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A study of chloroplast structure in 3

Megaceros species and 3 Dendroceros
species (Anthocerotae) indigenous to New
Zealand
a

Lesley J. Valentine , Ella O. Campbell & D. H. Hopcroft

Department of Botany & Zoology , Massey University , Palmerston

North, New Zealand
b

Electron Microscope Unit Applied Biochemistry Division , DSIR ,

Palmerston North, New Zealand
Published online: 05 Dec 2011.

To cite this article: Lesley J. Valentine , Ella O. Campbell & D. H. Hopcroft (1986) A study of chloroplast
structure in 3 Megaceros species and 3 Dendroceros species (Anthocerotae) indigenous to New Zealand,
New Zealand Journal of Botany, 24:1, 1-8, DOI: 10.1080/0028825X.1986.10409719
To link to this article: http://dx.doi.org/10.1080/0028825X.1986.10409719

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New Zealand Journal of Botany, 1986, Vol. 24 : 1-8

0028-825X/86/2401-0001 $2.50/0

9 Crown copyright 1986

A study of chloroplast structure in 3 Megaceros species

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and 3 Dendroceros s p e c i e s (Anthocerotae)

indigenous to N e w Zealand *
LESLEY J. VALENTINE
ELLA O. CAMPBELL
Department of Botany & Zoology
Massey University
Palmerston North, New Zealand
D. H. HOPCROFT
Electron Microscope Unit
Applied Biochemistry Division, DSIR
Palmerston North, New Zealand
Abstract
Investigation of the chloroplast in
three species of Megaceros by light microscopy and
transmission electron microscopy showed random
distribution of starch and absence of a pyrenoid.
Of three Dendroceros species similarly investigated, one resembled the Megaceros species, the
second had a deeply convoluted and widely channelled pyrenoid with oil as the reserve material, the
third showed a range of forms from one with a
widely channelled, convoluted pyrenoid surrounded by a starch envelope through intermediate
types to one in which the pyrenoid had extremely
narrow channels and no starch envelope.

natural or artificial. Currently six genera are recognised, namely Anthoceros, Phaeoceros, Megaceros,
Dendroceros, Notothylas, and Folioceros (Grolle
1983). Only the first four of these are represented
in New Zealand.
Much interest has been evoked by the uniplastid
condition of many Anthocerotae and by the presence of a pyrenoid, for these features are reminiscent of algae. However, most of the numerous
published papers on the structure and behaviour
of the chloroplasts in Anthocerotae deal with Phaeoceros and Anthoceros. Only Campbell (1907) and
Burr (1968) studied Megaceros in detail, including
one species later transferred to Dendroceros (Proskauer 1953). It is unfortunate that at the time the
taxonomy was not well understood.
The aim of the present study was to investigate
the structure of the chloroplast in three species of
Megaceros and three species of Dendroceros indigenous to New Zealand and so provide a basis for
comparison with other species classified in these
genera.
OUTLINE OF PREVIOUS WORK ON THE
C H L O R O P L A S T OF THE A N T H O C E R O T A E

It is generally accepted that, as in electron micrographs of other land plants, the chloroplast of the
Anthocerotae has five major components (Fig. 1
Dendroceros granulatus; Dendroceros validus; and 2). At the surface is a double membrane known
Megaceros arachnoideus; Megaceros denticulatus; as the chloroplast envelope (Fig. 2). Within this is
the stroma or ground substance which is usually
Megaceros flagellaris; Phaeoceros
uniform but may show a central, more electronopaque region termed the pyrenoid (Fig. 1).
Throughout the stroma are membrane systems
INTRODUCTION
called lamellae or thylakoids, that in certain areas
The Anthocerotae are considered to occupy an iso- are arranged into stacks (grana) (see Fig. 7) and in
lated position in the plant kingdom. Recently some the intergranal regions form an anastomosing netauthors have even placed them in a separate divi- work. Chlorophyll is considered to be located on
sion, Anthocerotophyta (Stotler & Crandall-Stotler the thylakoids. Starch grains are commonly present
1977; Schuster 1977, 1979; Bold et al. 1980). Ques- but vary in abundance according to the physiotions then arise as to whether the group is a uni- logical condition of the chloroplast; they are either
form one and whether the present subdivision is dispersed throughout the stroma (Fig. 2) or aggregated in the vicinRy of the pyrenoid (Fig. 1). In
most material fixed with OsO4 single or clustered
osmiophilic
globules (plastoglobuli) are conspicu*Based to some degree on the dissertation presented by
L. J. Valentine as part of the requirement for B.Sc. ous due to their affinity for stains; they occur either
free in the stroma or associated with lamellae (see
(Honours) Massey University.
Fig. 6). They appear to consist of lipid but their
Received 8 May 1985; accepted 25 June 1985
Keywords
Anthoceros; Anthocerotae; chloroplast; pyrenoid; starch; Dendroceros giganteus;

New Zealand Journal of Botany, 1986, Vol. 24

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CE

.]~,Y~~+'~-~~,,~

.3

\
,,

-+,

,~..

