J Appl Phycol (2013) 25:1171–1178
DOI 10.1007/s10811-012-9925-y
Compensation of the brown alga Undaria pinnatifida
(Laminariales; Phaeophyta) after thallus excision
under cultivation in Matsushima Bay, northern Japan
Xu Gao & Hikaru Endo & Makoto Yamana &
Kazuya Taniguchi & Yukio Agatsuma
Received: 8 September 2012 / Revised and accepted: 10 October 2012 / Published online: 21 October 2012
# Springer Science+Business Media Dordrecht 2012
Abstract In recent years, the crop yield of cultivated
Undaria pinnatifida (Harvey) Suringar has not been able
to meet commercial demand and so advances in cultivation
technology are strongly needed to increase production.
Interestingly, cultivation work has shown the yield of
U. pinnatifida sporophytes may be increased significantly
by thallus excision, which may cause compensatory growth
of the remaining tissues. To test this hypothesis and clarify
correlative mechanisms, we examined seasonal morpholog-
ical characteristics, photosynthetic rates, nutrient uptake
rates, and carbon and nitrogen contents of U. pinnatifida
sporophytes after thallus excision at a point 30 cm from the
meristem in late February and compared these parameters
with control kelps grown without excision, which were
cultivated together in Matsushima Bay, northern Japan.
Compared to control kelps, the length and dry weight of
blades increased significantly after excision, and the growth
phase was prolonged for about 1 month. The photosynthetic
rates, nutrient uptake rates, and carbon and nitrogen con-
tents of excised kelps were significantly higher than those of
the controls. After vegetative growth stopped, resources
accumulating in thalli were translocated significantly to
sporophylls for maturation, indicating maturation was not
negatively affected by thallus excision. These results indi-
cate U. pinnatifida exhibits a very strong compensatory
ability in response to thallus excision and consequently,
the yield could be increased due to an increase in harvest
frequency.
X. Gao : H. Endo : M. Yamana : K. Taniguchi : Y. Agatsuma (*)
Laboratory of Marine Plant Ecology,
Graduate School of Agricultural Science, Tohoku University,
Sendai, Miyagi Prefecture 981-8555, Japan
e-mail: agatsuma@bios.tohoku.ac.jp
Keywords Compensation . Cultivation . Thallus excision .
Undaria pinnatifida
Introduction
Compensatory growth is defined as a common strategy of
plants that reduces the deleterious influences of tissue loss
on plant fitness following damage (Strauss and Agrawal
1999). Many studies support the view that plants are nega-
tively influenced by damage (Rausher and Feeny 1980;
Abulfatih and Bazzaz 1984; Louda 1984; Karban and
Strauss 1993), which may result in resource decline through
a loss of nutrients or photosynthetic area, often leading to a
reduction in plant fitness. In contrast, within the last 30 years,
increasing evidence has shown that many plants are able to
compensate for losses by replacing lost tissue through rapid
growth (McNaughton 1983; Danckwerts 1993), and conse-
quently, growth produces an increase in biomass production
(Argall and Stewart 1984; Hicks and Reader 1995). The
degree of compensation following tissue loss may depend
on a number of variables, including plant species, amount of
tissue lost, resource availability, environmental conditions,
and seasonal timing of tissue removal (Maschinski and
Whitham 1989; Trumble et al. 1993; Simons and Johnston
1999). When compensation has been observed, it has been
attributed to some plant response mechanisms including in-
creased photosynthetic activity (Jãremo et al. 1996; Mabry
and Wayne 1997), increased growth rate (Danckwerts 1993;
Oba et al. 2000), and reallocation of stored resources
(Caldwell et al. 1981; Mabry and Wayne 1997).
Experimental studies on compensation in seaweeds or
aquatic plants are rare and little is currently known about
how these algae compensate for damage and how the damage
1172
may influence future fitness by causing modification in inter-
nal organization of plants. In recent years, some researchers
have given increasing attention to the compensatory ability of
marine plants. Macrocystis integrifolia Bory de Saint-Vincent
and Sargassum plants exhibited compensatory growth after
damage, which could be an important strategy of large sea-
weed species allowing them to tolerate grazing pressure (Cerda
et al. 2009; Hay et al. 2011). Similar responses have also been
observed in crustose coralline red alga and the seagrass
Posidonia oceanica (Linneaus) Delile (Littler et al. 1995;
Vergés et al. 2008). In contrast, no compensation of grazer-
induced losses was found in Ecklonia radiata (C. Agardh) J.
Agardh and Fucus vesiculosus L. (Steinberg 1995; Honkanen
and Jormalainen 2002). Truncation of Saccharina longicruris
(Bachelot de la Pylaie) Kuntze significantly reduced growth
rates, which was attributed to a reduction in photosynthetic
area rather than a loss of storage products (Chapman and
Craigie 1978). However, very few studies have focused on
the physiological responses of plants following damage includ-
ing responses related to photosynthesis and nutrient accumu-
lation, which may result in physiological compensation in
seaweeds. Also, little information is available with regard to
physiological compensation in large commercial species and
its potential application in mariculture production.
Undaria pinnatifida is extensively cultivated as one of
the most important and popular seafoods in Asian countries
(Saito 1972; Yamanaka and Akiyama 1993). In Japan, the
largest scale cultivation of this species occurs in Sanriku
district and Tokushima Prefecture; together these areas
account for about 90 % of the total production of this
species in Japan (Tokuda et al. 1994). However, in recent
years, the crop yield of this kelp has not been able to satisfy
increasing commercial demand. Therefore, the development
of new cultivation technology which can increase produc-
tion is strongly desired. Saito (1962) noticed an interesting
phenomenon while cultivating U. pinnatifida, noting it
could be harvested twice when thalli were excised above
the meristems. This finding indicated that thallus excision
might promote the growth of U. pinnatifida sporophytes and
prolong the harvest period by its substantial capacity of com-
pensation, but this hypothesis requires testing. Sanbonsuga et
al. (1987) found trimming Saccharina diabolica (Miyabe)
Lane, Mayes, Druehl and Saunders and leaving less than
30 cm from the base of the blade had a strong negative impact
