Rhode island

Phycologia (1992) Volume 31 (2), 164-179
Systematics of the freshwater red algal family
Lemaneaceae in North America
M.L. VIS AND R.O. SHEATH*
Department oj Botany, University oj Rhode Island, Kingston, RI 02881, USA
M.L. VIS AND R.G. SHEATH. 1992. Systematics of the freshwater red algal family Lemaneaceae in
North America. Phycologia 3 1 : 164-179.
Multivariate morphometrics and image analysis were used to determine the number of well-distin­
guished taxa in the freshwater red algal family Lemaneaceae (Batrachospermales, Rhodophyta) from
North America. Length, width, stalking, branching, presence of axial cortical filaments and sper­
matangial sorus size and shape were assessed. Two genera, Lemanea Bory and Paralemanea (P.c.
Silva) stat. nov. ( = Lemanea subgenus Paralemanea P.c. Silva), were recognized using internal
anatomical and spermatangial features. Lemanea has no cortical filaments around the central axis,
T- or L-shaped ray cells closely applied to the outer cortex and spermatangia in patches, whereas
Paralemanea has cortical filaments around the central axis, simple ray cells that do not abut the
outer cortex, and nodal spermatangial rings. Cluster analysis, based on the Gower similarity coef­
ficient, revealed six distinct morphological entities, three with characteristics of Lemanea and three
with characteristics of Paralemanea. These entities were statistically related to the type specimens
of the species recorded from North America. In Lemanea, L. borealis Atkinson and L. fluviati/is
(Linnaeus) C. Agardh were recognized. In addition, a new variety of L. fucina Bory was described,
L. fucina var. parva, which is significantly shorter (x = 6.0 cm) than the nominate variety (x = 15.9
cm). In Paralemanea, the following species were recognized: P. catenata ( Kiitzing) comb. nov.
(Basionym: L. catenata Kiitzing), synonymous with L. nodosa Kiitzing and L. pleocarpa Atkinson;
P. annulata ( Kiitzing) comb. nov. (Basionym: L. annulata Kiitzing), synonymous with L. australis
Atkinson and L. grandis (Wolle) Atkinson; and P. mexicana ( Kiitzing) comb. nov. (Basionym: L.
mexicana Kiitzing), synonymous with L. feldmannii Sanchez- Rodriguez et Huerta. There was no
obvious separation of species on the basis of physical and chemical parameters of the sampled
streams, but there were geographical distribution differences among taxa.
INTRODUCTION
The freshwater red algal family Lemaneaceae,
like other families of the order Batrachosper­
males, has a heteromorphic triphasic life history
consisting of chantransia, gametophyte and car­
po sporophyte phases (see Sheath 1984). How­
ever, its distinct cartilaginous, pseudoparenchy­
matous gametophytic thallus with internal
carposporophytes distinguishes it from other
closely related families. Within the Lemaneaceae
three gametophyte morphologies exist which dif­
fer in internal structure. One has cortical fila­
ments localized around a central axis with simple
ray cells that do not abut the large cells of the
outer cortex, and a second one has no axial cor­
tical filaments and T- or L-shaped ray cells close­
ly applied to the outer cortex (Sirodot 1872).
* Present address for correspondence: Department
of Biology, Memorial University of Newfoundland, St
John's, Newfoundland, Canada AlB 3X9.
164
Recently, Entwisle (1989) described a third mor­
phology for Australian plants consisting of cor­
tical filaments throughout the thallus interior and
no obvious ray cells or large, outer cortex cells.
The former two morphologies were originally in­
cluded in the genus Lemanea by Bory (1808),
while the latter structural type has been given the
name Psilosiphon by Entwisle (1989).
In North America and Europe, only the first
two morphological types have been described
(Starmach 1977). Sirodot (1872), believing these
two anatomies to be of generic importance, pro­
posed the genus Sacheria to include those species
that lack axial cortication, leaving Lemanea to
apply to those species that have axial cortication.
Unfortunately, among the species he assigned to
his new genus was L. corallina Bory ( ConJerva
fluviatilis Linnaeus), which Bory (1808, p. 178)
had designated the type of Lemanea, and this
species lacks axial cortication. Thus the name
Sacheria is a nomenclatural (homotypic) syn­
onym of Lemanea (Oreuter et at. 1988). Ketel
=
Vis and Sheath: Lemaneaceae systematics
(1887, p. 15) reduced Sacheria to the rank of
subgenus, and thereby recognized the co-ordi­
nate subgenus Lemanea; Hamel (1925, p. 59)
renamed the latter Eulemanea, and this arrange­
ment has been followed by subsequent research­
ers (Atkinson 1931; Starmach 1977; Bourrelly
1985). Silva (1959, p. 62) pointed out that both
of these names are illegitimate, and proposed the
substitute subgenus name Paralemanea P.e. Sil­
va for Eulemanea Hamel (lectotype: L. nodosa
Kiitzing).
In North America 16 species and infraspecific
taxa of Lemaneaceae have been reported (Atkin­
son 1931; Sanchez-Rodriguez & Huerta 1969;
Flint 1970). Differentiation among species of this
family has been problematical. In most taxo­
nomic schemes species are delineated largely by
variable and subjective features, e.g. whether
spermatangial rings are regular or irregular (Star­
mach 1977). Another feature often used to dis­
tinguish species is colour. However, colour varies
according to environmental conditions and the
physiological state of the alga (Palmer 1941; Is­
raelson 1942; Reed 1970). Israelson (1942) noted
that those populations that grow in direct sun­
light tend to be olive to light green, as compared
to those that grow in shade, which can be violet.
Hence the systematics of the Lemaneaceae are
in need of major revision. By utilizing quanti­
tative measurements of key morphological fea­
tures, sample size and variability may be deter­
mined, allowing for the numerical classification
of infrageneric taxa. Similar taxonomic proce­
dures have been successfully employed to classify
other problematic genera, such as the marine fil­
amentous brown alga Pilayella (Bolton 1979) and
the diatom Gomphoneis (Stoermer & Ladewski
1982). The aim of the present research was to
create a taxonomic scheme in which multivariate
morphometrics and image analysis in correlation
with distinct qualitative features are used to de­
termine the number of well-distinguished taxa
of the Lemaneaceae in North America.
MATERIALS AND METHODS
Field collections
Populations of the Lemaneaceae were sampled
throughout North America, from the north slope
of Alaska (68°N) and south-western Greenland
(66°N) in the north to central Mexico (19°N) in
the south, as part of a study conducted by Sheath
165
& Cole (1990) on the systematics of all freshwater
Rhodophyta in North America (Fig. 1). The algal
samples were immediately fixed in 2.5% buffered
glutaraldehyde to prevent morphological distor­
tion. In addition, the physical and chemical
properties of maximum depth, maximum width,
pH, specific conductance, temperature and mean
current velocity were measured from each stream
(Table I) as described by Sheath et al. (1989).