,.~===lm

I=H,=
m

Fig. 1 Chloroplast of Dendroceros validus.

P pyrenoid; S starch
Fig. 3 Chloroplast of Megaceros denticulatus.
S starch

Fig. 2 Chloroplast of Dendroceros giganteus.

CE chloroplast envelope; S starch
Fig. 4 Chloroplast ot Megaceros arachnoideus.
P1 plastoglobuli; S starch

function is uncertain. Similar globules within the

pyrenoid are called pyrenoglobuli (see Fig. 12).
The more important literature on the anthocerote chloroplast has been reviewed by Burr (1968)
and by Valentine (1984) and only an outline of the
salient points is presented here. Schmitz (1882,
1884) described the pyrenoid of anthocerotes, using
a term that he had already applied to a body found
in algal chloroplasts that reacted differently to

stains. Schimper (1885) concluded from his studies

of Anthoceros that the pyrenoid was composed of
protein. Campbell (1907) found that the chloroplast of M. tjibodensis lacked pyrenoids but vaguely
described a pyrenoid-like body in superficial cells
of M. salakensis. Both of these species are now
regarded as synonymous with M. flagellaris (Hasegawa 1983). The pyrenoid of Anthoceros was further described independently by Scherrer (1914) and

Valentine et al.--Anthocerotae chloroplast structure

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McAllister (1914) as being composed of a more or

less crowded "mass of disc or spindle-like bodies.
McAllister termed it a "multiple" pyrenoid to distinguish it from the single unit pyrenoids found in
the algae.
The advent of the electron microscope at first
resulted in conflicting and disappointing information due to difficulties in developing a satisfactory
method of fixation and embedding. However Burr
(1968) made a very detailed examination of five
Megaceros species using improved techniques and
correlated the results with those,derived from light
microscope studies. For comparative purposes she
also examined Phaeoceros ref. himalayensis and
consulted published accounts and figures of P. laevis and of other species. Burr distinguished three
types of chloroplast: (1) with a pyrenoid, (2) with
no pyrenoid, and (3) with a pyrenoid-like body. In
type (1) she placed three species of Megaceros. In
M. vincentianus (Lehm. & Lindenb.) Campb. she
found that the starch grains formed a loose sheath
around an irregularly shaped pyrenoid which, however, stained lightly as compared to Phaeoceros
species. In M. mexicanus Steph. and in an
unidentified culture from New Zealnd which she
named M. "New Zealand" the pyrenoid, though
present, was even less distinctly defined and in the
latter species starch occupied all the remainder of
the chloroplast. Quite different was type (2) as
exemplified by M. endiviaefolius Mont., for the
starch grains were evenly distributed throughout
the entire plastid and there was no trace of a pyrenoid. Type (3) was represented by M. grandis
(Angstr.) Steph. which she later called M. flagellaris
(Mitt.) Steph. (Burr 1969, 1970). H e r e she could
not identify a pyrenoid by conventional or histochemical staining. However, in mature cells the
starch was not evenly distributed but was aggregated in what she termed a "pyrenoid-like" region.
Nevertheless in young cells near the apex it was
randomly distributed.
From serial sections and ontogenetic studies of
M. flagellaris Burr considered that the substance
comprising the pyrenoid represents a modified part
of the stroma. No membrane separates them and
the boundary where the material of the pyrenoid
blends into regular stroma matrix is indistinct. The
lamellar system of the chloroplast consists of thylakoids arranged in flat sheets, grana, and convoluted channels. The channels especially produce a
sponge-like construction. She infers from this that
the pyrenoid may be a convoluted mass partitioned into a number of units by thylakoid channels.
Also relevant to the present study is a paper on
the pyrenoid of algae by Griffiths (1980). He found
that the granular pyrenoid matrix contained inclusions such as thylakoid tubules and pyrenoglobuli.