on growth and total harvest of this species. Therefore, to
maximize the crop yields, we assumed thalli of this kelp
should be excised at about 30 cm above the meristem for this
cultivation trial. The objective of the present study was to
examine the seasonal changes in morphological characteris-
tics, photosynthetic rates, nutrient uptake rates, and carbon
and nitrogen contents of cultivated U. pinnatifida sporophytes
after excision and compare these parameters with those of
J Appl Phycol (2013) 25:1171–1178
control thalli without excision, and to develop new cultivation
technology for increased production.
Materials and methods
Gametophytes of U. pinnatifida were obtained by induction
of zoospores from mature sporophytes cultivated in
Matsushima Bay (38°32′ N, 141°31′ E) in the summer of
2007. 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 to obtain a similar initial settlement density.
Culturing was first conducted indoors under controlled en-
vironmental conditions at 18 °C with a photon flux density
of 40 μmol photons m−2 s−1 and a photoperiod of 12 h
light:12 h dark. The culture medium was sterilized 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
many 4-cm sections. For field cultivation trials, 50 thread
sections were individually tucked into two 50-m-long,
15-mm diameter ropes at intervals of 1 m. Two ropes prepared
in this manner were deployed at the sea surface with floats at
intervals of 3 m in Matsushima Bay in October. To make
cultivation conditions as uniform as possible, stocking density
was adjusted to 15 plants per thread section in January 2008
and one 4-cm section was considered as one bunch. For the
experimental group, thalli were excised at about 30 cm above
the meristem in late February (Fig. 1). For the control group,
no excision was made during cultivation.
Measurements of morphological characteristics
To examine the seasonal changes in morphological char-
acteristics, three bunches of kelps from the experimental
group were collected randomly every 2 weeks from early
March to late May, and three bunches of control kelps
were collected from late February to late May. Seawater
temperatures were also measured by a bar thermometer
(accuracy 0.1 °C) at the time of sampling. These plants
were then immediately transported to the laboratory. They
were initially hung for at least 15 min to drain excess
seawater. Next, measurements of blade length were taken
from 30 plants in sequence starting from the largest one.
Then, they were dissected into midrib, blade, and sporo-
phyll, and each part was weighed after drying in a con-
vection oven at 60 °C for 1 week.
J Appl Phycol (2013) 25:1171–1178
Fig. 1 Chart of mature U. pinnatifida sporophyte showing excision
site
Measurements of photosynthesis and nutrient uptake
One bunch from both the excised and control kelps in addition
to those for morphological measurements was collected every
2 weeks from late February to late May and the four largest
plants were selected for use in measuring photosynthesis and
nutrient uptake. One disc with a surface area of approximately
2.0 cm2 was 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 and nutrient uptake. 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 ther-
mostat maintained at a constant water temperature and shaken
by a motor drive at 150 rpm min−1. The vessels were illumi-
nated from below by projector lamps with light reflected by
mirrors placed under the water bath. Photo slide projectors with
incandescent lamps were used as a light source. Irradiances
were regulated by using neutral density glass filters (Toshiba
TND-50, 25, 12.5, Japan) and measured with a quantum pho-
ton meter (LI-COR LI-192S,). The discs were incubated under
a photon flux density of 180 μmol photons m−2 s−1. The
monthly average seawater temperature from 1975 to 2004
measured daily at Enoshima (38°24′ N, 141°35′ E), a small
island near the study site, by the Miyagi Prefecture Fisheries
Technology Institute, was used as the incubation and experi-
mental temperature. For measurement of the photosynthetic
1173
rate, the discs were incubated for 30 min to allow them to adapt
to the experimental environment, and the oxygen evolution
produced from them was then measured every 3 min, six to
ten times. Four replicates were used for measurements of rates
of photosynthesis and nutrient uptake. The uptake rates of
NO3–N, NH4–N, and PO4–P were obtained from the differ-
ences between the concentrations analyzed by the autoanalyzer
(TRAACS 800; Bran–Luebbe, Japan) after a 60-min incuba-
tion of the discs and those in the controls. The fresh and dry
weights were measured after incubation. Nutrient uptake rates
were estimated using the following equation:
VN; P ¼ ðSt  St þT Þ  0:01=ðA  T Þ
where VN, P 0uptake rates of NO3–N, NH4–N, and PO4–P (μg
cm−2 h−1); t0time (h); T0time interval (h); St 0initial concen-
tration at time t (μg L−1); St + T 0final concentration at time t+T
(μg L−1); and A0area of disc (2.0 cm2).
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. The nutrient concentrations in seawater were almost
below the limit of detection. After sterilization, the seawater
was enriched by addition of NH4Cl, NaNO3, and NaH2PO4·12
H2O. For determination of seasonal photosynthesis and nutri-
ent uptake, the initial nutrient concentrations were set to
400 μg L−1 for NO3–N and NH4–N and 80 μg L−1 for PO4–P.
Analysis of carbon and nitrogen content
One bunch from both the excised and control kelps which
had never been previously used in this experiment was
collected every 2 weeks from late February to late May
and the four largest plants on of each stock were selected
for experimentation. Four discs with the surface face of
approximately 2.0 cm2 were cut from each part as follows:
the apical part of blade, the middle part with maximum
blade width, the margins of the meristem, and the middle
part of sporophyll with the maximum width. After measure-
ment of the dry weight, the discs were pulverized and used
for analysis of carbon and nitrogen contents by an elemental
analyzer (EAGER200, Fisons Instruments, USA).
Statistical analysis
Significant differences in morphological and physiological
parameters between months were analyzed with the
Kruskal–Wallis test followed by Tukey's HSD post hoc tests
as not all the data showed a normal distribution and homo-
geneous variance. The significant differences in morpholog-
ical and physiological characteristics between excised and
control kelps were analyzed by Mann–Whitney tests.
1174 J Appl Phycol (2013) 25:1171–1178