Type specimens
The type specimens of the species recorded in
North America were examined from the herbaria
NY, BH, L, PC, REN and MICH (acronyms as
in Holmgren et al. 1981).
(1) L. grandis (Wolle) Atkinson (holotype)
Rabh. Alg. Eur. #2538. Basionym: En­
tothrix graedis Wolle. Habitat: Bethle­
hem, Pennsylvania, 'in rivulis saxa oc­
cupans,' Juli 1877 (NY).
(2) L. borealis Atkinson (lectotype) #1108,
collected by e.D. Howe and W.F. Long.
Habitat: Bay of Islands, Newfoundland,
August 9, 190 I (NY).
(3) L. australis Atkinson (lectotype) e.M.P.
#444 determined by e. Mervin Palmer,
collected by G.F. Atkinson. Habitat: up­
per Otey's rapids, Morgan's Creek, Chap­
el Hill, North Carolina, Jan. 28, 1888
(BH).
(4) L. annulata Kiitzing (holotype) Herb.
Lugd. Bat. 10. Eur. As. #941.149 . . . 336.
Habitat: 'An Steinen am Wehre in der
Saale bei Halle,' no date (L).
(5) L. catenata Kiitzing (holotype) Herb.
Lugd. Bat. 10. Eur. As. #941.149 . . . 343.
Habitat: 'In Galliae, Germaniae occiden­
talis f1uviis,' no date (L).
(6) L. mexicana Kiitzing (holotype) Herb.
Lugd. Bat. 50. Amer. Sept. #941.96 . . .
41. Habitat: 'In rivulis alpinis mexica­
nis,' no date (L).
(7) L. nodosa Kiitzing (holotype) Herb. Lugd.
Bat. 10. Eur. As. #941.149 . . . 278. Hab­
itat: 'Ad rupes et saxa in torrente Her­
cyniae "Bode",' no date (L).
(8) L. pleocarpa Atkinson (paratype) e.M.P.
#637 determined by e. Mervin Palmer
15 Sept. 1952, collected by Robert Peter.
Habitat: on rocks in brook near Lexing­
ton, Kentucky, 1834 (MICH).
(9) L. pleocarpa Atkinson (holotype) e.M.P.
#610 determined by C. Mervin Palmer
166
Phyc% gia. Vol. 31 (2), 1992
ATLANTIC
OCEAN
0
a
400
I
"
a
800
I
' I
1200
'i
• .
1600 km
I
1000 mile.
100
80
Fig. 1. Location of North American stream sites from which populations of the Lemaneaceae were collected. The
numbers correspond to the stream numbers in Table 1. The bold lines indicate major drainage basins.
Dec. 15, 1952, collected by C.W. Short.
Habitat: fresh running water, Kentucky,
1842 (BH).
(10) L. jucina Bory (holotype) Herbier Bory
de St Vincent. Habitat: 'ruisseau courant
entre Vitre et Fougeres,' France, no date
(PC).
Herbarium packets vary in the number of
plants they contain because a population is usu-
Vis and Sheath: Lemaneaceae systematics
167
Table 1. Physical and chemical parameters of streams from which Lemanea and Paralemanea plants were collected
Stream
number
I
2
3
4
5
6
7
8
9
10
II
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
Location'
A K42
AK52
AK 103
AK106
AK 118
AK121
AK 122
AK 134
BC 5
BC 49
BC 52
BC 55
BC 64
WA 19
WA 102
OR 8
OR 102
OR 103
OR 107
OR 108
OR 109
OR 1 10
ID 101
CA 16
CA 20
CA 21
CO 101
MA N 2
WI 103
M I I05
O N OR
O N IA
ON 2
ON 3
ON 32
ON 39
ON 47
ON 56
ON 57
ON 101
OH 10
NY 1 16
43
AR 5
44
45
AR 6
OKI
46
47
48
49
50
51
52
53
54
55
IL 2
IN5
IN 7
PA I
WV 3
NC 22
NC NHC
NC
NC 300
RI 3
Name'
L. borealis
L. borealis
L. borealis
L. borealis
L. borealis
L. jluviatilis
L. jluviatilis
L. borealis
L. jluviatilis
L. jluviatilis
L. borealis
L. jluviati/is
L. jluviatilis
L. borealis
L. jluviatilis
L. jluviatilis
L. borealis
L. jluviatilis
L. jluviatilis
L. jluviatilis
L. jluviatilis
L. borealis
L. jluviatilis
P. annulata
P. annulata
L. jluviatilis
L. sp.
L. sp.
L. jluviatilis
L. jluviatilis
L. jluviatilis
L. jluviatilis
L. jluviatilis
L. jluviatilis
L. jluviatilis
L. jluviatilis
L. jluviatilis
L. jluviatilis
L. jluviatilis
P. sp.
L. jluviatilis and
P. annulata
L. fucina var.
parva
P. annulata
L. fucina var.
parva
L. jluviatilis
P. catenata
P. annulata
P. sp.
P. annulata
P. sp.
L. jluviatilis
P. annulata
P. annulata
L. jluviatilis
MaxiMean
Temmum Maximum current
width
velocity perature
depth
(cm)
(cm s-')
(m)
eC)
