J Appl Phycol
DOI 10.1007/s10811-013-0071-y
Effects of experimental thinning on the growth
and maturation of the brown alga Undaria pinnatifida
(Laminariales; Phaeophyta) cultivated in Matsushima Bay,
northern Japan
Xu Gao & Hikaru Endo & Kazuya Taniguchi & Yukio Agatsuma
Received: 17 April 2013 / Revised and accepted: 25 June 2013
# Springer Science+Business Media Dordrecht 2013
Abstract In northern Japan, massive production of high-
quality specimens of the kelp Undaria pinnatifida prior to
the traditional harvest season is strongly needed to meet
commercial demand. To address this need, we tested the
effects of controlled thinning by cutting small plants on the
growth and maturation of sporophytes cultivated in Matsushi-
ma Bay, northern Japan. In early December 2009, the stocking
densities of cultivated kelps were thinned to 10 and 5 plants
per 4 cm thread section in two experimental groups. In con-
trast, no thinning was conducted during cultivation until
March 2010 in the control group (about 16–20 plants per
4 cm thread section). Morphological features, photosynthesis,
and carbon and nitrogen contents were compared among the
three groups. Compared to kelps of control group, total length,
stipe width, the length and width of sporophyll, and dry
weights of blade and sporophyll showed significantly higher
values in kelps of the two experimental groups. However,
stipe length of kelps of control group was significantly greater
than those of the two experimental groups. The photosynthetic
rates and nitrogen contents of kelps of the two experimental
groups were significantly greater than those of the control
from January to March. No significant differences occurred
in all these parameters between kelps of the two experimental
groups. Based on these results, the growth and maturation of
U. pinnatifida sporophytes can be promoted greatly by exper-
imental thinning, and this will improve production of high-
quality specimens of kelps and increase economic returns
before the traditional harvest season.
X. Gao (*) : H. Endo : K. Taniguchi : Y. Agatsuma
Laboratory of Marine Plant Ecology, Graduate School of
Agricultural Science, Tohoku University, Sendai, Miyagi
Prefecture 981-8555, Japan
e-mail: algaepanda69@163.com
Keywords Cultivation . Thinning . Growth . Maturation .
Undaria pinnatifida . Phaeophyta
Introduction
Density dependence and intraspecific competition are closely
linked in plant populations (Begon and Mortimer 1986). In-
traspecific competition has been extensively investigated in
many agricultural and experimental populations of terrestrial
plants over the past few decades (Harper 1977; Antonovics
and Levin 1980; Schmitt et al. 1987; Thomas and Weiner
1989; Rice 1990; Jurik 1991; Yastrebov 1996). Most of these
studies have concluded that high population density has a
negative influence on survival, growth, and reproduction of
the individual plants. Due to genetic differences and timing of
recruitment, the difference in the initial size of plants occurs,
small plants being more affected by intraspecific competition
than larger ones and size inequality increasing with increasing
plant densities (Weiner and Thomas 1986; Rice 1990). Light
competition seems to be significant for terrestrial plants in
realizing the dominant and inhibiting other individuals, with
large plants shading small ones (Schmitt et al. 1986).
Density dependence has been considerably less studied in
seaweed stands, although the results of manipulative experi-
ments over the last decade indicated that the algal responses to
density are in many cases similar to those observed in terrestrial
plants. Therefore, negative effects of density on survival and
growth, resulting in self-thinning or density-dependent mortal-
ity, are common in macroalgae populations (Reed 1990;
Kendrik 1994; Creed et al. 1996; Arenas et al. 2002). In natural
population of the subtidal kelp Pterygophora californica, den-
sity can strongly influence patterns of growth and reproduction,
which may be due to mainly competition for light; however, this
probably varies with other factors such as nutrient dynamics
(Reed 1990; Creed et al. 1996). Similarly, it has been reported

