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INTRODUCTION TO FRESHWATER ALGAE
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INTRODUCTION TO FRESHWATER ALGAE Robert G. Sheath
John D. Wehr
Office of Provost and Vice President for Academic Affairs California State University, San Marcos San Marcos, California 92096
Louis Calder Center—Biological Station and Department of Biological Sciences Fordham University, Armonk, New York 10504
I. Introduction II. Classification A. Cyanobacteria B. Red Algae C. Green Algae D. Euglenoids E. Eustigmathophyte, Raphidiophyte, and Tribophyte Algae F. Chrysophycean Algae
G. Haptophyte Algae H. Synurophyte Algae I. Diatoms J. Dinoflagellates K. Cryptomonads L. Brown Algae III. Taxonomic Chapters in This Book A. Key Literature Cited
I. INTRODUCTION Algae are treated in this book in the same sense as they are in many introductory phycology texts (e.g., Van den Hoek et al., 1995; Sze 1998; Graham and Wilcox, 2000); that is, they are considered to be a loose group of organisms that have all or most of the following characteristics: aquatic, photosynthetic, simple vegetative structures without a vascular system, and reproductive bodies that lack a sterile layer of protecting cells. As such, algae are no longer regarded as a phylogenetic concept, but still represent an ecologically meaningful and important collection of organisms. Both prokaryotic (cells that have no membrane-bound organelles) and eukaryotic taxa (cells with organelles) are included. In addition, there is a wide range of vegetative morphologies, including the following: 1. Unicells: species that occur as solitary cells that may be nonmotile or motile. Motile cells may have one or more flagella or they may glide. A wide variety of forms exists among unicells, including those contained within a gelatinous sheath (Fig. 1A), with intricate cell walls Freshwater Algae of North America Copyright © 2003, Elsevier Science (USA). All rights of reproduction in any form reserved.
(Fig. 1B), having flexible cell shapes (Fig 1C), with two flagella of unequal length (Fig. 1D) or two equal flagella (Fig. 1E), with cells drawn out into hornlike extensions (Fig. 1F), and having cells contained in a hardened case or lorica (Fig. 1G). 2. Colonies: an aggregation of cells that are held together either in a loose (Fig. 1H and I) or tight, well organized fashion (Fig. 2B, D, and E). Depending on the algal taxon, colonies may contain a variable number of cells or they may be constant throughout their development (Fig. 2B). Colonies may contain flagellated or nonflagellated cells. The basis for cellular connection varies among colonies, including a surrounding gelatinous matrix (Fig. 1H and I), gelatinous stalks (Fig. 2A), common parental wall (Fig. 2B), and direct attachment at the cellular edges (Fig. 2C) or at the middle portion of each cell (Fig. 2C). Alternately, cells may be connected via their loricae (Fig. 2E). 3. Pseudofilaments: an aggregation of cells in an end-to-end fashion. The cells are not directly connected to each other; rather, they are spaced 1
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Robert G. Sheath and John D. Wehr
FIGURE 1 Unicellular and colonial forms of freshwater algae. A. Gloeocapsa (cyanobacterium), a unicell to small grouping of cells contained within concentrically layered gelatinous sheaths (arrows). B. Micrasterias (green alga, desmid), a unicell with many regular cell wall incisions (arrows) that form a series of lobes and lobules. C. Euglena (euglenoid), a unicell that does not produce walls and can readily change shape. D. Ochromonas (chrysophycean alga), a unicell with one long and one short apically inserted flagellum (arrows). E. Pyrenomonas (cryptomonad), a unicell with two equal subapically inserted flagella. F. Ceratium (dinoflagellate), a unicell with a theca composed of cellulose plates and cellular extensions or horns (arrows). G. Strombomonas (euglenoid), a flagellated unicell within a rigid lorica (arrow). H. Coelosphaerium (cyanobacterium), a colony with spherical cells loosely arranged at the periphery of a gelatinous matrix. I. Dermatochrysis (chrysophycean alga), a colony with spherical cells in a single layer scattered in a gelatinous matrix that has distinct perforations (arrows). Scale bars = 10 µm.
apart and contained in a common gelatinous matrix (Fig. 2F). 4. Filaments: a chain or series of cells in which the cells are arranged in an end-to-end manner, where adjacent cells share a common cross wall
(Figs. 2H–J, and 3B and C). Linear colonies can be distinguished from true filaments by the fact that abutting colonial cells each possess their own entire walls (Fig. 2D). Filaments may be arranged in a single series (uniseriate or
1. Introduction to Freshwater Algae
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FIGURE 2 Colonial, pseudofilamentous, and filamentous forms of freshwater algae. A. Porphyridium (red alga), a colony with spherical cells attached together by gelatinous strands (arrows). B. Crucigenia (green alga), a colony with consistent groups of four cells produced inside the walls of the parent cells. C. Tabellaria (diatom), a colony with cells attached at their edges in a zig-zag fashion. D. Asterionella (diatom), a linear colony with cells attached only at the central region. E. Dinobryon (chrysophycean alga), a colony with cells attached by their loricae (arrows). F. Chroodactylon (red alga), a pseudofilament with cells arranged in an endto-end pattern in a common gelatinous matrix (arrows), but not directly connected to each other. G. Zygnema (green alga), an unbranched filament without a gelatinous matrix. H. Lyngbya (cyanobacterium), an unbranched filament that is contained in a gelatinous sheath that is evident at the filament tip (arrow). I. Scytonema (cyanobacterium), a filament that produces double false branches (arrows) that result from breakage and further growth of each fragment. J. Bangia (red alga), a multiseriate filament in part with at least two cells across (arrows). Scale bars = 10 µm.
uniaxial) (Fig. 2G–I) or they may be in more than one series of cells (multiseriate or multiaxial) (Fig. 2J). Filaments may be unbranched (Figs. 2G and H) or they can produce branches in a new plane that are morphologically similar to the main axis (Fig. 3B) or that are quite distinct (Fig. 3C). Branching may be dichotomous or forked (Fig. 3B), alternate (Fig. 3C), opposite, or whorled (Fig. 3D). False branches are formed in
some cyanobacteria, such as Scytonema (Fig. 2I), by fragmentation and continued growth of one or both fragments. Other types of filaments include those that are heterotrichous, that is, they have a distinct prostrate system with attached erect branches. Differentiated filaments have specialized cells within the chain. The main axis may have a surrounding layer of small cells termed cortication (Fig. 3A).