pH
Specific
conductance Water
(/LS cm-') colour3
20
120
30
25
145
155
155
70
60
2 10
60
190
210
0
0
0
I
I
I
I
0
0
0
0
75
0
7.6
210
90
100
0
0
0
0
0
0
0
0
0
0
19
16
16
6. 1
40
60
50
21
19
19
22
21
24
21
22
15
7.1
6.3
6.7
8.2
6.6
6.8
6.6
5.7
7.0
200
135
100
300
40
70
100
95
225
0
I
I
I
I
0
7.8
8.2
10.0
2.0
20.0
11.3
2.1
10.0
4.3
9.9
5.4
5.0
15.0
4.0
I.S
45
60
> 100
69
45
>100
> 100
> 100
42
47
67
35
17
38
III
50
43
23
22
41
59
38
91
91
19
I
7
8
10
9
II
12
13
9
15
15
21
20
13
1.5
30
48
9
15.0
10.0
2.0
4.0
30.0
7.0
0.9
2.7
10.0
2.0
10
28
19
25
43
20
23
70
90
50
67
52
12
52
54
61
30
35
II
21
9
8
7
7
7
8
9
10
13
12
5.0
5.0
5.5
5.5
5.5
5.5
15.0
16.2
16.7
>100
47
37
72
88
42
10.0
> 100
6.4
8.6
8.0
7.9
8.0
0
4.7
24
9
118
56
47
78
33
33
37
74
0
8.0
70
22
14
8. 1
91
0
5.3
65
12
14
7.1
10
0
7.5
7.5
40
>100
20
31
15
15
7. 1
6.6
60
10
0
0
4.3
7.8
5.0
3.8
6.0
5.5
>100
56
60
32
30
16
18
52
71
58
35
15
14
17
9
4
17
7.7
8.6
8.6
5.5
6.8
7.0
350
420
500
80
113
42
0
0
0
0
0
I
168
Phycologia, Vol. 31 (2), 1 992
Table 1. Continued
Stream
number
Location I
56
57
NH WF
NH 5
58
59
60
61
62
63
64
65
66
67
VT 2
PQ 4
PQ 200
LAB 2
LAB 5
LAB 8
NF 202
NF 206
GLD 5
MEX 12
Name2
L. j/uviatilis
L. fucina var.
parva
L. j/uviatilis
L. borealis
L. borealis
L. borealis
L. borealis
L. borealis
L. borealis
L. borealis
L. borealis
P. mexicana
Mean
MaxiTemmum Maximum current
velocity perature
depth
width
(0C)
(cm S-I)
(m)
(cm)
pH
Specific
conductance Water
(/-tS cm-I) colour'
6.8
41
60
15
7.7
2 10
0
3.0
12.0
12.1
16.0
9. 1
20.0
7.9
3.5
3.0
30
40
80
100
40
50
57
45
39
50
67
61
78
68
49
38
80
1 10
8
7
7
6
4
9
10
13
12
5.7
7. 1
7.0
6.4
7.5
7.6
7.3
8.1
8.3
42
40
10
10
50
10
20
90
50
I
0
I
I
0
0
0
0
0
BC = British Columbia, WA = Washington, OR = Oregon, ID = Idaho, CA = California,
I AK = Alaska,
CO = Colorado, MAN = Manitoba, W I = Wisconsin, MI = Michigan, ON = Ontario, OH = Ohio, NY = New
York, AR = Arkansas, OK= Oklahoma, IL = Illinois, IN = Indiana, PA = Pennsylvania, WV = West Virginia,
NC = North Carolina, RI = Rhode Island, NH = New Hampshire, VT = Vermont, PQ = Quebec, LAB = Labrador,
NF = Newfoundland, GLD = Greenland, MEX = Mexico.
2 P = Paralemanea; L = Lemanea.
, 0 = colourless; I = yellow.
ally collected rather than a single plant. There­
fore, the type material of a taxon can range from
one plant to > 25 plants. These plants were re­
hydrated and measurements were made as de­
scribed below.
Other specimens
The following additional herbarium specimens
and topotypes were examined.
(1) L. fucina #69 collected by Bory. Habitat:
'Attachee aux pierres dans les eaux cou­
rantes des rivieres,' Vire, Caen, France,
Mai-Aout (PC).
(2) L. j/uviatilis #2086 collected by Sirodot.
Habitat: 'Ruisseau de Beaufort, France,'
18.iv.1869 (REN).
(3) L. rigida Sirodot (topotype) #2078 col­
lected by Sirodot. Habitat: 'Ruisseau de
Saint Lazare pres Monfort,' France, 22.v.
1878 (REN).
(4) L. rigida Sirodot (topotype) #2082 col­
lected by Sirodot '(Annee fort pluviense
favorable au developpement des fila­
ments).' Habitat: 'Ruisseau de Saint La­
zare pres Monfort,' France, fin Mars 1877
(REN).
(5) L. feldmannii Sanchez-Rodriguez et Huer­
ta (topotype) R.S. #MEX I 2 collected by
Robert Sheath. Habitat: in a stream 1 km
west of Cahllacan, Mexico, 22.ii.1990 (the
holotype was requested but no reply was
received).
(6) L. australis Atkinson (topotype) collected
by Roy Coomans. Habitat: Morgan' s
Creek, North Carolina, 25.viii.1 984.
Microscope and statistical procedures
A Southern Micro Instruments (1 20 Interstate
N. Parkway E., Atlanta, Georgia 3 03 3 9, USA)
Microcomp image analysis apparatus was em­
ployed to quantify vegetative and reproductive
morphological features of the specimens ana­
lysed. The equipment includes an Olympus Van­
ox microscope with an attached Hitachi CCTV
video camera which relays the image to an IBM
AT computer. The desired measurement is made
using a Microcomp digitizer pad as described by
Sheath (1989). The external vegetative features
of length (L), internodal diameter (ID) as a mea­
sure of width, stalk diameter (STD), nodal di­
ameter (ND) and number of branches were mea­
sured. The overall plant length and width have
been used to differentiate species, and were also
included (Starmach 1 977). To indicate stalked
or un stalked thalli, a condition which has been
used to differentiate subgenera, the ratio ID/STD
was used (Sirodot 1872). The ratio ND/ID shows
Vis and Sheath: Lemaneaceae systematics
169
Table 2. Morphometric features of cluster analysis groupings of spermatangial populations
Percentage of
branched Mean
Number
branch
plants
Mean
of popuin popu- number/
Group' lations Stalked lation
thallus length (cm)
A
7
No
� 12
0.0 1
B
2
Yes
� 12
0.1
C
3
Yes
�56
4.3
D
E
1
3
No
No
None
None
0
0
2.2
(0.6-4.0)'
5.2
(4.3-6.0)
6.0
(5.2-7.1)
9.5
4.3
(3.1-5.3)
Mean
width (mm)
ND/ID'
0.23
(0.14-0.35)
0.54
(0.5 1-0.57)
0.45
(0.37-0.5 I)
0.72
0.56
(0.43-0.63)
1.82
(1.52-2.10)
1.59
( 1. 32-1.86)
1.74
( 1.50-1.93)
1.89
1.5I
( 1. 38-1.75)
Axial
cortical
filaments
Spermatangia
No
Patches
No
Patches
No
Patches
Yes
Yes
Rings
Rings
, From Fig. 2.
, ND/ID = ratio of nodal diameter to internodal diameter.
3 Range of population means.
whether the thallus is slightly undulate or dis­
tinctly protruded at the nodes, an attribute which
has also been employed to distinguish the sub­
genera Lemanea and Paralemanea (Atkinson
1931). The number of branched plants was de­
termined because branching pattern is appar­
ently important for differentiation of specimens
of L. feldmannii with many branches from other
closely related species (Sanchez-Rodriguez &
Huerta 1969), and for distinguishing between the
two subgenera. Paralemanea shows little branch­
ing, while Lemanea exhibits much branching
(Sirodot 1872). The spermatangial sorus diam­
eter (SPD) and perimeter (SPP) were included in
the analysis of the spermatangial plants. Sper­
matangial sori were measured for the ratio SPDI
ND because they occur in rings around the nodes
in the subgenus Paralemanea, and in well-de­
fined patches on the nodes in Lemanea (Sirodot
1872).