3
He presents evidence to support the view that the
pyrenoid is primarily a device for storage of reserve
enzyme protein, especially ribulose-1, 5-diphosphate carboxylase m an important enzyme of the
photosynthetic carbon-fixation cycle. Various
structural modifications of the pyrenoid in different algal groups, he suggests, may be related to
secondary roles which have become associated with
this region of the chloroplast, for example, deposition of reserve carbohydrate or lipid and the facilitation of transport of materials. He also shows that
starch formation in algae may occur with or without a pyrenoid and that oil may replace starch as
a reserve material.
MATERIAL AND M E T H O D S
Sources of material

Megaceros arachnoideus (Steph.) Steph.: Glow

worm caves, Table Flat Road, Apiti, Manawatu.
(MPN 18663).
Megaceros denticulatus (Lehm.) Steph.: Forest floor,
Stewart Island. (MPN 18664).
Megaceros flagellaris (Mitt.) Steph.: [syn. M. grandis (Angstr.) Steph., M. salakensis Campb., M.
tjibodensis Campb.] Roadside drain, top of the
Pahiatua Track, Manawatu. (MPN 18686).
Dendroceros giganteus (Lehm. et Lindenb.) Prosk.:
[syn. M. endiviaefolius (Mont.) Steph.] Epiphytic on liverworts, wet bank, Wilmot Pass road
to Deep Cove, Fiordland. (MPN 18665).
Dendroceros granulatus Mitt.: [syn. D. nodulosus
Herz.] Epiphytic on nikau, Rhopalostylis sapida
Wendle et Drude, Piha, Auckland. (MPN 18662).
Dendroceros validus Steph.: [syn. D. allisonii Herz.]
Epiphytic on a twig, Waterfall Creek, Akatarawa Range. (WELT 8818).
Methods of investigation
The Megaceros species were maintained in culture
in Grow bowls in indirect sunlight on a medium
of sterilised silty loam moistened with a nutrient
solution recommended by Rink (1935).
Dendroceros granulatus was cultured similarly
but on nikau leaf bases. As material of D. validus
and D. giganteus was limited, it was used immediately after collection.
Specimens were studied with the light microscope using phase contrast and Nomarski optics and
with the transmission electron microscope. In preliminary light microscope studies at least 100 sections of each species were examined from all regions
of the thallus using as wide a range of specimens
as possible. Variations in chloroplast numbers and
shape were evident, as has been reported previously (Burr 1968, 1970; Campbell 1907). Consequently comparisons of plastid structure between

New Zealand Journal of Botany, 1986, Vol. 24

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~.,~

Fig. 5 Chloroplast of Megaceros flagellaris.

S starch
Fig. 6 Part of chloroplast of Megaceros arachnoideus.
PI plastoglobuli; T thylakoid network
Fig. 7 Part of chloroplast of Megaceros flagellaris.
G granal stack; T thylakoid network
Fig. 8 Part of chloroplast of Megaceros flagellaris.
CE chloroplast envelope; G granal stack; T thylakoid network

the different Megaceros species were restricted to

the mature cells of the upper epidermis, whereas
for the Dendroceros species material was selected
from the wings avoiding both the costa and the
marginal meristems.
At least two typical plants of each species were
selected for transmission electron microscopy.

Material was fixed in a modified Karnovsky fixative (2% formaldehyde 3% glutaraldehyde) in a

0.1M phosphate buffer system at pH 7.2 for 1-2 h
at room temperature. This was followed by
secondary fixation with 1% OsO4 in the same buffer
system for 1/2-1 h at room temperature. Dehydration was carried out in a graded acetone series and

Valentine et al.mAnthocerotae chloroplast structure

specimens were then infiltrated and embedded in
Polarbed 812 resin. Silver sections (c. 75 nm) were
cut on an ultramicrotome with a diamond knife.
After double staining with saturated uranyl acetate
followed by lead citrate they were picked up on 400
mesh copper grids and studied in a Philips 201C
transmission electron microscope.