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FIGURE 3 Filamentous, saclike, crustose, pseudoparenchymatous, and siphonous forms of freshwater algae. A. Compsopogon (red alga), a filamentous form with small cortical cells (arrows) covering the main filament. B. Cladophora (green alga), a filament that has dichotomous (forked) branches (arrows). C. Draparnaldia (green alga), a filament that has tuftlike lateral branches with cells that are considerably smaller than those of the main axis. D. Batrachospermum (red alga), a filament with whorllike lateral branches (arrows). E. Boldia (red alga), a saclike thallus that consists of a single layer of cells. F. Heribaudiella (brown alga), a crust that is tightly adherent to the rock substratum. G. Hildenbrandia (red alga), a cross section of a crust that shows vertical files of cells (arrows). H. Caloglossa (red alga), a pseudoparenchymatous thallus composed of a main filamentous axis (arrow) with tightly compacted lateral branches. I. Vaucheria (yellow–green alga), a siphonous thallus without cross walls separating the nuclei. Scale bars = 10 µm, except B = 250 µm, E = 1 cm, and F = 2 cm. Figure A courtesy of Tara Rintoul; Figure B from Vis et al. (1994) reprinted with permission of University of Hawaii Press; Figure E from Sheath (1984) with permission; Figure G courtesy of Alison Sherwood.
5. Pseudoparenchymatous structures: tissue-like thalli that consist of closely appressed branches of a uniseriate or multiseriate filament (Fig. 3H). Crustose forms may be composed of short, compacted filaments, such as the brown alga Heribaudiella (Fig. 3F) and the rhodophyte Hildenbrandia (Fig. 3G). 6. Parenchymatous forms: true tissues composed of a solid mass of cells that is three dimensional, variously shaped, and not filamentous in construction. The cells may be differentiated
into an outer photosynthetic layer (the cortex) and an inner non-photosynthetic region (the medulla). Most tissue-like forms in freshwater habitats are simple, such as the saccate red alga Boldia, which consists of a single layer of cells (Fig. 3E). 7. Coenocytic or siphonous forms: large multinucleate forms of various shapes without cross walls to separate the nuclei or other organelles. An example is the yellow–green alga Vaucheria (Fig. 3I).
1. Introduction to Freshwater Algae
Freshwater algae exhibit all of these morphologies, but the macroscopic pseudoparenchymatous and parenchymatous forms tend to be smaller than those found in marine systems (Sheath and Hambrook, 1990). In addition, planktonic (floating) forms are typically small and microscopic, and mostly consist of the simpler forms. In contrast, benthic (attached) algae include the entire range of morphologies, although flagellated taxa are less common than in plankton.
II. CLASSIFICATION Algae do not represent a formal taxonomic group of organisms, but rather constitute a loose collection of divisions or phyla with representatives that have the characteristics noted previously. The divisions are
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distinguished from each other based on a combination of characteristics, including photosynthetic pigments, starchlike reserve products, cell covering, and other aspects of cellular organization (e.g., Van den Hoek et al., 1995; Sze, 1998; Graham and Wilcox, 2000). There is little consensus among phycologists as to the exact number of algal divisions; 8–11 have been recognized in recent texts (Van den Hoek et al., 1995; Sze, 1998; Graham and Wilcox, 2000). The 12 major algal groups (divisions and classes) recognized in this book are distinguished from each other in Table I. Each of the major groupings is briefly presented in the following sections, but the reader should refer to the relevant chapter(s) for more details. The number of freshwater genera now reported (>800) from North America, as discussed in Chapters 3–22, has greatly increased from earlier treatises (e.g., Smith,
TABLE I Major Distinguishing Features of the Major Algal Groups Presented Herein Algal group (chapter number)
Photosynthetic pigmentsa
Chloroplast outer Thylakoid membranes associations
Starch-like reserveb
External coveringc
Cyanobacteria (3 & 4)
chla, PE, PC, APC
0
0
Cyanophycean
Pepitoglycan matrices or walls
0
Red algae (5)
chla, PE, PC, APC
2
0
Floridean
Walls with a galactose polymer matrix
0
Green algae (6–9)
chla, b
2
2–6
True
Cellulosic walls, scales
0 – many
Euglenoid Algae (10)
chla, b
3
3
Paramylon
Pellicle
1–2 emergent
Yellow–green and related algae (11)
chla, c
4
3
Chrysolaminarin
Mostly cellulosic walls
2 unequal if present
Chrysophyte algae (12)
chla, c fucoxanthin
4
3
Chrysolaminarin
None, scales, lorica
2 unequal
Haptophyte algae (13)
chla, c fucoxanthin
4
3
Chrysolaminarin
Nonsiliceous scales
2 equal + haptonema
Synurophyte algae (14)
chla, c fucoxanthin
4
3
Chrysolaminarin
Siliceous scales
2 unequal
Diatoms (15–19)
chla, c fucoxanthin
4
4
Chrysolaminarin
Siliceous frustule
1, reproductive cells only
Dinoflagellates (20)
chla, c peridinin
3
3
True
Theca
2 unequal
Cryptomonads (21)
chla, c PC or PE
4
2
True
Periplast
2 equal
Brown algae (22)
chla, c fucoxanthin
4
3
Laminarin
Walls with alginate matrices
2 unequal
Flagella
Source: Various phycology textbooks (e.g., Sze, 1998; and Graham and Wilcox, 2000). a chl = chlorophyll (green); PE = phycoerythrin (red); PC = phycocyanin (blue); APC = allophycocyanin (blue); fucoxanthin and peridinin (golden to brown). b All of the reserves are polymers of glucose. They differ by their linkages: cyanophycean and floridean α1, 4 and α1, 6 branches; true starch with amylose α1, 4 and amylopectin α1, 4 and α1, 6 branches; paramylon β1, 3; chrysolamin and laminarin β1, 3 and β1, 6 branches. Only true starch stains positively with iodine (purple to black). c Pellicle and periplast within plasma membrane; the rest are external to it.
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Robert G. Sheath and John D. Wehr
1950; Prescott, 1962), but is still highly tentative and likely to be an underestimate of the region’s biodiversity.
A. Cyanobacteria Cyanobacteria or blue–green algae are prokaryotes, that is, cells that have no membrane-bound organelles, including chloroplasts (Table I; Chap. 3). Other characteristics of this division include unstacked thylakoids, phycobiliprotein pigments, cyanophycean starch, and peptidoglycan matrices or walls. There are 124 genera reported from inland habitats in North America, of which 53 are unicellular or colonial (Chap. 3) and 71 are filamentous (Chap. 4). However, the taxonomy of this division is currently in a state of flux, as noted in Chapter 3, and the number of genera should be considered to be tentative. Cyanobacteria inhabit the widest variety of freshwater habitats on Earth and can become important in surface blooms in nutrient-rich standing waters (Chaps. 3 and 4). Some of these blooms can be toxic to zooplankton and fish, as well as livestock that drink water containing these organisms. Inland cyanobacteria also occur in extreme environments, such as hot springs, saline lakes, and endolithic desert soils and rocks.
B. Red Algae Rhodophyta or red algae represent a division that is characterized by chloroplasts that have no external endoplasmic reticulum and unstacked thylakoids, phycobiliprotein pigments, floridean starch, and lack of flagella (Table I; Chap. 5). They are predominantly marine in distribution; only approximately 3% of over 5000 species occur in truly freshwater habitats. In North America, 25 genera are recognized in inland habitats (Chap. 5). Freshwater red algae are largely restricted to streams and rivers, but also can occur in other inland habitats, such as lakes, hot springs, soils, caves, and even sloth hair (Chap. 5).
