination of the isolated strain revealed all of the morphological features of Capsosira, including a thallus consisting of rigid, vertical, parallel, knobby trichomes with clustered branches and trichomes formed of a series of single-celled vesicles (sensu Ku¨tzing, 1849) (Fig. 1a–e). Geitler (1932) noted intercalary or terminal heterocytes and hormogonia formed at the ends of upright filaments. In particular, the radiating pattern of thallus development due to pseudodichotomous branching (Fig. 1c, d) is very characteristic (Geitler 1932; Anagnostidis & Koma´rek, 1990). This new taxon differs from the only other species in the genus, C. brebissonii, in several key features, most notably vegetative cell dimensions, variability of the filaments and the phycobiont nature (Table 1). While Capsosira has been previously reported

16

Figure 1. Capsosira lowei. (a) Hormogonia; (b) Kinked uniseriate trichome with diffluent sheath; (c–d) Mature filaments radiating in parallel series, which dichotomously branch, and which can become multiseriate when mature, with cell division in two planes evident. Note that this life cycle stage lacked colonial mucilage; (e) Mucilaginous microcolonies; (f) Trichomes as they appear in the intercellular spaces within the lichen thallus. Note the ambiguity in discerning cell division in two planes, and the heterocytes, which were common in the lichen but rare in culture. Scale bars=5 lm.

from New England states by Tilden (1910) and a single stream from North Carolina by Whitford & Shumacher (1984), none of these habitats or drawings corresponded to our taxon.

Our newly described Rexia erecta gen. nov. et sp. nov. is unique in several key features. First, it is isopolar in trichome development (as in the family Scytonemataceae) but filaments taper apically

17 Table 1. Comparison of morphological characters from Capsosira species Taxa

Habitat

C. brebissonii1 Epiphytic on wood

Sheath

Close, thick,

Vegetative cell Vegetative width (lm)

cell length (lm)

4–5

4–6

Cell contents

Heterocytes

Nongranular

Intercalary

or aquatic plants colorless (occasionally in dead cells), or yellow, C. lowei

1

on moistened rock

unlamellated

Endosymbiont in

Facultative,

Hydrotheria venosa

clear, diffluent

or lateral

4.0–6.0 (8.0)

(2.4) 3.0–6.0 (7.2) Nongranular in Facultative, lichen thallus,

commonly

distinctly

intercalary,

granular

can be

in culture

terminal

Description sensu Geitler (1932).

(Fig. 2d), a characteristic of the Microchaetaceae (sensu Anagnostidis and Koma´rek 1990). The evident false branches (both double and single) arise without presence of heterocytes and typically disintegrate into hormogonia (Fig. 2a, e) or at times hormocytes (one celled hormogonia, Fig 2b, c, e). This is found in some families of the Stigonematales, specifically the Loriellaceae and Mastigocladaceae (Angnostidis and Koma´rek 1990). Heterocytes are extremely rare. The cell division in two planes is most similar to pseudodichotomous branching (cf. Koma´rek et al., 2003) (Fig. 2d), but is very rare, occurs only in short hormogonia, and does not precisely fit the description of this type of branching as reported in Angnostidis & Koma´rek (1990). The division in two planes, however, is unequivocal. The branches of the trichomes typically grow erect from the agar. Molecular results Near complete sequence data for a ca. 1150 (90%) base pair (bp) region of the 16S rRNA gene were obtained for the two strains, and deposited in Genbank (assession numbers AY452533 and AY452534 for Rexia erecta and Capsosira lowei, respectively). Representative taxa from all available sequences of Nostocalean and Stigonematalean taxa from Genbank were used as outgroups. In particular, we choose at least one member of every genus of the Stigonematales, which had a nearly complete 16S rDNA gene sequence deposited in Genbank. We also included strains from the Nostocales previously sequenced from our laboratory