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RESULTS

M. arachnoideus, M. denticulatus, and M.

flagellaris
The three species are treated together because of
the similarity of their chloroplasts. Under the light
microscope these are pleiomorphic, ranging from
discoid through spherical to irregular in shape. They
stain uniformly with protein-specific stains indicating the absence of a pyrenoid. Large, randomly
distributed starch grains are a dominant feature
(Fig. 3, 4, 5). In electron micrographs the thylakoids in certain regions of the stroma appear as a
characteristic, three dimensional, anastomosing
system of channels which produce a network structure (Fig. 6 and 7). Where this channelling occurs
marginally, in association with the chloroplast
envelope (Fig. 8), its appearance is similar to the
peripheral reticulum described in some C-4 pathway plants (Taylor & Craig 1971). In other regions
the thylakoids are stacked into grana (Fig. 7) which
at times seem to be formed by the invagination of
existing thylakoids (Fig. 6). These are connected by
intergranal regions where the thylakoids occur singly or in sheets (Fig. 9). The path of adjacent lamellations is often distorted by the large starch grains
(Fig. 5). Plastoglobuli are scattered throughout singly or in clusters (Fig. 4 and 6). The electron-dense
speckling visible in micrographs of M. flagellaris
(Fig. 7 and 8) was present in unstained sections.
After fixation tests with newly prepared fixatives
some freshly collected specimens were analysed
with an inductively coupled argon plasma emission
spectrometer. This revealed a high lead content (c.
54 ppm) as the only unusual feature.

D. giganteus
The chloroplasts correspond very closely with those
of the Megaceros species studied. The granal stacks,
however, are as a rule more sharply distinguishable
from the intergranal thylakoids (Fig. 10) and the
thylakoid channels described in the Megaceros species occur more frequently and uniformly (Fig. 2).
The starch grains are randomly distributed and
there is no pyrenoid. Plastoglobuli are infrequent
and are randomly distributed.

D. granulatus
In young cells under the light microscope the chloroplast appears laminate in surface view and occupies most of the width of the cell. In older cells it
may be cup-shaped and of irregular outline. In most
chloroplasts of mature cells, including those in close
association with the Nostoc colonies, there is a denser central pyrenoid area which may be circular,
ellipsoidal, or rather irregular. Staining reactions
with Coomassie blue or Picric acid indicate that it
is rich in protein. In electron micrographs thylakoids are visible in the stroma, for the most part
arranged in sheets, some of which extend throughout the length of the chloroplast (Fig. 11). Only in
the immediate vicinity of the pyrenoid is there a
tendency to form grana (Fig. 12). Plastoglobuli occur
mainly in the medial layer of the chloroplast (Fig.
11). The pyrenoid is more electron opaque than the
peripheral region and in section appears as some
13-50 units of varying shapes and sizes. Observations of serial sections show that these are all
parts of a single, deeply convoluted, "brain-like"
body. They are composed of granular material and
show no lamellar structures (Fig. 11 and 12). Pyrenoglobuli are abundant especially towards the
periphery of the pyrenoid and sometimes appear
to grade into the granules of the pyrenoid matrix
proper. Between the units thylakoids occur and are
similar to, and often continuous with, those of the
outer chloroplast. The chloroplasts are unusual in
that despite an investigation of both freshly collected and cultured material at various times of the
year, no starch was found. In the cytoplasm of each
cell there are 1-3 glistening oil droplets, 2.5-5.0 ~m
in diam., or occasionally several smaller ones. They
are soluble in ether and stain with Sudan IV.

D. validus
In young cells the chloroplast under the light
microscope is laminate. In older cells it tends to
be cup-shaped with curled up edges and a very
irregular outline. A central denser area, the pyrenoid, is evident and in some cells is surrounded
by a loose envelope of starch grains. In electron
micrographs the thylakoids in the stroma are seen
to be arranged in sheets and in grana which merge
with intergranal thylakoids. Only near the pyrenoid
is the lamellar arrangement distorted by starch
grains (Fig. 1). Plastoglobuli are sparsely scattered
throughout. The pyrenoid is approximately spherical in shape but was found to vary between two
forms. In some cells it is deeply convoluted and
widely channelled so that in section it appears as
up to 5 (-10) units of varying size and shape. Thylakoids occur in the channels between the units and
seem to be continuous with the lamellar system of
the outer chloroplast. A loose starch sheath is

Downloaded by [University of Chicago Library] at 10:09 15 November 2014

New Zealand Journal of Botany, 1986, Vol. 24

,,11

'

..g:

';',

,,:

llll.lm

13

41, ;',

,<

,l!,

.~(l~",.;,)Tllfi~'< :.~;,(~

'......

~,.~',... .'~ ,: :. ..... ~:~.~,_., ,,~.

Fig. 9 Part of chloroplast of Megaceros denticulatus.