C. Green Algae Chlorophyta or green algae constitute a division that has the following set of attributes: chloroplasts with no external endoplasmic reticulum, thylakoids typically in stacks of two to six, chlorophyll-a and -b as photosynthetic pigments, true starch, and cellulosic walls or scales (Table I). This is a diverse group in inland habitats of North America that includes 44 flagellated genera (Chap. 6), at least 129 coccoid and
nonmotile colonies (Chap. 7), 81 filamentous and plantlike genera (Chap. 8), and 48 conjugating genera and desmids (Chap. 9). Some members of the green algae (Charophyeae) are part of a lineage that is thought to be ancestral to higher plants. Green algae are widespread in inland habitats, but certain groups may have specific ecological requirements. For example, flagellated chlorophytes tend to be more abundant in standing waters that are nutrient rich (Chap. 6). Coccoid unicells and colonies are common in the plankton of standing waters and slowly moving rivers when nutrients, light and temperature are reasonably high (Chap. 7). The majority of filamentous and plantlike Chlorophyta are attached to hard surfaces in standing or flowing waters, but some can exist in the floating state or on soils or other subaerial habitats (Chap. 8). Filamentous conjugating green algae are most frequent in stagnant waters of roadside ditches and ponds, and in the littoral zones of lakes, where they can form free-floating mats or intermingle with other algae in attached or floating masses (Chap. 9). Desmids are more common in ponds and streams that have low conductance and moderate nutrient levels, and often intermingle with macrophytes.
D. Euglenoids Photosynthetic Euglenophyta or euglenoids have chloroplasts surrounded by three membranes, thylakoids in stacks of three, chlorophyll-a and -b as photosynthetic pigments, paramylon, and a pellicle (Table I; Chap. 10). Ten genera are reported from North American freshwater habitats (Chap. 10). Euglenoids are particularly abundant in the plankton of standing waters rich in nutrients and organic matter, and they can be associated with sediments, fringing higher plants, and leaf litter, although some may dominate in highly acidic environments (Chap. 10).
E. Eustigmatophyte, Raphidiophyte, and Tribophyte Algae Eustigmatophyte, raphidiophyte, and tribophyte algae comprise a loose group of algae that share the following characteristics: chloroplasts with four surrounding membranes, thylakoids in stacks of three, chlorophyll-a and -c as the typical photosynthetic pigments, and chrysolaminarin as the photosynthetic reserve product (where known) (Table I; Chap. 11). The yellow–green algae are quite diverse in freshwater habitats of North America: at least 90 genera have been reported, whereas the eustigmatophytes and raphdiophytes are relatively small groups that comprise
1. Introduction to Freshwater Algae
eight and three genera, respectively (Chap. 11). Many of these genera seldom have been reported. Members of this group of algae have been collected from a wide variety of habitats, but many are collected primarily in northern habitats (Chap. 11). They are both planktonic and associated with a variety of substrata.
F. Chrysophycean Algae Chrysophyceae or chrysomonads are distinguished by chloroplasts that have four surrounding membranes, thylakoids in stacks of three, fucoxanthin that typically masks chlorophyll-a and -c, and chrysolaminarin as the photosynthetic reserve. At least 72 genera are reported from inland habitats of North America (Chap. 12). Chrysophycean algae are typically associated with standing bodies of water that have low or moderate nutrients, alkalinity, and conductances, and a pH that is slightly acidic to neutral (Chap. 12). In addition, the majority of genera tend to be planktonic; attached forms occur to a lesser extent.
G. Haptophyte Algae Haptophyceae are characterized by chloroplasts that have four surrounding membranes, thylakoids in stacks of three, fucoxanthin that masks chlorophyll-a and -c, chrysolaminarin as the photosynthetic reserve, and a unique appendage associated with the flagellar apparatus, the haptonema (Table I; Chap. 13). Only three freshwater genera are found in North America (Chap. 13). The two common genera are planktonic in lakes and ponds, and occasionally form predominant blooms, particularly in areas with low conductance (Chap. 13). Chrysochromulina breviturrita has been used as an indicator of moderately acidic water.
H. Synurophyte Algae Synurophyceae is characterized by chloroplasts that have four surrounding membranes, thylakoids in stacks of three, fucoxonthin that masks chlorophyll-a and -c, chrysolaminarin as the photosynthetic reserve product, and siliceous scales (Table I; Chap. 14). Three genera are found in North American freshwater habitats (a fourth is known only from Australia), but the genera are species-rich, such as Mallomonus and Synura (Chap. 14). Synurophytes are exclusively freshwater phytoplankters in lakes, ponds, and slowly flowing rivers (Chap. 14). Habitats that support the largest flora are slightly acidic, low in conductance, alkalinity,
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and nutrients, and have moderate amounts of humic substances.
I. Diatoms Bacillariophyceae or diatoms are distinguished by chloroplasts that have four surrounding membranes, thylakoids in stacks of three, fucoxanthin that masks chlorophyll-a and -c, chrysolaminarin as the photosynthetic reserve product, and a siliceous frustule that makes up the external covering (Table I; Chap. 15). The diatoms are a complex and diverse group in terms of frustule morphology. The North American freshwater genera consist of 25 centrics (Chap. 15), 28 araphid and monoraphid diatoms (Chap. 16), 37 symmetrical naviculoid taxa (Chap. 17) 14 eunotioid and asymmetrical naviculoid diatoms (Chap. 18), and 14 keeled and canalled forms (Chap. 19). Diatoms are found in all freshwater habitats, including standing and flowing waters, and planktonic and benthic habitats, and they can often dominate the microscopic flora. Because diatoms inhabit a broad array of habitats but many have specific habitat requirements, they have been used in freshwater environment assessment and to monitor long-term changes in ecological characteristics (Chap. 23).
J. Dinoflagellates Pyrrhophyta or dinoflagellates are characterized by chloroplasts that have three surrounding membranes, thylakoids in stacks of three, peridinin that masks chlorophyll-a and -c, true starch, a nucleus that has condensed chromosomes in cell cycle phases, a theca covering, and frequently a transverse and posterior flagellum. (Table I; Chap. 20). There are 37 genera in North American freshwater habitats (Chap. 20). The dinoflagellates are typically minor components of the phytoplankton of lakes and ponds, but sometimes form dense blooms, particularly in the presence of high levels of nitrates and phosphates (Chap. 20).
K. Cryptomonads Cryptophyta, cryptomonads or cryptophyte algae, have chloroplasts that have four surrounding membranes in which a nucleomorph occurs between the outer and inner two membranes, thylakoids in loose pairs, phycocyanin or phycoerythrin that masks chlorophyll-a and -c, true starch as the photosynthetic reserve, a periplast, and two subapical flagella (Table I; Chap. 21). There are 12 genera reported from the inland waters of North America (Chap. 21).