for which also had complete ITS data and taxonomic certainty. Maximum likelihood analysis of the 16S rRNA gene sequence data resulted in four equally parsimonious trees with consistency index (CI)=0.601 and retention index (RI)=0.612 (Fig. 3). Overall, there was poor bootstrap support for most major clades and terminal branches. Capsosira lowei clustered with Nostoc commune with modest bootstrap support (80%). Further, these two were associated with a newly sequenced Aulosira sp. in a moderately supported clade (84%). Beyond this cluster, however, little bootstrap support was evident (70% DNA–DNA hybridization typically have >97% 16S sequence similarity. If 16S similarity is 100 mg l)1), hardness (>250 mg l)1), and pH of rivers in all the groups. Hardness, pH, alkalinity, and Cl explained most of the variation among diatom assemblages, based on ordination analysis. Factors related to water quality problems, such as BOD, P, NH4, and turbidity explained much less variability at the eastern US scale, but were more important in the four intermediate-scale regions. Diatom taxa abundance-weighted mean values for water chemistry characteristics varied among the four intermediate-scale regions, often greatly, and in proportion to the average measured values for each region. Design of calibration data sets for development of water quality indicators should account for spatial scale in relation to species dispersal, regional geochemistry and habitat types, and human-influenced water chemistry characteristics.

Introduction Diatoms are excellent indicators of the ecological condition of rivers and streams, and have been

used for water quality assessment for many decades. Many useful approaches are reviewed by Cholnoky (1968), Patrick (1973), Lowe (1974), Descy (1979), Lange-Bertalot (1979), Whitton &

28 Kelly (1995), Lowe & Pan (1996), and Stevenson & Pan (1999). Increasingly, diatoms are being used in monitoring programs in the United States (Charles, 1996; Barbour et al., 1999) and throughout the world (Whitton & Friedrich, 1991; Whitton & Rott, 1996; Prygiel et al., 1999). The geographic scale of the monitoring is expanding. Examples include the USGS National Water-Quality Assessment program (NAWQA) (Gurtz, 1994) and the US EPA Environmental Monitoring and Assessment Program (EMAP) (Pan et al., 1996) in the United States. One of the greatest limitations to more effective use of diatoms as water quality indicators is the lack of detailed information on the autecology of individual taxa and how this varies with spatial scale and along major environmental gradients (e.g., pH, conductivity, nutrients). This is especially important when diatom indicators are being developed for use on a large scale (e.g., national). Because of this limitation, existing metrics often do not work as well as we would like. Few large-scale studies have been designed to provide this autecological information. The objective of this study was to gain a better understanding of diatom ecology, especially in those areas necessary to make advances in use of diatoms as water quality indicators. We addressed several questions. How do diatom assemblages vary among study sites in the eastern United States? Which water chemistry characteristics have greatest influence on diatom assemblage composition overall, and how does their importance vary with spatial scale and geographic region? What is the relative importance of natural vs. ‘‘pollutionrelated’’ factors? How important are geographic factors that are unrelated to water chemistry in influencing diatom distributions (e.g., historical dispersal events)? What are the autecological characteristics of diatom taxa common in larger rivers and streams? How and by what amounts do they vary throughout the eastern US? What are the implications of our study results for designing large-scale diatom monitoring programs? Our analytical approach to address these questions involved several steps. We first used a clustering technique to examine underlying patterns in diatom distributions and to identify groups of samples with similar species composition.

We then examined how the sample groups related to geographic location and environmental characteristics. We used the cluster analysis groups to define intermediate-scale geographic regions for subsequent examination of spatial variability. We then used ordination analysis to examine relationships between diatom assemblages and water chemistry, within the entire dataset, and within the sets of samples in the geographic regions. Next, we calculated diatom taxa abundance-weighted mean (AWM) values of several water chemistry characteristics using the entire dataset and the sets of samples in the regions defined by the cluster analysis. We examined the spatial variability in ecological characteristics of individual taxa among the regions. We then interpreted these results, addressing questions concerning interaction of scale, spatial pattern, and environmental influences posed in the introduction. Finally, we examined the implications of the results for the design of diatom-based water quality monitoring programs. Water chemistry data and the full set of AWM calculations are available at http://diatom.acnat sci.org/autecology/.