16 60

Seawater temperature (oC)

14 50 a*

Oxygen evolution
a*

(µlO2 cm–2h–1)
12 40 a* a
a* a
10 30
8 A A A
20
B B B B
6
10
4
0
2
0 1.6
Feb. Mar. Apr. May b* b*
1.2 b* c

NH4 uptake rate

a

(µg cm–2h–1)
Fig. 2 Measured seawater temperatures in Matsushima Bay from a
February to May in 2007 0.8 C
B B B B
B
Results 0.4 A

0
Seawater temperatures in Matsushima Bay ranged from
6.9 °C in early February to 13.7 °C in late May (Fig. 2). 1.6

b* b*
Seasonal morphological characteristics 1.2 b*

NO3 uptake rate

(µg cm–2h–1)
a* a*
0.8
The seasonal changes in morphological characteristics of ex- c
cised and control kelps are shown in Fig. 3. The average blade 0.4
A A A
250 B AB
B B
0
200 A A A
Blade length (cm)

A A
B B
0.2
150 a* a*
a*
0.15 b*
PO4 uptake rate
(µg cm–2h–1)

100
b*
c* c* c* c*
50 0.1
b* A
a* c
0 B B B B B
0.05
C
80
0
Dry weight of blades (g)

Feb. Mar. Apr. May

60
A
A A A A c* c* Fig. 4 Seasonal gross photosynthetic rates and nutrient uptake rates in
40 excised (open) and control (filled) U. pinnatifida cultivated in Mat-
c c sushima Bay. Different small and large letters indicate significance
B level at P<0.05 between months. *Difference level at P<0.05 between
20 b* B
excised and control kelps within months. N04 for both kelps. Black
a* bars indicate standard deviations
0