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Robert G. Sheath and John D. Wehr
Cryptomonads are typically planktonic in lakes and ponds, and are particularly diverse in temperate regions (Chap. 21).
L. Brown Algae Phaeophyceae or brown algae are distinguished by chloroplasts that have four surrounding membranes, thylakoids in stacks of three, fucoxanthin that masks chlorophyll-a and -c, laminarin as the photosynthetic reserve, and alginates commonly as the wall matrix component. There are six genera of freshwater brown algae, four of which have been collected in North America (Chap. 22).
Brown algae are predominantly marine in distribution; less than 1% of the species are from fresh water. The inland species are benthic, either in lakes or streams, and distribution is quite scattered (Chap. 22).
III. TAXONOMIC CHAPTERS IN THIS BOOK The approach of this book is to break the major algal groups into manageable taxonomic units, resulting in multiple chapters for those divisions that have many freshwater representatives. The following key gives major characteristics to allow the reader to immediately proceed to the appropriate chapter to determine an unknown algal sample.
A. Key 1a.
Cells with no chloroplasts; typically blue–green colored throughout (occasionally black, purple, brown, or reddish).......................2
1b.
Cells with variously colored pigments localized in one or more chloroplasts..................................................................................3
2a.
Organisms unicellular or colonial (coccoid cyanobacteria)...................................................................................................Chapter 3
2b.
Organisms filamentous (filamentous cyanobacteria)............................................................................................................Chapter 4
3a.
Cells stain positively (purple to black) with iodine for true starch.................................................................................................4
3b.
Cells do not stain positively (orange to reddish brown) with iodine for starch..............................................................................9
4a.
Green-colored chloroplasts with chlorophyll-a and -b as predominant photosynthetic pigments....................................................5
4b.
Chloroplasts with other colors and predominant photosynthetic pigments........................................................................................8
5a.
Organisms flagellated in the vegetative state (flagellated green algae)...................................................................................Chapter 6
5b.
Organisms nonflagellated in the vegetative stage................................................................................................................................6
6a.
Organisms coccoid (nonmotile unicells of various shapes) or colonial in forms without conjugation (coccoid and colonial nonmotile green algae).......................................................................................................................Chapter 7
6b.
Organisms filamentous, plantlike, or with sexual reproduction by conjugation.................................................................................7
7a.
Organisms with filamentous, bladelike, or plantlike morphologies without conjugation (filamentous and plantlike green algae).................................................................................................................................Chapter 8
7b.
Organisms with coccoid or filamentous morphologies with conjugation (conjugating green algae filaments and desmids) .............................................................................................................................................................................................Chapter 9
8a.
Cells with golden-colored chloroplasts with peridinin as the predominant photosynthetic pigment; two separate flagella typically with transverse and posterior insertions (dinoflagellates)....................................................................................................Chapter 20
8b.
Cells with blue-, brown-, or red-colored chloroplasts with either phycocyanin or phycoerythrin as the predominant photosynthetic pigment; flagella subapical (cryptophyte algae) ..................................................................................................................Chapter 21
9a.
Cells with blue- or red-colored chloroplasts with phycocyanin or phycoerythrin as the predominant photosynthetic pigment (red algae).............................................................................................................................................................................Chapter 5
9b.
Cells green or golden colored with other predominant photosynthetic pigments..............................................................................10
10a.
Motile green-colored cells with a pellicle (layer below the plasma membrane that often appears as spiral strips on the cell) (euglenoids)........................................................................................................................................................................Chapter 10
10b.
Nonmotile or motile, yellow–green- or golden-colored cells; naked or walled cells without a pellicle ..............................................11
11a.
Yellow–green-colored chloroplasts with chlorophyll-a and -c as the predominant photosynthetic pigments (eustigmatophyte, raphidiophyte, and tribophyte algae).....................................................................................................Chapter 11
11b.
Golden-colored chloroplasts with fucoxanthin as the predominant photosynthetic pigment............................................................12
12a.
Cells with a silica frustule covering (diatoms)...................................................................................................................................13
1. Introduction to Freshwater Algae
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12b.
Cells with no covering or with one that is not a siliceous frustule (may be siliceous scales) .........................................................17
13a.
Frustules in the valve view are radially symmetrical or symmetrical in more than two planes (centric diatoms)..................Chapter 15
13b.
Frustules symmetrical in the valve view in one or two planes ..........................................................................................................14
14a.
Frustules without a raphe or with one-on-one valve only (araphid and monoraphid diatoms)............................................Chapter 16
14b.
Frustules with two raphes................................................................................................................................................................15
15a.
Raphe in an elevated keel or a canal (keeled and canalled raphid diatoms).........................................................................Chapter 19
15b.
Raphe not in a keel or canal............................................................................................................................................................16
16a.
Frustules bilaterally symmetrical in valve view (biraphid symmetrical diatoms) .................................................................Chapter 17
16b.
Frustules not bilaterally symmetrical in valve view (eunotioid and asymmetrical biraphid diatoms)...................................Chapter 18
17a.
Cells with a specialized appendage, the haptonema, in vegetative and/or reproductive stages (haptophyte algae)...............Chapter 13
17b.
Cells without a haptonema in any stage...........................................................................................................................................18
18a.
Vegetative cells with siliceous scales (synurophyte algae) ...................................................................................................Chapter 14
18b.
Vegetative cells without siliceous scales ....................................................................................................................................19
19a.
Exclusively benthic; often macroscopic thalli with no unicellular or colonial representatives; cell walls with alginates (brown algae).....................................................................................................................................................................Chapter 22
19b.
Mostly planktonic with some attached representatives; numerous unicellular or colonial representatives; mostly microscopic thalli; cell walls without alginates (chrysophyte algae)..................................................................................................................Chapter 12
LITERATURE CITED Graham, L. E., Wilcox, L. W. 2000. Algae. Prentice–Hall, Upper Saddle River, NJ, 640 pp., glossary, literature cited, and index. Prescott, G. W. 1962. Algae of the Western Great Lakes area. W. B. Brown, Dubuque, IA, 977 p. Sheath, R. G. 1984. The biology of freshwater red algae. Progress in Phycological Research 3:89–157. Sheath, R. G., Hambrook, J. A. 1990. Freshwater ecology, in: Cole, K. M., Sheath, R. G., Eds. Biology of the red algae. Cambridge University Press, Cambridge, UK, pp. 423–453.
Smith, G. M. 1950. Freshwater algae of the United States, 2nd ed. McGraw–Hill, New York, 719 p. Sze, P. 1998. A biology of the algae 3rd ed. McGraw–Hill, Boston, 278 p. Van den Hoek, C., Mann, D. G., Jahns, H. M. 1995. Algae. An introduction to phycology. Cambridge University Press, Cambridge, UK, 623 p. Vis, M. L., Sheath, R. G., Hambrook, J. A., Cole, K. M. 1994. Stream macroalgae of the Hawaiian Islands: A preliminary study. Pacific Science 48:175–187.