Fig. 13 Chloroplast of Dendroceros validus.
G granal stack
NC narrow stromal channels; P pyrenoid
Fig. 10 Part of chloroplast of Dendroceros giganteus.
Fig. 14 Part of chloroplast of Dendroceros validus.
G granal stack
P pyrenoid; WC wide stromal channels
Fig. 11 Chloroplast of Dendroceros granulatus.
P pyrenoid; P1 plastoglobuli
Fig. 12 Part of chloroplast of Dendroceros granulatus.
G granal stack; PY pyrenoglobuli; WC wide stromal channels

Downloaded by [University of Chicago Library] at 10:09 15 November 2014

Valentine et al.--Anthocerotae chloroplast structure

obvious (Fig. 1). Pyrenoglobuli are abundant and
are dispersed within the pyrenoidal matrix with a
tendency to an increased density and greater
osmiophilia at the periphery of the units. In other
cells the pyrenoid occupies a larger proportion of
the chloroplast (Fig. 13). In this form the numerous
channels which permeate the pyrenoidal matrix are
quite narrow. Pyrenoglobuli are abundant with a
tendency to congregate towards the margins of the
channels. Starch is almost absent. Intermediate
between these two forms are those where the pyrenoid shows both narrow and wide channels and
there is an irregular sheath of small starch grains
(Fig. 14).

DISCUSSION
The results obtained in this investigation indicate
that the level of organisation of the chloroplast in
Anthocerotae differs between species in regard to
lamellar arrangement, occurrence of a pyrenoid, and
the type and location of the reserve material. Comparisons may be made with both algae and other
land plants. However, the differences are so marked,
particularly in Dendroceros, that the species appear
to be relics of a previously much larger group. Until
all existing species have been studied, it is considered premature to postulate on relationships.
a. Lamellar system

In most species the thylakoids are arranged in grana

connected by intergranal regions. However, only in
D. giganteus (Fig. 10) do the grana approach the
clear definition seen in other land plants. More frequently, as in M. denticulatus, they end irregularly
and gradually merge into the intergranal region
which may take a braided form (Fig. 9). In certain
parts of the stroma parallel sheets of thylakoids
occur. In other parts there is a reticulate system of
interconnecting tubules known as channelling (Fig.
6) which Burr (1970) and Crandall-Stotler (1984)
have noted as a distinctive feature of Anthocerotae. D. granulatus differs from the other species in
that most of the stroma is occupied by massive
parallel sheets of thylakoids, with only occasional
grana mainly in the vicinity of the pyrenoid (Fig.
11 and 12).
b. The pyrenoid

In the three Megaceros species studied there is no

pyrenoid (Fig. 3, 4, and 5). In one of these, M. flagellaris, Burr (1970) found no pyrenoid but she
reported a pyrenoid in some Megaceros species such
as M. vincentianus. In M. flagellaris Burr (1970)
deduced a pyrenoid-like region on the basis of a
pyrenoid-like aggregation of starch grains, as had

7
Campbell (1907) in epidermal cells of M. salakensis, syn. of M. flagellaris (Hasegawa 1983). However, this deduction cannot be accepted, since from
work on algae it is now established that there is no
evidence that the pyrenoid contains the enzymes
associated with starch formation (Griffiths 1980).
M. flagellaris is widespread in Asia and the Pacific
Islands and shows great plasticity (Hasegawa 1983).
It is possible that the pattern of starch deposition
may vary with environmental conditions.
In Dendroceros giganteus also we found no pyrenoid (Fig. 2), thus confirming the observations of
Burr (1968) on this species which she called Megaceros endiviaefolius. As in Megaceros species the
mature cells of D. giganteus are multiplastid. The
other two species of Dendroceros have a pyrenoid,
a structure of frequent occurrence in algae and linking Anthocerotae with that group. In D. granulatus
the pyrenoid is a highly convoluted region of granular material which is deeply cleft into some 1350 units by stroma and thylakoid channels (Fig. 11
and 12). In D. validus the pyrenoid varies from a
type similar to that of D. granulatus although less
complex and with fewer units (Fig. 1), to one in
which the pyrenoid matrix is permeated by very
narrow channels (Fig. 13) so that in thicker sections
the whole appears as a single unit closely resembling the pyrenoid of a green alga Trebouxia, which
is a phycobiont of the lichen Ramalina menziesii
Tuck. (Griffiths 1980). Intermediate forms occur
also (Fig. 14). A possible explanation of the variation is that some parts of the thallus mature more
rapidly than others, for the wing enlarges considerably and becomes strongly folded and crispate.
The deeply lobed type of pyrenoid with an obvious
starch sheath tends to occur on the upper side of
the folds.

c. Reserve material

In the three Megaceros species and in Dendroceros

giganteus starch grains are randomly distributed
throughout the chloroplast (Fig. 2, 3, 4, and 5). In

D. validus (Fig. 1) some of the cells have a conspicuous starch sheath around the pyrenoid as in

Phaeoceros and many algae. In D. granulatus,

despite the presence of a pyrenoid, (Fig. 11 and 12),
oil replaces starch as the reserve material. This
condition has not been reported previously in
Anthocerotae but is known in some algae (Griffiths
1980).