Each population was randomly sampled by
placing all plants collected in a dish, swirling the
dish and examining the plant in the middle of
the field of view. Only intact and mature ga­
metophytes having spermatangial sori, internal
carposporophytes, or both, were measured. To
ensure uniformity, ND was measured using the
largest node on each plant; ID was measured just
above the lowermost node, and STD was mea­
sured just below the lowermost node. SPD and
SPP were measured on the largest node. Twenty­
five plants per population were measured. The
size of this standard sample was determined by
(s/Ex)2 where s
the following equation: n
=
=
prede­
mean and E
standard deviation, x
termined standard error (in this case 0.05)
(Southwood 1978). In addition to the quantita­
tive external morphological features, qualitative
internal features were examined using an Olym­
pus Vanox microscope to determine the presence
of axial cortical filaments, the type of ray cell,
and the ray cell's relationship to the outer cortex.
The Gower similarity coefficient was calculat­
ed in order to incorporate both quantitative and
qualitative data (Dunn & Everitt 1982). For the
qualitative data (internal structure) the coeffi­
cient is equal to one if the two populations are
the same for the particular feature, and is equal
to zero if they differ. For the quantitative data
(L, ID, ID/STD, ND/ID, branching and SPDI
ND) the following formula was used:
=
=
S ;ik
=
I - I X;k - xik I IRk
(1)
mean of population i for feature k,
where X;k
mean of population j for feature k, and Rk
xik
range of feature k. To determine the Gower
similarity coefficient, incorporating all the fea­
tures for the two populations, the following equa­
tion was utilized:
=
=
=
St
=
(S, + S2 + . . . + Sn)/n
(2)
calculated coefficient of either a qual­
where S
itative or a quantitative feature and n number
of coefficients. For the spermatangial plants both
the spermatangial features, SPD/ND and SPP,
and the vegetative feature, L, ID, ND/ID, IDI
STD, branching and internal structure, were used
to determine the Gower similarity coefficient. In
=
=
170
Phyc% gia, Vol. 31 (2), 1992
1.6
1.4
1.2
W
()
1
Z
«
I- 0.8
CJ)
is 0.6
c
D
0.4
0.2
0
60
4
63
66
18
29
22
19
45
43
57
47
48
50
54
POPULATION
Fig. 2. Dendrogram from the cluster analysis of the spermatangial plants of the Lemaneaceae examined during
this study, showing five groups, designated A, B, C, D and E. The population numbers correspond to the stream
numbers in Table I.
addition, for all mature plants, including those
without gametangia and the spermatangial plants,
the vegetative features of L, ID, ND/ID, IDI
STD, branching and internal structure were used.
Trends in the dissimilarity matrix calculated from
the similarity coefficients were analysed statis­
tically using cluster analysis with the unweighted
group average method (UPGMA) from the SAS
statistical software package (Anonymous 1985).
One-way analysis of variance (ANOVA) from the
Minitab statistical package (Ryan et al. 1985)
and Duncan's multiple-range test from SAS were
used to determine differences in population
means.
Sixty-eight populations were collected: 16
populations were analysed statistically using
spermatangial and vegetative features, and 44
populations, including the previous sixteen, were
analysed statistically using vegetative features
alone. Of the remaining populations, eight had
damaged tips, so that no measurement of length
could be made. These populations were not used
in the statistical analysis, but could be related to
the statistical groupings based on the diagnostic
features measured. The last 1 6 populations could
be assigned to a genus on the basis of internal
structure and species identified if diagnostic fea­
tures were present.
The types and additional specimens were
matched to the cluster analysis groupings by
qualitative features and by use of Duncan's mul­
tiple-range test and ANOVA in the means of quan­
titative features. When types were not available,
descriptions from the literature (Sirodot 1 872;
Atkinson 1890, 1931) were relied upon for iden­
tification.
RESULTS AND DISCUSSION
Cluster analysis
A cluster analysis of the Gower coefficients for
spermatangial plants is shown in Fig. 2. There
are five distinct groups based on the measured
features (Table 2). Groups A, B and C are similar
in that they have no axial cortical filaments, and
T- or L-shaped ray cells closely applied to the
outer cortex (Fig. 3 ), and spermatangia in patches
on the nodes (SPD/ND ::; 0.4) (Fig. 4). However,
the three groups differ in stalking (Fig. 5). Group
A has no stalk (ID/STD ::; 1.3) (Fig. 6), the only
exception being population #29 (ID/STD = 1 .6).
By contrast, both Groups B and C are stalked
(ID/STD :::: 1.5) (Figs 7, 8). Groups B and C do
not differ statistically in distinguishing features
(P < 0.05), except for branching. Group B has
::; 12% branched plants per population, and
Group C has :::: 56% branched plants per popu­
lation.
Groups D and E differ from the previous three
groups in having a central axis with cortical fil­
aments and simple ray cells which do not abut
the outer cortex (Fig. 9), and spermatangia in
rings (SPD/ND :::: 0.9) around the nodes (Fig.
10). Both groups are unstalked (ID/STD ::; 1.2)
Vis and Sheath: Lemaneaceae systematics
O.3mm
O.5cm
6
1 71
O.5mm
4
O.5cm
7
Figs 3�. Diagnostic features and species of Lemanea in North America.
Fig. 3. Internal structure consisting of a central axis without cortical filaments (arrowhead) and T- or L-shaped
ray cell (double arrowhead) closely applied to the outer cortex.
Fig. 4. Spermatangia in patches (arrowheads) on node.
Fig. 5. A stalked plant with definite constriction (arrowhead) and an unstalked plant with no constriction.
Fig. 6. Representative population (#65) of L. borealis. The population numbers correspond to the stream numbers
in Table I.
Fig. 7. Representative population (#34) of L. fluviatilis showing stalked region (arrowhead) and few branches
(double arrowhead).