INTRODUCTION TO FRESHWATER ALGAE Robert G. Sheath
John D. Wehr
Office of Provost and Vice President for Academic Affairs California State University, San Marcos San Marcos, California 92096
Louis Calder Center—Biological Station and Department of Biological Sciences Fordham University, Armonk, New York 10504
I. Introduction II. Classification A. Cyanobacteria B. Red Algae C. Green Algae D. Euglenoids E. Eustigmathophyte, Raphidiophyte, and Tribophyte Algae F. Chrysophycean Algae
G. Haptophyte Algae H. Synurophyte Algae I. Diatoms J. Dinoflagellates K. Cryptomonads L. Brown Algae III. Taxonomic Chapters in This Book A. Key Literature Cited
I. INTRODUCTION Algae are treated in this book in the same sense as they are in many introductory phycology texts (e.g., Van den Hoek et al., 1995; Sze 1998; Graham and Wilcox, 2000); that is, they are considered to be a loose group of organisms that have all or most of the following characteristics: aquatic, photosynthetic, simple vegetative structures without a vascular system, and reproductive bodies that lack a sterile layer of protecting cells. As such, algae are no longer regarded as a phylogenetic concept, but still represent an ecologically meaningful and important collection of organisms. Both prokaryotic (cells that have no membrane-bound organelles) and eukaryotic taxa (cells with organelles) are included. In addition, there is a wide range of vegetative morphologies, including the following: 1. Unicells: species that occur as solitary cells that may be nonmotile or motile. Motile cells may have one or more flagella or they may glide. A wide variety of forms exists among unicells, including those contained within a gelatinous sheath (Fig. 1A), with intricate cell walls Freshwater Algae of North America Copyright © 2003, Elsevier Science (USA). All rights of reproduction in any form reserved.
(Fig. 1B), having flexible cell shapes (Fig 1C), with two flagella of unequal length (Fig. 1D) or two equal flagella (Fig. 1E), with cells drawn out into hornlike extensions (Fig. 1F), and having cells contained in a hardened case or lorica (Fig. 1G). 2. Colonies: an aggregation of cells that are held together either in a loose (Fig. 1H and I) or tight, well organized fashion (Fig. 2B, D, and E). Depending on the algal taxon, colonies may contain a variable number of cells or they may be constant throughout their development (Fig. 2B). Colonies may contain flagellated or nonflagellated cells. The basis for cellular connection varies among colonies, including a surrounding gelatinous matrix (Fig. 1H and I), gelatinous stalks (Fig. 2A), common parental wall (Fig. 2B), and direct attachment at the cellular edges (Fig. 2C) or at the middle portion of each cell (Fig. 2C). Alternately, cells may be connected via their loricae (Fig. 2E). 3. Pseudofilaments: an aggregation of cells in an end-to-end fashion. The cells are not directly connected to each other; rather, they are spaced 1
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Robert G. Sheath and John D. Wehr
FIGURE 1 Unicellular and colonial forms of freshwater algae. A. Gloeocapsa (cyanobacterium), a unicell to small grouping of cells contained within concentrically layered gelatinous sheaths (arrows). B. Micrasterias (green alga, desmid), a unicell with many regular cell wall incisions (arrows) that form a series of lobes and lobules. C. Euglena (euglenoid), a unicell that does not produce walls and can readily change shape. D. Ochromonas (chrysophycean alga), a unicell with one long and one short apically inserted flagellum (arrows). E. Pyrenomonas (cryptomonad), a unicell with two equal subapically inserted flagella. F. Ceratium (dinoflagellate), a unicell with a theca composed of cellulose plates and cellular extensions or horns (arrows). G. Strombomonas (euglenoid), a flagellated unicell within a rigid lorica (arrow). H. Coelosphaerium (cyanobacterium), a colony with spherical cells loosely arranged at the periphery of a gelatinous matrix. I. Dermatochrysis (chrysophycean alga), a colony with spherical cells in a single layer scattered in a gelatinous matrix that has distinct perforations (arrows). Scale bars = 10 µm.
apart and contained in a common gelatinous matrix (Fig. 2F). 4. Filaments: a chain or series of cells in which the cells are arranged in an end-to-end manner, where adjacent cells share a common cross wall
(Figs. 2H–J, and 3B and C). Linear colonies can be distinguished from true filaments by the fact that abutting colonial cells each possess their own entire walls (Fig. 2D). Filaments may be arranged in a single series (uniseriate or
1. Introduction to Freshwater Algae
3
FIGURE 2 Colonial, pseudofilamentous, and filamentous forms of freshwater algae. A. Porphyridium (red alga), a colony with spherical cells attached together by gelatinous strands (arrows). B. Crucigenia (green alga), a colony with consistent groups of four cells produced inside the walls of the parent cells. C. Tabellaria (diatom), a colony with cells attached at their edges in a zig-zag fashion. D. Asterionella (diatom), a linear colony with cells attached only at the central region. E. Dinobryon (chrysophycean alga), a colony with cells attached by their loricae (arrows). F. Chroodactylon (red alga), a pseudofilament with cells arranged in an endto-end pattern in a common gelatinous matrix (arrows), but not directly connected to each other. G. Zygnema (green alga), an unbranched filament without a gelatinous matrix. H. Lyngbya (cyanobacterium), an unbranched filament that is contained in a gelatinous sheath that is evident at the filament tip (arrow). I. Scytonema (cyanobacterium), a filament that produces double false branches (arrows) that result from breakage and further growth of each fragment. J. Bangia (red alga), a multiseriate filament in part with at least two cells across (arrows). Scale bars = 10 µm.
uniaxial) (Fig. 2G–I) or they may be in more than one series of cells (multiseriate or multiaxial) (Fig. 2J). Filaments may be unbranched (Figs. 2G and H) or they can produce branches in a new plane that are morphologically similar to the main axis (Fig. 3B) or that are quite distinct (Fig. 3C). Branching may be dichotomous or forked (Fig. 3B), alternate (Fig. 3C), opposite, or whorled (Fig. 3D). False branches are formed in
some cyanobacteria, such as Scytonema (Fig. 2I), by fragmentation and continued growth of one or both fragments. Other types of filaments include those that are heterotrichous, that is, they have a distinct prostrate system with attached erect branches. Differentiated filaments have specialized cells within the chain. The main axis may have a surrounding layer of small cells termed cortication (Fig. 3A).
