INTRODUCTION

Undaria pinnatifida (Harvey) Suringar, 1873 is

an invasive brown algae, native from Japan, south-

ern China and Korea (Saito 1975). This species

was introduced in several coastal areas and has

become established in the Mediterranean Sea,

European Atlantic, New Zealand, Australia, Tas-

mania and Argentina. The arrival of Undaria to the

Mediterranean coast was reported by Perez et al.

(1981), and it is believed that it was introduced

along with the Japanese oyster Cassostrea gigas

for cultivation (Boudouresque et al. 1985; Floc’h

et al. 1991). Later, Undaria was recorded along

the coast of Brittany and was subsequently regis-

tered on the Atlantic coasts of England and Spain

(Perez et al. 1984; Santiago Caamaño et al. 1990;

Fletcher and Manfredi 1995). Numerous works on

MARINE AND FISHERY SCIENCES 33 (1): 77-94 (2020). https://doi.org/10.47193/mafis.3312020061805

DEVELOPMENT MORPHOLOGY OF Undaria pinnatifida SPOROPHYTES

(PHAEOPHYCEAE, ALARIACEAE) IN CALETA CORDOVA (CHUBUT, ARGENTINA)

MARÍA VICTORIA ALVAREZ1, 2 and ALICIA BORASO2

1Departamento de Biología, Facultad de Ciencias Naturales y Ciencias de la Salud,

Universidad Nacional de la Patagonia San Juan Bosco (UNPSJB),

Ruta Nacional Nº 1 km 4 s/n, Comodoro Rivadavia, Argentina

e-mail: marivikalvarez@gmail.com

2Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET),

Instituto de Desarrollo Costero “Dr. H. C. Héctor E. Zaixso”, Centro de Investigación y

Transferencia “Golfo San Jorge”, Universidad Nacional de la Patagonia San Juan Bosco (UNPSJB),

Ruta Nacional Nº 1 km 4 s/n, Comodoro Rivadavia, Argentina

ABSTRACT. Undaria pinnatifida is an invasive brown algae that has been found on the Argentine coast since 1992.

This work aims to follow the ontogeny of sporophytes, from egg fecundation to thallus senility, and thereby contribute

to information on the development of the species in San Jorge Gulf. Sporophytes obtained in the laboratory were used

to study the first stages of development, while samples collected from field population were used to describe advanced

stages. Morphological observations were carried out on fronds, stipes, midrib, sporophylls and holdfasts of thalli at dif-

ferent developmental stages, and they was interpreted related to its functionality. Sporophytes described as typical and

distant forms were found, and their location in the coastal zone was determined. Primary growth of sporophyte begins

in the intercalar meristoderm located between the frond and the stipe. The upper portion of the intercalar meristem pro-

duces a row of small pinnules, and its lower portion is the origin of the lateral stipe ribbons. The thallus area and growth

in thickness occur through a meristoderm in the frond surface. Characteristic morphological structures such as gland

cells, filaments and trumpet cells, and cryptostomata were observed. Some of the gland cells lead to the formation of

hair-filled cryptostomata. This work contributed to increase the knowledge of anatomical characteristics of the thallus

at different moments of development of this invasive species.

Key words: Morphology, Undaria pinnatifida, invasive species, San Jorge Gulf, sporophytes, meristoderm.

the introduction and dispersal of Undaria on the

European coasts (Hay 1990; Rismondo et al.

1993; Salinas et al. 1996; Cecere et al. 2000;

Peteiro 2008; Minchin and Nunn 2014; Minchin et

al. 2017, among many others), the Northeast

Pacific (Silva et al. 2002; Aguilar-Rosas et al.

2004; Thornber et al. 2004; Dietrich and Lonhart

2010) and the Southern hemisphere (Hay and

Luckens 1987; Stapleton 1988; Sanderson 1990;

Campbell and Burridge 1998) can be mentioned.

