A new macroscopic riverine red algal species,
Lemanea manipurensis
sp. nov. (Batrachospermales) is described from Manipur in northeast India. It has a sparsely branched, pseudoparenchymatous thallus with a single, central axial filament that lacks cortical filaments. Spermatangia occur generally in isolated, low and indistinct patches or form an almost continuous ring around the axis. Carposporophytes project into the hollow thallus cavity without an ostiole. The most striking morphological feature is the carposporophyte with very short gonimoblast filaments having cylindrical, narrow and sparsely branched sterile filaments, the terminal cell of each branch with a single, large, elongate carpospore. The widely distributed
L. fluviatilis
has spherical carpospores in long branched chains. Phylogenetic analysis of
rbc
L sequence data and comparison with other Batrachospermales clearly show that our specimens do not align with other species of
Lemanea
and
Paralemanea
investigated thus far. Five specific names attributed in previous literature (1973-2014) to
Lemanea
from Manipur,
L. australis, L. catenata, L. fluviatilis, L. mamillosa
, and
L. torulosa
are rejected until critical anatomical and molecular evidence is available for specimens from the Manipur river systems. Taxa referable to
Paralemanea
were not confirmed for India in this study. In view of the high demand for food and medical uses of
L.manipu rensis
in northeast India, conservation measures are needed for its long term survival. The present paper constitutes the first combined morphological / molecular study on a freshwater red alga from India.
INTRODUCTION
The red algae occur widely in marine habitats and less commonly in terrestrial and freshwater habitats as unicellular, colonial, simple filamentous, flat-bladed and more complex pseudo-parenchymatous forms with quite varied reproductive patterns. The order Batrachospermales is an exclusively freshwater group comprised of three distinct evolutionary lineages, all with uniaxial shoots, pseudoparenchymatous morphologies. The molecular phylogeny and classification are somewhat controversial. The order includes two families, Batrachospermaceae with 6 genera (
Batrachospermum, Nothocladus, Petrohua, Psilosiphon, Sirodotia
and
Tuomeya
) and Lemaneaceae with two genera [
Lemanea
Bory (1808)
and
Paralemanea
(Silva) Vis and Sheath (
Vis and Sheath 1992
)].
Lemanea
and
Paralemanea
occur in boreal to warm temperate regions of the northern hemisphere (
Vis and Sheath 1992
,
Eloranta and Kwandrans 2007
) with a single record of
Paralemanea
in the southern hemisphere from Brazil (
Necchi and Zucchi 1995
).
Petrohua
Saunders (in
Vis et al. 2007
), a
Lemanea
-like monotypic genus from Chile, has structural and reproductive features similar to Lemaneaceae but differs molecularly.
Psilosiphon
, a monotypic genus from Australia (
Entwisle 1989
), is related t othese other genera and was placed previously in its own family, Psilosiphonaceae (
Sheath et al. 1996
,
Vis et al. 1998
), but currently is placed in the family Batrachospermaceae (
Entwisle et al. 2009
).
Khan (1973)
was the first to report a member of the Lemaneaceae (
Lemanea mamillosa
Kützing) in the Indian subcontinent. Among the approximately 70 taxonomic entities distributed in 19-20 genera of non-marine red algae recorded in India,
Lemanea
has been reported for more than 4 decades (1973-2015) under 5 specific epithets (
Ganesan and West 2013
,
2013
). Judging from the descriptions and figures for
Lemanea
plants in India and comparing them with current literature, the generic disposition and specific identities of these Indian records are problematic.
The precise taxonomic identity of the Indian
Lemanea
specimens is relevant in view of their various uses: 1) as an edible alga (called Nungsham-“hair of stones”) (
Fig. 1A
) collected in rivers of Manipur and sold fresh in local markets (
Fig. 1B
) and in dried packets (
Fig. 1C
) also sold on the internet, 2) medical uses (
Bhosale et al. 2012
) by numerous tribal populations of the remote northeast states of India, and 3) potential for biofuels (
Rout et al. 2011
). Based on freshly collected material (
Fig. 1A
) from Manipur state, we presented preliminary morphological observations on this entity (
Ganesan and West 2013
). Manipur (
Fig. 1D
) is in the Indo-Burma Biodiversity Hotspot region and requires more extensive sampling. The previous morphological observations are supported here with molecular
rbc
L data to show that these Manipur specimens belong to the genus
Lemanea
and represent a new species.
(A) Lemanea manipurensis growing on stones from Chakpi River. (B) Woman selling freshly collected Lemanea (Nungsham) at a market in Manipur. (C) Packet (100 g) of dried Nungsham for sale on the internet (20 rupees). (D) Map of NE India showing Manipur and other states in the Indo-Burma Biodiversity Hotspot region. Scale bar represents: A, 5 mm.
MATERIALS AND METHODS
Lemanea
specimens were collected by J. Rout and M. Thajamandhi in the Chakpi River, Thoubal district, Imphal, Manipur, India on December 23, 2013. For morphological studies, the materials were preserved in 4% formalin, voucher specimens were mounted on herbarium paper and specimens for molecular analyses were blotted dry with tissue and placed in small snap lock plastic bags containing silica gel beads.