Study area and database We addressed our objectives using a unique set of data created at The Academy of Natural Sciences (ANS) during the past half century. In 1948, under the direction of Dr. Ruth Patrick, Academy scientists began conducting integrated biological– chemical–physical studies at sites on rivers and streams throughout the country. These studies were undertaken at the request of corporations, citizens groups and government agencies wanting information on the condition or ‘‘health’’ of rivers. Many of these studies were repeated over a span of many years, and some are ongoing. The studies usually involved collecting and identifying diatoms and other algae, invertebrates, and fish, and measuring a standard set of water quality variables. Assessments of ‘‘health’’ were based largely on the diversity of biological groups measured (Patrick, 1950, 1951). Standardized techniques were used to collect diatom assemblages, and to evaluate spatial and temporal variation in water quality and biological integrity. Results of these studies were published in Academy reports prepared for the project sponsors, and many have been summarized

29 and synthesized by Patrick (1994, 1995, 1996, 1998a, b, 2000, 2003) in a series of books on rivers of the United States. From the large amount of data available, we selected 186 samples for this study. Each had welldocumented diatom counts and corresponding water chemistry data. We selected samples to represent a wide geographic area, a wide range in physical and chemical characteristics, and both good and poor water quality conditions. The samples were collected between 1951 and 1991 from 116 sites on 47 rivers from Maine to Texas (Fig. 1). Maximum separation of sites was about 2800 km. The rivers are generally larger in size than in most river diatom studies, ranging from 4th to 10th order (lower Mississippi R.). Most samples were collected in the vicinity of industrial facilities, typically one at a site upstream from an effluent source and two at sites downstream. Most differences between upstream and downstream assemblages were minor; however, there were some major differences. Some sites were sampled at intervals of about 10 years; water quality changed during these periods. Most sites were sampled between July and October. Fewer than 10 samples, all from southern rivers, were collected in March, April, May and November. The rivers varied considerably in size and hydrology. Types of water quality problems addressed by the river studies included: nutrient enrichment and biochemical oxygen demand (BOD) associated with wastewater treatment plants, industrial effluent discharges, urban development, dams and impoundments, oil well brine, high turbidity due to various causes, and acid mine drainage. Some sites were influenced by estuarine conditions. All samples were collected from natural substrates, and were usually a composite of collections from all the microhabitats in the sampling area. Water quality data (Table 1) to accompany the diatom counts were sometimes limited. A complete set of measurements was available for only 104 samples, and included pH, total alkalinity, total hardness, conductivity, temperature, Ca, Mg, Na, K, SO4, Cl, dissolved oxygen (DO), BOD, total PO4, soluble reactive phosphorus (SRP), NO3, NH4, turbidity, total Si, and Fe. Correlations among variables are shown in Table 2. This set was used to investigate the relative importance of relationships of chemical characteristics with

diatom assemblages. The water chemistry data for the main set of 186 samples (Table 1) had between 1 and 30 missing values for each variable. This data set was therefore used primarily to calculate AWMs of chemistry variables for diatom taxa, and to assess the geographic variation in ecological characteristics of the taxa. The ‘‘health’’ of a site was categorized based on assignments made or implied in the ANS reports: healthy=1; semi-healthy=2; polluted=3; very polluted=4. Ruth Patrick made the majority of the health assessments, based primarily on the diversity of all biological groups (e.g., Patrick, 1950, 1951), including diatoms, and factors such as water chemistry and local pollution sources. In many cases, determinations were based on quantitative comparisons of biological diversity with sites in the same region that were minimally influenced by human activity. When sites were not specifically categorized in reports, we made assignments in a manner consistent with the approaches used in these reports. Thirty-two samples were identified as originating from sites designated as ‘‘polluted’’ or ‘‘very polluted.’’ Other sites were designated ‘‘healthy’’ (34) or ‘‘semihealthy’’ (104); 16 samples were not classified because information was insufficient. The ‘‘semihealthy’’ category often included situations where human influence was obvious, but biological diversity was still relatively high.

Methods Diatom sample material was digested with nitric acid at boiling temperatures. After settling, liquid was decanted. Distilled water was then added, the samples were allowed to settle again, and the liquid overlying the diatom material removed. This process was repeated several times. Subsamples of the cleaned diatom suspension were distributed on cover slips and affixed to microscope slides with Hyrax mounting medium. All counts were made using research quality microscopes at 1000 or 1250 magnification. Diatom counts were made over a period of 40 years by 8 diatomists (Raymond Cummins, Roger Daum, Robert Grant, Luzern Livingston, Katherine Pearson, Christine Parker Smith, Noma Ann Roberts, and John Wallace). Dr. Charles

30

Figure 1. Location of 116 ANS study sites on 47 rivers, each studied during 1 to 3 years. Symbols represent eight groups of samples based on multivariate analysis (TWINSPAN) (see text for explanation). Lines separate the four major TWINSPAN Groups: NE=Northeast; SE=Southeast; WA=West of Appalachians; GC=Gulf Coast.