for Laminaria digitata that plants grew more slowly and were
more likely to die at higher densities (Creed et al. 1998).
However, very few studies have focused on the influence of
plant density on the cultivated populations of large commercial
kelps, and little information is available with regard to the
potential application of thinning in mariculture production.
The annual kelp Undaria pinnatifida (Laminariales;
Phaeophyta) is one of the major commercial seaweeds endemic
to cold temperate waters of Japan (Akiyama and Kurogi 1982),
although it has been known as an invasive species (Hay 1990;
Sanderson 1990; Casas and Piriz 1996; Campbell et al. 1999;
Stuart et al. 1999; Silva et al. 2002; Aguilar-Rosas et al. 2004).
This species has been extensively cultivated as one of the most
important and popular seafood resources in Asian countries
(Saito 1972; Yamanaka and Akiyama 1993). In Japan, most
cultivation of U. pinnatifida occurs along the coasts of Miyagi,
Iwate, and Tokushima Prefectures; together these areas account
for about 90 % of the total production of this species in Japan
(Tokuda et al. 1994). In northern Japan, high-quality fresh U.
pinnatifida sporophytes are found during the growth period,
which can be harvested before the traditional harvest date
(March), and its price is four to five times higher than normal
because of its tender thalli and excellent taste. The demand for
this kind of sporophyte has increased steadily in recent years,
and thus the development of new cultivation technology which
can increase its production is strongly needed.
Saito (1962) noticed a phenomenon while farming U.
pinnatifida: that the growth of sporophytes could be promoted
greatly by experimental thinning. This finding may be due to
the improvement of light and nutrient conditions derived from
a reduction in stocking density, but this hypothesis requires
testing. All parts of U. pinnatifida sporophytes (blade, stipe,
and sporophyll) are important nutritional food, and they have
different market values, thus it should also be determined that
the growth of all parts can be promoted by experimental
thinning or not. In addition, to maximize the crop yields, it
is necessary to clarify the suitable density after experimental
thinning, which could be applied in cultivation production.
The objective of the present study was to examine the sea-
sonal changes in morphological features, photosynthetic rates,
and carbon and nitrogen contents of cultivated sporophytes after
experimental thinning to different extents and compare these
parameters with those of control thalli without thinning, and to
develop potential new cultivation techniques for increased pro-
duction of high-quality sporophytes.
Materials and methods
Production of seedlings and cultivation trial
Gametophytes of U. pinnatifida were obtained by induction of
zoospores from mature sporophytes cultivated in Matsushima
J Appl Phycol
Bay (38°32′ N, 141°31′ E) in the summer of 2009. After the
zoospores were released into seawater aquaria, the water was
stirred to a homogeneous consistency to make the zoospores
attach to 2-mm diameter plastic fiber threads at a similar initial
settlement density. Culturing was first conducted indoors un-
der controlled environmental conditions at 18 °C with a pho-
ton flux density of 40 μmol photons m–2 s–1, and a photope-
riod of 12-h light:12-h dark. The culture medium was filtered
seawater with additional nitrate (PESI; Tatewaki 1966), to
which GeO2 (20 μg mL–1) had been added to inhibit the
growth of diatoms and protozoa. The water was aerated to
mix the nitrate and seawater evenly. The culture medium was
replaced every 15 days. After several months of culture, the
seedlings grew to 1–2 cm long on average. The threads on
which the young sporophytes attached were cut into 4-cm
sections with an approximated density of four to five plants
per centimeter. For field cultivation trials, 50 thread sections
were individually tucked into three 50 m long, 15 mm
diameter ropes at intervals of 1 m. The three ropes
prepared in this manner were deployed at the sea surface
with floats at intervals of 3 m in Matsushima Bay in
October. For the experimental groups, small sporophytes
were cut in early December, and stocking densities were
adjusted to ten and five plants per thread section, respec-
tively. For the control group, no alteration in stocking
density was made during cultivation.
Measurements of morphological features
To examine the changes in morphological features, each three
sections from each of the two experimental and control groups
were collected randomly every month from mid-December to
mid-March. These plants were immediately transported to the
laboratory and then were initially hung for at least 15 min to
drain excess seawater. Next, measurements of total length,
stipe length, stipe width, sporophyll length, and sporophyll
width were taken from ten plants in sequence starting from the