For microscopic observations a mounting medium including stain was prepared as 0.02% aniline blue WS in 50% corn syrup and 0.5% phenol (to prevent contamination by bacteria and fungi). Surface views and cross sections were prepared on a microscope slide, removing water carefully with blotting paper, adding a drop of mounting medium and arranging the specimens with a fine needle and forcep tip. The medium was stirred gently to allow good penetration of the stain without disrupting the sections. The material was allowed to absorb the stain for about thirty minutes. A cover slip was then gently placed on the slide. After 1-2 days each slide was sealed with a clear fingernail polish to prevent the medium from drying and receding under the cover slip margins. Photographs were taken with a Zeiss binocular research compound microscope (Carl Zeiss, Jena, Germany) and Canon G3 camera (Canon, Tokyo, Japan). The holotype photo (
Fig. 2A
) was taken with a Canon G10 camera. Photographic plates were made using Adobe Photoshop CS4.
Lemanea manipurensis E. K. Ganesan, J. A. West, Zuccarello et J. Rout sp. nov. Specimens for B-D lightly stained with aniline blue. (A) Holotype. Dried thallus showing natural colour, minimal branching and elongate basal stolon. (B) Slightly squashed apical sector of branch showing the outer cell layers and central axial filament. (C) Slightly squashed midsection of branch showing the axial filament devoid of cortical filaments. (D) Cross section of branch showing the four basal cells of the outer whorl branchlets at a node. Scale bars represent: A, 5 mm; B & C, 30 μm; D, 20 μm.
Total DNA was isolated from silica gel-dried material using a modified CTAB procedure (
Zuccarello and Lokhorst 2005
). Amplification and sequencing of the plastid-encoded large subunit of the ribulose bisphosphate carboxylase / oxygenase gene (
rbc
L) used amplification primers presented in
Freshwater and Rueness (1994)
(F8-R753, F577-rbcL-st). Amplified products were checked for correct length (approximate 1,000 bp length), purity and yield on 1% agarose gels. Polymerase chain reaction products were cleaned using ExoSAP-IT (USB, Cleveland, OH, USA) and commercially sequenced (Macrogen Inc., Daejeon, Korea). The outgroups used were
Thorea
and
Nemalionopsis
of the sister order Thoreales (
Müller et al. 2002
,
Johnston et al. 2014
).
Sequences were edited, assembled and aligned using the Geneious software package (Biomatters, available from
http://www.geneious.com/
). Alignment was straight forward as no gaps were found in the data set. The program jModeltest version 2 (
Darriba et al. 2012
) was used to find the model of sequence evolution. Maximum likelihood (ML) was performed with RAxML 7.2.8 (
Stamatakis 2006
). RAxML was performed with all threes codons partitioned and the GTR + gamma model and 500 non-parametric bootstrap replicates.
Bayesian inference was performed with MrBayes v3.1.2 (
Ronquist and Huelsenbeck 2003
). Analyses consisted of two independent simultaneous runs of one cold and three incrementally heated chains, and 3 × 10
6
generations with sampling every 1,000 generations. Codons were partitioned. The log files of the runs were checked with Tracer v1.5 (
Rambaut and Drummond 2007
) and a burn-in sample of 100 trees was removed from each run before calculating the majority rule consensus tree.
RESULTS
Our results indicate that the species collected in the Chakpi River is a new species of
Lemanea
that we describe here.
- Lemanea manipurensisE. K. Ganesan, J. A. West, Zuccarello et J. Rout sp. nov.
Diagnosis.
Plants to 10 cm long, growing in clusters on stones, green to dark purple, with or without a basal constriction to form a stalk, shoots to 650 µm diam., with sparse irregular branching in the lowermost region of the erect shoots (
Figs 1A
&
2A
), ultimate branches with attenuated apices (
Fig. 2B
); basal
Chantransia
phase sometimes evident; hair cells absent, four ray cells of a single type formed at right angles on each cell of the single central axial filament (
Fig. 2C
&
D
), internal corticating filaments lacking (
Fig. 2C
); outer cortex cells cylindrical, compact (7-9 µm diam. × 11-12 µm long) in side view, irregular to quadrate shape in surface view (
Fig. 1B
&
C
); monoecious, spermatangia (3-5 µm diam. × 10-12 µm long) in irregular sub-prominent patches or incomplete irregularly shaped rings (to 130 µm wide) around the axial nodes (
Fig. 3A
-
C
); carposporophytes projecting into the thallus cavity, gonimoblast filaments short and simple to repeatedly branched (
Fig. 3D
-
G
), each terminal cell forming a single, large, elongate cylindrical carpospore with round ends, 38-54 µm diam. and 85-115 µm long, filled with abundant, colourless spheres (3-5 µm diam.) and a prominent central nucleus (
Fig. 3F
). There is no ostiole opening (
Fig. 3D
) for carpospore release so presumably release occurs when the gametophyte disintegrates.
Lemanea manipurensis E. K. Ganesan, J. A. West, Zuccarello et J. Rout sp. nov. All specimens lightly stained with aniline blue. (A) Small spermatangial patches around an old branch perimeter. (B) Spermatangial patches extend almost continuously around a young branch perimeter. (C) Branch cross section with small spermatangial patch erumpent on outer cortex. (D) Cross section with carposporophytes projecting into the hollow branch center. (E) Surface view of several carposporophytes in a whorl projecting inwardly. (F) Single carpospores terminal on carposporophyte branches. Numerous small colourless spherical bodies (arrowheads) and central nucleus (arrows) visible in each carpospore. (G) Individual carposporophyte removed from thallus to show repeated branching and terminal carpospores. Scale bars represent: A, 65 μm; B, 25 μm; C, 100 μm; D-G, 40 μm.
