The growth and hole formation of
Ulva australis
were examined at seven coastal areas of Korea between July and August, 2013. Animal species and weight growing on the
Ulva
fronds were estimated at Haseom, Pohang, and Woedo. The effects of wave exposure on the morphological features and residential animals of
Ulva
fronds were investigated at wave-exposed and sheltered sites of Seongsan on October 19, 2013.
U. australis
had different frond areas (82-665 cm
2
), hole areas (2.5-6.3 cm
2
), and hole numbers (9.8-41.3 holes) at the seven sites. Within 0.1 m
2
of
Ulva
frond, hole areas ranged from 0.37 to 5.94 cm
2
, and between 4.9 and 36.2 holes were observed. Fourteen residential animal species were observed at the three evaluated sites, 75.0 (Haseom) to 408.7 individuals 100 g
−1
Ulva
(Pohang) per site. The dominant residential species at each site differed with
Amphithoe
sp. at Haseom,
Monodonta
spp. at Pohang, and
Pagurus
sp. at Woedo. The growth (frond area, wet weight) and hole number of
Ulva
fronds, and the number of residential animals were significantly greater in samples collected from the sheltered shore than the wave-exposed shore of Seongsan. The present results showed
U. australis
grew well at sheltered shores and had more holes on the fronds due to abundance of residential animals. The dominant residential animals (crabs, gammaridea, and snails) were similar in the
Ulva
populations of sheltered and wave-exposed shores, but greater species diversity was observed at the exposed shore (18 species ver. 11 species). In conclusion,
U. australis
is a keystone species providing habitat to various invertebrates and frond holes are positively correlated to the number of residential animals.
INTRODUCTION
Ulva australis
Kjellman (formerly called
Ulva pertusa
) grows on the rocky shores of Korea, and could play an important role as a primary producer in coastal ecosystems as do many seaweeds. The species occasionally forms extensive mats called green tide in coastal areas around the world due to its fast growth and high reproductive capacity (
Fletcher 1996
,
Han et al. 2003
,
Hiraoka et al. 2004
,
Kim et al. 2011
,
Deng et al. 2012
). However, there are no available data on whether
U. australis
plays an ecological role as a bioengineer, providing habitat, nursing grounds, and food sources for various marine animals, to increase the biodiversity in Korea.
Some macroalgal fronds have innate holes, as found in the two brown algae,
Agarum clathratum
and
Costaria costata
, some of which are made by biotic activities (endophytes, grazers) or through wave action (
De Bettignies et al. 2012
,
Kim et al. 2014
). For example,
Undaria pinnatifida
are affected by a pinhole disease that resultings from infection by the harpacticoid copepods
Amenophia orientalis
and
Parathalestris infestus
, causing the fronds to have many small holes (
Park et al. 2008
). Holes are also produced by herbivorous grazers in the process of eating (
Menge 1978
), and wounds associated with grazing and wave action were shown to increase kelp erosion in
Ecklonia radiata
(
De Bettignies et al. 2012
).
Ulvella operculata
(=
Acrochaete operculata
) is an endophyte that produces degradative lesions in
Chondrus crispus
fronds, while green endophytes make holes in the fronds of
Grateloupia
spp. (
Correa et al. 1988
,
Correa and McLachlan 1991
,
1992
,
Kim et al. 2014
).