80
Dry weight of sporophylls (g)

length of control kelps did not change significantly from late

B d
60
February to late April (p>0.05) but decreased thereafter
B (p<0.05). In contrast, the average blade length of excised
40 B
kelps increased significantly from 45.9 cm in early March to
A A c 85.2 cm in early April (p<0.05). The average dry weight of
A
b
20 A blades of control kelps increased slightly from late February to
a a
a a maximum of 46.6 g in early April (p>0.05), but then
0 decreased (p<0.05). In contrast, the average blade weight of
Feb. Mar. Apr. May
excised kelps increased significantly from early March to
Fig. 3 Seasonal blade length, dry weights of blade and sporophyll of excised early April (p<0.05) and then increased slightly to a maxi-
(open) and control (filled) U. pinnatifida cultivated in Matsushima Bay.
Different small and large letters indicate significance level at P<0.05 between
mum of 44.8 g in late May (p>0.05). The average blade
months. *Difference level at P<0.05 between excised and control kelps weight of excised kelps were significantly smaller than that
within months. N030 for both kelps. Black bars indicate standard deviations of the control kelps in March (p<0.05), whereas in May,
J Appl Phycol (2013) 25:1171–1178 1175

6
Apical part Middle part Meristem
c* c*

Dry weight (mg cm–2)

5 c*
C
c* b* b*
b b B
4 B a
a a a a c
3 B B B B b c
B B BC a C
a C
2 A A A A A A
A A A
1
0
2.5
Carbon content (mg cm–2)

2
b* b* c*
bc* b*
C b*
1.5 B B B B
a a B ac
a a
1 a B B b c
a AB B a a B
B
0.5 A A a AB
AB
A A A
A A
0
Nitrogen content (mg cm–2)

0.25 c*
c* b* b*
0.2 bc* b*
C B
BC B B
a a ac
0.15 c a a a
ab
B
BC BC a a a B B
a B B
0.1 B A A A A
A A
A
A
0.05

0
Feb. Mar. Apr. May Feb. Mar. Apr. May Feb. Mar. Apr. May

Fig. 5 Seasonal dry weight and carbon and nitrogen contents of three indicate significance level at P<0.05 between months. *Difference
parts of blade in excised (open) and control (filled) U. pinnatifida level at P<0.05 between excised and control kelps within months.
cultivated in Matsushima Bay. Different small and large letters N04 for both kelps. Black bars indicate standard deviations

excised kelps weighed significantly more than the control
kelps (p<0.05). No significant changes occurred in the aver-
age sporophyll weight of control kelps from late February to
early April (p>0.05); it increased significantly in April
(p < 0.05) and then increased slightly to a maximum of
47.3 g in late May. The average dry weight of sporophylls of
excised kelps did not vary significantly from early March to
early April (p>0.05), but it then increased significantly from
early April to a maximum of 54.5 g in late May (p<0.05).
Seasonal photosynthetic rates and nutrient uptake rates
Seasonal photosynthetic rates and uptake rates of NH4–N,
NO3–N and PO4–P of blade tissue near the meristem of ex-
cised and control kelps are shown in Fig. 4. The photosynthetic
rates of control kelps showed significant seasonal variation
(p<0.05) but did not differ significantly among months for
excised kelps (p>0.05). The photosynthetic rates of excised
kelps were significantly higher than those of the control kelps
from early March to late April (p<0.05). However, no signif-
icant differences were found in May (p>0.05).
The uptake rates of NO3–N, NH4–N, and PO4–P of both
excised and control kelps differed significantly among
months (Fig. 4; p<0.05). In control kelps, the uptake rates
of NH4–N were 2.1–3.5 times higher than those of NO3–N
during the experiment. However, in the excised kelps, the
uptake rates of both forms were similar. The uptake rates of
NO3–N and NH4–N of excised kelps were significantly
higher than those of the control kelps from late March to
late April and from early March to early May, respectively
(p<0.05). The uptake rate of PO4–P of excised kelps was
significantly higher than that of the control kelps during the
experimental period except in late May (p<0.05).
Seasonal dry weight and carbon and nitrogen contents
Seasonal dry weight and carbon and nitrogen contents of discs
from three blade parts of excised and control kelps varied
significantly during the study period (Fig. 5). In control kelps,
these parameters increased significantly from late February to
late March and decreased significantly thereafter (p<0.05). In
excised kelps, all these parameters increased significantly
from early March to late April and decreased significantly
until late May (p<0.05). All these parameters in all blade
parts of excised kelps were significantly higher than
those of the control kelps in April (p<0.05).
Seasonal dry weight and carbon and nitrogen contents of
discs from sporophyll of excised and control kelps also varied
seasonally, but there were only minor differences between the
two kelp treatments (Fig. 6). All these parameters showed
1176 J Appl Phycol (2013) 25:1171–1178