The holotype specimen is deposited in the Royal Botanic Gardens Melbourne, National Herbarium of Victoria, Australia (MEL 2381649). Isotype specimens are also deposited in the University of Michigan Herbarium (MICH 1210723) and University / Jepson Herbaria, University of California, Berkeley (UC / JEPS). Specimens (
Figs 1A
&
2A
) were collected December 23, 2013, near Chakpi village on the Chakpi River (24°16′ N, 93°52′ E) growing profusely on stones at 755 m above sea level (water temperature was 14℃ at the time of collection). The river flows through the villages of Serou and Sugnu in the Thoubal district, 75 km from the capital city Imphal of Manipur state.
L. manipurensis
is probably more widespread in Manipur river systems, but more sampling is needed to confirm this. The species is named for the state of Manipur, the only location in India where
Lemanea
is currently known.
Phylogenetic analysis.
The phylogenetic tree (
Fig. 4
) of the Batrachospermales and Thoreales using
rbc
L gene sequences clearly shows a monophyletic Lemaneaceae, including both
Lemanea
and
Paralemanea
. The phylogeny reveals that
L. manipurensis
is molecularly distinct and in a sister lineage to other
Lemanea
samples accessed from Genbank, with weak support (ML BP 68). The
rbc
L phylogeny shows great genetic variation in the genus
Lemanea
and the most commonly sequenced species (
L. fluviatilis
) is not monophyletic based on that species name assigned to nucleotides in Genbank.
Maximum-likelihood topology, created in RAxML, of rbcL sequence data of the Batrachospermales. Support values at each node are bootstrap values from RAxML (left) and Bayesian posterior probability (right). Asterisk (*) indicates strong support (≥95%, ≥0.95) in all analyses. Outgroups were Thorea and Nemalionopsis (Thoreales). B., Batrachospermum.
GenBank accession number.
KP407869.
DISCUSSION
Morphologically the specimens we examined clearly belong to the genus
Lemanea
(
Table 1
).
Diagnostic differences betweenLemaneaandParalemanea
Based on Vis and Sheath (1992), Sheath et al. (1996, 2006), Carmona Jimenez and Necchi (2002), Kumano (2002), Mannino et al. (2003), Sheath (2003), Kučera and Marvan (2004), Xie et al. (2004), Eloranta and Kwandrans (2007), Kučera et al. (2008), Eloranta et al. (2011) (compare however with Kučera and Marvan 2004, p. 168, Fig. 3A-D), Sheath and Sherwood (2011).
Among the approximately 19-20 non-marine red algal genera known hitherto from the Indian sub-continent (
Ganesan and West 2013
,
2013
),
Lemanea
is reported only from Manipur state, and occurs mostly during the colder months (December to February) when harvesting, drying and packaging are done for sale in local markets and online stores (
Fig. 1A
-
C
) as food and for ethnobotanical / medical uses (
Bhosale et al. 2012
). Manipur state is located at elevations of 50-3,300 m above sea level) and has various rivers, of which the Chakpi, Imphal, Iril, Manipur and Thoubal are well known (24°16′ N, 93°52′ E) (
Singh and Gupta 2014
, Fig. 1).
Lemanea
specimens have been collected and reported from all five rivers (
Singh and Gupta 2010
,
2010
,
2011
,
Gupta and Singh 2012
). Critical observations on the anatomical and reproductive details, supplemented by molecular sequences data are lacking for specimens collected here. Five different specific names, i.e.,
L. australis
Atkinson [now
Paralemanea grandis
(Wolle) Kumano],
L. catenata
Kützing [now
Paralemanea catenata
(Kützing) M. Vis et R. Sheath],
L. fluviatilis
(Linneaus) C. Agardh,
L. mamillosa
Kützing, and
L. torulosa
Sirodot have been assigned during more than four decades (1973-2015) for the Indian
Lemanea
/
Paralemanea
populations (
Table 2
).
Synopsis of references (1973-2014) for the five specific epithets applied toLemaneaplants from Manipur State
aLemanea australis: A taxonomic synonym of Paralemanea grandis (Wolle) Kumano. bL. catenata: A taxonomic synonym of Paralemanea catenata (Kutzing) Vis et Sheath. cL. mamillosa: A species of Lemanea with entirely different set of features morphologically quite distinct from L. fluviatilis. dL. torulosa: A taxonomic synonym of Paralemanea torulosa (Roth) Sheath and Sherwood (see for more details, Vis and Sheath 1992, Kumano 2002, Eloranta et al. 2011, Guiry and Guiry 2015). NA, not available.
We believe the binomial
L. mamillosa
was misapplied by
Khan (1973)
. He said “from the outer ends of the T shaped cells, ascending and descending lateral filaments were formed.” More importantly,
Khan (1973
, p. 173, Fig. B) misjudged large carpospores with numerous, small, colourless spheres and a large central nucleus as spermatangia.