The effects of environmental factors on the growth and eco-physiological features of
Ulva
spp. have been thoroughly examined (
Talylor et al. 2001
,
Choi et al. 2010
,
Mantri et al. 2011
). In
U. australis
, physiological responses to exposure to copper and UV light (
Han and Han 2005
,
Han et al. 2008
), as well as various environmental factors (i.e., temperature, light intensity, and nutrients, etc.), have been reported (
Floreto et al. 1994
). In addition,
U. australis
were found to display antioxidant, allelopathic, and antihyperlipidemic activities (
Floreto et al. 1994
). Ecologically, ephemeral algae such as
Ulva
spp. are food resources for gastropod herbivores (
Lubchenco 1983
,
Geertz-Hansen et al. 1993
,
Giannotti and McGlathery 2001
). However, the growth, hole formation, and ecological role of
U. australis
as a habitat and food resources of marine animals have not yet been determined. Thus, the aims of this study were to examine the growth and hole formation of
U. australis
, and to investigate the effects of wave action on the growth of the species and on the abundance of residential animals. Finally, whether hole formation in the
U. australis
fronds is correlated with wave action and residential animals was discussed.
MATERIALS AND METHODS
U. australis
frond samples were collected at seven study sites located on Jeju Island and along the Eastern, Western, and Southern coasts of the Korean Peninsula between the end of July and early August, 2013 (
Fig. 1
). At each site, 30
U. australis
fronds were randomly sampled. All of the samples were photographed, and Image J software was used to count the number of holes and for measurement of frond and hole area. Hole area (y) and frond area (x) were plotted, and an equation was calculated. The differences in frond area, number of holes, and hole area per 0.1 m
2
of
Ulva
fronds were compared among the seven populations. In addition, more than 100 g wet weight of
Ulva
fronds were collected from Haseom, Pohang, and Woedo in order to examine the abundance and species composition of the residential animals on the
Ulva
fronds. The animals living on the
Ulva
fronds were sorted, identified, counted, and weighed for each population, and then the number and weight of the animals per 100 g of
Ulva
fronds was determined.
Map of sampling sites of Ulva australis fronds (●) and residential animals (◎) on the coastal areas of Korea. Collection site (★) of Ulva fronds and residential animals at wave-exposed and sheltered shores.
To examine the effects of wave action on the growth and hole formation of
U. australis
fronds, as well as on the abundance of residential animals, samples were also collected from wave-exposed and sheltered sites of Seongsan, Jeju, Korea on October 19, 2013 (
Fig. 1
). The levels of wave exposure were measured using a dynamometer, which was made following the protocol of
Bell and Denny (1994)
. Relative levels of wave exposure, from zero (no movement) to 1 (full tie length), were calculated using the distance moved by a rubber indicator connected to a practice golf ball with a nylon cable tie. The wave-exposed site of Seongsan displayed relatively higher wave action (0.7 of 1.0) than the sheltered site (0.2).
Statistical analyses were performed using STATISTICA version 5.0 (StatSoft Inc., Tulsa, OK, USA). One-way ANOVAs were performed separately in order to test for differences in the morphological features of the seven populations, including the frond area, hole area, and hole number per 0.1 m
2
of
Ulva
frond. One-way ANOVA was used to test the effects of wave action on the growth and hole formation of
Ulva
fronds for the Seongsan populations. Prior to analysis, the homogeneity in the variance was tested using Cochran’s test. Tukey’s multiple comparison was employed, when significant differences between means were detected (
Sokal and Rohlf 1995
).
RESULTS
- Growth and hole formation inUlva australisfronds
The average frond area of the
U. australis
population (n = 30 fronds) ranged from 82.88 cm
2
at Muchangpo to 665.91 cm
2
at Woedo, Jeju (
Table 1
). The differences in frond area were statistically significant (F
6,203
= 37.52, p < 0.001), with remarkably larger values observed in the Woedo population (
Table 1
). The hole area ranged from 2.51 to 6.33 cm
2
per frond, demonstrating the largest values in the Pohang population and smallest in the Haseom population. However, significant differences were not observed in terms of the hole area (F
6,203
= 2.44, p > 0.05). An average of 9.8 to 41.3 holes were observed per frond, with the greatest among the seven study sites observed for the Jindo population (
Table 1
). Hole areas (y) were positively correlated with the frond areas (x) of
U. australis
(
Fig. 2
) for the samples taken from Pohang (y = 0.019x
1.14
, r
2
= 0.77), Uljin (y = 0.023x
0.95
, r
2
= 0.70), Muchangpo (y = 0.037x
1.08
, r
2
= 0.53), Haseom (y = 0.002x
1.37
, r
2
= 0.79), Wando (y = 0.001x
1.70
, r
2
= 0.75), Jindo (y = 0.001x
1.80
, r
2
= 0.67), and Woedo (y = 0.001x
1.19
, r
2
= 0.68).