Fig. 8. Population (#57) holotype specimen of L. fucina var. parva with stalked region (arrowhead) and prolific
branches (double arrowhead).
with no branching, but they can be distinguished
from each other on the basis of size. The plants
in Group D are rarely under 6.5 cm, with only
three plants being ::;;6.5 em, and the plants in
Group E are seldom greater than 5.5 cm (four
plants � 6.5 cm). The mean length and width of
0.56 mm) are sig­
9.5 cm) (x
Group D (x
nificantly greater than those of Group E (x 4.3
0.72 mm) (P < 0.05) (Figs 11, 1 2).
cm) (x
A cluster analysis of the Gower coefficient of
all the mature plants shows six groups (Fig. 14),
=
=
=
=
which are distinguished on the basis of the veg­
etative feature used in the above spermatangial
plant cluster (Table 3 ). Groups A, B, C, D and
E have the same vegetative features as described
previously. The variability of the features is
greatest for Groups A and B, due to the larger
number of populations (Table 3). Most of the
populations in Group A are un stalked, except for
1.6) and #28 (IDI
populations #29 (ID/STD
2.2). These two populations clustered
STD
with Group A, based primarily on small size.
=
=
172
Phyc% gia. Vol. 31 (2), 1992
Figs 9-13. Diagnostic features and species of Paralemanea in North America.
Fig. 9. Internal structure consisting of a central axis with cortical filaments (arrowhead) and simple ray cell
(double arrowhead) not abutting the outer cortex.
Fig. 1 0. Spermatangia in nodal ring (arrowhead).
Fig. 1 1 . Representative population (#47) of P. catenata. The population numbers correspond to the stream
numbers in Table 1.
Fig. 1 2. Representative population (#54) of P. annulata.
Fig. 13. Representative population (#67) of P. mexicana showing the whorled branching (arrowhead) and
rebranching (double arrowhead).
The length of population #29 and the length and
width of population #28 are significantly differ­
ent from those of 1 8 of the 20 populations of
Group B (P < 0.05); and the width of population
#29 is significantly smaller than that of Group B
(P < 0.05). Thus the taxonomic status of pop­
ulations #29 and #28 is unclear; it may be that
these populations are intermediate between
Groups A and B. The amount of branching per
population in Group B is :s 48%, . with 1 8 of the
20 populations having < 3 0% branched plants.
Groups B and C differ not only in the number
of plants with branches per population, but also
in the number of branches per plant. In Group
B,five branches per plant is the maximum, and
only one plant was found to have this number.
More commonly,branched plants in Group B
have 2-4 branches. By contrast,Group C plants
Vis and Sheath: Lemaneaceae systematics
173
1.6
1.4
1.2
W 1
()
z
«O.B
l(/) 0 6
F
E
O ·
0.4
POPULATION
Fig. 14. Dendrogram from the cluster analysis of all mature plants of the Lemaneaceae examined during this
study, showing six groups, designated A, B, C, D, E and F. The population numbers correspond to the stream
numbers in Table I.
typically have 6-8 branches and up to 18 branch­
1.1 ) and
es. Group F is unstalked (ID/STD
has axial cortical filaments and simple ray cells
that do not abut the outer cortex, similar to the
situation in Groups D and E. It is distinguished
from these groups on the basis of branching (Fig.
13). Group F has 96% of the plants branched, in
comparison to Groups D and E which have no
branched plants (Figs 11-13).
The features separating Groups A, B and C
from Groups D, E and F are both internal and
external, with no indication of overlap of key
characteristics between the two groups. It is pro­
posed that, since the difference between the two
morphologies is always consistent, they should
=
be recognized as representing distinct genera. The
genus Lemanea, in accordance with the type spe­
cies, L. jluviatilis, is retained for those species
that have no cortical filaments around the central
axis, T- or L-shaped ray cells closely applied to
the outer cortex and spermatangia in patches on
the nodes as in Groups A, B and C (Figs 3, 4).
The genus Paralemanea (P.e. Silva) stat. nov. is
proposed for those species that have cortical fil­
aments around the central axis, simple ray cells
not abutting the outer cortex, and nodal sper­
matangia rings as in Groups D, E and F (Figs 9,
10).
GROUP A: Group A and the lectotype of L.
borealis share many morphological features (Ta-
Table 3. Vegetative morphometric features of cluster analysis groupings of all mature populations
Group'
Number
of populations
PercentMean
age of
branched
branch
plants in number/
Stalked population thallus
A
16
No
,,; 12
0.01
B
20
Yes
,,;48
0.2
C
3
Yes
�56
4.3
D
E
I
3
No
No
None
None
0
0
No
96
11.4
F
Mean
length (cm)
Mean
width (mm)
ND/ID2
2.3
(0.6-4.1)3
4.8
(2.8-1 1.2)
6.0
(5.2-7.1)
9.5
4.3
(3.1-5.3)
7.9
0.25
(0. 13-0.35)
0.50
(0.33-0.67)
0.45
(0.37-0.5 I)
0.72
0.56
(0.43-0.63)
0.50
1.78
( 1.31-2.27)
1.50
( 1.22-1.86)
1.74
( 1.50-1.93)
1.89
1.5I
( 1.38-1.75)
1.82
, From Fig. 14.
ND/ID = ratio of nodal diameter to internodal diameter.
3 Range of population means.
2
Axial
cortical
filaments
No
No
No
Yes
Yes
Yes
174
Phycologia, Vol. 31 (2), 1992
Table 4. Morphometric features of type and herbarium specimens examined
Specimen
Number of
Mean
Plants
specibranch
with
mens
branches number/ Length
examthallus
(cm)
(%)
ined Stalked
L. annulata
( )2
L. australis
L. australis (topotype)
7
( )
L. borealis
L. catenata
25
( )
L. feldmannii (topotype)
L. fluviatilis
25
9
(additional specimen)
L. fucina
L. fucina
No
(9)
No
No
( 13)
No
No
(7)
No
Yes
I
( )
0
0
0
0
0
0
0
0
0
0
96
22
1 1.4
0.2
100
100
34
>3
(additional specimen)
L.
L.
L.
L.
L.
grandis
mexicana
nodosa
pleocarpa
pleocarpa (paratype)
L. rigida
L. rigida
I
2
20
25
25
1
( )
3
9
No
No
No
No
No
(8)
Yes
Yes
None
52
None
None
None
0
3
0
0
0
100
89
31.7
5.6
4.3
(7)
5.0
(5)
2.3
>8.4
(7)
7.9
17.0
Axial
cortical
filaWidth
(mm) ND/IDI ments
0.55
(9)
0.61
0.58
(13)
0.23
0.69
(7)
0.50
2.00
(9)
1.55
1.62
(9)
1.64
1.85
(7)
1.82
22.0
15.9
(10)
6.0
8.0
>14.8
(12)
19.4
20.6
Yes
Yes
Yes
No
Yes
1.26
1.62
1.79
1.95
2.3
(8)
Rings
(7)
Rings
Rings
(4)
Yes
No
No
0.45
0.46
0.71
1.19
0.93
(8)
Spermatangia
Patches
(6)
Yes
Yes
Yes
Yes
Yes
No
No
ND/ID = ratio of nodal diameter to internodal diameter.