Reimer supervised the identifications and enumerations during most of this period, and required the analysts to document new taxa by making drawings in special notebooks and by adding a microscope slide with a circled specimen to the ANS Diatom Herbarium. Dr. Reimer kept a record of all taxonomic name changes during the years of study. Diatom counts were entered into the North American Diatom Ecological Database (NADED) at the ANS. Original data were recorded on paper forms or stored electronically on computer floppy disks. The taxa included in each count were reviewed carefully, and were changed when necessary to make them consistent with taxonomic nomenclature used at the ANS during the mid1980s. In many cases this required the additional effort of examining original slides and making partial recounts of some slides. The number of diatom valves or cells counted varied among samples, ranging relatively evenly

from about 100 to 2500. Sample sets for some rivers had both high and low counts. Types of analyses included standard counts of 400–800 frustules, multiple 100 frustule counts of samples from different microhabitats, and detailed and semi-detailed (Hohn, 1961) counts. Only the ‘‘first row’’ portion of detailed and semi-detailed counts were entered; full counts can total up to 40,000 frustules. The ‘‘first row’’ counts were typically the first 500–1000 frustules counted, all of which were identified and counted. In subsequent rows, common taxa were not counted. We recognize that the relatively large range in number of frustules counted could have influenced the results of statistical and multivariate analyses. Output from the various analyses were sufficiently robust, however, to indicate that the large range in count size did not substantially influence the results (see Results). For multivariate analyses we used the 377 taxa, of the total of 818, that occurred with a minimum abundance of 0.5% in 2 or more samples.

31 Table 1. Summary statistics for water chemistry characteristics of sample locations Parameter

Units

Mean

Median

Minimum

Maximum

Temperature

C

24.4

25.1

24.9

24.8

7.8

37.5

8.7

32.7

DO 6.5

mg/l 6.5

6.7 0.5

6.6 11.2

0.5

11.4

pH

Units

7.2

7.3

7.2

7.3

3.4

8.8

3.4

8.8 )41.5

238

4

1600

Total alkalinity

mg/l

65

53

71

54

)41.5

220

Hardness

mg/l

155

95

129

100

4

740

Conductivity 693

l S/cm 284

NC 30

NC 1200

NC

NC

Turbidity

Units

64

33

0.3

381

77

44

0

660

Total Solids

mg/l

602

251

46

9506

307

252

46

2616

BOD

mg/l

2.7

1.8

0.1

29

2.6

2.0

0.1

29

Ca 29

mg/l 25

30 1.4

25 95

1

135

Mg

mg/l

21

9

1

308

14

8

1

144

NH-4

mg/l

0.28

0.06

0.002

4.9

0.34

0.12

0.001

4.9 2

519

SO4

mg/l

59

21

49

22

1

295

NO3 0.85

mg/l 0.32

1.7 0.002

0.3 5.9

0.002

100

Cl

mg/l

212

18

1

4597

100

18

1

2090

SRP

l g/l

103

35

1

1836

NC

NC

NC

NC

Total phosphorus

l g/l

156

77

3

796

93

36

0.3

1836

Fe 308

l g/l 100

308 1

100 8750

0.5

8750

Top level of numbers are for the 186-sample set. Numbers in bottom level are for the 104-sample set. Values were missing for many of the 186-sample set. NC=not calculated, because too few data were available.