ACKNOWLEDGMENT
We wish to thank Dr J. Lee, Biochemistry Division, DSIR,
Palmcrston North for the chemical analysis of Megaceros

flagellaris.

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REFERENCES

Bold, H. C.; Alexopoulos, C. J.; Delevoras, T. 1980: Morphology of plants and fungi, ed. 4. New York, Harper and Row.
Burr, F. A. 1968: Chloroplast structure and division in
Megaceros species. Unpubl. Ph.D. thesis, University of California, Berkeley.
1969: Reduction in chloroplast number during
gametophyte regeneration in Megacerosflagellaris.
Bryologist 72: 200-209.
1970: Phylogenetic transitions in the chloroplasts of the Anthocerotales. I. The number and
ultrastructure of the mature plastids. American
journal of botany 57 : 97-110.
Campbell, D. H. 1907: Studies on some Javanese Anthocerotaceae. I. Annals of botany 21: 467-486.
Crandall-Stotler, B. 1984: Musci, hepatics and anthocerores m an essay on analogues. In: Schuster, R. M.
ed. New manual of bryology. Vol. 2 Nichinan,
Hattori Botanical Laboratory. Pp. 1093-1129.
Griffiths, D. J. 1980: The pyrenoid and its role in algal
metabolism. Science progress Oxford 66 : 537-553.
Grolle, R. 1983: Nomina generica Hepaticarum; references, types and synonymies. Acta botanica Fennica 121: 1-62.
Hasegawa, J. 1983: Taxonomical studies on Asian Anthocerotae. III. Asian species of Megaceros. Journal
of the Hattori Botanical Laboratory 54: 227-240.
McAllister, F. 1914: The pyrenoid of Anthoceros. American journal of botany 1: 79-93.
Proskauer, J. 1953: Studies on Anthocerotales. IV. Bulletin Torrey Botanical Club 80: 65-75.

N e w Z e a l a n d J o u r n a l of Botany, 1986, Vol. 24

Rink, W. 1935: Zur Entwicklungsgeschichte, Physiologie
und Genetik der Lebermoosgattungen Anthoceros
und Aspiromitus. Flora, N.F. 30: 87-130.
Scherrer, A. 1914: Untersuchungen uber Bau und Vermehrung der Chromatophoren und das Vorkommen von Chondriosomen bei Anthoceros. Flora
107: 1-56.
Schimper, A. W. F. 1885: Untersuchungen uber die Chlorophyllkorper und die ihnen homologen Gebilde.
Jahrbucher fur wissenschaftliche Botanik 16 : 1-247.
Schmitz, F. 1882: Die Chromatophoren der Algen. Bonn,
M. Cohen & Son. Pp. 1 -176.
1884: Beitrage zur Kenntniss der Chromatophoren. Jahrbucher fur wissenschaftliche Botanik
15:1-177.
Schuster, R. M. 1977: The evolution and early diversification of the Hepaticae and Anthocerotae. In:
Frey, W.; Hurka, H.; Overwinkler, F. eds. Beitrage
zur Biologie der niederen Pflanzen. Stuttgart, G.
Fischer. Pp. 107-.115.
1979: The phylogeny of the Hepaticae. In:
Clarke, G. C. S.; Duckett, J. G. eds. Bryophyte systematics. London & New York, Academic Press.
Pp. 41-82.
Stotler, R. & Crandall-Stotler, B. 1977: A checklist of the
liverworts & hornworts of North America. Bryologist 80: 405-4218.
Taylor, A. O. and Craig, A. S. 1971: Plants under climatic
stress. II. Plant physiology 47: 719-725.
Valentine, L. J. 1984: A comparison of selected New
Zealand species of Megaceros & Dendroceros
(Anthocerophyta) with special reference to chloroplast gross morphology & ultrastructure. Unpubl.
B.Sc.(Hons.) dissertation, Massey University.