( ) = see each characteristic for sample size.
bles 3 and 4). Both are unstalked (ID/STD �
1.2), little branched (� 12%), and have an inter­
nal structure consisting of a central axis without
cortical filaments and T- or L-shaped ray cells
closely applied to the outer cortex. The mean
values of L. borealis are in the middle ofthe range
of Group A for the features of length, width and
ND/ID. Lemanea borealis does not differ sig­
nificantly from five of the populations of Group
A in length, four in width and seven in ND/ID
(n 25, P < 0. 05). Hence, Group A corresponds
with this species. The diagnostic features of L.
borealis are un stalked, little branched plants, a
range in mean length per population of 0.6-4.1
cm and a mean width 0.13-0.35 mm, sperm a­
tangia in patches, no axial cortical filaments, and
T- or L-shaped ray cells closely applied to the
outer cortex (Atkinson 1904, and this study). In
a later paper, Atkinson ( 1931) suggested that L.
borealis may be a variety or the same as L. rigida,
based on scattered carposporophytes throughout
the gametophyte. Although these two species do
have this trait and have an internal structure in
common, they differ in stalking, size and branch=
ing. The topotypes of L. rigida are characterized
by a stalk (qualitative observation), a mean length
of 19.4 cm (n
3) and 20.6 cm (n
9), 100%
and 89% branched plants per population and 148 branches per plant (Table 4). Therefore, L.
borealis and L. rigida are considered to be sep­
arate entities.
GROUP B: Group B is unlike any of the types
measured (Tables 2-4). However, it closely re­
sembles the description of L. fluviatilis given by
Sirodot (1872, pp. 70, 7 1) and a Sirodot type
specimen of L. fluviatilis from Ruisseau de Beau­
fort, France, measured during this study (Table
4). A drawing and description by Dillenius ( 1741,
p. 39 & fig. 47) are all that remain of the original
material of Conferva fluviatilis Linnaeus. Few
distinguishing characteristics are shown in the
drawing or given in the description, so that this
material is of little taxonomic value. Rather, it
appears that current concepts of this species are
based on the detailed descriptions ofSirodot (At­
kinson 1890; Israelson 1942; Starmach 1977) and
this description and a Sirodot specimen are also
used here. The specimen is stalked (qualitative
=
=
175
Vis and Sheath: Lemaneaceae systematics
observation), little branched (2C% branched
plants per population and one branch per plant),
and has an internal structure of a central axis
with no cortical filaments and T - or L-shaped
ray cells closely applied to the outer cortex. In
addition, Sirodot (1 872, p. 71) states that the
spermatangia occur in patches. From the speci­
men and description,Group B is recognized as
L. fluviatilis. Other features ofthe species include
a mean population length of 2.8-11.2 cm and a
mean width of 0.33-0.67 mm.
GROUP c: The features ofGroup C closely match
those of the holotype and an additional Bory
herbarium specimen of L. Jucina (Tables 2-4).
The internal structure consists of a central axis
without cortical filaments and T- or L-shaped
ray cells closely applied to the outer cortex. The
spermatangia of Group C and the additional
specimen occur in patches (SPD/ND :s 0.4) and
the patch size for this specimen is in the range
of Group C. The holotype,additional specimen
of L. Jucina and Group C are very branched
( � 56%). However,the additional specimen of L.
Jucina is significantly longer (12.6-20.0 cm) than
Group C (5.2-7.1 cm) (n
10, P < 0.05), and
the holotype is also longer (22.0 cm). Hence,we
propose a new variety of this species,L. Jucina
var. parva var. nov. (Fig. 8), which is formally
described below.
GROUP D: The diagnostic features of Group D
are like those measured for the holotypes of L.
nodosa, L. catenata and the para type of L. pleo­
carpa (Tables 2-4). The central axis has cortical
filaments and the ray cells are simple,not abut­
ting the outer cortex. The plants are un stalked
(ID/STD :s 1.2) and unbranched. Group D and
L. nodosa do not differ significantly in length and
width (n 25, P < 0.05). The mean length (� 8.4
cm) of L. catenata is in the range of L. nodosa
and Group D,but cannot be statistically tested
with those populations. The measured mean
length of L. pleocarpa is � 1 4.8 cm. However,
Atkinson (1 93 1 , p. 2 3 6), in his original descrip­
tion,states that the length is 8-20 cm,spanning
the range of the other populations. The width of
Group D does not differ statistically from that
of L. nodosa and L. catenata (n
7, P < 0.05).
The width of L. pleocarpa is significantly larger
than that of the other populations (n
7, P <
0.05). The ND/ID ratio does not differ statisti­
cally among Group D and the type specimens (n
7, P < 0.05). Both Group D and L. catenata
have spermatangia in rings (SPD/ND 1). Con­
sequently,it is proposed that L. nodosa, L. ca=
=
=
=
=
=
tenata and L. pleocarpa be treated as one species,
for which the oldest name is Lemanea catenata,
and Group D then refers to this species. How­
ever,the basic structure of Lemanea catenata is
that of the genus Paralemanea, and transfer to
this genus is proposed below. The diagnostic fea­
tures of Paralemanea catenata (Kiitzing) comb.
nov. are a central axis with cortical filaments,a
simple ray cell not abutting the outer cortex,
spermatangia in nodal rings and plant popula­
tions of mean length 8.0 to > 14.8 cm and mean
width 0.69-0.93 mm.
GROUP E: Group E is similar to the holotypes
of L. annulata and L. grandis and the lectotype
and topotype of L. australis (Tables 2-4). Group
E and the type specimens have a central axis with
cortical filaments and simple ray cells not abut­
ting the outer cortex,which is characteristic of
the genus Paralemanea, and it is proposed that
these entities are placed in this genus. In addi­
tion, the plants are unstalked (lD/STD :s 1.2)
and unbranched. The lengths of Group E, L. an­
nulata and the topotype of L. australis do not
differ significantly (n
5, P < 0.05). Although
the length of the type specimen of L. grandis
could not be measured,Atkinson (1 93 1 , p. 235)
states that this species was 4-6 cm in length,well
within those values for the group. The width of
all the types is within the range of Group E, and
the lectotype and topotype of L. australis are not
significantly different from that of populations
#48 and 50, and the holotypes of L. annulata
and L. grandis are not statistically different from
populations #50 and 54 (n
7, P < 0.05). The
spermatangia of Group E, L. annulata and the
lectotype of L. australis occur in rings (SPD/ND
� 0.9) and Duncan's test shows no significant
difference in SPP among these plants (n
7, P
< 0.05). Consequently, it is proposed that L.
annulata, L. grandis and L. australis be treated
as one species,for which the oldest name is Le­
manea annulata. Paralemanea annulata (Kiitz­
ing) comb. nov. is characterized by axial cortical
filaments,simple ray cells not abutting the outer
cortex, spermatangia in nodal rings and un­
stalked plants with mean population length 3 . 1 5.3 cm and mean width 0.43-0.63 mm.
