Early development, life history and ecological habits of

Grateloupia constricata Li et Ding

Yuanyuan Ding

1†

, Yao Bian

1†

, Huina Wang

, Jing Liu

, Jingrui Li

, Hongwei Wang

College of Life Sciences, Liaoning Normal University, Dalian 116000, China

Received 23 August 2019; accepted 20 April 2020

©Chinese Society for Oceanography and Springer-Verlag GmbH Germany, part of Springer Nature 2020

Abstract

As the largest genus of Halymeniaceae, Grateloupia has been widely reported. Here, we observed the life history

and early development of Grateloupia constricata Li et Ding and investigated the effects of temperature,

irradiance, and photoperiod on the discoid crust and sporeling development of G. constricata under laboratory

conditions. We observed that the type of carpospore development was “mediate discal type”. The life history

included homotypic gametophyte (haploid), carposporophyte (diploid), and tetrasporophyte (diploid), with

typical isomorphic alternation of generations. The results of double factorial analysis showed that both single

factorial effects and interaction among temperature, photoperiod, and irradiance were obviously significant on

the discoid crust and sporeling development. Furthermore, we found that the optimum combination of condition

for the early growth and development of G. constricata was temperature 20°C, irradiance 80 μmol photons/(m

·s)

and photoperiod 16L:8D. This study provides the theoretical basis and technical support for the conservation of

the Grateloupia germplasm, artificial breeding, large-scale cultivation and sustainable development.

Key words: carpospore, life history, alternation of generations, temperature, irradiance, photoperiod

Citation: Ding Yuanyuan, Bian Yao, Wang Huina, Liu Jing, Li Jingrui, Wang Hongwei. 2020. Early development, life history and ecological

habits of Grateloupia constricata Li et Ding. Acta Oceanologica Sinica, 39(10): 155–161, doi: 10.1007/s13131-020-1662-5

1 Introduction

The marine alga Grateloupia constricata (Halymeniaceae,

Rhodophyta) was identified as a new species based on the mor-

phological and reproductive structure characteristics of female

gametophytes collected by Weixin Li from Qingdao, Shandong

Province, China in June 1984 (Xia et al., 2004).

The morphology of G. constricata is distinctive. The thalli are

upright, clustered, purplish red, up to 5–10 cm high and 1–1.5 cm

wide with pinnately branched 1–2 orders. Abundant branches

are opposite, alternate or partial with stick or long cones, usually

constricted or tapered at the base. There is a disciform holdfast at

the bottom of the algae for adsorbing on rock or shellfish (Fig. 1).

As a typical intertidal alga, G. constricata grows on the rocks in

the high and medium tidal zones and matures in August (Xia et

al., 2004).

Grateloupia constricata is an important economic species

which has not been artificially cultivated, probably because the

life history and ecological habit are still unknown (Fang et al.,

2011). In this study, we observed the life history, especially the

early development of G. constricata in detail under laboratory

condition. We also conducted the double-factorial experiment to

investigate the interaction among temperature, irradiance and

photoperiod on the discoid crust and sporeling development. We

found out the optimum conditions for early growth of G. con-

stricata, which could be the theoretical basis and technical sup-

port for the conservation of the Grateloupia germplasm, artificial

breeding, large-scale cultivation, sustainable development and

utilization.

2 Materials and methods

2.1 Sample collection and processing

The mature G. constricata (LNU17060506, LNU17060512,

LNU17060517, LNU17060565) used in this experiment were col-

lected at the First Swimming Beach, Luxun Park and Maidao of

Qingdao, Shandong Province in June 2017. We collected healthy

and fully developed gametophyte with mature cystocarps and the

tetrasporophyte with tetrasporangia, placed them in an incubat-

or filled with seawater. Female gametophytes with 80% mature

cystocarps were chosen and rinsed repeatedly with sterile seawa-

ter, and then washed with a brush to remove dirt, micro-organ-

isms and other miscellaneous algae on the surface of the algae.

The prepared algae were placed in a well-ventilated area to dry

for 1 h, then transferred to a sterile Petri dish with sufficient Prov-

asoli’s Enriched Seawater (PES). Seven glass slides were placed at

the bottom in each dish for the spore adhering and collection

(Provasoli, 1968). When the number of spores observed with an

optical microscope (100×) reached 20–30, the algae were re-

moved. GeO

(2 mg/L) was added to prevent the growth of other

algae and the culture solution was replaced every 2 d. After the

straight stereo appeared, the slides were transferred to a culture

cylinder (10 cm×10 cm×5 cm) for further cultivation.