Deb et al. (1986)
questioned Khan’s identification of
L. mamillosa
and referred their specimens to
L. australis
. A careful analysis of the description and figures by
Deb et al. (1986)
also raised serious doubts about the taxonomic identity of specimens they examined. The central axial filament was covered by slender descending corticating filaments, two types of ray cells were seen and the outermost cortex with spermatangial nodal rings that are features of
Paralemanea
(
Deb et al. 1986
, Pl. II, Fig. 2). They pointed out that the carpospores of the Indian material were comparatively larger (45-63 × 72-126 μm) than those of
L. australis
given by
Atkinson (1890)
for the North American specimens. Voucher specimens of Deb and others were stated to have been deposited at the Botanical Survey of India: “Sugnu, Feb 1971 & Dec 1973, Sh. Singh. S. n. (BSIS).” However, these were not traceable during our (EKG and JW) visit to the BSIS Herbarium, Kolkata, W. Bengal in November 2013. Sugnu is near where our specimens for the present study were collected.
Desikachary et al. (1990)
concluded, based on observations of
Deb et al. (1986)
, that they were
L. mamillosa
. The issue was further clouded by
Desikachary et al. (1990
, Fig. 20A-P) stating that several figures of North American
L. mamillosa
populations (
Mullahy 1952
, Figs 17-23 & 25-33) were similar to the Indian populations. Both sets of figures clearly show that axial filaments with many down-growing cortical filaments characteristic of
Paralemanea
.
Bhosale et al. (2012)
studied the morphology of abundant fresh material from the same general area as our present collection site (Chakpi River, Thoubal District) and concluded that the Indian specimens were misidentified earlier and that they should be referred to the widely distributed
Lemanea fluviatilis
. However, these authors failed to observe some critical anatomical and reproductive details, e.g., there is no mention or illustration to show if the axial filament is naked or surrounded by cortical filaments. More importantly, the nature of the mature carpospores in their studies (
Bhosale et al. 2012
, Fig. 2G) clearly showed a single, large and terminal carpospore on each gonimoblast branch which is in agreement with our specimens. In other words, the nature, shape and size of carpospores shown by
Bhosale et al. (2012)
are in sharp contrast to
L. fluviatilis
, where carpospores are generally spherical and in simple or branched chains (see
Sheath and Sherwood 2011
, Pl. 42E & F,
Guiry and Guiry 2015
). Identification as
L. fluviatilis
by
Bhosale et al. (2012)
was followed subsequently in other studies on biofuel production (
Rout et al. 2011
), nutrient content (
Singh and Gupta 2010
,
2010
), treatment of diabetes (
Devi 2011
), trace elements (
Bino-Devi et al. 2011
), biosynthesis of gold nanoparticles (
Sharma et al. 2014
) and anti-urolithiatic agent (
Mikawlrawng et al. 2014
).
Singh and Gupta (2010
,
2010
,
2011
,
2014)
and
Gupta and Singh (2012)
extensively studied the ecology of
Lemanea
populations and identified five different species. These are, in addition to
L. fluviatilis
from the Thoubal River, (1)
L. australis
, (2)
L. torulosa
from Manipur and Imphal Rivers, (3)
L. mamillosa
from Iril River, and (4)
L. catenata
from Iril River in the Manipur River systems. However, critical details on thallus anatomy and reproductive features were not provided.
Gupta and Singh (2012
, p. 23, Table 2) and
Singh and Gupta (2010
, p. 52, Table 2) further confused this issue showing in a comparative table that some populations had axial cortical filaments (
L. mamillosa
and
L. catenata
), while in others (
L. australis, L. torulosa
, and
L. fluviatilis
) these filaments were not shown. Also, excepting
L. fluviatilis
, all the other species had spermatangia in rings. The bionomial
L. catenata
was used throughout their studies but the present binomial is
Paralemanea catenata
(Kützing) Vis et Sheath. Most of their illustrations were habit views without anatomical details in illustrations i.e., with or without axial filaments in the 5 species they identified.
Singh and Gupta (2010a
, p. 54, Pl. 5b) illustrated “spermatangial sori in rings between the internodes” in
L. catenata
. These appear to be the large carpospores characteristic of
L. manipurensis
. Finally,
Deb et al. (1986)
,
Bhosale et al. (2012)
,
Gupta and Singh (2012)
, and
Singh and Gupta (2010)
did not provide appropriate magnification scales in their photographic and line-drawing illustrations. Many of the above identifications referred to species unknown in India and lacked photographic evidence of critical details.
Among the records of the
Lemanea
/
Paralemanea
species complex in countries neighbouring India,
Faridi (1971)
mentioned
Lemanea
and four other freshwater red algae,
Chroodactylon
(as
Asterocytis
),
Audouinella, Batrachospermum
, and
Compsopogon
, in a diagnostic key to the freshwater red algae of Pakistan. Later (
Faridi 1975
) mentioned
L. mamillosa
from Northwest frontier (Parachinar), but without description or illustration of the specimens he examined.
Nizamuddin (1988)
remarked that “Faridi’s collections are not available to make any comments on their occurrence in Pakistan.”
Xie et al. (2004)
studied 4 species of
Lemanea
and 2 species of
Paralemanea
from China.