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FIGURE 3 Filamentous, saclike, crustose, pseudoparenchymatous, and siphonous forms of freshwater algae. A. Compsopogon (red alga), a filamentous form with small cortical cells (arrows) covering the main filament. B. Cladophora (green alga), a filament that has dichotomous (forked) branches (arrows). C. Draparnaldia (green alga), a filament that has tuftlike lateral branches with cells that are considerably smaller than those of the main axis. D. Batrachospermum (red alga), a filament with whorllike lateral branches (arrows). E. Boldia (red alga), a saclike thallus that consists of a single layer of cells. F. Heribaudiella (brown alga), a crust that is tightly adherent to the rock substratum. G. Hildenbrandia (red alga), a cross section of a crust that shows vertical files of cells (arrows). H. Caloglossa (red alga), a pseudoparenchymatous thallus composed of a main filamentous axis (arrow) with tightly compacted lateral branches. I. Vaucheria (yellow–green alga), a siphonous thallus without cross walls separating the nuclei. Scale bars = 10 µm, except B = 250 µm, E = 1 cm, and F = 2 cm. Figure A courtesy of Tara Rintoul; Figure B from Vis et al. (1994) reprinted with permission of University of Hawaii Press; Figure E from Sheath (1984) with permission; Figure G courtesy of Alison Sherwood.
5. Pseudoparenchymatous structures: tissue-like thalli that consist of closely appressed branches of a uniseriate or multiseriate filament (Fig. 3H). Crustose forms may be composed of short, compacted filaments, such as the brown alga Heribaudiella (Fig. 3F) and the rhodophyte Hildenbrandia (Fig. 3G). 6. Parenchymatous forms: true tissues composed of a solid mass of cells that is three dimensional, variously shaped, and not filamentous in construction. The cells may be differentiated
into an outer photosynthetic layer (the cortex) and an inner non-photosynthetic region (the medulla). Most tissue-like forms in freshwater habitats are simple, such as the saccate red alga Boldia, which consists of a single layer of cells (Fig. 3E). 7. Coenocytic or siphonous forms: large multinucleate forms of various shapes without cross walls to separate the nuclei or other organelles. An example is the yellow–green alga Vaucheria (Fig. 3I).
1. Introduction to Freshwater Algae
Freshwater algae exhibit all of these morphologies, but the macroscopic pseudoparenchymatous and parenchymatous forms tend to be smaller than those found in marine systems (Sheath and Hambrook, 1990). In addition, planktonic (floating) forms are typically small and microscopic, and mostly consist of the simpler forms. In contrast, benthic (attached) algae include the entire range of morphologies, although flagellated taxa are less common than in plankton.
II. CLASSIFICATION Algae do not represent a formal taxonomic group of organisms, but rather constitute a loose collection of divisions or phyla with representatives that have the characteristics noted previously. The divisions are
5
distinguished from each other based on a combination of characteristics, including photosynthetic pigments, starchlike reserve products, cell covering, and other aspects of cellular organization (e.g., Van den Hoek et al., 1995; Sze, 1998; Graham and Wilcox, 2000). There is little consensus among phycologists as to the exact number of algal divisions; 8–11 have been recognized in recent texts (Van den Hoek et al., 1995; Sze, 1998; Graham and Wilcox, 2000). The 12 major algal groups (divisions and classes) recognized in this book are distinguished from each other in Table I. Each of the major groupings is briefly presented in the following sections, but the reader should refer to the relevant chapter(s) for more details. The number of freshwater genera now reported (>800) from North America, as discussed in Chapters 3–22, has greatly increased from earlier treatises (e.g., Smith,
TABLE I Major Distinguishing Features of the Major Algal Groups Presented Herein Algal group (chapter number)
Photosynthetic pigmentsa
Chloroplast outer Thylakoid membranes associations
Starch-like reserveb
External coveringc
Cyanobacteria (3 & 4)
chla, PE, PC, APC
0
0
Cyanophycean
Pepitoglycan matrices or walls
0
Red algae (5)
chla, PE, PC, APC
2
0
Floridean
Walls with a galactose polymer matrix
0
Green algae (6–9)
chla, b
2
2–6
True
Cellulosic walls, scales
0 – many
Euglenoid Algae (10)
chla, b
3
3
Paramylon
Pellicle
1–2 emergent
Yellow–green and related algae (11)
chla, c
4
3
Chrysolaminarin
Mostly cellulosic walls
2 unequal if present
Chrysophyte algae (12)
chla, c fucoxanthin
4
3
Chrysolaminarin
None, scales, lorica
2 unequal
Haptophyte algae (13)
chla, c fucoxanthin
4
3
Chrysolaminarin
Nonsiliceous scales
2 equal + haptonema
Synurophyte algae (14)
chla, c fucoxanthin
4
3
Chrysolaminarin
Siliceous scales
2 unequal
Diatoms (15–19)
chla, c fucoxanthin
4
4
Chrysolaminarin
Siliceous frustule
1, reproductive cells only
Dinoflagellates (20)
chla, c peridinin
3
3
True
Theca
2 unequal
Cryptomonads (21)
chla, c PC or PE
4
2
True
Periplast
2 equal
Brown algae (22)
chla, c fucoxanthin
4
3
Laminarin
Walls with alginate matrices
2 unequal
Flagella
Source: Various phycology textbooks (e.g., Sze, 1998; and Graham and Wilcox, 2000). a chl = chlorophyll (green); PE = phycoerythrin (red); PC = phycocyanin (blue); APC = allophycocyanin (blue); fucoxanthin and peridinin (golden to brown). b All of the reserves are polymers of glucose. They differ by their linkages: cyanophycean and floridean α1, 4 and α1, 6 branches; true starch with amylose α1, 4 and amylopectin α1, 4 and α1, 6 branches; paramylon β1, 3; chrysolamin and laminarin β1, 3 and β1, 6 branches. Only true starch stains positively with iodine (purple to black). c Pellicle and periplast within plasma membrane; the rest are external to it.
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1950; Prescott, 1962), but is still highly tentative and likely to be an underestimate of the region’s biodiversity.
A. Cyanobacteria Cyanobacteria or blue–green algae are prokaryotes, that is, cells that have no membrane-bound organelles, including chloroplasts (Table I; Chap. 3). Other characteristics of this division include unstacked thylakoids, phycobiliprotein pigments, cyanophycean starch, and peptidoglycan matrices or walls. There are 124 genera reported from inland habitats in North America, of which 53 are unicellular or colonial (Chap. 3) and 71 are filamentous (Chap. 4). However, the taxonomy of this division is currently in a state of flux, as noted in Chapter 3, and the number of genera should be considered to be tentative. Cyanobacteria inhabit the widest variety of freshwater habitats on Earth and can become important in surface blooms in nutrient-rich standing waters (Chaps. 3 and 4). Some of these blooms can be toxic to zooplankton and fish, as well as livestock that drink water containing these organisms. Inland cyanobacteria also occur in extreme environments, such as hot springs, saline lakes, and endolithic desert soils and rocks.
B. Red Algae Rhodophyta or red algae represent a division that is characterized by chloroplasts that have no external endoplasmic reticulum and unstacked thylakoids, phycobiliprotein pigments, floridean starch, and lack of flagella (Table I; Chap. 5). They are predominantly marine in distribution; only approximately 3% of over 5000 species occur in truly freshwater habitats. In North America, 25 genera are recognized in inland habitats (Chap. 5). Freshwater red algae are largely restricted to streams and rivers, but also can occur in other inland habitats, such as lakes, hot springs, soils, caves, and even sloth hair (Chap. 5).