2.2 Preculture for experimental condition setting

The spore-attached slides were pre-cultured in an illumina-

tion incubator (LHR-250-GB) under the following conditions:

temperature (20±2)°C, irradiance 80 μmol photons/(m

·s), salin-

ity 30±1 and photoperiod 12L:12D. When the diameter of discoid



Foundation item: The National Natural Science Foundation of China under contract No. 31570209.

*Corresponding author, E-mail: [email protected]

†

These authors contributed equally to this work.



Acta Oceanol. Sin., 2020, Vol. 39, No. 10, P. 155–161

https://doi.org/10.1007/s13131-020-1662-5

http://www.hyxb.org.cn

E-mail: [email protected]

crusts reached about 50 μm, the slides were transferred to the

specific environmental conditions for further experiments.

2.3 Double factorial experiments

We signed two types of double factorial experiments: temper-

ature vs. irradiance and temperature vs. photoperiod. All experi-

mental factors were remained the same as the preculture condi-

tions except for the double factors we chose. The pre-cultured

discoid crusts were placed at temperature of 5°C, 10°C, 15°C,

20°C, 25°C, 30°C, respectively. The irradiances were set to 50, 80

and 110 μmol photons/(m

·s), respectively. The photoperiods

were set to 8L:16D, 12L:12D and 16L:8D, respectively. A total of

18 combinations were detected with three parallel samples for

each combination (Table 1). We randomly selected ten disks

from each experimental group to measure their diameters after

14 d of culture. Sporelings with a height of about 500 μm were

placed at the same experimental conditions to measure their

heights after 21 d of cultivation.

2.4 Observations and data analyses

Photographs were taken using an Olympus BH2 microscope

(Olympus Beijing Co. Ltd., China). The images were mounted on

a Nikon camera DL C300-L (Nikon Corporation, Japan) and visu-

alized in Photoshop Adobe System. The progress of protoplast

transform was recorded with an Olympus BX53 ﬂuorescence mi-

croscope and digitally photographed. The images were captured

using the Olympus IPP software package and visualized in Pho-

toshop Adobe System. The relative growth rate (RGR, %/d) of

discoid crusts and sporelings were determined using the formula

RGR=(lnI

–lnI

)/t×100%. I

represents the initial diameter of disc-

oid crusts or the initial height of sporelings. I

represents the disc-

oid crust diameter or sporeling height after t d of cultivation.

Double factorial analysis was performed through Two-way AN-

OVA using SPSS 22.0 according to an adjusted P-value (<0.05).

An F-test was used to test for differences in the ranges of SD.

3 Results

3.1 Early development process of carpospores

Carposporophytes were formed within the female gameto-

phyte cortex of G. constricata. Matured carpospores were crim-

son and raised on the surface of female gametophyte with dia-

meter of 200–350 μm. Cystocarp holes, with diameter of 50–80 μm,

were discovered on the carpospores (Fig. 2a). Afterwards, car-

pospores overflowed from carpospore holes and attached to the

slide (Fig. 2b). The carpospores were spherical or elliptical, light

red in color, with diameter of about 15 μm (Fig. 2c). After cul-

tured for 24 h, carpospores began to germinate.

The germination progress was as follows: Firstly, protoplast of

the carpospores was depressed to one side and moved to the de-

pressed side (Fig. 3a). Meanwhile, the opposite side of the car-

pospores began to protrude and elongate to form a germination

tube. Then, protoplasts began to move towards to the germina-

tion tubes from the carpospores and finally filled the tip of ger-

mination tube (Figs 3b–d). When septum was formed between

the germination tube and translucent colloidal substance at its

original place, the cells in the germination tube began to divide

(Figs 2d–g). Subsequently, they entered the discoid crust stage of

early development, with the largest diameter reaching about

310 μm (Figs 2h–i). The adjacent discoid crusts fused with each

other and formed larger discoid crusts with 1–5 protrusions in the

center of the discoid crusts, then the protrusions grew into up-

right thalli (Figs 2j–l). After about another 30 d, the upright thalli

differentiated into upright branches (Fig. 2m). Upright branches

continued to grow for about 50 d and formed young sporelings.

Afterwards, they continued to develop into bifurcated sporeling

(Figs 2n–o). The development processes of the tetraspores and

carpospores were similar.

3.2 Life history of Grateloupia constricata

The life history of G. constricata included sexual reproduc-

tion and asexual propagation (Fig. 4). In sexual reproduction:

Gametophytes were dioecious. Spherical and colorless sper-

matangia were generated from epidermal cells of mature male

gametophyte of G. constricata, from which mature spermatia

were released. Carpogonial branch ampullar and auxiliary cell

ampullar were differentiated from inner cortex of G. constricata.