Frond features ofUlva australiscollected around coasts of Korea
Values represent mean ± standard error (n = 30 fronds). Different letters indicate significant differences between groups of means, found with the Tukey’s honestly significant difference tests.
Correlation between hole and frond areas of Ulva australis (n = 30 fronds) collected at the seven study sites from East (A), West (B), South (C), and Jeju (D), Korea.
Examination of a fixed area of the frond revealed hole area (cm
2
0.1 m
−2
frond) to be between 0.37 and 5.94 cm
2
, with hole numbers (0.1 m
−2
frond) in the range of 4.9 to 36.2 (
Table 1
). The smallest area and number of holes were observed for the Woedo population, even though the frond area was the largest of the seven
Ulva
populations examined. Hole area (cm
2
0.1 m
−2
frond) was the largest for the Muchangpo population, while the hole number was greatest in the Pohang population (
Table 1
).
- Residential animals of threeUlvapopulations
Fourteen species of marine animals were found in the
Ulva
fronds, with 3 to 13 species found at each location (
Table 2
). The species richness was the greatest at Woedo and the lowest at Haseom. The number of animals (100 g
−1
frond) varied from 75.0 at Haseom to 408.7 at Pohang. In terms of the number of animals, the dominant species differed according to the region, with gammaridea (
Amphithoe
sp., 95.43%) identified for Haseom, snails (
Monodonta
spp., 92.75%) for Pohang, and crab (
Pagurus
sp., 49.20%) for Woedo. The average animal weight (100 g
−1
frond) was minimal, making up 0.60 g wet weight at Haseom and 32.91 g at Woedo. The dominant animals in terms of the average weight were also the same, with gammaridea (
Amphithoe
sp., 54.06%) for Haseom and snails (
Monodonta
spp., 52.09%) for Pohang. However,
Lunella coronate coreensis
was dominant in terms of weight at Woedo.
Species and wet weight (g) of animals inhabiting theUlva australisfronds (100 g) collected from three study sites in Korea
Species and wet weight (g) of animals inhabiting the Ulva australis fronds (100 g) collected from three study sites in Korea
- Effects of wave action onUlvafronds and invertebrate abundance
The frond area and weight of
U. australis
at the sheltered station of Seongsan were twice those at the exposed shores, with significantly difference between the two levels of wave exposure (
Table 3
). While no significant difference was observed in hole area (0.1 m
2
frond), the number of holes was significantly greater in the sample from the sheltered shore than from the wave-exposed shore (
Table 3
).
Effects of wave exposure on the frond area, hole area, and hole number ofUlva australiscollected from the exposed and sheltered shores of Seongsan, Jeju, Korea
Values represent mean ± standard error (n = 30 fronds).
In the
U. australis
populations of Seongsan, the average frond weight at the sheltered shores was twice as large as that at the exposed shores, measured at 1.84 ± 0.41 ver. 0.99 ± 0.13 g wet weight (mean ± SE, n = 5 replicates) (
Table 4
). However, no significant differences were observed between those exposed to waves in terms of the individual weight of the
Ulva
fronds (F
1,8
= 3.99, p > 0.05). At the sheltered shore, the number of animals (100 g
−1
Ulva
) was four times greater (F
1,8
= 6.23, p < 0.05) than at the waveexposed shore, while the animal weight was only slightly greater (F
1,8
= 0.31, p > 0.05) (
Table 4
). That is, the animals inhabiting
Ulva
fronds were abundant in both number and weight at the sheltered shores of Seongsan.