In particular, on the Argentine coast (Figure 1)

it was first detected in Nuevo Gulf in 1992 (Piriz

and Casas 1994; Casas and Piriz 1996). By 1997,

the species expanded 4.6 km north and 6.1 km

south, while in 1999 it was found 12 km north

and 22 km south (Piriz and Casas 2001; Casas et

al. 2008). At the end of 2000, Undaria was regis-

tered on the coast of Camarones Bay (approxi-

mately 300 km south of Nuevo Gulf). In mid-

2005, Undaria was observed for the first time on

the shores of Puerto Deseado estuary, 600 km

south of the first point of entry (Martin and

Cuevas 2006), and since then no records of the

species further south have been made. During the

first years of the invasion, the species only

spreaded to the south, suggesting that Valdés

Peninsula represented a natural barrier to its dis-

persal; notwithstanding it was observed in San

José Gulf in 2008. Consequently, it is estimated

that its arrival to San Matías Gulf was in 2010

(Pereyra et al. 2014), while its presence on the

coasts of Buenos Aires Province (Mar del Plata

city) was documented in 2011 (Meretta et al.

2012), thus leading to the speculation that it could

reach Uruguay and even southern Brazil (Della-

torre et al. 2014).

The introduction of U. pinnatifida can occur

accidentally, as in the case of the Mediterranean

Sea (Perez et al. 1984), the Venice Lagoon (Curiel

et al. 1994), New Zealand (Hay and Luckens

78 MARINE AND FISHERY SCIENCES 33 (1): 77-94 (2020)

Figure 1. Study area indicating locations in the Patagonian coast of Argentina.

1987) and Argentina (Piriz and Casas 1994), or

intentionally for aquaculture. This species was

first introduced for culture experiments on the

coast of Brittany (Perez et al. 1984; Castric-Fey et

al. 1993) and was subsequently introduced in

Spain for the same purpose (Perez-Cirera 1997;

Peteiro 2001 in García and Peteiro 2015). The

most important vector of accidental dispersion is

via maritime traffic through fouling on ship hulls,

such as gametophytes or small sporophytes, or

through spores in ballast water discharge

(Williams and Smith 2007). Dispersion through

fouling is mentioned by Fletcher and Manfredi

(1995) for Southern England, Curiel et al. (2002)

for the Island of Venice, and Minchin and Nunn

(2014) for Northern Europe, among others. The

introduction of Undaria through ballast water

discharge has been reported for New Zealand,

Tasmania and Argentina (Hay and Luckens 1987;

Sanderson 1990; Piriz and Casas 1994).

Distribution and reproductive stages of

Undaria in Argentine coast were analyzed by

Casas and Piriz (1996) after its entry into Nuevo

Gulf. Subsequently, same authors studied the

impact of the species on the environment and

how it dispersed (Casas and Piriz, 2001). In the

north of Argentine Patagonia, Pereyra et al.

(2015) analyzed the expansion of the species in

San Antonio Bay.

Macroalgae are characterized by their large-

sized thalli, made up of a pinnate frond with a

midrib, a stipe that separates the holdfast from the

frond and in which the sporophylls develop upon

reaching reproductive maturity, and a holdfast

that adheres to the hard substrate (Guiry and

Guiry 2014). This basic morphology presents an

appreciable degree of variability (Yendo 1911;

Okamura 1915; Castric-Fey et al. 1999; Cecere et

al. 2000; Uwai et al. 2006) which has been

thought to have genetic or plasticity components

in the face of spatial or seasonal environmental

variability. According to different authors (Stuart

et al. 1999; Shibneva and Skriptsova 2012), most

recognized forms of U. pinnatifida sporophytes

are: a) Distant form, which corresponds to an

elongated stipe, as long as the lamina, with large

sporophylls limited to the basal area of the stipe

and without proliferations; b) Typical form, with

short stipe thalli and comparatively shallow sinus-

es between adjacent pines, far from the midrib.

Upper parts of the sporophyllic zone are formed

of large sporophylls (folds) confluent with the

base of the frond; and c) Narutensis form (Yendo

1911) (=typical form, Okamura 1915), with very

short stipes, slightly folded sporophyll zone, and

ligulated proliferations of the sporophyll margins.

This study analyzes the ontogeny of the sporo-

phyte, and aims to describe the developmental

stages of U. pinnatifida, from egg fertilization to

senility of the thallus. It represents a contribution

to the knowledge of anatomical characteristics of

the thallus at different moments of development

of this invasive species, which have not yet been

described for Caleta Cordova population (San

Jorge Gulf).

