a developmental sequence for paraphyses inacademic.uprm.edu/isastre/merced and...

A developmental sequence for paraphyses in

Neckeropsis (Neckeraceae)

AMELIA MERCED-ALEJANDRO

Biology Department, University of Puerto Rico-Mayaguez Campus, P.O. Box

9012, Mayaguez, Puerto Rico 00681-9012; current address: Department of

Biology, Box 90338, Duke University, Durham, NC 27708-0338, U.S.A.

e-mail: [email protected]

INES SASTRE-DE JESUS

Biology Department, University of Puerto Rico-Mayaguez Campus, P.O. Box

9012, Mayaguez, Puerto Rico 00681-9012

e-mail: [email protected]

ABSTRACT. Some species of Neckeropsis have leaf-like structures that develop on the

perichaetia after fertilization of the archegonia. It has been suggested that these structures

are either ligulate perichaetial leaves or multiseriate paraphyses. Using light microscopy, a

detailed morphological and ontogenetic description was done for the paraphyses in the

reproductive branches of N. disticha. Important developmental stages were also described

for nine other species of Neckeropsis (N. exserta, N. lepineana, N. nitidula, N. obtusata, N.

nano-disticha, N. crinita, N. undulata, N. fimbriata and N. andamana) to document the

development of the different types of paraphyses. Transitions between uniseriate and

multiseriate paraphyses were documented at different stages in the development of the

fertilized branch. These were interpreted as a transition series similar to the heteroblastic

sequence in branch leaves; where the uniseriate and multiseriate paraphyses correspond to

the juvenile and mature stages, respectively. Of the nine species, five possess multiseriate

paraphyses that are fully developed at different points of the progression series. In N. nano-

disticha and N. crinita the paraphyses are thinner and fully developed at early mature stage,

while in N. undulata and N. disticha the fully developed paraphyses are narrowly ligulate

and represent the middle mature stage in the developmental sequence. In Neckeropsis

andamana and N. fimbriata the paraphyses are ligulate to lanceolate and correspond to the

late mature stage. These results provide ontogenetic data for paraphyses, and could

establish the states and direction of this character for a phylogenetic analysis.

KEYWORDS. Paraphyses, ontogeny, Neckeropsis, perichaetia, ramenta.

¤ ¤ ¤

In systematic studies developmental data are a key

feature to generate a hypothesis of homology for

phylogenetic analyses. The selection of characters and

character states constitutes the exercise of making a

‘‘best estimate’’ (Newton & De Luna 1999); thus

information about the development of structures can

The Bryologist 112(2), pp. 342–353 0007-2745/09/$1.35/0Copyright E2009 by The American Bryological and Lichenological Society, Inc.

make this estimate more informed. Ontogenetic data

can also provide new taxonomic characters, ordering

and polarization of characters. In mosses the parallels

between ontogeny and phylogeny are noticeable in

the developmental sequence of the branch leaves.

Mishler (1988) described several instances in which

ontogeny were used to clarify transformational

homologies, as in the leaves of Fissidens.

Although paraphyses are documented in almost

all moss groups, there are no developmental studies

about this structure. Studies about paraphyses are

limited to describing the different types of paraphyses

but do not deal with the development and

transformations of these structures. The lack of

studies about the origin and modifications of the

paraphyses can represent a problem when evaluating

this character for taxonomic and phylogenetic

analyses.

Janzen (1921) described an ample spectrum of

morphologies of paraphyses occurring in both male

and female gametoecia. Saito (1975) defined them as

‘‘filaments occurring side by side with antheridia,’’

while Newton and De Luna (1999) used the term

paraphyses for hyaline uniseriate structures

surrounding the archegonia before fertilization. All

definitions agree in placing paraphyses in the

reproductive branch. Other filamentous structures

found in the reproductive branches are axillary hairs;

these are present in the axils of growing leaves and at

branch apices. Axillary hairs were defined for

taxonomic purposes and morphological characters of

these structures for pleurocarpous mosses were

pointed out by Hedenas (1989). The difference

between paraphyses and axillary hairs is primarily

defined by position; but also paraphyses are

morphologically more variable. Ignatov and Hedenas

(2007) called attention to perichaetia where the

gradual transition between axillary hairs and

paraphyses ‘‘clearly suggest the homology of these

structures.’’ Saito (1975) stressed the necessity of a

careful study of the morphology and origin of

paraphyses before reevaluating them as a taxonomic

character.