Lemanea simplex
C. -C. Jao and
L. sinica
C. -C. Jao were described by
Jao (1941)
and
L. crassa
S. L. Xie et Z. X. Shi and
L. ramosa
S. L. Xie et Z. X. Shi were described by
Xie et al. (2004)
. Since there are no other reports of these species they may be endemic to different regions of China. The carposporophyte structure and carpospore shape and size of
L. simplex
and
L. sinica
are similar to those of
L. manipurensis
specimens. The specific differences between
L. manipurensis
and
L. sinica
are shown in
Table 3
. Except for thallus height and branching mode,
L. manipurensis
is remarkably similar to
L. sinica
although carpospore size is slightly larger. No other reports of
L. sinica
are known in China or elsewhere. Future molecular studies on
L. sinica
would undoubtedly reveal whether or not it differs from
L. manipurensis
. The type locality of
L. sinica
is Chun-tien, Yunnan (32°03′01″ N, 110°36′50″ E), while that of the Indian species is Chakpi, Thoubal district, Manipur (24°16′ N, 93°52′ E), perhaps not a very significant geographical distance but the many diverse river systems and mountain ranges between these localities may be formidable barriers for dispersal.
Synopsis of salient differences betweenLemanea manipurensissp. nov. andL. sinicaJao
Based on Jao (1941), Xie et al. (2004), Hu and Wei (2006), and the present study.
In the five Manipur river systems,
Lemanea
populations may be abundantly distributed in the different river segments. Hence the possibility of cryptic speciation among the different populations cannot be ruled out. Only critical molecular studies would clarify this point.
Lemanea
and
Paralemanea
are known to grow together in the same ecological habitat and there are instances where the same herbarium packet contained more than one species (
Palmer 1941
). Harvested material of
Lemanea
from different places and the processed dried packets sold in the local markets may be helpful on morphological and molecular bases in resolving whether
Paralemanea
species also occur in India.
Lemanea, Paralemanea, Petrohua
, and
Psilosiphon
species offer few reliable morphological characteristics to separate them at the generic level. As stated by
Sheath (2003
, pp. 208, 216 & 217) the presence or absence of axial filament cortication and the configuration of spermatangial rings or patches should be the most useful features in defining
Lemanea
and
Paralemanea
, but these 2 generic attributes apparently are not consistent, thus raising doubts about the generic status of
Paralemanea
as different from
Lemanea
. In any case molecular analyses in this and other published work suggest
Paralemanea
is paraphyletic leaving the issue unresolved.
The landmark publication by
Jao (1941)
on
L. sinica
is overlooked in many later publications on the Lemaneaceae.
Jao (1941
, p. 271, Pl. VII, Figs 50-52) described
L. sinica
specimens with “the antheridial bands are mostly in complete rings around the antheridial zones. In older portions of the thallus they are occasionally slightly interrupted but also kept a band-shape. Probably the interrupting is due to the hypertrophy of the tissue beneath the antheridial bands. In addition to the ordinary antheridial bands, small antheridial sori sometimes appear on the old carpogonial zones.”
Xie et al. (2004)
said in their
Lemanea
species key that
L. sinica
has “Spermatangia in perfect rings” but they did not obtain any new
L. sinica
specimens.
Hu and Wei (2006)
stated “the antheridia are always in well-defined bands” without further evidence.
Jao (1941)
clearly mentioned the “naked central axis” lacks cortical filaments and commented that it is a “peculiar combination of the characteristics of two genera” in
L. sinica
.
Kučera and Marvan (2004)
, in a taxonomic study of the Lemaneaceae in the Czech Republic, characterized
Lemanea
with a central axis with or without cortical filaments. According to them, “the regular formation of spermatangia in rings varies with age and the magnification used.” These variable features in spermatangial formation in their material of
L. fluviatilis
were also shown in illustrations (
Kučera and Marvan 2004
, p. 168, Fig. 3A-D,
Simić and Djordjević 2011
, p. 515).
Xie et al. (2004)
in their study of Chinese Lemaneaceae, mentioned that in
Paralemanea parvula
(Sirodot) S. L. Xie & Z. X. Shi, spermatangia are found in patches (
Xie et al. 2004
, p. 886, Fig. 13).
Eloranta et al. (2011
, p. 96) preferred to keep
P. parvula
in
Lemanea
as an uncertain species, but notably remarked that “spermatangial papillae form separate or sometimes coalescent tubercles.” Anatomical details, i.e., whether cortical filaments are present or not in
P. parvula
is not known in Chinese and European specimens.
Eloranta et al. (2011)
did not include the reference of
Xie et al. (2004)
. The above mentioned instances clearly show the ambiguity of using some anatomical and reproductive features to differentiate
Lemanea
and
Paralemanea
.