MATERIAL AND METHODS

Study area is located in the central zone of San

Jorge gulf (Figure 1), where U. pinnatifida is pres-

ent. The coast of Caleta Cordova (45° 44′ 22″ S,

67° 22′ 26.9″ W) is made up of sedimentary rock

with tidal pools and channels. Tides are character-

ized as semi-diurnal with average amplitude of

6 m (Zaixso et al. 2009). Middle and upper

mesolithic horizon are covered with mussel

Perumytilus purpuratus, while in the lower infra-

littoral zone Corallina officinalis can be found

together with banks of Aulacomya atra and mus-

sel Mytilus platensis (Gil and Zaixso 2008).

Morphological and anatomical observations of

first stages of thallus development were studied

in sporophytes obtained from cultures of gameto-

phyte in the laboratory. More advanced stages

were studied in sporophytes collected from field

population.

ALVAREZ AND BORASO: DEVELOPMENT MORPHOLOGY OF UNDARIA PINNATIFIDA IN ARGENTINA

Thalli at different developmental stages were

collected randomly each month from lower inter-

tidal and upper subtidal zones of the rocky shore

of Caleta Cordova during extraordinarily low

tides or through scuba diving when necessary.

Sporophytes were collected from April 2017 to

November 2017 because of during December to

March there are very few sporophytes on the

ground, and most of them are senile with dam-

aged structures. A total of 80 observations of

Undaria thalli were made.

Gametophyte cultures were obtained monthly

from spores released by fertile sporophytes. Ten

cultures were started each month. Sporophyll

materials located on slides were cultured inside

glass containers filled with 150 ml of enriched

seawater renewed weekly. Gametophyte cultures

were maintained in filtered seawater enriched

with 1 ml of stock solution (3 g nitrates, 0.3 g

phosphates, 0.7 g iron chloride, and 2 g EDTA per

liter of seawater). Cultures were maintained

between 10-14 °C (taking into account tempera-

tures in natural conditions during harvest months)

and irradiation of 40-80 µM m2 s-1 from a 40-Watt

fluorescent lamp (Pang and Wu 1996) under a

12:12 light: dark cycle. Development of sporo-

phytes in these cultures continued until the frond

reached about 3 mm in length.

In order to understand development stages at

tissue level, sections ranging from 2 cm long to

fully developed sporophytes were taken, covering

the meristematic and mature areas of the frond,

midrib, sporophyll, stipe and holdfast of each

specimen. Microscopic observations and photo-

graphic records of these events were taken.

Whole-mount slides, cross sections and longitu-

dinal sections were made by hand with a stain-

less-steel razor blade. Photographs of unstained

sections were taken with a Samsung digital cam-

era and a Zeiss Standard 25 microscope. A sample

of specimens was deposited in the Herbario

Regional de la Patagonia (HRP) at the Universi-

dad Nacional de la Patagonia San Juan Bosco,

Comodoro Rivadavia (HRP 7480 to HRP 7502).

The development of the sporophyte was divided

into stages according to an increasing order of

structural complexity with respect to the number

of cells (in the embryonic stages), tissue differen-

tiation, presence of structures (such as glandular

cells, cryptostomata and trumpet cells), length of

the frond, presence of pinnae, and the reproductive

state of the thalli. The development of the sporo-

phytes was divided into the following stages:

- Embryonic postzygotic thalli (Figure 2 A).

- Embryonic laminar thalli, initially monolay-

ered, up to 2-3 mm long (Figure 2 B).

- Pre-sporophyllic juvenile thalli, before pinnae

differentiation, less than 10 cm long (Figure 2 D).

- Pre-sporophyllic juvenile thalli, with differen-

tiated pinnae, up to 30 cm long (Figure 2 E).

- Thalli, longer than 30 cm, vegetative or repro-

ductive, with an active growth zone between

the frond and stipe (Figure 2 G, 2 I and 2 J).

- Senile thalli of variable size with zones

between frond and stipe completely filled with

well-developed sporophyll, and immature

juvenile thalli with blades and stipes damaged

by environmental conditions (Figure 2 K).

RESULTS

Embryonic thalli

Two successive embryonic stages were identi-

fied. The first one was the postzygotic embryonic

thalli, which was monoseriate filament of 2-20

cells long. This stage began with the longitudinal

division of the filament apical cell and the devel-

opment of growth zones along the edge of the

tiny frond (Figure 2 A). The second stage was the

embryonic laminar thalli with a length of 2-3 mm

(Figure 2 B).