In pleurocarpous mosses, like Neckeropsis,

reproductive branches consist of perigonial or

perichaetial leaves and their enclosed gametangia.

Antheridia and archegonia are produced from the

apical cell of the branch, and paraphyses are

frequently documented as intermingled with them.

Species in this genus have different types of

paraphyses surrounding the sporophyte; their strong

resemblance to leaves has led to the question if they

are modified perichaetial leaves (Touw 1962), and

have led to a specialized term for them, ramenta

(sing. ramentum). However, true paraphyses are not

considered homologous to leaves (Touw 1962), and

the general definition states that they are cell-

filament structures associated with the reproductive

organs of bryophytes (Newton & De Luna 1999;

Schofield & Hebant 1984).

Touw (1962) briefly described the development

of this leaf-like structure, but he did not clarify its

homology. In that study he recognized two types of

female gametoecia, each one divided into two

subtypes. The first type has paraphyses that remain

filiform (uniseriate) and hyaline: in the 1a subtype

(Fig. 1a) the perichaetial leaves do not increase much

in length after fertilization, while in the 1b (Fig. 1b)

the inner perichaetial leaves elongate before

maturation of the sporophyte. The second type is

characterized by leaf-like paraphyses that appear after

fertilization and are as long as or longer than the

sporophyte; the 2a subtype (Fig. 1c) contains hyaline

filiform paraphyses (some 2–3 cells wide) and after

fertilization numerous filiform to ligulate paraphyses

grow around the base of the fertilized archegonia and

the branch axis elongates resulting in a stem vaginula

that he called ‘‘pseudopodium.’’ In the 2b subtype

(Fig. 1d) unfertilized female branches have very

short leaf-like paraphyses or none, after fertilization

the stem vaginula is short or absent and the inner

perichaetial leaves elongate greatly.

Touw (1962) recognized that the first type is

common in other Neckeraceae but the second type is

apparently limited to Neckeropsis. The Neotropical

species, Neckeropsis disticha and N. undulata have 2a

subtype gametoecia (Fig. 1d). Touw pointed out that

in this type, ‘‘transitions… are found between

filiform and ligulate paraphyses, but it seems that the

filiform paraphyses of the young gametoecia are not

transformed into ligulate leaves.’’ He also noted that

N. andamana ‘‘looks like being surrounded by

perichaetial leaves, but on closer examination, some

of these leaves appear to be paraphyses, inserted in

Merced-Alejandro & Sastre-De Jesus: Paraphysis development in Neckeropsis 343

the vaginula and surrounded by a slender whorl of

decrepit archegonia.’’ These examples illustrate that

at some point the distinction between leaves and

paraphyses is not completely clear.

This study aims to clarify the origins and

homology of the multiseriate structure in Neckeropsis

frequently described as paraphyses or ramenta. To

this end, an ontogenetic study of the leaf-like

paraphyses was undertaken for female branches of

Neckeropsis disticha and it was complemented by

comparative studies of reproductive branch

organization in other species representing the four

distinct types of female gametoecia.

MATERIALS AND METHODS

Neckeropsis species were selected to include

representatives of the four types of female gametoecia

described by Touw (1962); type 1a N. exserta, type 1b

N. lepineana, N. nitidula and N. obtusata, type 2a N.

disticha and N. undulata, type 2b N. crinita, N.

andamana, N. fimbriata, and a transition between 2a

and 2b N. nano-disticha. Species selected were

described from the Neotropics (Sastre-De Jesus

1987), Africa (Enroth 1993), Asia and the Pacific

(Touw 1962). Fresh specimens of Neckeropsis disticha

with reproductive branches or sporophytes in various

stages were collected in Puerto Rico. Voucher

Figure 1. Female gametoecia types in Neckeropsis (adapted from Touw 1962. Used with permission). a 5 type 1a; b 5 type 1b; c

5 type 2a; d 5 type 2b.

344 THE BRYOLOGIST 112(2): 2009

specimens are deposited in MAPR; herbarium

specimens were examined for non-American species

(Table 1).

Six major reproductive stages (modified from

Greene 1960) were identified and collected for N.

disticha: reproductive branches (archegonia without

fertilization), branches with fertilized archegonia

(swollen venter), embryonic sporophytes (before the

separation of calyptra and vaginula), young

sporophytes (capsule not swollen, with calyptra),

immature sporophytes (green capsule) and mature

sporophytes.