Water chemistry data were obtained from the ANS river survey reports and entered into the NADED database. Typically, reports contained data for a standard set of characteristics that had been measured one to five times during a 1-week period. If only a summary value was reported, we used that value. If not, we calculated and entered

the mean value, or median (in cases where one or two values were very different from the others). The several chemists involved in the ANS studies used different analytical methods. All were stateof-the-art methods for the time. Most are described in earlier editions of Standard Methods for the Examination of Water and Wastewater

32 Table 2. Pearson correlation matrix of all water chemistry characteristics in the 104-sample dataset SRP

0.10

Cl

0.12

0.04

Hardness

0.59

0.10

0.64

Temp

0.11

0.03

0.20

0.05

Cond

0.30

)0.05 0.60

0.74

%DO sat

0.23

)0.17 )0.29 )0.06 )0.13 )0.21

Total alk

0.10

0.11

0.19

0.64

0.32 0.17

0.17 0.58

)0.02 0.30 0.02 0.67 )0.03 0.59

)0.17 0.02 )0.15 0.29

0.01

BOD

0.04

0.40

0.27

0.23

0.19

)0.48 0.14

0.26

Si

)0.27 )0.10 )0.07 )0.09 )0.05 0.16

)0.16 0.00

)0.09 )0.14 )0.08

Ca

0.67

0.15

0.47

0.95

0.02

0.63

)0.04 0.69

)0.06 0.57

0.23

)0.10

Mg

0.42

0.06

0.73

0.92

0.08

0.79

)0.10 0.51

0.06

0.70

0.24

0.02

0.79

NH4

)0.04 0.21

0.02

0.07

0.05

0.20

)0.37 0.05

0.19

0.11

0.36

0.01

0.09

0.06

SO4

0.41

0.59

0.76

0.05

0.62

)0.08 0.36

0.18

0.66

0.35

)0.23 0.69

0.77

NO3 Fe

0.12 0.25 0.06 0.36 )0.29 0.23 )0.09 0.30 )0.07 0.37 0.28 0.10 )0.37 )0.01 )0.13 )0.42 )0.14 )0.18 0.01 )0.48 0.00 )0.20 )0.03 0.02

0.40 0.28 0.20 0.30 )0.43 )0.41 0.08 )0.38 )0.30

pH

Ca

0.22

SRP

Cl

0.18

0.15

0.37

)0.06

0.76

Turbidity 0.01 Total solids 0.23

0.28

Hard Temp Cond %DO T Alk Turb T Sol BOD Si

(published by the American Public Health Association). We recognize that the use of different methods is a source of uncertainty, and that some chemical data are more accurate and precise than others. However, we believe the uncertainty introduced is acceptable given the geographic scale at which we are working, and the magnitude of differences among the sites. If there was significant doubt about some aspect of chemistry data, (e.g., units, method, sample location), we excluded those data from our analyses. We used TWINSPAN (Hill, 1979) to identify groups of samples with similar taxonomic composition. To determine robustness of these groupings, we ran several analyses, each time varying the dataset in some way, or selecting a different set of program options. For example, we ran individual analyses (1) with all taxa included, (2) with only the 377 taxa that occurred in abundance of at least 0.5% in 2 or more samples, (3) excluding the 12 most common taxa (those that occurred in 60 or more samples), and (4) removing the 32 sites with health categorized as ‘‘polluted’’ or ‘‘very polluted’’. Percent abundance counts and log10+1 of percentages were both used. We varied the five cut levels used to define pseudospecies to assess the relative influence of rare and common

Mg

0.12

NH4 SO4

NO3

taxa, but in most cases used the default values of 0, 2, 5, 10 and 20%, or their logarithmic equivalents. Default values were used for other program options. Final selection of TWINSPAN groups was based on the first three divisions of samples. To explore relationships between diatom assemblages and water chemistry, we used several options within the CANOCO program (ter Braak, 1986; ter Braak et al., 1995; ter Braak & Sˇmilauer, 1998). We performed principal components analysis (PCA) of all water chemistry variables in the 104 sample dataset to determine the main chemistry gradients within the dataset. To select a subset of chemistry variables to use in ordination analysis, we used stepwise forward selection in canonical correspondence analysis (CCA) to choose chemistry variables that represented the major gradients, but did not correlate strongly with each other in explaining variability among diatom assemblages. We used Detrended CCA (DCCA; detrending by segments) to quantify the variation in diatom assemblages explained by the selected chemistry characteristics within the entire dataset, and in the sets of samples in the intermediate-scale geographic regions. We chose DCCA, which is based on unimodal responses of species to environmental gradients, because lengths of