GROUP F: Group F is the topotype of L. Jeld­
mannii and is similar to the holotype of L. mex­
icana in many diagnostic features (Tables 3 and
4). Both populations have a corticated central
axis with simple ray cells that do not abut the
outer cortex,as in the genus Paralemanea, and
are unstalked (ID/STD :s 1 .1). The width and
=
=
=
176
Phycologia, Vol. 31 (2),1992
ND/ID are not significantly different (n
25,P
< 0.05). The topotype of L. feldmannii is longer
than that of L. mexicana (n
25, P < 0.05).
These two populations have the same whorled
branching pattern, and both are reported from
Mexico only, geographically disjunct from the
other Lemaneaceae populations (Kiitzing 1857;
Sanchez-Rodriguez & Huerta 1 969). Therefore,
it is proposed that Lemanea feldmannii and L.
mexicana be treated as one species, with the lat­
ter being the oldest name. Paralemanea mexi­
cana (Kiitzing) comb. nov. is characterized by
the features of axial cortical filaments, simple ray
cells not abutting the outer cortex, unstalked
plants, of length 3.6-11.4 cm and width 0.290.62 mm, and a whorled branch and rebranching
pattern.
=
=
Other specimens examined
The other populations collected in the survey are
identified using the diagnostic features of the spe­
cies (Table I). Populations #8, 61, 62, and 64
belong to L. borealis. Added to L. jluviatilis are
populations #13,17,20,21 ,24,30,36,38,46,
52 and 58. Populations #24, 25,41,part of 42,
44,49 and 51 have similar internal structure and
no branching, like P. catenata and P. annulata.
However, only populations #24, 25,part of 42
and 44 could be placed with certainty in P. an­
nulata on the basis of mean width (0.38-0.61
mm) (n
25,P < 0.05).
=
Ecology and distribution
There is overlap among species in all ofthe stream
parameters (Table I), and no conclusive state­
ments can be made regarding the separation of
groups based on these features. M ost populations
occur in cool waters (x
1 3°C),which is typical
of the Lemaneaceae in other parts of the world
(summarized by Sheath & Hambrook 1 990). Le­
manea borealis and L. jluviatilis have the widest
ranges of distribution, which could be due to a
greater tolerance of conditions, but is probably
due to the larger number of populations ana­
lysed. H owever, the geographical distribution of
the populations collected suggests that there are
some differences in distribution of the genera and
species (Fig. 1). The genus Lemanea appears to
have a more northern distribution, being con­
centrated in the northern U.S.A., Canada and
Greenland, whereas most of the populations of
=
Paralemanea are from south-eastern U.S.A. and
northern California. Lemanea borealis is found
primarily in the north, ranging from the north
slope of Alaska to Oregon in the west, and from
western Greenland to central Quebec in the east.
Palmer (1 945) also described a similar entity from
Colorado and Utah. Atkinson (1931) reported
this entity from a number of locations through­
out North America, but he does not use all the
diagnostic features for identification. The distri­
bution ofL. jluviatilis is from south-central Alas­
ka to northern California in the west, extending
into the range of L. borealis. In the east, these
groups do not appear to coexist with L. jluviatilis,
being confined to lower latitudes from southern
Ontario to North Carolina. Other reports of L.
jluviatilis have been from New Jersey, South Car­
olina, Alabama and California by Wolle (1887),
Ontario by Palmer (1945) and Oregon by Atkin­
son (1931). Two of the populations of L. fucina
var. parva are from south-central U.S.A., geo­
graphically disjunct from the populations of L.
borealis and L. jluviatilis, but the third is from
New Hampshire, well within the range of L. jlu­
viatilis. No populations of L. fucina var. parva
occur in the west. There have been many pub­
lished accounts of L. fucina from Vermont and
New Hampshire (Flint 1947),Wisconsin (Pres­
cott 1962),and North Carolina and Massachu­
setts (Atkinson 1931 ). However, it is unclear from
the descriptions whether these populations are
L. fucina, L. fucina var. parva or L. jluviatilis.
The holotype and paratype ofL. pleocarpa, which
is synonymous with Paralemanea catenata, were
collected in Kentucky (Atkinson 1 931 ). Both P.
catenata and P. annulata can be found in Indi­
ana, but the latter species is also found in Cali­
fornia, Arkansas, West Virginia and North Car­
olina. Flint (1 947) reported the same alga (as L.
australis) from Vermont, Alabama and New
Hampshire, and noted that it seems to be com­
mon in the south-eastern U.S.A., but less com­
mon in the north-eastern U.S.A. Atkinson (1 931 )
reported this species (as L. australis) from North
Carolina, South Carolina, Maryland, West Vir­
ginia, Georgia and Mississippi, from Pennsyl­
vania and Maryland (as L. grandis) and from
California, Indiana, Nevada, Oregon and Wash­
ington (as L. annulata). The distribution of P.
annulata appears to extend to the edge of the
ranges of L. borealis, L. jluviatilis, L. fucina var.
parva and P. catenata. Paralemanea mexicana
seems to be localized in central Mexico, geo-
Vis and Sheath: Lemaneaceae systematics
graphically disjunct from the other species of the
Lemaneaceae.
TAXONOMIC PROPOSALS AND
REVISED DESCRIPTIONS
Lemaneaceae e. Agardh, Species A lgarum 2: 1 .
1828 ('[Ordo] Lemanieae'). Lemanea Bory, An­
nales de Museum d'Histoire Naturelle de Paris
12: 178, 1808.
Lemaneafluviatilis (Linnaeus) e.
Agardh (Lemanea corallina Bory, nom. illeg.).
DESCRIPTION: Spermatangial sori in patches;
internal structure of a central axis without cor­
tical filaments and T- or L-shaped ray cells close­
ly applied to outer cortex.
TYPE SPECIES:
Lemanea fluviatilis (Linnaeus) e. Agardh, Dis­
positio algarum sueciae, p. 25, 1 8 1 1 .
Conferva fluviatilis Linnaeus, Spe­
cies Plantarum, p. 1 1 65, 1753.
HETEROTYPIC S YN
ONYM:
Sacheria fluviatilis
Sirodot, Annales des Sciences Naturelles Series
5 Botanique 16: 70, 1 872.
BASIO
NY
M:
Lemanea borealis Atkinson, Torreya 4: 26, 1904
Lemanea fucina var. parva var. nov.