Weight ofUlva australisand abundance of residential animals collected at the wave exposed and sheltered shores of Seongsan, Jeju, Korea
Weight of Ulva australis and abundance of residential animals collected at the wave exposed and sheltered shores of Seongsan, Jeju, Korea
A total of 19 species or taxon was found in the
Ulva
population of Seongsan, with 18 species observed at the exposed shore and 11 species at the sheltered location. With respect to the
Ulva
fronds, an abundance of crabs, gammaridea, and snails was observed, irrespective of exposure to waves (
Table 5
). At the exposed shores, the dominant species were Gammaridea sp. with subdominant species of
Cantharidus
and
Assiminea
. However, Anomura sp. was dominant, with
Cantharidus
sp. as the subdominant species at the sheltered shores.
Animal species and abundance (100 g−1wet wt. fronds) in samples collected at exposed and sheltered shores of Seongsan, Jeju, Korea
DISCUSSION
The growth and hole formation of
Ulva australis
displayed significant difference among the populations along the coast of Korea. Frond area was eight times greater at Woedo than in the Muchangpo and Wando populations.
Ulva
spp. is a notorious species that produces green macroalgal blooms in eutropicated or disturbed areas caused by anthropogenic activities on the coast of Korea and around the world (
Taylor et al. 2001
,
Han et al. 2003
,
Kim et al. 2011
). Generally, green tides of
Ulva
spp. tend to occur at sites with soft bottom, including mud, silt or sand, with floating
Ulva
species (
Hiraoka et al. 2004
,
Kim et al. 2011
). So far, there have been no reports of green tide due to
U. australis
growth on rocky shores, but this species is becoming dominant in the coastal areas of Korea (
Choi et al. 2010
). In addition, it is known to grow well in wide range of salinities as do many green tide algae such as
Ulva fasciata, U. rigida
, and
U. lactuca
(
Zavodnik 1975
,
Morand and Briand 1996
,
Giannotti and McGlathery 2001
). Thus, it is very important to examine the growth of
U. australis
in coastal areas of Korea, and to elucidate the environmental factors regulating the growth of the species in the field population. The growth of
Ulva
spp. is determined by abiotic factors, including temperature, light intensity and nutrients, as well as by top-down control through marine invertebrate grazing (
Floreto et al. 1994
,
Giannotti and McGlathery 2001
,
Talylor et al. 2001
,
Choi et al. 2010
,
Mantri et al. 2011
). The present results demonstrated that the growth of
U. australis
was controlled by wave activity and herbivorous animals in the field population.
In the present study, 14 species of marine animal were observed in three
U. australis
populations examined, while 19 species were observed in the populations from Seongsan, Jeju, indicating that this species is a bioengineer that increases the biodiversity of various marine animals by providing a habitat, nursery grounds, and food sources, like seaweeds do (
Terawaki et al. 2001
,
Eklöf et al. 2005
). The dominant animal species growing on the
Ulva
populations differed according to the study sites, but gammaridea (
Amphithoe
sp.), gastropod (
Monodonta
spp.), and crab (
Pagurus
sp.) were most commonly observed. The abundance of grazers was positively correlated with the hole number in the
Ulva
fronds for the Pohang and the Seongsan populations. These results indicate that the
Ulva
population provides habitats and food resources for various marine invertebrated grazers, which make holes in the fronds. In addition, decayed
Ulva
fronds can become foodstuff for filter feeders or detritus feeders as a component of particulate and dissolved organic matter, as reported in studies of
Ulva lactuca
(
Giannotti and McGlathery 2001
) and kelp (
Mann 2000
).
Wave activity was also found to influence the growth and hole number of
Ulva
fronds in the Seongsan populations.