Germ tube (Figure 3 A) and first gametophyte

cells were produced during the first two weeks

after liberation of viable spores. Female gameto-

80 MARINE AND FISHERY SCIENCES 33 (1): 77-94 (2020)

ALVAREZ AND BORASO: DEVELOPMENT MORPHOLOGY OF UNDARIA PINNATIFIDA IN ARGENTINA

Figure 2. General external development. A) Embryonic post-zygotic thallus. B) Embryonic laminar thallus. C) Stipe before the

formation of lateral wings. D) Pre-sporophyllic thallus with entire frond. E) Pre-sporophyllic thallus with pinnae. F) Ini-

tial stage of sporophyllic thallus with active growing zone between frond and stipe, and beginning of lateral wings. G)

Stipe with folded sporophyll. H) Pinnulae growing into pinnae at the frond base. I) Sporophyll with frills restricted to the

basal portion. This sporophyte corresponds to the distant form. J) Sporophyll in a more mature stage. K) Thallus with

sporangial sori also developing on the basal portion of the frond without active growing zone remaining between the

frond and the stipe. Sporophyte corresponds to the typical form.

50 mm

1 mm

5 mm

5 cm

10 cm

5 cm

10 cm

1 cm

2 cm

10 cm

1 cm

phytes produced lateral rows of short filaments

(Figure 3 B) with apical oogonia. After this, in the

same conditions, mature male gametophytes (Fig-

ure 3 C) formed spermatangium which released

one or more biflagellate anterozoids, that fertil-

ized the oogonium.

Embryonic laminar thalli were initially mono-

layered (Figure 3 D). Solitary phaeophycean

hairs with a basal meristem were seen on the sur-

face or margins of small embryonic fronds less

than 1 mm long (Figure 3 E, 3 F and 3 G). These

hairs were deciduous and left scars at their inser-

82 MARINE AND FISHERY SCIENCES 33 (1): 77-94 (2020)

Figure 3. Embryonic thalli. A) Germ tube. B) Female gametophytes. C) Male gametophytes. D) Transversal section of single-

layered thallus. E) Hair primordium at the thallus margin. F) Phaeophycean hair. G) Subapical hair. H) Uniseriate rhi-

zoids. I) ‘Y’-shaped thickened central ribbon at the base of the embryonic frond.

EFD

50 mm

10 mm

HIG

50 mm10 mm

10 mm

5mm

tion points. The presence of these hairs could

indicate a nutrient deficit in the culture medium

used.

When the frond was about 2 mm long, its low-

ermost cells elongated and formed the beginning

of the cylinder stipe, which adhered to the sub-

strate through a few uniseriate lateral rhizoidal

filaments (Figure 3 H). Thalli with this character-

istic were collected from intertidal tide pools dur-

ing autumn. At this stage, the frond was still

monolayered and had a margin of small quadran-

gular cells (Figure 3 G); a region of smaller,

apparently meristematic cells between the flat-

tened frond and the cylindrical basal zone was

observed. At the basal zone of the most advanced

laminar embryonic thallus, a central darker rib-

bon similar to letter ‘y’ was frequently observed

(Figure 3 I).

Pre-sporophyllic juvenile thalli

It was established that the embryonic stage was

over and the pre-sporophyllic juvenile stage had

started when the layer of meristoderm could be

distinguished. Frond midrib began as a central

ribbon of cells when the multilayered frond was

only a few millimeters long. Meristodermic zone

between the frond and the stipe could already be

observed when the thallus was a few centimeters

long. In this growing zone, short pinnulae were

formed along the lower margins of the midrib

(Figure 2 H). Later, pinnulae flattened and

formed the lateral frond pinnae (Figure 2 I).

The apex of young pinnae had only one meris-

toderm layer (Figure 4 A); however, a few layers

of undifferentiated cells were produced inwardly

close to the apex (Figure 4 B), and long medullary

cells and a thin cortex of pigmented cells with

some young gland cells were also observed. At

the center of the fronds, and also along the sinuses

of the growing pinnae, subepidermic cells pro-

duced some additional filaments which grew

inwards and reached the cortex on the other side

(Figure 4 C).