It is significant that the five species of
Lemanea
(
L. crassa, L. manipurensis, L. ramosa, L. simplex
, and
L. sinica
) from the Southeast Asian continent are remarkably similar, producing just a single and elongate terminal carpospore on each short simple to branched carposporophyte filament with narrow cylindrical cells. Most other species of
Lemanea
and
Paralemanea
produce spherical carpospores serially in simple or branched chains (catenate). Detailed and comparative morphological and molecular data would clarify whether this group of
Lemanea
species warrants segregation into a new genus, different from closely related genera like
Lemanea
,
Paralemanea
, and
Petrohua
. A case in point is that extensive molecular and morphological data on
Batrachospermum
species
sensu lato
resulted in the segregation of
Kumanoa
from
Batrachospermum
with spirally twisted carpogonial branches and axial carposporophytes (
Entwisle et al. 2009
) and
Sheathia
with hetero-corticated thalli, carpogonia on undifferentiated cells and exserted carposporophytes (
Salomaki et al. 2014
).
It is noteworthy that
Necchi et al. (2013)
found a very low genetic diversity between species of the two genera
Composopogon
and
Compsopogonopsis
(Compsopogonales, Rhodophyta) based on global sampling and molecular data. Species of these 2 genera were distinguished hitherto by
caeruleus
morphology (without cortication) for
Compsopogon
species and
leptoclados
morphology (with cortication) for
Compsopogonopsis
species.
Necchi et al. (2013)
concluded that only one genus,
Compsopogon
, can be recognized.
It is still too early to provide a complete molecular and morphological story concerning generic and species delimitations for
Lemanea
and
Paralemanea
.
Acknowledgements
Morgan Vis kindly provided a copy ofAtkinson (1890). Interlibrary loan facilities of the University of Melbourne, Michael Wynne and S. Tripathi obtained some early and recent literature not easily accessible to us. P. S. Yadava (Manipur University, Imphal) provided liquid preserved material and some information about the edible Nungsham sold in the local markets. Ms. M. Thajamandhi assisted J. Rout in field collections and processing of liquid preserved, herbarium and silica gel material for DNA extraction. Tim Entwisle provided very helpful advice on the manuscript before submission. Funding was provided mostly from the personal pensions of Ganesan and West.
Atkinson G. F.
1890
Monograph of the Lemaneaceae of the United States
Ann. Bot.
4
177 -
229
Bhosale R. A.
,
Chaugule B. B.
2010
Freshwater algae as potential source of polyunsaturated fatty acids: review
Int. J. Algae
12
335 -
356
Bhosale R.
,
Rout J.
,
Chaugule B.
2012
The ethnobotanical study of an edible freshwater red alga, Lemanea fluviatilis (L.) C. Ag. from Manipur, India
Ethnobot. Res. Appl.
10
69 -
76
Bino-Devi Ch.
,
Sharat Singh N. K.
,
Singh N. R.
,
Rajendro Singh N.
,
Sudarshan M.
,
Chakraborty A.
,
Ram S. S.
2011
Trace elements in Nungsham, the red edible algae of Manipur
Int. J. Appl. Biol. Pharm. Technol.
2
198 -
203
Bory de Saint-Vincent J. B.
1808
Mémoire sur le genre Lemanea de la famille des Conferves
Ann. Mus. Hist. Nat.
12
177 -
190
Carmona Jimenez J.
,
Necchi O.
2002
Taxonomy and distribution of Paralemanea (Lemaneaceae, Rhodophyta) in central Mexico
Cryptogam. Algol.
23
39 -
49
Darriba D.
,
Taboada G. L.
,
Doallo R.
,
Posada D.
2012
jModelTest 2: more models, new heuristics and parallel computing
Nature Methods
9
772 -
Deb D. B.
,
Krishna B.
,
Mukherjee M. K.
,
Bhattacharya S.
,
Chowdhury A. N.
,
Das H. B.
,
Singh S. T.
1974
An edible alga of Manipur (Lemanea australis): presence of silver
Curr. Sci.
43
629 -
Deb D. B.
,
Krishna B.
,
Singh S. T.
,
Desikachary T. V.
,
Raja Rao V. N.
1986
Taxonomy of Algae
University of Madras
Madras
Life history of a Lemanea species from Manipur
213 -
221
Desikachary T. V.
,
Krishnamurthy V.
,
Balakrishnan M. S.
1990
Rhodophyta. Vol. 1. Part II A
Madras Science Foundation
Madras
279 -
Devi A. P.
2011
Plants used by Meitei community of Manipur for the treatment of diabetes
Assam Univ. J. Sci. Technol. Biol. Environ. Sci.
7
63 -
66
Devi W. I.
,
Devi G. S.
,
Singh C. B.
2011
Traditional herbal medicine used for the treatment of diabetes in Manipur, India
Res. J. Pharm. Biol. Chem. Sci.
2
709 -
715
Eloranta P.
,
Kwandrans J.
2007
Freshwater red algae. Rhodophyta. Identification guide to European taxa, particularly to those found in Finland
Norrilinia
15
1 -
103
Eloranta P.
,
Kwandrans J.
,
Kusel-Fetzmann E.
,
Schagerl M.
2011
Süßwasserflora von Mitteleuropa Band 7. Freshwater Flora of Central Europe
Spectrum Akademischer Verlag
Heidelberg
Rhodophyceae and Phaeophyceae
1 -
155
Entwisle T. J.
1989
Psilosiphon scoparium gen. et sp. nov. (Lemaneaceae), a new red alga from south-eastern Australian streams
Phycologia
28
469 -
475
Entwisle T. J.
,
Vis M. L.
,
Chiasson W. B.
,
Necchi O. Jr.
,
Sherwood A. R.