Carpogonial branch contained two cells, hypogynous cell and

carpogonium with a long trichogyne at bottom. The ellipsoid

auxiliary cells were characterized as bigger and deeper in color

compared with other cells. When mature spermatium attached to

trichogyne, the nucleus of spermatium got into the carpogonia of

the female gametophyte to form zygotes with the egg cells. The

fertilized carpogonium fused with the hypogynous cell to form a

Table 1.  Combinations of conditions for double factorial experi-

ments

Temperature vs. Irradiance Temperature vs. Photoperiod

Group T I Group T P

1 5 50 1 5 8:16

2 5 80 2 5 12:12

3 5 110 3 5 16:8

4 10 50 4 10 8:16

5 10 80 5 10 12:12

6 10 110 6 10 16:8

7 15 50 7 15 8:16

8 15 80 8 15 12:12

9 15 110 9 15 16:8

10 20 50 10 20 8:16

11 20 80 11 20 12:12

12 20 110 12 20 16:8

13 25 50 13 25 8:16

14 25 80 14 25 12:12

15 25 110 15 25 16:8

16 30 50 16 30 8:16

17 30 80 17 30 12:12

18 30 110 18 30 16:8

    Note: T represents temperature (°C), I irradiance (μmol

photons/(m

·s)), and P photoperiod (L:D).

2 cm



Fig. 1.  The field habitat of Grateloupia constricata Li et Ding.

a. The female gametophyte of G. constricata Li et Ding (arrow),

and b. the male gametophyte of G. constricata Li et Ding (arrow).

156 Ding Yuanyuan et al. Acta Oceanol. Sin., 2020, Vol. 39, No. 10, P. 155–161 

fusion cell. Afterward, zygotes in fusion cells enter the auxiliary

cells to continue developing through the connecting filaments,

which was previously formed between fusion cells and auxiliary

cells. Then, gonimoblasts were derived from auxiliary cells and

continued to divide. Finally, cystocarps emerged. Mature cysto-

carps scattered over both surfaces of blades, presenting as deep-

red spots. When carposporangium matured, carpospores were

released through a pore in the outer surface and began to gemin-

ate and divide, further formed discoid crusts and turned into up-

right thalli, finally tetrasporophytes.

In asexual propagation, the inner cortical cells of the sporo-

phyte in G. constricata produced tetrasporocytes, which then

a b c

d e f

g h i

j k l

m n o

300 μm

3 μm

20 μm

20 μm 20 μm 20 μm

20 μm

120 μm 1 mm

40 μm

10 μm



Fig. 2.  The development of carpospores in G. constricata Li et Ding. a. Distribution of carposporophytes (ch represents cystocarp

hole), b–c. carpospores, d. transformation of protoplasts, e–h. division of carpospores, i. formation of discoid crust, i–k. fusion of

discoid crusts, l. formation of upright thalli, m. upright branches, and n–o. growth of sporeling.

 Ding Yuanyuan et al. Acta Oceanol. Sin., 2020, Vol. 39, No. 10, P. 155–161 157

formed tetrasporangia. After cruciform division, tetraspores were

formed and released. The development process was similar to

the carpospores of G. constricata, which finally germinated into

female and male gametophytes.

Thus, the life history of G. constricata included homotypic

gametophytes (haploid), carposporophytes (diploid), and tet-

rasporophytes (diploid). The gametophytes were morphologic-

ally similar to tetrasporophytes, which indicated that G. con-

stricata belonged to isomorphic alternation of generations.

3.3 Effects of ecological factors on early development

Temperature, irradiance and photoperiod are typical abiotic

factors to affect the development and growth of intertidal algae

(Fortes and Lüning, 1980; Liu and Dong, 2001; Ouyang et al.,

10 μm

b c d

10 μm 10 μm 10 μm



Fig. 3.  The germination and transform progress of protoplast. The colored section was the merge effects of spontaneous fluorescence

of chlorophyll and lycopene. a. Carpospores without germination, b. germination tube appeared and the protoplast started to move, c.

protoplast continued moving, and d. protoplast filled the tip of germination tube.

distribution of cystocarp

released of carpospore

carpospores

transformation of protoplasts

carpospore germination

carpospore division

discoidal crust

fused discoid crusts

upright thalli

upright branch

carposporeling

tetrasporaphite

distribution of tetrasporaphite

tetraspore

transformation of protoplasts

tetrapore germination

discoidal crust

fused discoid crusts

upright thalli

upright branch

tetrasporeling

male gametophyte female gametophyte

spermatangium

carpogonial branch ambulla

tetrasporeling

transformation of

protoplasts



Fig. 4.  The life history of G. constricata Li et Ding.