In young areas of the frond, the meristoderm

with hyaline gland cells, the cortical tissue and

the medulla (Figure 4 D) with young trumpet

cells in formation could be observed (Figure 4 E).

A few intermediate layers of somewhat elongat-

ed, less pigmented cells were observed between

the outer pigmented cortex and the medulla.

Young medulla consisted of trumpet cells that

could be differentiated very early on (Figure 4 F),

and anticlinal filaments with diameters averaging

10 µm, forming a net, which could be either

dense (Figure 4 G) or lax (Figure 4 H).

The external aspect of the surface differed

depending on the age of the epidermal tissue, the

distance to the growing margin and the presence

of gland cells and hair-filled cryptostomata. In the

younger zones, each meristodermic cell con-

tained several parietal chloroplasts (Figure 4 I),

and as the thallus became older the chloroplasts

filled the cell volume (Figure 4 J).

Gland cell and cryptostomata formation

Gland cells differentiated from meristoderm

cells at the frond margins. Gland cells were denser

(ca. 300 cells mm-2) in young thalli (< 5 cm long)

(Figure 5 A and 5 B) and in the apical portions of

pinnae in more developed thalli. As the frond

grew, gland cells became sparser and were found

further from the frond margin. In older thalli, some

gland cells could be found in the middle of the

frond and the midrib, but never as dense as in

young growing zones. Most of gland cells

increased in volume and their content became hya-

line (Figure 5 B). They were usually very conspic-

uous because of their larger volume and the pur-

ple/burgundy to yellow color (Figure 5 C).

Enlarged cells at the surface were displaced

below the meristoderm and became transition

cells (TC) (Figure 5 D), which in turn produced

the hair-filled cryptostomata. A pore opened in

the meristoderm immediately over TC (Figure 5

E). TC developed several outgrowths towards the

inside of the thallus (Figure 5 F) and divided into

small, lenticular cells with thickened edges

ALVAREZ AND BORASO: DEVELOPMENT MORPHOLOGY OF UNDARIA PINNATIFIDA IN ARGENTINA

84 MARINE AND FISHERY SCIENCES 33 (1): 77-94 (2020)

Figure 4. Frond structure. Longitudinal sections at the margin of a very young, monolayered thallus. A) Small meristoderm cells

at the lobe apex. B) Single-layered cortex near to the apex. C) Cross section of a young portion of the frond with trans-

verse medullary filaments. D) Cross section showing continuity between cortex and medulla. E) Formation of trumpet

cells in the young medulla. F) Trumpet cells in older medulla. G) Cross sections in fully developed frond, compact

medulla. H) Lax medulla. I) Surface view of meristoderm cells with chloroplasts. J) Surface view of meristoderm cell

with chloroplasts at an older zone.

ABC

DEG

HIJ

50 mm

50 mm50 mm50 mm

20 mm

100 mm

20 mm

20 mm10 mm

ALVAREZ AND BORASO: DEVELOPMENT MORPHOLOGY OF UNDARIA PINNATIFIDA IN ARGENTINA

Figure 5. Gland cells and cryptostomata. A) Dark gland cells (GC) in young thalli. B) Hyaline GC in a young frond. C) GC super-

ficial view. D) Transition cell (TC). E) Pore. F) Filaments growing inwards. G) Lenticular cells cross section of TC outer

surface. H-J) Formation of cryptostomata.

CDE

HIJ

50 mm

20 mm

10 mm

20 mm

5mm

100 mm

towards the outer surface (Figure 5 G). The

lenticular cells became flat, polygonal with

hexagonal outlines (Figure 5 H), which then

divided transversely producing the hair primordia

at the center of their outer surface. After some

elongation, hairs appeared as a tuft through the

pore in the meristoderm (Figure 5 I and 5 J).

Hairs were firmly anchored into the thallus

through the basal filamentous tissue of the crypt.

They continued developing until reached several

millimeters long and were observed as hyaline

spots on the adult thalli at the naked eye.