Reproductive branches were studied under the

stereoscope and light microscope and

microphotographed. Samples selected for the other

nine species included 3–4 stages: mature perichaetia

and/or perigonium, early fertilized or juvenile (when

available) and mature sporophyte.

The position of the perichaetial leaves and the

morphology, length and relative quantity of

paraphyses were examined and recorded for each of

the stages. Paraphyses were described by their relative

cell wall thickness, relative size and number of cells in

each paraphysis, color (hyaline, chlorophyllose, red-

brown), cell width (the lines or series of cells) and

paraphysis form (regular, irregular, filiform, ligulate).

On fertilized branches, the receptacle that sustains

the gametangia was described and the appearance

and development of the vaginula was followed in all

stages. The elongation of the perichaetial leaves,

gametangia position and paraphyses, and the types of

paraphyses present were examined from early-

fertilized stages through sporophyte maturation.

In addition, reproductive branches of N. disticha

with and without fertilized archegonia, and

embryonic sporophytes were infiltrated in paraffin

(based on Johansen 1940) and plastic resin for

sectioning (for details see: Merced-Alejandro 2004).

Slides were examined under a light microscope using

bright field microscopy and were

microphotographed. Identification of the

components of the reproductive branches was made

when possible, specifically the antheridia, archegonia

(fertilized or not), paraphyses (uniseriate or

multiseriate), perichaetial leaves and receptacle.

A developmental hypothesis for the paraphyses

on fertilized branches was developed from data

collected from each species and studied stages. The

species were compared to synthesize a general

development scenario for paraphyses in Neckeropsis

that could be applied to other bryophyte groups.

RESULTS

Development of paraphyses and the reproduc-

tive branch in N. disticha. The reproductive branches

of Neckeropsis disticha are mostly synoicous, although

male branches were also found. The perichaetia

consist of 8–10 leaves of which the outer leaves are the

early juvenile leaves and the inner are the later juvenile

leaves (following La Farge-England 1996; Mishler &

De Luna 1991). The inner perichaetial leaves are

gradually longer (to more than twice as long) than the

outer perichaetial leaves. Before fertilization

paraphyses are hyaline, uniseriate and thin-walled; the

paraphyses are intermingled with the antheridia and

archegonia and inserted at the apex of the

reproductive branch, the receptacle (Fig. 2a).

After fertilization new uniseriate paraphyses

appeared; these were short (2–4 cells) and reddish

with thin cell walls (Fig. 2b). At a very early stage, the

hyaline paraphyses started to divide at the base

(Fig. 2c). Following this, numerous hyaline

paraphyses were recorded. Later, in the swollen

Table 1. List of Herbarium specimens examined.

Species Specimen

N. andamana (Mull. Hal.) Paris Bartlett 14666 (L)

Williams s.n. (L)

N. crinita Griff. Touw 8440 (L)

N. disticha (Hedw.) Kindb. Sastre & Merced 3284 (MAPR)

Sastre 3285 (MAPR)

N. exserta Hook. in Schwagr. Touw 8439 (L)

Touw 9439 (L)

Touw 9500 (L)

Touw 10805 (L)

N. fimbriata Harv. Den Hoed 460 (L)

Touw 8139 (L)

N. lepineana (Mont.) M. Fleisch. Hennipman 5246 (L)

N. nano-disticha (Geh.) M. Fleisch. Weber 1290 (L)

N. nitidula (Mitt.) Broth. Touw 18914 (L)

Touw 19111 (L)

N. obtusata Mont. Touw s.n. (L)

Touw 18913 (L)

Touw 19168 (L)

N. undulata (Hedw.) Reichardt Sastre 3283 (MAPR)


venter stage, longer chlorophyllose, 2–5-seriate

paraphyses were documented (Fig. 2d) and small

leaf-like structures were identified as multiseriate

paraphyses (Fig. 2e); these appeared around the base

of the fertilized archegonium. The paraphyses ranged

from uniseriate to biseriate or variously seriate at

some point and to slim multiseriate paraphyses of

different width but with thick cell walls. Some of the

multiseriate paraphyses had a narrow base that

consisted of one or two reddish cells; others had a

broad base with several reddish cells. In this stage,

paraphyses presented great variation; the receptacle

of the branch remained flat and the perichaetial

leaves elongated a little (Fig. 3a). During the

development of the sporophyte there were no visible

sign of any branch or leaf primordium around the

vaginula and the fertilized archegonium (Fig. 3b).