2009
Systematics of the Batrachospermales (Rhodophyta): a synthesis
J. Phycol.
45
704 -
715
Faridi M. A. F.
1971
The genera of fresh-water algae of Pakistan and Kashmir
Biologia
12
123 -
142
Faridi M. A. F.
1975
Batrachospermum in Pakistan
Biologia
21
107 -
109
Freshwater D. W.
,
Rueness J.
1994
Phylogenetic relationships of some European Gelidium (Gelidiales, Rhodophyta) species, based on rbcL nucleotide sequence analysis
Phycologia
33
187 -
194
Ganesan E. K.
,
West J. A.
2013
Nomenclatural changes for some freshwater red algae from India
Algae
28
45 -
51
Ganesan E. K.
,
West J. A.
2013
On the identity of an edible macroscopic freshwater (riverine) red alga from Manipur, north-east India
National Conference on ”Frontiers in Algology and Algal Biotechnology” [NCFAAB]
Visva-Bharati University, Santiniketan
6 -
Guiry M. D.
,
Guiry G. M.
2015
AlgaeBase
World-wide electronic publication, National University of Ireland
Galway
Available from:
Gupta A.
,
Singh R. M.
2012
Lemanea in lotic environment of Manipur, North-East India: distribution, ecology and need for conservation of Lemanea
Lamhat Academic Publishing
Saarbrücken
80 -
Hu H.
,
Wei Y.
2006
The freshwater algae of China: systematics, taxonomy and ecology
Science Press
Beijing
1023 -
Jain A.
,
Roshnibala S.
,
Kanjilal P. B.
,
Singh R. S.
,
Singh H. B.
2007
Aquatic/semi-aquatic plants used in herbal remedies in the wetlands of Manipur, Northeastern India
Ind. J. Tradit. Knowl.
6
346 -
351
Jain A.
,
Sundriyal M.
,
Roshnibala S.
,
Kotoky R.
,
Kanjilal P. B.
,
Singh H. B.
,
Sundriyal R. C.
2011
Dietary use and conservation concern of edible wetland plants at Indo-Burma Hotspot: a case study from northeastern India
J. Ethnobiol. Ethnomed.
7
29 -
Jao C. C.
1941
Studies on the freshwater algae of China. VIII. A preliminary account of the Chinese freshwater Rhodophyceae
Sinensia
12
245 -
290
Johnston E. T.
,
Lim P. -E.
,
Buhari N.
,
Keil E. J.
,
Djawad M. I.
,
Vis M. L.
2014
Diversity of freshwater red algae (Rhodophyta) in Malaysia and Indonesia from morphological and molecular data
Phycologia
53
329 -
341
Khan M.
1973
On edible Lemanea Bory de St. Vincent, a fresh water red alga from India
Hydrobiologia
43
171 -
175
Kučera P.
,
Grulich V.
,
Fránková M.
,
Bureš P.
2008
Distribution of freshwater red algal family Lemaneaceae (Rhodophyta) in the Czech Republic: an update
Fottea
8
125 -
128
Kučera P.
,
Marvan P.
2004
Taxonomy and distribution of Lemanea and Paralemanea (Lemaneaceae, Rhodophyta) in the Czech Republic
Presilia (Praha)
76
163 -
174
Kumano S.
2002
Freshwater red algae of the world
Biopress Ltd.
Bristol
375 -
Mannino A. M.
,
Barone R.
,
Raimondo F. M.
2003
First record of Paralemanea catenata (Rhodophyta) from Italian Peninsula
Bocconea
16
1053 -
1058
Mao A. A.
,
Hynniewta T. M.
,
Sanjappa M.
2009
Plant wealth of northeast India with reference to ethnobotany
Indian J. Tradit. Knowl.
8
96 -
103
Mikawlrawng K.
,
Kumar S.
2014
Current scenario of urolithiasis and the use of medicinal plants as antiurolithiatic agents in Manipur (North East India): a review
Int. J. Herb. Med.
2
1 -
12
Mullahy J. H.
1952
The morphology and cytology of Lemanea australis Atk
Bull. Torrey Bot. Club
79
471 -
484
Muller K. M.
,
Sherwood A. R.
,
Pueschel C. M.
,
Gutell R. R.
,
Sheath R. G.
2002
A proposal for a new red algal order, the Thoreales
J. Phycol.
38
807 -
820
Necchi O.
,
Fo A. S. G.
,
Salomaki E. D.
,
West J. A.
,
Aboal M.
,
Vis M. L.
2013
Global sampling reveals low genetic diversity within Compsopogon (Compsopogonales, Rhodophyta)
Eur. J. Phycol.
48
152 -
162
Necchi O.
,
Zucchi M. R.
1995
Record of Paralemanea (Lemaneaceae, Rhodophyta) in South America
Algol. Stud.
78
33 -
38
Nizamuddin M.
1988
Occurrence of the genus Bangia Lyngbye (Bangiales, Rhodophyta) from Chitral, North West of Pakistan
Pak. J. Bot.
20
45 -
48
Palmer C. M.
1941
Lemanea herbarium packets containing more than one species
Butler Univ. Bot. Stud.
5
222 -
223
Rambaut A.
,
Drummond A. J.
2007
Tracer
Available from:
Ronquist F.