largest one (Fig. 1). Then, they were carved into midrib, blade,
and sporophyll, and each part was weighed after drying in a
convection oven at 60 °C for 1 week.
Analysis of carbon and nitrogen contents
One section from each of the two experimental and control
groups in addition to those for morphological measurements
was collected every month from mid-December to mid-
March, and the four largest plants of each section were
selected for experimentation. Eight discs with the surface
face of approximately 2.0 cm2 were cut from the margins of
the meristem. After measurement of the dry weight, the discs
were pulverized and used for analysis of carbon and nitrogen
contents by an Elemental Analyzer (EAGER200, Fisons In-
struments, USA).
J Appl Phycol
Fig. 1 Morphological measurements of U. pinnatifida. TL total length,
STL stipe length, STW stipe width, SPL sporophyll length, SPW sporo-
phyll width
Measurement of photosynthesis
One section from each of the two experimental and control
groups which had never been previously used in this exper-
iment was collected every month from mid-December to
mid-March, and the four largest plants of each bunch were
selected for use in measuring photosynthesis. Two discs with
a surface area of approximately 2.0 cm2 were cut from each
plant using a cork borer 1.6 cm in diameter from the margins
of the meristem. These discs were incubated in flowing
seawater for 12 h before measurements, to allow recovery
from cutting damage.
An improved differential gas volumeter called “Product–
meter” (Yokohama et al. 1986) was used to measure rates of
photosynthesis. These discs were placed in a reaction vessel
containing 10 mL sterilized seawater (GF/F, Whatman), while
a control vessel contained 10 mL sterilized seawater only. The
reaction and control vessels were attached to Product-meters
and immersed in a water bath with a thermostat maintained at
a constant water temperature and shaken by a motor drive at
150 rpm. The vessels were illuminated from below by projec-
tor lamps with light reflected by mirrors placed under the
water bath. Photo slide projectors with incandescent lamps
(Philips KP–10s 100 V, 300 W) were used as a light source.
Irradiances were regulated by using neutral density glass
filters (Toshiba TND–50, 25, 12.5,) and measured with a
quantum photon meter (LI–COR LI–192S, USA). The discs
were incubated for 30 min to allow them to adapt to the
experimental environment, and the oxygen evolution pro-
duced from them was then measured every 3 min six to ten
times.
For measurement of photosynthetic rate, the discs were in-
cubated under six temperatures (5, 10, 15, 20, 25, and 30 °C)
and a photon flux density of 180 μmol photons m–2 s–1. The
initial nutrient concentrations of sterilized seawater were set to
400 μg L–1 for NO3–N and NH4–N, and 80 μg L–1 for PO4–P.
The nutrient concentrations in seawater were almost below the
limit of detection. Seawater used in experiments was obtained
from the coast of Ishinomaki, which is near the study site and
which had similar temperatures and nutrient conditions
to Matsushima Bay. Eight replicates were used for pho-
tosynthesis measurement.
Statistical analysis
Two-way analysis of variance (ANOVA) was used to com-
pare the morphological features and carbon and nitrogen
contents among months and among kelps from the three
groups. In addition, a separated two-way ANOVA was used
to analyze the photosynthesis versus temperature (P–T)
curves among temperatures and among kelps from the three
groups from December 2009 to March 2010. All of the
variables were tested for normality and homogeneity prior
to conducting ANOVA. When a significant difference was
identified by ANOVA, Tukey’s multiple comparison test was
used for comparison of means. Differences were considered
to be significant at a probability of 5 % (P<0.05).
Results
Morphological features
The seasonal changes in morphological features of kelps of
the two experimental groups and the control are shown in
Fig. 2. All of these morphological parameters differed sig-
nificantly among months for kelps of all three groups
(P<0.05). The average total lengths of kelps of both the
two experimental groups were significantly greater than
those of the control from January to March (P<0.05). Com-
pared to kelps of the control group, the average stipe lengths
of kelps of both the two experimental groups were signifi-
cantly shorter in January and March (P<0.05); however, the
average stipe widths were significantly greater in February
and March (P<0.05). The average sporophyll lengths of
kelps of both the two experimental groups were significantly
greater than those of the control in January and February
(P<0.05). The average sporophyll widths of kelps of both
the two experimental groups were significantly greater than
those of the control from January to March (P<0.05). Sig-
nificant differences in all these parameters were not found
 J Appl Phycol