In a transverse section of a fertilized branch, the

perichaetial leaves enclosed the paraphyses and two

fertilized archegonia, one more developed than the

other (Fig. 3c). Various types of paraphyses were

identified: uniseriate paraphyses were the structures

with only one cell, distributed between the

perichaetial leaves and the archegonia and the

structures surrounding the dominant fertilized

archegonia were identified as multiseriate

paraphyses, which were 4–10 cells in breadth

(Fig. 3d).

After the swollen venter stage, the fertilized

archegonium started to elongate and before the

calyptra formation the leaf-like paraphyses were

noticeable and consisted of light green multiseriate

paraphyses—longer than the perichaetial leaves. The

uniseriate and biseriate paraphyses were less obvious

Figure 2. Reproductive branch in Neckeropsis disticha. a. Antheridia (ant) and archegonia (arch) in plastic resin section. b. Early

fertilized archegonia with uniseriate paraphyses. c. Cell division in the base of paraphyses. d. Later fertilized archegonia with

biseriate and slender multiseriate paraphyses. e. New multiseriate paraphyses and new uniseriate paraphyses.


because they were fewer than in the earlier stages.

The axis of the reproductive branch started to

elongate, mainly between the fertilized archegonia

and the perichaetial leaves (Fig. 3e).

In the next stage, when the calyptra separates

from the vaginula, the stem vaginula has almost

reached its complete length and the multiseriate

paraphyses were nearly as long as the sporophyte

(Fig. 3f). Uniseriate paraphyses are visible

intermingled with the aborted archegonia along the

stem vaginula; none of the biseriate or thinner

multiseriate paraphyses (4–6-seriate) was present.

Figure 3. Fertile reproductive branch of N. disticha. a. Plastic resin section of branch with uniseriate and multiseriate paraphyses.

b. Plastic resin section of receptacle and vaginula. c., d. Plastic resin cross section showing uniseriate paraphyses (p) and different

wide multiseriate paraphyses (mp). e. Plastic resin section of the elongation of the vaginula (v), paraphyses (p), perichaetial leaves

(pl). f. Young sporophyte with long multiseriate paraphyses. g. Multiseriate paraphysis.


The seta began to grow and achieved its complete

length at the next stage, after that the capsule

expanded and the stem vaginula reached its total

length. While the sporophyte matures, the uniseriate

paraphyses become scarcer. At this time the leaf-like

structure surrounding the sporophyte consists of

more than 20 multiseriate paraphyses, generally of

10–15 but to as many as 23 lines of cells (Fig. 3g).

Reproductive branches in other species

of Neckeropsis. The male reproductive branches of

Neckeropsis have short perigonial leaves and all

specimens examined contained short hyaline,

uniseriate paraphyses (8–12 cells) with thin to regular

cell walls. In N. fimbriata and N. undulata paraphyses

of two to three or more lines of cells were observed;

also in these two taxa and N. nano-disticha a few

small leaves were found inside the inner perigonial

leaves.

Female reproductive branches sometimes

differed from the male and the variation between

inner and outer perichaetial leaves was more

noticeable; both branches consisted of about ten

ovate leaves (except the perigonium of N. lepineana,

that is more robust). Inner perichaetial leaves were

more than twice as long as the outer leaves. All

reproductive branches contained very short

uniseriate paraphyses (6–10 cells) but shorter

paraphyses of 2–4 cells were present in N. fimbriata,

N. andamana and N. crinita; these were hyaline to

reddish and not intermingled with the archegonia

but located near the axial part of the inner

perichaetial leaves.

The species with the first type (Fig. 1a, b) of

reproductive branches: N. lepineana, N. obtusata, N.

exserta and N. nitidula, have only uniseriate

paraphyses (Table 2). After fertilization, perichaetial

leaves are considerably longer and numerous, hyaline

to light green, uniseriate paraphyses were present

(Fig. 4a). The paraphyses of N. lepineana are longer

(more than three times longer than before

fertilization) and have thicker cell walls than N.

obtusata, in which the paraphyses were only a little

longer than the archegonia. In N. nitidula different

kinds of paraphyses were identified: short paraphyses

of few (8) long thin-walled cells and long paraphyses

(.20) of short cells, some of these paraphyses have

thin cell walls and others have thick walls. Tab

le2.