,
Huelsenbeck J. P.
2003
MrBayes 3: Bayesian phylogenetic inference under mixed models
Bioinformatics
19
1572 -
1574
Rout J.
,
Chaugule B.
,
Bhosale R.
,
Bhatnagar S. K.
,
Saxena A.
,
Krann S.
2011
Algae Biofuel
Stadium Press
New Delhi
Potential of a red alga, Lemanea for use as a source of biofuel
111 -
115
Salomaki E. D.
,
Kwandrans J.
,
Eloranta P.
,
Vis M. L.
2014
Molecular and morphological evidence for Sheathia gen. nov. (Batrachospermales, Rhodophyta) and three new species
J. Phycol.
50
526 -
542
Sharma B.
,
Purkayastha D. D.
,
Hazra S.
,
Thajamanbi M.
,
Bhattacharjee C. R.
,
Ghosh N. N.
,
Rout J.
2014
Biosynthesis of fluorescent gold nanoparticles using an edible freshwater red alga, Lemanea fluviatilis (L.) C. Ag., and antioxidant activity of biomatrix loaded nanoparticles
Bioprocess Biosyst. Eng.
37
2559 -
2565
Sheath R. G.
,
Wehr J. D.
,
Sheath R. G.
2003
Freshwater Algae of North America: Ecology and Classification
Academic Press
San Diego, CA
Red Algae
197 -
224
Sheath R. G.
,
Müller K. M.
,
Vis M. L.
,
Entwisle T. J.
1996
A re-examination of the morphology, ultrastructure and classification of genera in the Lemaneaceae (Batrachospermales, Rhodophyta)
Phycol. Res.
44
233 -
246
Sheath R. G.
,
Müller K.
,
Sherwood A.
,
Shea T.
,
Stekoll M. S.
2006
Phylogenetic relationships of members of the freshwater red algal family Lemaneaceae from North America, Europe and Africa
Phycological Society of America
Phycol. Soc. Am. 60th Annu. Meet. Northwest Algal Symp.
Juneau, AK
57 -
Sheath R. G.
,
Sherwood A. R.
,
John D. M.
,
Whitton B. A.
,
Brook A. J.
2011
The Freshwater Algal Flora of the British Isles. An Identification Guide to Freshwater and Terrestrial Algae
Cambridge University Press
Cambridge
159 -
180
Simić S.
,
Djordjević N.
2011
Lemanea fucina Bory, 1808 (Lemaneaceae, Rhodophyta), a rare species with a variable morphology: first record in the Republic of Montenegro
Arch. Biol. Sci. Belgrade
63
511 -
515
Singh I. L.
,
Muralidharan P.
2014
Evaluation of hepatoprotective and anti-oxidant activity of Lemanea fluviatilis on CCI4 induced hepatotoxicity in rats
Res. J. Pharm. Biol. Chem. Sci.
5
976 -
982
Singh M. R.
,
Gupta A.
2010
Morphological characteristics of rare and endangered species of Lemanea (Rhodophyta) from the rivers of Manipur, North-east India
Botanique
14
47 -
54
Singh M. R.
,
Gupta A.
2010
Nutritional composition of edible Lemanea australis Atkinson (Lemaneaceae, Rhodophyta) from Manipur river systems, India
PGTD of Botany, R. T. M. University
Nagpur
100 -
107
Singh M. R.
,
Gupta A.
,
Tiwari D.
2011
Advances in Environmental Chemistry
Excel India Publishers
New Delhi
Factors affecting the occurrence of Lemanea, Rhodophyta from the Rivers of Manipur, North-east India
233 -
236
Singh M. R.
,
Gupta A.
,
Gupta A.
2014
Ecoplanning, Biodiversity and Climate Change
Pointer Publishers
Jaipur
Biomass and productivity study of red algae from rivers of Manipur, North East India
118 -
134
Stamatakis A.
2006
RAxML-VI-HPC: maximum likelihoodbased phylogenetic analyses with thousands of taxa and mixed models
Bioinformatics
22
2688 -
2690
Vis M. L.
,
Harper J. T.
,
Saunders G. W.
2007
Large subunit rDNA and rbcL gene sequence data place Petrohua bernabei gen. et sp. nov. in the Batrachospermales (Rhodophyta), but do not provide further resolution among taxa in this order
Phycol. Res.
55
103 -
112
Vis M. L.
,
Saunders G. W.
,
Sheath R. G.
,
Dunse K.
,
Entwisle T. J.
1998
Phylogeny of the Batrachospermales (Rhodophyta) as inferred from rbcL and 18S ribosomal RNA gene sequences
J. Phycol.
34
341 -
350
Vis M. L.
,
Sheath R. G.
1992
Systematics of the freshwater red algal family Lemaneaceae in North America
Phycologia
31
164 -
179
Xie S. -L.
,
Shi Z. -X.
,
Wang R. -N.
2004
Taxonomy of the Lemaneaceae (Batrachospermales, Rhodophyta) in China
Acta Bot. Sin.
46
883 -
888
Zuccarello G. C.
,
Lokhorst G. M.
2005
Molecular phylogeny of the genus Tribonema (Xanthophyceae) using rbcL gene sequence data: monophyly of morphologically simple algal species
Phycologia
44
384 -
392