33 DCCA axes varied from 3 to 4, and the data matrix contained a large proportion of zeros (Lepsˇ & Sˇmilauer, 2003). Also, DCCA eliminated the ‘‘horseshoe’’ effect apparent when CCA was used. We eliminated variables from the analyses if the variance inflation factor (VIF) was greater than 20. For all analyses, we transformed (log10+1) both species and water chemistry data (except pH). We used CCA in the CANOCO program to partition the variation in diatom assemblage composition due to environmental and spatial factors. We used data for the 104 samples with complete water chemistry, but included only the variables pH, alkalinity, hardness, Cl, BOD, SRP, and turbidity. To develop spatial data, we centered latitude and longitude on their means, and then calculated the cubic trend surface regression for x, y, x2, x3, y2, y3, xy, xy2, and yx2, where x=latitude and y=longitude. We then used forward selection in CCA to determine which combination of these variables contributed most to explaining the variation in diatom distributions. All except xy and yx2 made a statistically significant contribution (p0.5%. When calculating the ‘‘health’’ AWM

values, we used counts for taxa in a sample only if the relative abundance was greater than 0.5% and maximum abundance was >2% in at least one sample; data for sites influenced by acid mine drainage were not used.

Results Diatom taxa In all, 818 diatom taxa were identified within the 186 samples selected. Of these, 191 taxa occurred in only 1 sample. There were 377 taxa that occurred with a minimum abundance of 0.5% in 2 or more samples. Fifteen taxa occurred in onehalf or more of the samples; 56 occurred in onequarter or more. The most frequently occurring taxa are considered generalists, and most are often associated with poorer water quality conditions. Large-scale patterns in assemblage distributions We used results of the several TWINSPAN analyses of the 186 sample dataset to define four major Groups and four minor Groups of samples. This set of groups is described below and represents a synthesis of results from all TWINSPAN analyses. Most samples always occurred in the same group. Those that sometimes fell into different groups were assigned to groups in which they occurred most frequently. Final assignments of the least stable samples, those few that tended to shift among groups more than others, were made with the objectives of keeping samples from the same river together and of maintaining similar water chemistry characteristics among groups. The four major TWINSPAN Groups corresponded with geographic regions (Fig. 1; river names are listed in legends for Fig. 4). Each of these four groups is henceforth referred to by a two-letter code indicating its geographic location: 3 (NE), 4 (SE), 6 (WA), and 8 (GC). There were substantial differences in water chemistry among the eight TWINSPAN Groups (Fig. 2). Group NE (Northeast, Group 3) includes all samples from that region except those from three of the minor TWINSPAN Groups (Group 1, Pennsylvania sites significantly affected by acid mine drainage (pH7.5) than sites in other groups. Group

7, a minor group, consists of sites on the high hardness Ottawa/Auglaize rivers in a limestone area of northwestern Ohio. Group GC (Gulf Coast, Group 8) sites are all relatively near the Gulf of Mexico. They had the highest chloride (>100 mg l)1) and hardness (>250 mg l)1) of all groups. In some TWINSPAN runs, the furthest upstream site on the Guadalupe R. was included with the samples in Group WA (it was the Group GC site closest geographically to Group WA). Also, the Loosehatchie R., Tennessee, sites were sometimes included in Group GC, though they were usually included in Group WA. These sites were geographically near Group GC sites, and have a high turbidity level, in common with many of its members.

35 Relationships between diatom assemblages and water chemistry characteristics Water chemistry characteristics explain a considerable amount of the variation among diatom assemblages. We examined diatom – water chemistry relationships at both large and intermediate regional scales. We defined ‘‘large scale’’ as the eastern US, and ‘‘intermediate scale’’ as the four regions based on the TWINSPAN analysis (Groups NE, SE, WA, and GC; Fig. 1). Large scale PCA of the 18 chemistry variables in the 104 sample data set extracted two major water quality gradients. The first PCA axis correlates strongly with major-ion chemistry variables: hardness, Mg, Ca, conductivity, SO4, total solids, and Cl, in order of decreasing correlation coefficient (Table 3). Total alkalinity, pH and Fe are less highly expressed on this axis. The second axis correlates with variables often associated with human influences on water quality: percent DOsat, pH, BOD, NH4, SRP, and turbidity (Table 3). The stepwise forward selection in CCA, with all water chemistry variables in the 104 sample set,