30
the growth phase of this kelp was also prolonged for about
Dry weight (mg cm–2)
25 B b
AB B AB AB 1 month, which resulted in an extension of the harvest period.
20 A Compared to kelps without excision, excised kelps experi-
B
15 a a a a a enced an almost 50 % increase in biomass production. The
10
conclusions provide important information for increasing pro-
duction levels for U. pinnatifida cultivation.
5
Compensatory growth is often supported by enhanced
0 photosynthesis in higher plants (McNaughton 1979; Strauss
10 and Agrawal 1999; Tiffin 2000). In the present study, com-
Carbon content (mg cm–2)

c pared to control kelps without excision, the photosynthetic

8 C b rates of excised kelps were also strongly enhanced. This was
AB B
A considered to be partly caused by a notable improvement in
6 A C
b B the external light environments, as also happens with higher
4 a plants (Jãremo et al. 1996; Mabry and Wayne 1997). After
a a
2 thallus excision, photosynthesis of remaining tissues was
stimulated by greater light penetration, which may result in
0 an increase in the concentration of pigments and photosyn-
0.8 b thetic activity. This supports the report of Gevaert et al. (2002)
Nitrogen content (mg cm–2)

stating that Saccharina latissima developed higher levels of

0.6 A A
A B
A A
0.4 a a
a a
0.2
0
Feb. Mar. Apr.
Fig. 6 Seasonal dry weight and carbon and nitrogen contents of the
middle part of sporophyll in excised (open) and control (filled) U.
pinnatifida cultivated in Matsushima Bay. Different small and large
letters indicate significance level at P<0.05 between months. N04 for
both kelps. Black bars indicate standard deviations
significant seasonal variation (p<0.05), but in excised kelps,
the dry weight and nitrogen contents did not differ significant-
ly from early March to late April (p>0.05) and, during that
time period, remained lower values than those of the control
kelps. Then, they increased significantly (p < 0.05) and
exceeded the values of control kelps in early May. The carbon
contents of excised kelps increased significantly from March
to early May (p<0.05) and exceeded the value of control kelps
in early May. All these parameters decreased significantly
from early May to late May (p<0.05).
Discussion
In the present study, the excised kelps exhibited a marked
increase in morphological parameters and significantly higher
photosynthetic rates, nutrient uptake rates, and carbon and
nitrogen contents. These results suggest the growth of
U. pinnatifida sporophytes was greatly promoted by thallus
excision, indicating this kelp species has a significant and
large compensatory capacity when damaged. Consequently,
A 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.
a
1978; Bird et al. 1982; Lingnell and Pedersen 1987;
Lapointe 1981) and photosynthetic activity (Levy and Gantt
1990). Excised kelps in our study also exhibited significantly
May higher nutrient uptake rates and cellular nitrogen contents in
response to the great loss of stored resources, which may be
related to the improvement of the nutrient environment. The
greater ability of nutrient accumulation of excised kelps may
induce the concentration of pigments and support increased
photosynthesis and compensatory growth.
Harrison et al. (1986) indicated nitrate and ammonium
were taken up by Saccharina groenlandica simultaneously
from the ambient environment, but uptake rates were un-
equal when both nitrate and ammonium were present in the
medium. Similar results have been demonstrated by many
researchers, suggesting the uptakes of NO3–N by some
seaweed species has been inhibited or suppressed when
NH4–N was present (D'Elia and DeBoer 1978; Haines and
Wheeler 1978; Hanisak and Harlin 1978; Thomas and
Harrison 1987; Smit 2002). In this study, the uptake of
NH4–N was 2.1–3.5 times higher than that of NO3–N in
control kelps. However, after thallus excision, the uptake
rates of both forms were enhanced significantly and became
similar. This result indicated the occurrence of considerable
physiological change in their internal organization derived
from thallus excision. Further studies are needed to eluci-
date the physiological mechanism of this new finding.
The dry weight and cellular nitrogen content of sporophylls
of excised kelps exhibited a marked increase starting in April,
and they exceeded those of control kelps in May (Figs. 3 and
6). This means the vegetative growth of excised kelps stopped
in April and the accumulated resources from photosynthesis