Typ

eo

fth

ep

arap

hys

esp

rese

nt

acco

rdin

gto

rep

rod

uct

ive

bra

nch

stag

e.P

5p

eric

hae

tia,

Pg

5p

erig

on

ia,

F5

fert

iliz

edar

cheg

on

ia,

E5

earl

yst

ages

of

spo

rop

hyt

e,M

5

mat

ure

spo

rop

hyt

e.

Sp

ecie

s

Par

aph

yses

Per

ich

aeti

al

Typ

e

Sh

ort

un

iser

iate

Lo

ng

un

iser

iate

Inte

rmed

iate

(bis

eria

teto

nar

row

lym

ult

iser

iate

)

Sm

all

leaf

-lik

e

Sli

mlo

ng

mu

ltis

eria

te

Sli

mto

Lig

ula

te

Lig

ula

teto

Lan

ceo

late

N.

exse

rta

PM

1a

N.

lep

inea

na

PF

M1

b

N.

nit

idu

laP

FF

M1

b

N.

obtu

sata

PF

MP

1b

N.

na

no-

dis

tich

aP

PP

Pg

M2

a–2

b

N.

crin

ita

P--

----

--P

M2

b

N.

un

du

lata

PE

Pg

EP

gE

M2

a

N.

dis

tich

aP

EP

gE

Pg

EM

2a

N.

fim

bria

taP

Pg

Pg

—M

2b

N.

an

dam

an

aP

FF

EM

2b


The mature sporophyte-bearing branch of N.

exserta has an elongate vaginula that encloses a small

portion of the seta; the elongation occurred at the

end of the branch leaving the barely elongate

perichaetial leaves at the lower part of the axis. The

axis had aborted archegonia and antheridia located

above the region of the leaves (but not all over the

axis) and multiple hyaline paraphyses reached the

lower part of the capsule (.10 cells); these

paraphyses were uniseriate with thick-walled cells. In

N. nitidula, N. obtusata and N. lepineana paraphyses

were longer than the archegonia, reaching the lower

Figure 4. Reproductive branch and mature sporophyte of N. nitidula. a. Fertile archegonium with uniseriate paraphyses. b.

Mature sporophyte with elongate perichaetial leaves (pl). Reproductive branch and mature sporophyte of N. nano-disticha. c.

Unfertilized female branch with biseriate paraphyses. d. Mature sporophyte with slim multiseriate paraphyses (p) and elongate

perichaetial leaves (pl). Reproductive branch and mature sporophyte of N. crinita. e. Unfertilized female branch with uniseriate

paraphyses and leaflike structure. f. Mature sporophyte with multiseriate paraphyses and short stem vaginula (v).


part of the capsule; except in N. lepineana where

paraphyses were much longer. In these three species

the perichaetial leaves were considerably elongate,

reaching beyond the mouth of the capsule, and the

paraphyses and archegonia were restricted to the

upper part of the reproductive axis (Fig. 4b). The

vaginula is hardly elongate in N. nitidula, enclosing

only the foot, but in N. lepineana and N. obtusata the

stem elongates between the perichaetial leaves,

enclosing part of the seta.

The rest of the species have the second type of

reproductive branches, these species present different

types of paraphyses in each developmental stage

(Table 2). In unfertilized female branches of N.

nano-disticha paraphyses were uniseriate to biseriate

(Fig. 4c). The mature sporophyte of N. nano-disticha

had narrow multiseriate paraphyses (5–7 lines of cells

at the base) that reached beyond the mouth of the

capsule; these numerous paraphyses were light green

to yellow and were located intermingled with the old

antheridia and remnants of uniseriate paraphyses on

the elongate stem vaginula (Fig. 4d). Some of the

inner perichaetial leaves elongated considerably,

reaching half the length of the capsule. In some

species the small leaves found inside the perigonia

were also present in the perichaetia of N. nano-

disticha, N. crinita (Fig. 4e) and N. obtusata. The

mature sporophyte of N. crinita also had slim

multiseriate paraphyses and elongate perichaetial

leaves, but a shorter stem vaginula (and seta) with

aborted archegonia and short uniseriate paraphyses

(Fig. 4d). The multiseriate paraphyses of N. nano-

disticha had thick and smooth cell walls, but in N.

crinita the paraphyses had thick walls with papillae,

making the leaf-like paraphyses serrate, with small

ramifications (1–2 cells) at the base.