Midrib and stipe

Sections of the midrib and stipe had a similar

structure. Globose cells in the cortex were

observed in the cross section of the midrib (Figure

6 A) with the notable presence of a net-like struc-

ture of trumpet filaments in the medullary zone

(Figure 6 B). In the longitudinal section these cells

elongated longitudinally (Figure 6 C). Cross sec-

tion of the very young stipe had an external layer

of strongly pigmented cells, a cortical zone

formed of about ten rows of small cells (Figure 6

D) and a filamentous medulla (Figure 6 E). At the

end of the pre-sporophyllic stage, the stipe was

already compact and cortex cells became transver-

sally globose and somewhat elongated longitudi-

nally (Figure 6 F and 6 G). The medulla was lim-

ited to a thin, flat cell layer located in the middle

of the frond. In this study, thalli up to 30 cm long

remained at the pre-sporophyllic stage. At the end

of this stage, two lateral wings were formed along

the young stipe (Figure 2 F).

Sporophyllic thalli

Thalli over 30 cm long showed some signs of

sporophyll development. This development

began at an early stage or just when pinnae could

be distinguished on the frond. The lateral ribbon

of the stipe generated sporophylls (Figure 2 F and

2 G). The surface of the lateral fringes along the

stipe grew faster than the stipe in length, and this

difference in growth led to the formation of the

adult sporophyll frills. At first, the younger por-

tion of the sporophyll adjacent to the primary

meristematic zone was unfolded (Figure 2 G); as

it matured (Figure 2 I, 2 J and 2 K) frills were

seen along most of the stipe, and the entire length

of the stipe was covered with frills when sporo-

phyll development was completed. By this stage,

no meristematic zones were left (Figure 2 K).

Specimens with characteristics of Figure 2 I

were collected between August and September in

the upper subtidal, and these thalli belonged to

the distant form. Thalli with characteristics of

Figure 2 J were found in tidal pools of the lower

intertidal and upper subtidal during spring

months. These thalli belonged to the typical form.

Meristoderm, cortical and medullary layers

were observed in the transverse section of sporo-

phylls. The most distinctive feature was the pres-

ence of sori with unilocular sporangia and para-

physes on both sporophyll surfaces (Figure 6 H, 6

I, 6 J and 6 K). Parparaphyses capped by mucilagi-

nous masses protected the sporangia until the

spores were released (Figure 6 J and 6 K).

Senescent thalli

While sporophytes grew, distal zones of the

fronds became damaged, and fronds became

shorter and wider. In senescent thalli, which had

attained full sporophyll development, reproduc-

tive sori also developed on the lowest pinnae of

the frond (Figure 6 L). At the end of the growth

cycle, thalli which have lost the entire frond but

still adhered by the holdfast presented remains of

the sporophyll. These thalli were observed more

frequently at intertidal tide pools or detached

from the substrate during the summer.

Adhesion of the adult thalli

The holdfast was formed by dichotomic rami-

fications or haptera (Figure 7 A, 7 B, 7 C and 7

D). Holdfasts adapted anatomically according to

86 MARINE AND FISHERY SCIENCES 33 (1): 77-94 (2020)

the substrate. On hard substrates such as rock or

encrusting coralline algae, the holdfast of the

adult thallus consisted of a few sturdy branches

(Figure 7 C). In contrast, haptera were crowded

and medium sized on flat fronds, and when they

were attached to branches of Corallinaceae, such

as Corallina sp., haptera usually had several

small branches (Figure 7 D). The medullary zone

had cylindrical cells in a longitudinal direction,

with the absence of trumpet filaments (Figure 7

ALVAREZ AND BORASO: DEVELOPMENT MORPHOLOGY OF UNDARIA PINNATIFIDA IN ARGENTINA

Figure 6. Midrib, stipe and sporophyle. Midrib: cross section (A), detail of medullary filaments (B), longitudinal section of

midrib (C). Cross section of a young thallus stipe: cortex (D), flattened medulla (E), cross section with cortex in more

developed thallus (F), idem in longitudinal section (G). Successive stages of development of sori: initial stages (H), later

stage with gelatinous surface (I), detail of paraphyses with gelatinous distal walls (J), later stage with mature sporangia

(K), cross section at the lower portion of the frond in a senescent thallus, partially covered with sori (L). c: cortex. m:

medulla.