J Appl Phycol (2013) 25:1171–1178
and nutrient uptake began to translocate rapidly from blades to
sporophylls. Therefore, we suggest the development of spor-
ophylls and subsequent reproduction was not affected nega-
tively by thallus excision. Next, the dry weight and carbon and
nitrogen contents per unit area of sporophylls in both excised
and control kelps decreased in May. Saito (1962) reported that
the release of U. pinnatifida zoospores was mostly dependent
on seawater temperature and was observed when seawater
temperatures reached 13 °C. Seawater temperatures in the
study region reached 13 °C in early May, so the release of
zoospores should be considered as the cause of the decrease in
dry weight and carbon and nitrogen contents.
Our results indicate that compensatory growth by U. pinna-
tifida might be achieved in response to tissue losses inflicted by
artificial excision. Similarly, it has been proposed that many
kelp species counteract negative influences of damage by
compensatory growth (Toth and Pavia 2002; Pansch et al.
2008; Cerda et al. 2009). The compensatory response might
be facilitated by resource translocation, as most kelps have
specialized tissues for internal long-distance transport similar
to those of higher plants (Schmitz 1981; Raven 2003). Also,
the ability to compensate tissue losses caused by damage
appears to be related to the amount of tissue lost.
Compensatory growth against herbivory has been found in
many marine plants, and this could be important for those
species that tolerate low and moderate grazing intensities
(Steneck 1982; Littler et al. 1995; Vergés et al. 2008; Cerda
et al. 2009). In contrast, elevated grazing pressures might
drastically reduce the potential for compensation in marine
plants. For example, Steinberg (1995) found no compensatory
growth in the kelp E. radiata grazed by sea urchin, which
occasionally removed up to 50 % of the biomass of individual
algae. However, in this study, U. pinnatifida still exhibited high
compensatory ability even when about 80 % of the biomass of
thalli was removed, which is unusual for compensatory growth
in kelp species. U. pinnatifida is one of the most productive
seaweeds in the world and has become established in many
regions outside of its place of origin as one of the few pan-
demic marine invaders (Hay and Luckens 1987; Sanderson
1990; Fletcher and Manfredi 1995; Casas and Piriz 1996; Silva
et al. 2002; Aguilar-Rosas et al. 2004). Its ability to colonize
seems to be supported by its high compensatory ability to
counteract negative influences of damage.
In conclusion, photosynthesis, nutrient uptake, and resource
accumulation of U. pinnatifida sporophytes were greatly pro-
moted by thallus excision in late February, in conjunction with
compensatory growth and increased biomass production. These
results suggest that controlled excision might be a new technique
with great industrial significance, which could be widely applied
in mariculture production of this kelp in Japan and other parts of
the world. Simons and Johnston (1999) reported that the degree
of compensation depends on the timing of the damage event.
Plants are more likely to compensate if the damage occurs early
1177
in the growing season, before the reproductive phase has started
(Maschinski and Whitham 1989; Lehtila and Syrjänen 1995;
Lennartsson et al. 1998). Therefore, further studies should be
conducted to improve this technique and to clarify the best
period during which this kelp can efficiently compensate the
losses caused by thallus excision. In addition, further studies also
might include where the excision occur on the blade for maxi-
mum biomass harvest per plant for the season and determine
how much of the compensatory growth occurred as a result of
the improvement of extra environmental conditions when ex-
cised and how much was due to a reaction of this kelp.
Acknowledgments We sincerely thank Professor M. Kokubun of the
Graduate School of Agricultural Science, Tohoku University for his
critical comments on this manuscript. We also 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 staffs of the Miyagi Prefecture
Fisheries Technology Institute and Akita Prefecture Fisheries Promo-
tion Institute for using seawater for culture experiment and for provid-
ing the long-term seawater temperature of Enoshima, Professor O.
Nishimula and Mr. Chiba for helping with the analysis of nutrient
concentration, and assistant professor K. Ito for helping with the