158 Ding Yuanyuan et al. Acta Oceanol. Sin., 2020, Vol. 39, No. 10, P. 155–161 

2010; Wei et al., 2013). In order to explore the interaction of eco-

logical factors on the early development of G. constricata, we de-

signed two types of double-factorial experiments include temper-

ature vs. irradiance and temperature vs. photoperiod. The RGR of

discoid crust and upright thalli were tested to evaluate growth

state.

For the temperature vs. irradiance experiment, we dis-

covered that the RGR of discoid crusts and sporelings increased

from 5°C to 20°C and declined from 20°C to 30°C (Fig. 5). The

highest RGR of discoid crusts and sporelings occurred at temper-

ature of 20°C and irradiance of 80 μmol photons/(m

·s) (10.583%±

0.032% for discoid crusts, 8.869%±0.119% for sporelings). The

diameters of discoid crusts and sporelings respectively reached

(220±1.414) μm and (3.22±0.117) mm at the optimum condition.

The results of double factorial analysis showed that both temper-

ature and irradiance had significant effects on the growth of disc-

oid crusts and sporelings as the single factors. Intriguingly, we

found that there was an obvious interaction between temperat-

ure and irradiance (Table 2).

For the temperature vs. photoperiod experiment, the highest

RGR of discoid crusts and sporelings were at 20°C in each level of

photoperiod. When the photoperiod was 16L:8D, the RGR of

discoid crusts and sporelings in each level of temperature reach

the maximum except the sporelings cultured at 25°C (Fig. 6). Syn-

thetically, the optimum combination of temperature and pho-

toperiod condition for the growth of discord crusts and sporel-

ings was at 20°C and 16L:8D with the highest RGR

(10.251%±0.129% for discoid crusts, 9.670%±0.074% for sporel-

ings). The diameters of discoid crusts and sporelings reached

(210±5.437) μm and (3.81±0.085) mm at the optimum condition,

respectively. The results of double factorial analysis were similar

to that of temperature vs. irradiance, which showed a strong in-

teraction between temperature and photoperiod (Table 3).

4 Discussion

The knowledge of sporogenesis and morphological character-

istics including size and type are indispensable to distinguish and

identify different species of algae (Shunpei and Hassei, 1947).

Here, we observed and recorded the growth and development of

spores of G. constricata in detail. The results showed that the type

of carpospore development was “mediate discal type” and the life

history of G. constricata was the typical isomorphic alternation of

generations, which were consistent with G. filicina, type species

of Grateloupia, and other Grateloupia species such as G.

ramosissima, G. livida, G. tenuis, G. dalianensis, G. huanghaien-

sis and G. lanceolata (Figs 2 and 4) (Qian, 2014; Zhao, 2012; Song,

2013; Cao et al., 2015; Tian et al., 2017). Meanwhile, we found fu-

sion of discoid crusts, a phenomenon that two or more discoid

crusts fused to form a larger discoid crust (Figs 2j–k). As a univer-

sal event, fusion of discoid crusts occurred during early develop-

ment period in many species of Grateloupia and other Rhodo-

phyta (Chen and Ren, 1985; Vera et al., 2008; Li et al., 2010; Wang

Table 2.  The double factorial analysis of early growth in the various conditions of temperature and irradiance

Factor

RGR (discoid crusts) RGR (sporelings)

df F SS P df F SS P

Temperature 5 879.23 76 525.65 1.49×10

–36

5 703.68 21.78 7.88×10

–35

Irradiance 2 269.50 9 382.48 2.19×10

–22

2 142.56 1.77 7.82×10

–18

Interaction 10 42.91 7 469.52 5.37×10

–17

10 17.56 1.09 5.16×10

–11

    Note: df represents degree freedom, F F-test, SS Stdev Square, and P P-value.

a b

5 10 15

50 80

Irradiance/μmol photons·m

·s

110

Temperature/℃

The RGR of discoid crusts/%

The RGR of sporelings/%

25 30

5 10 15 20

Temperature/℃

25 30

50 80

Irradiance/μmol photons·m

·s

110



Fig. 5.  Effects of different temperatures and irradiances on the development of G. constricata Li et Ding discoid crusts (a) and

sporelings (b).

5 10 15 20

Temperature/℃

The RGR of discoid crusts/%

25 30

8:16 12:12

Photoperiod (L:D)

16:8

5 10 15 20

Temperature/℃

The RGR of sporelings/%

25 30

8:16 12:12

Photoperiod (L:D)

16:8



Fig. 6.  Effects of different temperatures and photoperiods on the development of G. constricata Li et Ding discoid crusts (a) and

sporelings (b).