provided a statistical basis for excluding only two variables from ordination analyses. Of the 18 variables, 16 are significant components of a multiple regression model based on Monte Carlo permutation tests ( p30–80%) in several samples, many of which were from disturbed sites. The nature of the disturbance varied considerably, however: below the tailrace of large dams, below industrial outfalls with abnormally high metal concentrations, in habitat highly disturbed by log drives, barge traffic, and other activities. It was also in samples from less disturbed sites, usually in smaller, higher gradient

rivers. Thus, populations of A. minutissima may be good indicators of disturbance in lowland, slowerflowing rivers in the eastern United States, but not necessarily good in terms of diagnosing the type of disturbance. Implications and recommendations for design of diatom-based water quality monitoring programs This study provides information relevant to key questions concerning diatom-based monitoring programs, particularly in terms of developing new ecological data appropriate for sites to be monitored, and applicability of currently existing information: How should a calibration set be designed to provide appropriate autecological data on diatom taxa for making environmental assessments? How large a geographic area is appropriate? Can data from large and small scale data sets both be used? What water chemistry and other environmental characteristics should be measured? Over what range? How applicable are ecological data from other studies? We propose some general guidelines and recommendations based on our results. Calibration sets should be designed to meet the objectives of the ultimate goal for which they are being developed. This means that the calibration samples should contain as many as possible of the taxa occurring in the sites to be assessed and that the quality of the environmental data of most importance in assessments be maximized. These two objectives should determine the geographic size of a calibration data set and the parameters to measure. The geographic size of a calibration study area could be relatively large if all the individual sites within it meet the above criteria; if they do not, it might need to be restricted to a relatively small area. Because natural geochemical characteristics (e.g., pH, alkalinity, hardness, Cl) can strongly influence distributions of taxa and their AWM values, these parameters should be measured and their range minimized, unless they are the primary variable of interest (e.g., pH for acid mine drainage studies). Variation in major physical factors (e.g., river size, substrate, light) should be minimized as well. If these factors are measured, their influence can be taken into account when assessing the influence of human activities to make any disturbance signal clearer. The ranges of

55 variables of most interest (e.g., phosphorus concentration) should be as great as possible, however, so that distributions of taxa along these gradients can be characterized as accurately as possible. Our results suggest that regions larger than the four intermediate-scale regions we defined for this study would be inappropriate for developing calibration sets, but do not suggest how much improvement might result from going to even smaller regions. Use of Level III ecoregions or USGS Water Resource regions for defining boundaries of calibration-set regions would be consistent with our results, as long as the criteria discussed above are met. Based on the DCCA results (Figs. 3 and 4), major-ion chemistry is more important over larger scales, and factors related to human influences on water quality (SRP, BOD/DO) become more important at intermediate scales. This suggests that the spatial scale for calibration sets used to develop indicators of basic geochemical characteristics (e.g., pH, hardness, chloride) could be larger than indicators for factors significantly influenced by human activities (e.g., phosphorus). It also suggests that ecological data for major-ion chemistry from large calibration sets might be more reliable than data on human-influenced characteristics. Clearly, calibration sets should take into account the local environmental context, particularly regarding interaction of natural characteristics and human influences. Another consideration is that these results and implications may apply more to larger rivers, of the size range included in this study, and less to calibration sets of smaller-size streams. When using or developing ecological data for particular parameters, it is important to be aware of the relative roles of natural vs. human influences on water bodies in the calibration set. For example, diatom taxa may respond differently to high P concentration in an area with naturally high values as compared to areas where the P is high due to discharges from wastewater treatment plants or industrial facilities. Errors in interpretation might result, therefore, if P AWM values from calibration sets with a significant number of samples from naturally high P sites were used in assessments of the effects of P

loading for sites in regions with naturally low P values. Acknowledgements This research was funded primarily by the US Environmental Protection Agency through an Exploratory Research Grant (R821676), and also by the Patrick Center’s Endowment for Innovative Research. We thank Marina Potapova for providing many useful comments on the data analysis and the manuscript. Peggy Burkman entered diatom counts into computer files, Robin Davis helped with technical editing, and Jamie Carr prepared the map.