between kelps of the two experimental groups during this 60

experiment (P>0.05).
The seasonal changes in dry weight of blade, midrib, and bB bA
40 bB

Blade (g)
sporophyll of kelps of the two experimental groups and the bA
bB
control are shown in Fig. 3. All of these parameters differed bB
bA
significantly among months for kelps of all three groups 20 bA
aA
(P<0.05). The average dry weights of blade and sporophyll aA aA
of kelps of both the two experimental groups were significantly 0
aA
greater than those of the control in January and February 30

bA
300 bA
bB bB 20

Midrib (g)
bB
Total length (cm)

bB bA bA
aA
200 bB bB
aA aA bA bA
cA 10 aA
aA bcA
bA
100 aA aA aA
aA
0
0 60
60
bA bB
Stipe length (cm)

Sporophyll (g)
bB
40 40 bA
bA bB
aA abA abA bB
bA
aA bA
20 abA abA bB
aA 20 bB
bA

0 aA aA aA abA
aA
8 0
cB
Dec. Jan. Feb. Mar.
cB
Fig. 3 Seasonal dry weights of thallus, blade, midrib, and sporophyll of
Stipe width (cm)

6 bB
bA bB U. pinnatifida sporophytes of the two experimental groups (ten plants
4 bA per section: filled circles; five plants per section: open circles) and the
aA bA bA control (open squares) cultivated in Matsushima Bay. Different small
2 aA aA and large letters indicate statistical significance (P<0.05) among
aA months and among groups, respectively. N=10 for all groups. Black
0 bars indicate standard deviations
40
Sporophyll length (cm)

bB bA
30 (P<0.05). However, there were no significant differences in
bB
bA the average midrib weights between kelps of each experimental
20 bB
bB group and the control during this experiment (P>0.05). Simi-
cA
10 aA bcA larly, significant differences in all these parameters did not
aA abA occur between kelps of the two experimental groups during
0 aA
this experiment (P>0.05).
20
bB
Sporophyll width (cm)

bB Carbon and nitrogen contents

15
bB
bB
bB Seasonal carbon and nitrogen contents of discs from the
10
bB
bA margins of the meristems of kelps of the two experimental
aA bA
5 bA groups and the control are shown in Fig. 4. There were no
aA
aA significant seasonal variations in carbon contents of kelps of
0
Dec. Jan. Feb. Mar. all three groups (P>0.05). The carbon contents of kelps of
Fig. 2 Seasonal total length, stipe length, stipe width, sporophyll both the experimental groups were slightly higher than those
length, and sporophyll width of U. pinnatifida sporophytes of the two of the control from December to March (P>0.05). The nitro-
experimental groups (ten plants per section: filled circles; five plants per gen contents of kelps of all three groups showed significant
section: open circles) and the control (open squares) cultivated in
variations among months (P<0.05). The nitrogen contents of
Matsushima Bay. Different small and large letters indicate statistical
significance (P<0.05) among months and among groups, respectively. kelps of both the two experimental groups were significantly
N=10 for all groups. Black bars indicate standard deviations higher than those of the control from January to March
J Appl Phycol