measurement of carbon and nitrogen content.
References
Abulfatih HA, Bazzaz FA (1984) The influence of defoliation on the perfor-
mance of Ambrosia trifida plants. J Coll Sci King Saud Univ 15:55–61
Aguilar-Rosas R, Aguilar-Rosas LE, Avila-Serrano G, Marcos-Ramirez
R (2004) First record of Undaria pinnatifida (Harvey) Suringar
(Laminariales, Phaeophyta) on the Pacific coast of Mexico. Bot
Mar 47:255–258
Argall JF, Stewart KA (1984) Effects of decapitation and benzylade-
nine on growth and yield of cowpea (Vigna unguiculate (L.)
Walp.). Ann Bot 54:439–444
Bird KT, Habig C, DeBusk T (1982) Nitrogen allocation and storage
patterns in Gracilaria tikvahiae (Rhodophyta). J Phycol 18:344–348
Casas GN, Piriz ML (1996) Surveys of Undaria pinnatifida (Laminar-
iales, Phaeophyta) in Golfo Nuevo, Argentina. Hydrobiologia 326/
327:213–215
Caldwell MM, Richards JH, Johnson DA, Nowak RS, Dzurec RS
(1981) Coping with herbivory: photosynthetic capacity and re-
source allocation in two semiarid Agropyron bunchgrasses. Oeco-
logia 50:14–24
Cerda O, Karsten U, Rothäusler E, Tala F, Thiel M (2009) Compensatory
growth of the kelp Macrocystis integrifolia (Phaeophyceae, Laminar-
iales) against grazing of Peramphithoe femorata (Amphipoda, Ampi-
thoidae) in northern-central Chile. J Exp Mar Biol Ecol 377:61–67
Chapman ARO, Craigie JS (1978) Seasonal growth in Lamianria
longicruris: relations with reserve carbohydrate storage and pro-
duction. Mar Biol 46:209–213
Chapman ARO, Markham JW, Lüning K (1978) Effects of nitrate
concentration on the growth and physiology of Laminaria sac-
charina (Phaeophyta) in culture. J Phycol 14:195–198
Danckwerts JE (1993) Reserve carbon and photosynthesis—their role
in regrowth of Themeda triandra, a widely distributed subtropical
graminaceous species. Funct Ecol 7:634–641
1178
D'Elia CF, DeBoer JA (1978) Nutritional studies of two red algae. II.
Kinetics of ammonium and nitrate uptake. J Phycol 14:266–272
Fletcher RL, Manfredi C (1995) The occurrence of Undaria pinnatifida
(Phaeophyceae, Laminariales) on the south coast of England. Bot
Mar 38:355–358
Gevaert F, Creach A, Davoult D, Holl AC, Seuront L, Lemoine Y
(2002) Photo-inhibition and seasonal photosynthetic performance
of the seaweed Laminaria saccharina during a simulated tidal
cycle: chlorophyll fluorescence measurements and pigment anal-
ysis. Plant Cell Environ 25:859–872
Haines KC, Wheeler PA (1978) Ammonium and nitrate uptake by the
marine macrophytes Hypnea musciformis (Rhodophyta) and Mac-
rocystis pyrifera (Phaeophyta). J Phycol 14:319–324
Hanisak MD, Harlin MM (1978) Uptake of inorganic nitrogen by Codium
fragile subsp. tomentoroides (Cholorophyta). J Phycol 14:450
Harrison PJ, Druehl LD, Lloyd KE, Thompson PA (1986) Nitrogen
uptake kinetics in three year-classes of Laminaria groenlandica
(Laminariales: Phaeophyta). Mar Biol 93:29–35
Hay CH, Luckens PA (1987) The Asian kelp Undaria pinnatifida
(Laminariales, Phaeophyta) found in a New Zealand harbor. NZ
J Bot 57:329–332
Hay KB, Poore AGB, Lovelock CE (2011) The effects of nutrient
availability on tolerance to herbivory in a brown seaweed. J Ecol
99:1540–1550
Hicks SL, Reader RJ (1995) Compensatory growth of three grasses
following simulated grazing in relation to soil nutrient availability.
Can J Bot 73:141–145
Honkanen T, Jormalainen V (2002) Within-alga integration and compen-
sation: effects of simulated herbivory on growth and reproduction of
the brown alga Fucus vesiculosus. Int J Plant Sci 163:815–823
Jãremo J, Nilsson P, Tuomi J (1996) Plant compensatory growth:
herbivory or competition? Oikos 77:238–247
Karban R, Strauss SY (1993) Effects of herbivores on growth and repro-
duction of their perennial host, Erigeron glaucus. Ecology 74:39–46
Lapointe BE (1981) The effects of light and nitrogen no growth, pigment
content and biochemical composition of Gracilaria folifera v. agus-
tissima (Gigartinales, Rhodophyta). J Phycol 17:90–95
Lehtila K, Syrjänen K (1995) Compensatory responses of two Melampyrum
species after damage. Funct Ecol 9:511–517
Lennartsson T, Nilsson P, Tuomi J (1998) Induction of overcompensation
in the field Gentian, Gentianella campestris. Ecology 79:1061–1072
Levy I, Gantt E (1990) Development of photosynthetic activity in
Porphyridium purprueum (Rhodophyta) following nitrogen star-
vation. J Phycol 26:62–68
Lingnell A, Pedersen M (1987) Nitrogen metabolism in Gracilaria
secundata (Harv.). Hydrobiologia 151/152:431–441
Littler MM, Littler DS, Taylor PR (1995) Selective herbivore increases