DIAGNOSIS: Plantae 2.9-7.1 cm alta, 0.34-0.67 mm
latis cum stipes, rami multi (0-18) (it = 6), panni
spermatangifera in nodi. Axis nuda in centro. Cel­
lulae radia cum forma T aut forma L, contiguus
cortex.
DESCRIPTION: Plants 2.9-7.1 cm long, 0.3�.67
mm in diameter, stalked and very branched (018) (x
6). Spermatangia in circular patches on
nodes. Internal structure consisting of a central
axis without cortical filaments and T- or L-shaped
ray cells applied to the outer cortex.
HOLOTYPUS: R.O. Sheath, specimen #NH5.
Concheco River crossing Route 16, 0.2 km north
of Rochester, New Hampshire (43°18'N, 7 1 °W).
Stream segment characteristics: 6.8 m maximum
width, 41 cm maximum depth, 60 cm S-I mean
current velocity, 1YC, 7.7 pH, 210 /-LS cm- I spe­
cific conductance, colourless water. Collected by
R.O. Sheath and M. Koske, 26.v.1989. UBC
A8264.
ADDITIONAL SPECIMENS: R.O. Sheath, speci­
men #AR5. In a river at the junction of Route
71 and 270, 4.6 km east of Polk Co., Arkansas.
=
177
Collected by R.O. Sheath and D. Kaczmarczyk,
25.iii.1 989; R.O. Sheath, specimen #OK I . In a
river crossing Route 59 east of Page, Arkansas,
4.8 km east of Route 259. Collected by R.O.
Sheath and D. Kaczmarczyk, 25.iii.1989. De­
posited in NFLD.
Paralemanea (P. e . Silva) stat. nov.
BASIO NY
M : Lemanea subg. Paralemanea P.e.
Silva, Taxon 8: 62, 1959.
TYPE SPECIES: Paralemanea catenata (Kiitzing)
comb. nov. ( Lemanea nodosa Kiitzing, Species
algarum p. 528, 1849).
DESCRIPTION: Spermatangial sori in rings
around nodes; internal structure of cortical fila­
ments around central axis and simple ray cells
not abutting the outer cortex.
SPECIES: as follows.
=
Paralemanea catenata (Kiitzing) comb. nov.
BASIO NY
M : Lemanea catenata Kiitzing, Phy­
cologia germanica p. 261 , 1845.
HETEROTYPIC SYNONYMS: Lemanea nodosa
Kiitzing, Species Algarum p. 528, 1849; Lema­
nea pleocarpa Atkinson, Botanical Gazette 42:
236, 1931.
DESCRIPTION: Un stalked, unbranched plants;
mean length � 8 cm and mean width � 0.7 mm.
Paralemanea annulata (Kiitzing) comb. nov.
BASJO NY
M : Lemanea annulata Kiitzing, Phy­
cologia germanica p. 261, 1 845.
HETEROTYPIC S YN
ONYMS: Lemanea australis
Atkinson, Annales 0/ Botany 4: 2 1 8, 1 890; En­
tothrix grandis Wolle, Bulletin o/the Torrey Bo­
tanical Club 6: 183, 1 87 7 . Lemanea grandis
(Wolle) Atkinson, Botanical Gazette 14: 292,
1 889.
DESCRIPTION: Unstalked, unbranched plants;
mean length c. 3.1 -5.3 cm and mean width ""
0.43-0.63 mm.
Paralemanea mexicana (Kiitzing) comb. nov.
BASIO NY
M : Lemanea mexicana Kiitzing, Ta­
bulae phycologicae oder A bbildungen der Tange
7: 34, 1 857.
HETEROTYPIC S YN
O NY
M : Lemanea /eldmannii
Sanchez-Rodriguez et Huerta, Ciencia (Mexico)
27: 27, 1969.
DESCRIPTION: Un stalked plants with many
whorled branches.
178
Phycologia, Vol. 31 (2), 1 992
Representative specimens of each infrageneric
taxon are deposited in NFLD.
greatly appreciated. Financial support was made
available by the University of Rhode Island Bot­
any Department and by N.S.F. Grant No.
BRS8906986 to RGS.
SYNOPTIC KEY OF THE
LEMANEACEAE IN NORTH AMERICA
( I) Central axis without cortical filaments;
(I)
ray cells T - or L-shaped, closely applied
to the outer cortex; spermatangia in
patches on nodes; plants stalked or un­
stalked . . . . . . . . . . . . . . . . . . . (Lemanea) (2)
Central axis with cortical filaments; ray
cells simple, not abutting the outer cor­
tex; spermatangia in rings on nodes;
plants un stalked . . . . . . . (Paralemanea) (4)
(2) Plants unstalked, seldom branched,
width < 0.4 mm . . . . . . . . . L. borealis
(2) Plants stalked, little to much
branched, width > 0.3 mm . . . . . . (3)
Few plants per population branched «
50%); if branched usually .::0; 4 branches
per plant . . . . . . . . . . . . . . . . . . . L. fluviatilis
Many plants per population branched ( >
50%); i f branched usually > 4 branches
per plant . . . . . . . . . . . . L. jucina var. parva
(4) Plants with many branches usually
in rebranching whorls . . . . P. mexicana
(4) Plants unbranched . . . . . . . . . . . . . . (5)
Plants small; mean length < 6 cm and
mean width < 0.7 mm . . . . . . . P. annulata
Plants large; mean length 2: 8 cm and
mean width 2: 0 .7 mm . . . . . . . . P. catenata
.
(3)
(3)
(5)
(5)
ACKNOWLEDGEMENTS
The authors would like to express their sincere
thanks to Tim Entwisle, Paul Hargraves, Marilyn
Harlin, James HeItshe, Orlando Necchi Junior
and Paul Silva for their critical comments on the
manuscript. We would also like to acknowledge
the following individuals who contributed or as­
sisted with the collection of specimens: JoAnn
Burkholder, Paul Catling, Roy Coomans, Julie
Hambrook, Beverly Hymes, Donald Kaczmar­
czyk, Mary Koske, Mary Morison and Katherine
Van Alstyne. Type specimens were generously
provided by The New York Botanical Gardens,
L.H. Bailey Hortorium, Rijksherbarium, Mu­
seum National d'Histoire Naturelle (Laboratoire
de Cryptogamie), Universite de Rennes (Labora­
toire de Botanique) and the Herbarium of the
University of Michigan. Assistance with prepa­
ration of this manuscript from Glen Thursby is
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STOERMER
Accepted 25 September 1991