ABC

DEF

GHIJ

50 mm

20 mm50 mm

20 mm20 mm50 mm

50 mm20 mm20 mm20 mm

20 mm1 mm

88 MARINE AND FISHERY SCIENCES 33 (1): 77-94 (2020)

Figure 7. Holdfast. A) Young holdfast with two levels of dichotomy. B) Young holdfast with several levels of dichotomy. C) Adult

holdfast with a few branches on encrusting corals. D) Adult holdfast with many branches on Corallina officinalis. E)

Haptera longitudinal section, cylindrical cells of the medullary zone. F) Haptera cross section, cortical zone. G) Haptera

apex detached from the hard substrate. H) Surface between haptera and rocky substrate. I) Haptera longitudinal section

with undifferentiated cortical tissue and very thin epidermis. J) Haptera apex with undifferentiated cells. K) Haptera apex

in contact with Lophurella.

ABC

DEF

GHI

50 mm

20 mm

2 cm

2 mm

5 cm 50 mm

20 mm

50 mm

20 mm50 mm

E), while the cortical zone of the holdfast was

characterized by the presence of ovoid cells (Fig-

ure 7 F). The contact points of the haptera with

substrates were apical (Figure 7 G) or in the

abaxial zone. On hard rock, haptera surface cells

could be globose, hyaline and relatively undiffer-

entiated at the contact points (Figure 7 H). In the

cylindrical zones of the holdfast not in contact

with the substrate, the haptera was made mostly

of longitudinally elongated cells (Figure 7 I) cov-

ered by a stratum of flattened superficial cells;

this stratum was absent from the zones in contact

with the different substrates (Figure 7 J).

When the thalli lived on thin, cylindrical algae,

such as Lophurella hookeriana, haptera was sur-

rounding their thalli, and somewhat a denser cel-

lular tissue of smaller cells on both surfaces was

formed (Figure 7 K).

DISCUSSION

Morphology of Undaria pinnatifida has a

genetic base and can also be affected by environ-

mental factors (Saito 1972; Stuart et al. 1999;

Park 2012). Sporophytes found in Undaria popu-

lation from Caleta Cordova corresponded to those

described as typical and distant forms, which

matches the findings of Casas (2005) in Nuevo

Gulf. Thalli of the distant form were found at

greater depths, corresponding to the subtidal

level, while thalli of the typical form were found

at tidal pools.

Very evident transformations among embryonic

stages were observed, in which the thallus consist-

ed of a uniseriate frond adhered to the substrate

only through the gametophyte, and adult thallus

with different tissues showed marked specializa-

tion and complexity. Five main elements can be

distinguished in the thallus of Undaria: frond,

stipe, midrib, sporophyll and holdfast. These ele-

ments have been considered here to elucidate the

deep transformations from the initial uniseriate fil-

ament to the complex adult thallus of U. pinnatifi-

da. Developmental differences observed between

these portions of the thallus might be related to

their distinct functionalities. Descriptions made in

this work are comparable with those made by

Casas (2005) for specimens from Nuevo Gulf.

Laminariales have a primary intercalary meris-

toderm that determines the general course of

growth (Lee and Yoon 1998; Castric-Fey et al.

1999). In this study, meristoderm was observed

between the frond and the stipe in U. pinnatifida.

In the upper portion a row of small lateral cilia or

pinnules was produced, from which the pinnae of

the frond was developed. Adult frond morpholo-

gy depends on the number of pinnules, which pre-

sented a very variable trait in samples from Cale-

ta Cordova population. The final area of the frond

is attained by the subsequent growth, which takes

places through the meristoderm on the surface of

the thallus.

Main functions of fronds are photosynthesis

and nutrient absorption, both of which depend on

the frond surface area. In the frond, the photosyn-

thetic meristoderm gives rise to an inner, color-

less layer of larger cells, which in turn produces a

lax medullary zone. The loss of the frond apical

tissue, observed even in young thalli, is effective-

ly balanced by the pinnae and midrib elongation.

This is characteristic of Laminares, in which new

tissue formation and distal tissue loss occur at the

same time (Larkum 1986; Skriptsova et al. 2004).