In the branches with the fertilized archegonia of

N. undulata, various types of paraphyses were

present: new uniseriate paraphyses with thick cell

walls, biseriate paraphyses, irregularly-seriate

paraphyses and small leaf-like paraphyses (Fig. 5a).

At the stage of the juvenile sporophyte the branch

contained many multiseriate paraphyses, some as

wide as on the mature branches and many others

slim and biseriate; in this stage the paraphyses were

more heterogeneous and presented many

intermediate forms between biseriate and

multiseriate. The sporophyte and reproductive

branch of N. undulata was similar to N. disticha; the

inner perichaetial leaves elongated after fertilization

and the elongate stem vaginula held old archegonia

and paraphyses and enclosed a great part of the seta

(Fig. 5b).

In Neckeropsis andamana the branch with the

early-fertilized archegonium had a few small hyaline

to reddish paraphyses and some new multicellular

structures. After the separation of the calyptra,

paraphyses were multiseriate and looked like ligulate

to lanceolate leaves of different widths, not

completely developed. Aborted archegonia were

displaced by the multiseriate paraphyses, the

reproductive branch increased little in length, the

elongate perichaetial leaves were located at the base

and the small stem vaginula had archegonia and

remains of uniseriate paraphyses (Fig. 5c).

Neckeropsis andamana and N. fimbriata had a wider

type of multiseriate paraphyses that looked like

ligulate to lanceolate leaves located under the

vaginula. In N. fimbriata the multiseriate paraphyses

were also restricted to the upper part of the axis and

the differentiation from the leaves was evident; the

short stem vaginula contained only the foot and the

minute seta (Fig. 5d).

The multiseriate paraphyses of Neckeropsis

undulata were wider than those in N. nano-disticha

and N. crinita (10–15 lines of cells). In mature

sporophytes most of the uniseriate and biseriate

paraphyses were gone and the branch looked less

robust than at earlier stages. The leaf-like paraphyses

of N. andamana had folds near the serrate margins

and some appeared to have costae (also documented

by Touw 1962), but on closer examination this was

disproved. Between the multiseriate paraphyses,

small (2–3 cells) uniseriate paraphyses were found.

The leaf-like paraphyses of N. fimbriata were serrate

like the perichaetial leaves and before the complete

maturation of the sporophyte new multiseriate

paraphyses appeared.

DISCUSSION

To establish the origin and homology of the

paraphyses in N. disticha we followed the

development of these structures by examining

consecutive growing stages of the reproductive


branches. Before fertilization paraphyses are short,

hyaline and uniseriate and after fertilization these

start to elongate and broaden to form irregular

paraphyses. The paraphyses ranged from uniseriate

to biseriate or of three or more lines of cells. During

the swollen venter stage, until the calyptra separation,

various types of paraphyses develop; Touw (1962)

interpreted these as transitions. Neither the widened

paraphyses nor the other slender multiseriate

paraphyses form the final stage.

Although the multiseriate structures (Fig. 2e) of

early stages look like leaves and their development is

similar to Bopp’s (1984) characterization of leaf

development; these structures do not develop from a

primordium (bud) of a metamer (Fig. 3b).

According to the current knowledge about the

development of the sexual branches the apical cell of

these stopped growing and the gametangium

differentiates from the apical cell (Ignatov & Hedenas

2007; La Farge-England 1996; Mishler & De Luna

1991). Therefore, multiseriate paraphyses are not

homologous to leaves. Rather the leaf-like structures

should be considered as multiseriate paraphyses by

their position on the gametoecia and their similarity to

the multiseriate paraphyses that develop before them.

We recognize the different types of paraphyses

that develop during the maturation of the

sporophyte as a transition series, similar to the

heteroblastic series of leaves in a branch (Mishler &

De Luna 1991) and the transition series of the

pseudoparaphyllia around a branch primordium

(Ignatov & Hedenas 2007). Each of the patterns

observed represents a different expression where the

development stopped. Although we find a similar

pattern of development and phyllotactic

arrangements as described for pseudoparaphyllia and

Figure 5. Reproductive branch and mature sporophyte of N. undulata. a. Fertile archegonium with multiseriate paraphyses. b.