biomass of its prey—a chiton–coralline reef-building association.
Ecology 76:1666–1681
Louda SM (1984) Herbivore effect on stature, fruiting, and leaf dy-
namics of a native crucifer. Ecology 65:1379–1386
Mabry CM, Wayne PW (1997) Defoliation of the annual herb Abutilon
theophrasti—mechanisms underlying reproductive compensa-
tion. Oecologia 111:225–232
Maschinski J, Whitham TG (1989) The continuum of plant responses
to herbivory: the influence of plant association, nutrient availabil-
ity and timing. Am Nat 134:1–19
McNaughton SJ (1979) Grazing as an optimization process—grass
ungulate relationships in the Serengeti. Amer Natur 113:691–703
McNaughton SJ (1983) Compensatory plant growth as a response to
herbivory. Oikos 40:329–336
Oba G, Mengistu Z, Stenseth NC (2000) Compensatory growth of the
African dwarf shrub, Indigofera spinosa, following simulated
herbivory. Ecol Appl 10:1133–1146
J Appl Phycol (2013) 25:1171–1178
Pansch C, Gómez I, Rothäusler E, Véliz K, Thiel M (2008) Species-
specific defense strategies of vegetative versus reproductive
blades of the pacific kelps Lessonia nigrescens and Macrocystis
integrifolia. Mar Biol 155:51–62
Rausher MD, Feeny P (1980) Herbivory, plant density, and plant
reproductive success: the effect of Battus philenor on Aristolochia
reticulata. Ecology 61:905–917
Raven JA (2003) Long-distance transport in non-vascular plants. Plant
Cell Environ 26:73–85
Saito Y (1962) Fundamental study of propagation of Undaria pinnatifida.
Performance reports of the Fisheries laboratory of Tokyo University
3:1–101 (in Japanese)
Saito Y (1972) Effects of environmental factors on morphological
characteristics of Undaria pinnatifida and the breeding of hybrids
in the genus Undaria. In: Abott I A and Kurogi, M (Eds) Con-
tributions to the systematics of benthic marine algae of the North
Pacific. Japanese Society of Phycology, pp 117–133
Sanbonsuga Y, Machiguchi Y, Saga N (1987) Productivity estimation
and evaluation of the cultivation factors in biomass production of
Laminaria. Bull Hokkaido Reg Fish Res Lab 51:45–50
Sanderson JC (1990) A preliminary survey of the distribution of the
introduced macroalga Undaria pinnatifida (Harvey) Suringer on
the east coast of Tasmania. Bot Mar 33:153–157
Schmitz K (1981) Translocation. In: Lobban C, Wynne M (eds) The
biology of seaweeds. Blackwell, Oxford, pp 534–558
Silva PC, Woodfield RA, Cohen AN, Harris LH, Goddard JHR (2002)
First report of the Asian kelp Undaria pinnatifida in the north-
eastern Pacific Ocean. J Appl Phycol 4:333–338
Simons AM, Johnston MO (1999) The cost of compensation. Am Nat
153:683–687
Smit AJ (2002) Nitrogen uptake by Gracilaria gracilis (Rhodophyta):
adaptations to a temporally variable nitrogen environment. Bot
Mar 45:196–209
Steinberg PD (1995) Interaction between the canopy dwelling echinoid
Holopneustes purpurescens and its host kelp Ecklonia radiata.
Mar Ecol Prog Ser 127:169–181
Steneck RS (1982) A limpet-coralline alga association—adaptations
and defenses between a selective herbivore and its prey. Ecology
63:507–522
Strauss SY, Agrawal AA (1999) The ecology and evolution of plant
tolerance to herbivores. Trends Ecol Evol 14:179–185
Tatewaki M (1966) Formation of a crustose sporophyte with unilocular
sporangia in Scitosiphon lomentaria. Phycologia 6:62–66
Thomas TE, Harrison PJ (1987) Rapid ammonium uptake and nitrogen
interactions in five intertidal seaweeds grown under field condi-
tions. J Exp Mar Biol Ecol 107:1–8
Tiffin P (2000) Mechanisms of tolerance to herbivore damage: what do
we know? Evol Ecol 14:523–536
Tokuda H, Kawashima S, Ohno M, Ogawa H (1994) Cultivation of
“Wakame”, Undaria pinnatifida. In: Seaweeds of Japan. Midori
Shobo Co., Ltd., Japan. 98 pp (in Japanese)
Toth GB, Pavia H (2002) Lack of phlorotannin induction in the kelp
Laminaria hyperborean in response to grazing by two gastropod
herbivores. Mar Biol 140:403–409
Trumble JT, Kolodney-Hirsh DM, Ting IP (1993) Plant compensation
for arthropod herbivory. Annu Rev Entomol 38:93–119
Vergés A, Pérez M, Alcoverro T, Romero J (2008) Compensation and
resistance to herbivory in seagrasses: induced responses to simu-
lated fish consumption. Oecologia 155:751–760
Yamanaka R, Akiyama K (1993) Cultivation and utilization of Undaria
pinnatifida (wakame) as food. J Appl Phycol 5:249–253
Yokohama Y, Katayama N, Furuya K (1986) An improved type of
“Productmeter”, a differential gas-volumeter, and its application
to measuring photosynthesis of seaweeds. Jpn J Phycol 34:37–42