C. Green Algae Chlorophyta or green algae constitute a division that has the following set of attributes: chloroplasts with no external endoplasmic reticulum, thylakoids typically in stacks of two to six, chlorophyll-a and -b as photosynthetic pigments, true starch, and cellulosic walls or scales (Table I). This is a diverse group in inland habitats of North America that includes 44 flagellated genera (Chap. 6), at least 129 coccoid and
nonmotile colonies (Chap. 7), 81 filamentous and plantlike genera (Chap. 8), and 48 conjugating genera and desmids (Chap. 9). Some members of the green algae (Charophyeae) are part of a lineage that is thought to be ancestral to higher plants. Green algae are widespread in inland habitats, but certain groups may have specific ecological requirements. For example, flagellated chlorophytes tend to be more abundant in standing waters that are nutrient rich (Chap. 6). Coccoid unicells and colonies are common in the plankton of standing waters and slowly moving rivers when nutrients, light and temperature are reasonably high (Chap. 7). The majority of filamentous and plantlike Chlorophyta are attached to hard surfaces in standing or flowing waters, but some can exist in the floating state or on soils or other subaerial habitats (Chap. 8). Filamentous conjugating green algae are most frequent in stagnant waters of roadside ditches and ponds, and in the littoral zones of lakes, where they can form free-floating mats or intermingle with other algae in attached or floating masses (Chap. 9). Desmids are more common in ponds and streams that have low conductance and moderate nutrient levels, and often intermingle with macrophytes.
D. Euglenoids Photosynthetic Euglenophyta or euglenoids have chloroplasts surrounded by three membranes, thylakoids in stacks of three, chlorophyll-a and -b as photosynthetic pigments, paramylon, and a pellicle (Table I; Chap. 10). Ten genera are reported from North American freshwater habitats (Chap. 10). Euglenoids are particularly abundant in the plankton of standing waters rich in nutrients and organic matter, and they can be associated with sediments, fringing higher plants, and leaf litter, although some may dominate in highly acidic environments (Chap. 10).
E. Eustigmatophyte, Raphidiophyte, and Tribophyte Algae Eustigmatophyte, raphidiophyte, and tribophyte algae comprise a loose group of algae that share the following characteristics: chloroplasts with four surrounding membranes, thylakoids in stacks of three, chlorophyll-a and -c as the typical photosynthetic pigments, and chrysolaminarin as the photosynthetic reserve product (where known) (Table I; Chap. 11). The yellow–green algae are quite diverse in freshwater habitats of North America: at least 90 genera have been reported, whereas the eustigmatophytes and raphdiophytes are relatively small groups that comprise
1. Introduction to Freshwater Algae
eight and three genera, respectively (Chap. 11). Many of these genera seldom have been reported. Members of this group of algae have been collected from a wide variety of habitats, but many are collected primarily in northern habitats (Chap. 11). They are both planktonic and associated with a variety of substrata.
F. Chrysophycean Algae Chrysophyceae or chrysomonads are distinguished by chloroplasts that have four surrounding membranes, thylakoids in stacks of three, fucoxanthin that typically masks chlorophyll-a and -c, and chrysolaminarin as the photosynthetic reserve. At least 72 genera are reported from inland habitats of North America (Chap. 12). Chrysophycean algae are typically associated with standing bodies of water that have low or moderate nutrients, alkalinity, and conductances, and a pH that is slightly acidic to neutral (Chap. 12). In addition, the majority of genera tend to be planktonic; attached forms occur to a lesser extent.
G. Haptophyte Algae Haptophyceae are characterized by chloroplasts that have four surrounding membranes, thylakoids in stacks of three, fucoxanthin that masks chlorophyll-a and -c, chrysolaminarin as the photosynthetic reserve, and a unique appendage associated with the flagellar apparatus, the haptonema (Table I; Chap. 13). Only three freshwater genera are found in North America (Chap. 13). The two common genera are planktonic in lakes and ponds, and occasionally form predominant blooms, particularly in areas with low conductance (Chap. 13). Chrysochromulina breviturrita has been used as an indicator of moderately acidic water.
H. Synurophyte Algae Synurophyceae is characterized by chloroplasts that have four surrounding membranes, thylakoids in stacks of three, fucoxonthin that masks chlorophyll-a and -c, chrysolaminarin as the photosynthetic reserve product, and siliceous scales (Table I; Chap. 14). Three genera are found in North American freshwater habitats (a fourth is known only from Australia), but the genera are species-rich, such as Mallomonus and Synura (Chap. 14). Synurophytes are exclusively freshwater phytoplankters in lakes, ponds, and slowly flowing rivers (Chap. 14). Habitats that support the largest flora are slightly acidic, low in conductance, alkalinity,
7
and nutrients, and have moderate amounts of humic substances.
I. Diatoms Bacillariophyceae or diatoms are distinguished by chloroplasts that have four surrounding membranes, thylakoids in stacks of three, fucoxanthin that masks chlorophyll-a and -c, chrysolaminarin as the photosynthetic reserve product, and a siliceous frustule that makes up the external covering (Table I; Chap. 15). The diatoms are a complex and diverse group in terms of frustule morphology. The North American freshwater genera consist of 25 centrics (Chap. 15), 28 araphid and monoraphid diatoms (Chap. 16), 37 symmetrical naviculoid taxa (Chap. 17) 14 eunotioid and asymmetrical naviculoid diatoms (Chap. 18), and 14 keeled and canalled forms (Chap. 19). Diatoms are found in all freshwater habitats, including standing and flowing waters, and planktonic and benthic habitats, and they can often dominate the microscopic flora. Because diatoms inhabit a broad array of habitats but many have specific habitat requirements, they have been used in freshwater environment assessment and to monitor long-term changes in ecological characteristics (Chap. 23).
J. Dinoflagellates Pyrrhophyta or dinoflagellates are characterized by chloroplasts that have three surrounding membranes, thylakoids in stacks of three, peridinin that masks chlorophyll-a and -c, true starch, a nucleus that has condensed chromosomes in cell cycle phases, a theca covering, and frequently a transverse and posterior flagellum. (Table I; Chap. 20). There are 37 genera in North American freshwater habitats (Chap. 20). The dinoflagellates are typically minor components of the phytoplankton of lakes and ponds, but sometimes form dense blooms, particularly in the presence of high levels of nitrates and phosphates (Chap. 20).
K. Cryptomonads Cryptophyta, cryptomonads or cryptophyte algae, have chloroplasts that have four surrounding membranes in which a nucleomorph occurs between the outer and inner two membranes, thylakoids in loose pairs, phycocyanin or phycoerythrin that masks chlorophyll-a and -c, true starch as the photosynthetic reserve, a periplast, and two subapical flagella (Table I; Chap. 21). There are 12 genera reported from the inland waters of North America (Chap. 21).