Mature sporophyte with multiseriate paraphyses and stem vaginula (v). Reproductive branch and mature sporophyte of N.

lepineana. c. Young sporophyte with multiseriate paraphyses. d. Mature sporophyte with multiseriate paraphyses growing at the

end of small stem vaginula (v).


scaly leaves by Ignatov and Hedenas (2007), the

starting point in this case are paraphyses. Following

Mishler and De Luna (1991) the new multiseriate

paraphyses are the young paraphyses (from a mature

stage), while the biseriate and other paraphyses are

fully developed juvenile forms. The resulting

multiseriate paraphyses that form the final structure

are the fully developed mature paraphyses. In

contrast to the heteroblastic development of leaves

on a branch, the whole developmental series of the

paraphyses does not remain on the branch and are

probably ephemeral. The progressive sequence of

paraphyses is arranged around the fertilized

archegonium, leaving the multiseriate paraphyses

nearer and the other transitions farther from it.

For the other five species of Neckeropsis the

developmental sequence of the paraphyses contribute

to a more elaborate and complete scenario (Table 2).

The first type of paraphysis to appear is uniseriate

and hyaline; these should be considered the

paraphyses earliest juvenile phase: first the

paraphyses with thin cell walls and then the thick-

walled ones. Consequently, the biseriate and thin

multiseriate paraphyses would be late juvenile

paraphyses. The mature phases of paraphyses would

be the multiseriate leaf-like paraphyses. For example

the early stage is noticeable as fine long paraphyses in

N. nano-disticha and N. crinita, the next stage would

correspond to the wider paraphyses of N. disticha

and N. undulata, and finally the late mature

paraphyses would be the ligulate to lanceolate

structures in N. fimbriata and N. andamana. Between

these phases numerous transitions are present.

Neckeropsis nitidula, N. obtusata and N.

lepineana have only the juvenile types of paraphyses

and the elongation of perichaetial leaves occurs after

fertilization similar to what has been documented in

other pleurocarpous species as modifications

involved after fertilization. These species have

elongation of the reproductive stem around the foot

and differentiation of the vaginula. In N. exserta the

elongation of the axis is similar to the stem vaginula

and the paraphyses are in the juvenile stage. The

short paraphyses (2–4 cells) located near the inner

perichaetial leaves of N. fimbriata, N. andamana and

N. crinita could also be considered axillary hairs

following the definition of Saito (1975) and Hedenas

(1989). We define them as paraphyses base on the

overall similarities and we suggest that they share

similar functional and genetic background.

An interesting point is that some non-fertilized

reproductive branches have biseriate and multiseriate

paraphyses, as is the case of the perigonia of N.

fimbriata, N. nano-disticha and N. undulata and the

perichaetia of N. obtusata, N. crinita and N. nano-

disticha. A possible explanation is that the serial

development of paraphyses is independent of

fertilization but depends on the viable time of the

fertile branch. However fertilization prolongs and

accelerates the maturation of the branch and in

consequence of the paraphyses.

CONCLUSIONS

The leaf-like structures in some species of

Neckeropsis, previously deemed ramenta, are

homologous to multiseriate paraphyses. Different

types of paraphyses during the maturation of the

fertilized archegonium represent separate stages in

the developmental sequence of the paraphyses. The

numerous transitions found are stages between

juvenile (uniseriate) and mature (multiseriate)

paraphyses, each of them being representations of

where the development stops.

The leaf-like structures surrounding the

sporophyte consist of mature multiseriate

paraphyses; these present a progression in various

species. In N. nano-disticha and N. crinita the

multiseriate paraphyses are thinner and are fully

developed at the early mature stage while the

paraphyses of N. undulata and N. disticha are in a

middle stage; these paraphyses are wider than the

former two species. Neckeropsis andamana and N.

fimbriata present the late mature stage with

paraphyses that look like slender lanceolate leaves.

The ontogenetic data provided would be useful

for the phylogenetic analysis of the genus Neckeropsis,

but this information can also be applied to

understand paraphyses and other structures in other

moss taxa. More ontogenetic studies should be

promoted to elucidate other problematic structures,

including the development of reproductive branches.

ACKNOWLEDGMENTS

We thank the reviewers, especially B. Crandall-Stotler and

Sharon Bartholomew-Began.


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ms. received September 26, 2007; accepted November 3, 2008.


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