1.2 80
December
aA aA
Carbon content (mg cm–2)
aA aA aA 60
aA aA aA aA aA bcA cA
0.9 aA aA
bA bcA cA
40 bA
cA
aA bcA aA
0.6 aA
aA bA aA
20 aA
aA aA aA
0.3
0
80
January cB
0 cB
60 cB
0.2 bB bB
cB
bB bB

Gross photosynthesis rate (µLO2 cm–2 s–1)

40 cA cA
Nitrogen content (mg cm–2)

aA
0.15 bB aA bA
aA bA
bB 20 aA
bB bB bB
bB aA
bA aA
0.1 abA 0
abA
aA 80
aA aA February
0.05 cB cB
60 cB cB
dB

0 bA dB
40 dA
Dec. Jan. Feb. Mar. aA dA
aA aA bA
aA cA
Fig. 4 Seasonal carbon and nitrogen contents of the margins of the 20 bcA
meristems in U. pinnatifida sporophytes of the two experimental groups aA
abA
(ten plants per section: grey; five plants per section: black) and the 0
control (white) cultivated in Matsushima Bay. Different small and large
letters indicate statistical significance (P<0.05) among months and 80
March
among groups, respectively. N=8 for all groups. Black bars indicate
cB
standard deviations 60 cB
cB
cB
bA
40
(P<0.05). Significant differences in carbon and nitrogen con- aA cA aA
aA bA bcA
tents did not occur between kelps of the two experimental 20
aA
aA b A aA
groups during this experiment (P>0.05). aA aA aA

0
Photosynthesis 0 5 10 15 20 25 30 35
Temperature ( C)
Gross photosynthetic rates calculated per area of discs from Fig. 5 Photosynthesis―temperature curves at 180 μmol photons m–
2 –1
the margins of the meristems of kelps of the two experimental s per unit area of U. pinnatifida sporophytes of the two experimental
groups (ten plants per section: filled circles; five plants per section: open
groups and the control from December to March are shown in
circles) and the control (open squares) cultivated in Matsushima Bay
Fig. 5. The gross photosynthetic rates increased with the rise from December 2009 to March 2010. Different small and large letters
in temperatures up to 25 °C but decreased thereafter for kelps indicate statistical significance (P<0.05) among temperatures and
of all three groups (P<0.05). No significant differences in among groups, respectively. N=8 for all groups. Black bars indicate
standard deviations
gross photosynthetic rates at all temperatures occurred be-
tween kelps of each experimental group and the control in
December (P>0.05). Although there were no significant dif- in gross photosynthetic rates did not occur at all temperatures
ferences in gross photosynthetic rates of kelps of all three between kelps of the two experimental groups during this
groups at 5–15 °C (P>0.05), significant higher values of kelps experiment (P>0.05).
of both the two experimental groups were found at 15–30 °C
compared to those of the control in January (P<0.05). In
February, significant higher gross photosynthetic rates of Discussion
kelps of both the two experimental groups were found from
20 to 30 °C compared to those of the control (P<0.05). In To the best of our knowledge, this study is the first to report the
March, the gross photosynthetic rates of kelps of both the two influence of alteration of stocking density on the growth and
experimental groups were significantly higher than those of maturation of kelps in the order Laminariales. In the present
the control at 20 and 25 °C (P<0.05). Significant differences study, compared to sporophytes of U. pinnatifida without