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Hydrobiologia (2006) 561:59–69  Springer 2006 R.J. Stevenson, Y. Pan, J.P. Kociolek & J.C. Kingston (eds), Advances in Algal Biology: A Commemoration of the Work of Rex Lowe DOI 10.1007/s10750-005-1604-4

Short-term effects of elevated velocity and sediment abrasion on benthic algal communities Steven N. Francoeur1,* & Barry J. F. Biggs2 1

Department of Biology, Eastern Michigan University, 316 Mark Jefferson, Ypsilanti, MI 48197, USA National Institute of Water and Atmospheric Research, P.O. Box 8602, Christchurch, New Zealand (*Author for correspondence: E-mail: [email protected]) 2

Key words: periphyton, disturbance, flood, suspended sediment, biomechanics, biomass removal, scour

Abstract Of the mechanisms that remove benthic algae during flood disturbances, relatively little is known about the effects of sediment scour. We investigated suspended sediment scour using naturally colonized benthic algal communities exposed to realistic velocities and suspended sediment concentrations in a laboratory flowtank. Increased velocity alone removed benthic algal biomass, and high suspended sediment concentrations further increased algal removal. Efficacy of biomass removal by velocity and suspended sediments was community-specific; communities with a tightly adherent cohesive mat physiognomy were resistant to removal, despite taxonomic similarity to easily disturbed communities. In addition, some taxa were more susceptible to removal by disturbance than others. The duration of scour and physical refugia on the substratum also influenced algal biomass removal. Our results indicate that suspended sediment scour may be an important mechanism for algal removal during flood events, and some variability in biomass removal among flood events may be the result of differences in suspended sediment load.

Introduction Flood disturbance can greatly reduce lotic benthic algal biomass and alter community composition (e.g., Grimm & Fisher, 1989; Uehlinger, 1991; Biggs, 1996; Peterson, 1996; Francoeur et al., 1998). In certain streams, flood-induced regulation of benthic algal biomass can be the dominant organising factor, affecting the distribution and abundance of algae and consequently higher trophic levels (e.g., Resh, et al., 1988; Poff & Ward, 1989; Fisher & Grimm, 1991; Biggs, 1995). Removal of benthic algal biomass by flood disturbance can occur by three mechanisms: (1) direct removal of algae by the elevated shear stress caused by increased water velocity, (2) abrasion of algae from substrata by mobilized sediments, and (3) molar action of tumbling gravel/cobble substrata upon which algae grow. These 3 mech-

anisms are interrelated because both sediment suspension and mobilization of large substrata are dependent on increased water velocity. Because streams differ in fine sediment supply and bed sediment stability, the intensity of suspended sediment abrasion and molar action will vary among streams, even for flood events of equal discharge and velocity (see Duncan & Biggs, 1998; Biggs et al., 1999; Biggs et al., 2001). Recent research and current theory suggest that velocity increases alone may not be sufficient to explain the degree of benthic algal biomass removal during floods (Horner et al., 1990; Uehlinger, 1991; Biggs, 1996). In laboratory experiments, increased water velocity (up to 1.5 m s)1) by itself could not remove a tightly adherent, basal layer of algae (Biggs & Thomsen, 1995). The role of molar action (e.g., gravel/cobble movement) in determining lotic algal biomass and community composition has

60 also received theoretical consideration (Biggs et al., 2001), and experimental investigation has shown that algae can be removed by the molar action of tumbling cobbles (Power & Stewart, 1987). Suspended sediment scour during floods can drastically alter benthic algal communities (Uehlinger, 1991; Biggs, 1996; Jowett & Biggs, 1997). Grimm & Fisher (1989) hypothesized that the lack of difference in the amount of chlorophyll a removed by floods between cobble-boulder riffles and adjacent fine gravel/sand runs was the result of suspended sediment abrasion. Additionally, low algal biomass on faces of boulders exposed to flow has been attributed to suspended sediment scour (Blinn & Cole, 1991). In contrast, areas of relatively high biomass may persist on large substrata after flooding (e.g., Uehlinger, 1991; Francoeur et al., 1998), perhaps in part because they are elevated above the zone of sediment scour. Few efforts have been made to test the assumption that suspended sediment abrasion can remove benthic algal biomass from substrata or to quantify the magnitude of suspended sediment scouring. Relatively small increases in total inorganic suspended sediments (from 6 to 25 mg l)1) caused short-lived (