 Ding Yuanyuan et al. Acta Oceanol. Sin., 2020, Vol. 39, No. 10, P. 155–161 159

et al., 2012; Song, 2013; Jiang et al., 2016; Tian et al., 2017). The

fusion of multiply discoid crusts could enhance the ability to fix

and resist the sour of sea water.

Temperature, photoperiod and Irradiance have been widely

reported to affect the growth and development of marine algae

and macroalgae (Fortes and Lüning, 1980; Liu and Dong, 2001;

Ouyang et al., 2010; Wei et al., 2013). To analyze the ecological

habits of G. constricata, we designed two type of double-factorial

experiments. We founded that the optimum combination of con-

ditions for the early development of G. constricata spores was as

follows: temperature 20°C, irradiance of 80 μmol photons/(m

·s)

and photoperiod 16L:8D, which was identical with the results of

G. asiatica published by Adharini and Kim (2014). Grateloupia

constricata can grow well in the temperature range of 10–25°C,

and the relative growth rate of the discoid crusts and sporelings is

the largest at 20°C (Fig. 5). The discoid crusts of G. asiatica can

grow well at 10–20°C, best at 20°C (Adharini and Kim, 2014). In

the suitable temperature range, the spores can develop into disc-

oid crusts quickly and then develop into sporelings. Therefore,

the temperature tolerance of the G. constricata is wide enough to

be the eurythermal species. When the temperature was under

10°C or above 25°C, the RGR of discoid crusts and sporelings de-

creased significantly (Fig. 5).

Generally, algae at spore stage are more sensitive to irradi-

ance. High irradiance levels can damage photosynthetic pig-

ments in cells and thereby negatively impact growth (Ouyang et

al., 2010). In our study, the optimum irradiance of discoid crusts

and sporelings of G. constricata was 80 μmol photons/(m

·s).

When the irradiance was 50 μmol photons/(m

·s) and 110 μmol

photons/(m

·s), the growth of discoid crusts and sporelings was

slower compared with that under the irradiance of 80 μmol

photons/(m

·s) (Fig. 5). The reason might be explained as the ir-

radiance of 110 μmol photons/(m

·s) and 50 μmol photons/(m

·s)

exceeded and hardly reached the light saturation point of the G.

constricata, respectively. Both situations might inhibit the syn-

thesis of chlorophyll a and decrease the photosynthetic rate.

Therefore, the energy from photosynthesis was insufficient to

maintain algae growth and development. On the other hand,

photoperiod adjusted algae growth by changing the illumination

time to affect the energy absorbed by the algae growth. As a

single ecological factor, longer illumination time might improve

the growth rate of G. constricata (Jiang et al., 2009). Our results

further verified this and we discovered that the photoperiod of

16L:8D was the optimum condition for the early growth of G. con-

stricata (Fig. 6).

The double factorial analysis showed that the interactions of

temperature vs. irradiance and temperature vs. photoperiod both

had significant effects on discoid crust development and sporel-

ing growth (P<0.01, Tables 2 and 3). Studies have shown that at

moderate temperatures, low irradiance culture condition is more

conducive to the development of the discoid crusts of G. yingge-

haiensis and G. dalianensis (Zhao, 2012; Wang et al., 2014).

However, high irradiance is more suitable for the development of

discoid crusts in G. tenuis (Cao et al., 2015). According to the res-

ults, we suggested that the interactions of different ecological

factors should be considered for cultivation and utilization of G.

constricata.

5 Conclusions

This research reported the life history, especially the early de-

velopment, and ecological habits of G. constricata. The develop-

mental type of carpospore and tetraspore was mediate discal

type. The life history included haploid of gametophyte, diploid of

carposporophyte and tetrasporophyte, which showed a typical

isomorphic generation alternates because of the similar morpho-

logy characteristics of gametophyte and tetrasporophyte. The

double factorial analysis of temperature vs. photoperiod and

temperature vs. irradiance showed significant interactions on the

discoid crusts and sporelings development. The optimum condi-

tions for early growth of G. constricata were temperature 20°C, ir-

radiance 80 μmol photons/(m

·s) and photoperiod 16L:8D.

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Photoperiod 2 366.98 14 978.04 1.14×10

–24

2 335.45 2.95 5.31×10

–24

Interaction 10 46.54 9 498.19 1.42×10

–17

10 80.85 3.55 1.34×10

–21

    Note: df represents degree freedom, F F-test, SS Stdev Square, and P P-value.

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