experimental thinning, two experimental groups of thinned
kelps exhibited a marked increase in most morphological pa-
rameters and significantly higher photosynthetic rates and ni-
trogen contents. These results suggest the growth and matura-
tion of U. pinnatifida sporophytes were greatly enhanced by
experimental thinning, which was thought to be caused by an
improvement in ambient environmental conditions. Conse-
quently, it is possible to harvest a large amount of high-quality
sporophytes of U. pinnatifida prior to the traditional harvest
season, and this will improve economic returns because of
higher demand.
In the present study, the kelps remaining after experimen-
tal thinning showed significant higher values in almost all
morphological parameters compared to kelps of control
group without thinning (Figs. 2 and 3). Similar results were
also obtained in many other macroalgae, which reported a
strong negative correlation between growth rate and stocking
density (Lapointe and Tenore 1981; DeBusk et al. 1986; Wu
et al. 1989; Hurtado et al. 2001; Nagler et al. 2003; Pereira
et al. 2006). On a physiological basis, the photosynthetic
rates of remaining kelps after thinning were strongly en-
hanced compared to kelps of control group (Fig. 4). This
was considered to be partly caused by a notable improve-
ment in the external light environments, as also happens with
higher plant (Schmitt et al. 1986). After experimental thin-
ning, the photosynthesis of remaining plants was stimulated
by an improvement in the external light penetration, which
may result in an increase in the concentration of pigments
and photosynthetic activity. This supports the report from
Gevaert et al. (2002) stating that Saccharina latissima de-
veloped higher levels of pigmentation to cope with strong
exposure to irradiance. It is generally known that cellular
nitrogen content has a great impact on pigments such as
chlorophyll (Chapman et al. 1978; Bird et al. 1982; Lingnell
and Pedersen 1987; Lapointe 1981) and photosynthetic ac-
tivity (Levy and Gantt 1990). The remaining kelps after
thinning in our study also exhibited significantly higher cell
nitrogen contents in response to the reduction of stocking
density (Fig. 5), which may be related to the improvement of
the nutrient environment. The greater ability of nutrient
accumulation of remaining kelps may induce the concentra-
tion of pigments and support increased photosynthesis and
rapid growth of blade. Then, most of the accumulated re-
sources produced in blades began to translocate rapidly to
sporophylls, leading to their enlargement (Figs. 2 and 3).
A classic example of morphological plasticity is the re-
distribution of growth toward stem elongation exhibited by
higher plants of many species growing in dense populations
(Harper 1977). In brown algae, the morphological character-
istics also vary in response to population density (Charrier
et al. 2012). In the present study, the stipe of kelps of the
control group without thinning became significantly thinner
and longer in comparison with the remaining kelps after
J Appl Phycol
experimental thinning (Fig. 2). This result indicates that the
morphological character of the stipe of U. pinnatifida was
greatly influenced by shading effects, which is considered
partially due to the variation of intraspecific competition
situation for light. This kelp exhibited great capacity to react
to the presence or absence of neighbors with changes in the
pattern of morphological development. Similar responses
have also been observed in natural populations of other
species. For example, in both kelp and fucoid species, plants
growing in a high population density became taller than those
growing in a low population density because of the stipe
elongation (Schiel 1985; Hymanson et al. 1990; Holdbrook
et al. 1991; Sjøtun and Fredriksen 1995; Arenas et al. 2002;
Wernberg 2005).
In this study, there were no significant differences in all
parameters between the remaining experimental kelps after
thinning to ten and five plants per section. Thus, thinning to
ten plants per section is suitable to be applied for U.
pinnatifida cultivation in Matsushima Bay because of its
higher yield. Additionally, there were no significant differ-
ences in the growth in blade and sporophyll between kelps of
both the two experimental groups from January to March.
Thus, we consider that it is suitable to harvest kelps after
experimental thinning in January, resulting in an increase in
the rate of utilization of cultivation area. In conclusion, it is
likely that early enlargement of blade and sporophyll by
appropriate experimental thinning will improve production
of high-quality specimens of kelps and increase economic
returns before mid-harvest season. This conclusion provides
important information that may have a great potential for
wide application in commercial cultivation of this kelp in
Japan and other parts of the world.
Acknowledgments We sincerely thank Mr M. Ise of the Shiogama
Daiichi Fisheries Cooperative Association for providing the seedlings
used in the present study and for his kind cooperation with kelp
cultivation and collection; the staff of the Miyagi Prefecture Fisheries
Technology Institute for using seawater for culture experiment; and
Assistant Professor K. Ito for helping with the measurement of carbon
and nitrogen content.
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