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Robert G. Sheath and John D. Wehr
Cryptomonads are typically planktonic in lakes and ponds, and are particularly diverse in temperate regions (Chap. 21).
L. Brown Algae Phaeophyceae or brown algae are distinguished by chloroplasts that have four surrounding membranes, thylakoids in stacks of three, fucoxanthin that masks chlorophyll-a and -c, laminarin as the photosynthetic reserve, and alginates commonly as the wall matrix component. There are six genera of freshwater brown algae, four of which have been collected in North America (Chap. 22).
Brown algae are predominantly marine in distribution; less than 1% of the species are from fresh water. The inland species are benthic, either in lakes or streams, and distribution is quite scattered (Chap. 22).
III. TAXONOMIC CHAPTERS IN THIS BOOK The approach of this book is to break the major algal groups into manageable taxonomic units, resulting in multiple chapters for those divisions that have many freshwater representatives. The following key gives major characteristics to allow the reader to immediately proceed to the appropriate chapter to determine an unknown algal sample.
A. Key 1a.
Cells with no chloroplasts; typically blue–green colored throughout (occasionally black, purple, brown, or reddish).......................2
1b.
Cells with variously colored pigments localized in one or more chloroplasts..................................................................................3
2a.
Organisms unicellular or colonial (coccoid cyanobacteria)...................................................................................................Chapter 3
2b.
Organisms filamentous (filamentous cyanobacteria)............................................................................................................Chapter 4
3a.
Cells stain positively (purple to black) with iodine for true starch.................................................................................................4
3b.
Cells do not stain positively (orange to reddish brown) with iodine for starch..............................................................................9
4a.
Green-colored chloroplasts with chlorophyll-a and -b as predominant photosynthetic pigments....................................................5
4b.
Chloroplasts with other colors and predominant photosynthetic pigments........................................................................................8
5a.
Organisms flagellated in the vegetative state (flagellated green algae)...................................................................................Chapter 6
5b.
Organisms nonflagellated in the vegetative stage................................................................................................................................6
6a.
Organisms coccoid (nonmotile unicells of various shapes) or colonial in forms without conjugation (coccoid and colonial nonmotile green algae).......................................................................................................................Chapter 7
6b.
Organisms filamentous, plantlike, or with sexual reproduction by conjugation.................................................................................7
7a.
Organisms with filamentous, bladelike, or plantlike morphologies without conjugation (filamentous and plantlike green algae).................................................................................................................................Chapter 8
7b.
Organisms with coccoid or filamentous morphologies with conjugation (conjugating green algae filaments and desmids) .............................................................................................................................................................................................Chapter 9
8a.
Cells with golden-colored chloroplasts with peridinin as the predominant photosynthetic pigment; two separate flagella typically with transverse and posterior insertions (dinoflagellates)....................................................................................................Chapter 20
8b.
Cells with blue-, brown-, or red-colored chloroplasts with either phycocyanin or phycoerythrin as the predominant photosynthetic pigment; flagella subapical (cryptophyte algae) ..................................................................................................................Chapter 21
9a.
Cells with blue- or red-colored chloroplasts with phycocyanin or phycoerythrin as the predominant photosynthetic pigment (red algae).............................................................................................................................................................................Chapter 5
9b.
Cells green or golden colored with other predominant photosynthetic pigments..............................................................................10
10a.
Motile green-colored cells with a pellicle (layer below the plasma membrane that often appears as spiral strips on the cell) (euglenoids)........................................................................................................................................................................Chapter 10
10b.
Nonmotile or motile, yellow–green- or golden-colored cells; naked or walled cells without a pellicle ..............................................11
11a.
Yellow–green-colored chloroplasts with chlorophyll-a and -c as the predominant photosynthetic pigments (eustigmatophyte, raphidiophyte, and tribophyte algae).....................................................................................................Chapter 11
11b.
Golden-colored chloroplasts with fucoxanthin as the predominant photosynthetic pigment............................................................12
12a.
Cells with a silica frustule covering (diatoms)...................................................................................................................................13
1. Introduction to Freshwater Algae
9
12b.
Cells with no covering or with one that is not a siliceous frustule (may be siliceous scales) .........................................................17
13a.
Frustules in the valve view are radially symmetrical or symmetrical in more than two planes (centric diatoms)..................Chapter 15
13b.
Frustules symmetrical in the valve view in one or two planes ..........................................................................................................14
14a.
Frustules without a raphe or with one-on-one valve only (araphid and monoraphid diatoms)............................................Chapter 16
14b.
Frustules with two raphes................................................................................................................................................................15
15a.
Raphe in an elevated keel or a canal (keeled and canalled raphid diatoms).........................................................................Chapter 19
15b.
Raphe not in a keel or canal............................................................................................................................................................16
16a.
Frustules bilaterally symmetrical in valve view (biraphid symmetrical diatoms) .................................................................Chapter 17
16b.
Frustules not bilaterally symmetrical in valve view (eunotioid and asymmetrical biraphid diatoms)...................................Chapter 18
17a.
Cells with a specialized appendage, the haptonema, in vegetative and/or reproductive stages (haptophyte algae)...............Chapter 13
17b.
Cells without a haptonema in any stage...........................................................................................................................................18
18a.
Vegetative cells with siliceous scales (synurophyte algae) ...................................................................................................Chapter 14
18b.
Vegetative cells without siliceous scales ....................................................................................................................................19
19a.
Exclusively benthic; often macroscopic thalli with no unicellular or colonial representatives; cell walls with alginates (brown algae).....................................................................................................................................................................Chapter 22
19b.
Mostly planktonic with some attached representatives; numerous unicellular or colonial representatives; mostly microscopic thalli; cell walls without alginates (chrysophyte algae)..................................................................................................................Chapter 12
LITERATURE CITED Graham, L. E., Wilcox, L. W. 2000. Algae. Prentice–Hall, Upper Saddle River, NJ, 640 pp., glossary, literature cited, and index. Prescott, G. W. 1962. Algae of the Western Great Lakes area. W. B. Brown, Dubuque, IA, 977 p. Sheath, R. G. 1984. The biology of freshwater red algae. Progress in Phycological Research 3:89–157. Sheath, R. G., Hambrook, J. A. 1990. Freshwater ecology, in: Cole, K. M., Sheath, R. G., Eds. Biology of the red algae. Cambridge University Press, Cambridge, UK, pp. 423–453.
Smith, G. M. 1950. Freshwater algae of the United States, 2nd ed. McGraw–Hill, New York, 719 p. Sze, P. 1998. A biology of the algae 3rd ed. McGraw–Hill, Boston, 278 p. Van den Hoek, C., Mann, D. G., Jahns, H. M. 1995. Algae. An introduction to phycology. Cambridge University Press, Cambridge, UK, 623 p. Vis, M. L., Sheath, R. G., Hambrook, J. A., Cole, K. M. 1994. Stream macroalgae of the Hawaiian Islands: A preliminary study. Pacific Science 48:175–187.