Yendo (1909) noted the presence of dark gland

cells which were more abundant in very young

thalli and young margins of pinnae. Our observa-

tions confirmed the greater abundance of gland

cells at the growth zones of the fronds. The pres-

ent study showed that hair-filled cryptostomata

originated from gland cells. Pang and Lüning

(2004) indicated that the quantity of hairs on the

surface of fronds is critical for the quality of com-

mercially harvested Undaria. These authors also

suggested that the presence of hairs on the fronds

was a response to a greater demand for nutrients

originated from the expanded surface-volume

ALVAREZ AND BORASO: DEVELOPMENT MORPHOLOGY OF UNDARIA PINNATIFIDA IN ARGENTINA

ratio of the frond. Hairs could also play an impor-

tant role in the prevention of herbivory (Schaf-

felke et al. 2005). In Argentina, Teso et al. (2009)

registered scraped-off biofouling species on

Undaria thalli. No signs of herbivory were

observed in the present study.

Stipe and midrib of the frond contribute to the

flexibility of the thallus and the orientation and

movement of the frond. Stipe is longer at greater

depths in order to locate fronds in areas with

greater illumination (Cremades-Ugarte et al.

2006). These data agreed with observations in the

coast of Caleta Cordova, where thalli correspon-

ding to the distant form were found in the subtidal

zone exposed to lower light intensity. Saito

(1975) reported Undaria growing on sites with

low to medium exposition to waves, while Rus-

sell et al. (2008) note its presence in higher

dynamic conditions. In Caleta Cordova and near-

by locations inside San Jorge gulf, U. pinnatifida

populations are found in relatively protected

sites, like small bays.

In the midrib and the stipe, the inner cortex is

more developed with several colorless cell layers.

The medullary zone is reduced to a thin plate,

while the multi-layered compact cortex con-

tributes to flexibility and strength, both necessary

for withstanding water movements and for nutri-

ent and gas absorption. Stipes maintains it struc-

ture until the end of the sporophyte life cycle.

Midrib would have a function similar to that of

the sieve tubes of vascular plants due to the pres-

ence of structures such as screened plates, fila-

ments and trumpet cells in their medullary zone.

This structure is the most important site for the

translocation of photoassimilates from the apical

area to the basal area of the frond (Wu and Meng

1997).

The folded structure of the sporophyll gener-

ates an increase in the surface of the sori, favoring

the reproductive capacity of this species, a char-

acteristic of invasive species. The sporophyll

structure is similar to the frond but thicker. Fertile

sporangia are produced on its surface in an almost

continuous layer. Schaffelke et al. (2005) report-

ed that functional zoospores are only liberated

from the most mature zones of the sporophyll, far

from the meristem. This assertion is true only for

younger fertile thalli, since sporophyll develop-

ment continues until it occupies the entire length

of the stipe.

The capacity to adhere to the available substra-

ta is essential for survival in each developmental

stage of Undaria, and is a characteristic of the

opportunistic seaweed able to rapidly colonize

new or disturbed substrata and artificial floating

structures (Hay 1990; Valentine and Johnson

2003, 2004). Undaria can also develop as an

epibion of marine invertebrates (Cremades-

Ugarte 2006). Embryonic frond is at first adhered

through the gametophyte and is later attached by

a few, thin, very characteristic lateral filaments.

In the juvenile stage, a holdfast primordium is

formed, whose haptera later divide dichotomical-

ly. The holdfast has a less complex structure than

the frond or the stipe, with a single layer of epi-

dermis and a cortex. However, a greater diversity

of tissues can be found at the contact points of the

haptera with different kinds of substrate.

Morphological structures observed in this

study are typical of this species and provide infor-

mation on the characteristics of the thallus at each

stage of development, which will be useful for

subsequent analyses.

ACKNOWLEDGEMENTS

We thank Lic. Juan Manuel Zaixso and Dr.

Mauro Marcinkevicius for their assistance in the

field, and Dr. Patricia Leonardi for her observa-

tions. This study is part of the PhD thesis of

María Victoria Alvarez at the Universidad

Nacional de la Patagonia San Juan Bosco, sup-

ported by a student grant from the Consejo

Nacional de Investigaciones Científicas y Técni-

cas (CONICET).

90 MARINE AND FISHERY SCIENCES 33 (1): 77-94 (2020)

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Received: 26 March 2020

Accepted: 26 May 2020

94 MARINE AND FISHERY SCIENCES 33 (1): 77-94 (2020)