U. australis
grew better and had more holes at the sheltered shore, where more residential invertebrates were present than at exposed shore. The holes in macroalgal fronds can be produced either genetically, or as a result of biotic or abiotic activities, including those of endophytes, grazers, or wave activity, as observed for
C. crispus, U. pinnatifida
, and
E. radiata
(
Correa et al. 1988
,
Park et al. 2008
,
De Bettignies et al. 2012
,
Kim et al. 2014
). The present results indicate that the holes in the
U. australis
fronds are mainly related to grazing pressure.
Marine invertebrate grazers, such as gastropods, amphipods, and isopods reduce macroalgal biomass by making holes in the fronds (
Giannotti and McGlathery 2001
,
Martins et al. 2014
). In the present study, the dominant animal species in the
Ulva
populations were gammaridea, gastropods, and crab, which usually make holes or tear the fronds while feeding.
Park et al. (2008)
reported that small holes of
U. pinnatifida
fronds are made by the feeding activities of copepods,
A. orientalis
and
P. infestus
.
Hauxwell et al. (1998)
reported that amphipod and isopod grazers consumed significant amounts of macroalgae in the field. Grazing is a form of biological stress that can damage
Ulva
tissue by producing holes, which may result in loss of biomass due to secondary physical factors, including wave action, pathogens, and abrading sediments. However, a laboratory feeding experiment was not performed on the three dominant residential animals observed herein. Thus, to make the conclusion that residential animals caused the frond holes on the
U. australis
, more detailed experiments should be conducted in the future. In simulated wound experiments, the biomechanical properties of
E. radiata
fronds exposed to strong wave activity during the winter exhibited a significant reduction as a result of holes (or cuts), increased kelp pruning rates, and substantial reduction in biomass (
De Bettignies et al. 2012
).
In conclusion,
U. australis
populations play an important ecological role as a habitat and as foodstuff for many marine invertebrates, and their population structures differ according the location in terms of frond area, hole number and hole area. In addition, growth and hole number of
Ulva
fronds around the coast of Korea are affected by wave activity, as well as by the number of herbivorous animals, such as isopods and gastropods.
Acknowledgements
This research was financially supported by a grant from the Marine Biotechnology Program Funded by the Ministry of Ocean and Fisheries of the Korean Government. It was also supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF), funded by the Ministry of Education, Science and Technology (NRF-2011-0012519).
Bell E. C.
,
Denny M. W.
1994
Quantifying “wave exposure”: a simple device for recording maximum velocity and results of its use at several field sites
J. Exp. Mar. Biol. Ecol.
181
9 -
29
DOI : 10.1016/0022-0981(94)90101-5
Choi T. S.
,
Kang E. J.
,
Kim J.
,
Kim K. Y.
2010
Effect of salinity on growth and nutrient uptake of Ulva pertusa (Chlorophyta) from an eelgrass bed
Algae
25
17 -
26
DOI : 10.4490/algae.2010.25.1.017
Correa J. A.
,
McLachlan J. L.
1992
Endophytic algae of Chondrus crispus (Rhodophyta). IV. Effects on the host following infections by Acrochaete operculata and A. heteroclada (Chlorophyta)
Mar. Ecol. Prog. Ser.
81
73 -
87
DOI : 10.3354/meps081073
Correa J. A.
,
Nielsen R.
,
Grund D. W.
1988
Endophytic algae of Chondrus crispus (Rhodophyta). II. Acrochaete heteroclada sp. nov., A. operculata sp. nov., and Phaeophila dendroides (Chlorophyta)
J. Phycol.
24
528 -
539
De Bettignies T.
,
Thomsen M. S.
,
Wernberg T.
2012
Wounded kelps: patterns and susceptibility to breakage
Aquat. Biol.
17
223 -
233
DOI : 10.3354/ab00471
Deng Y.
,
Tang X.
,
Huang B.
,
Ding L.
2012
Effect of temperature and irradiance on the growth and reproduction of the green macroalga, Chaetomorpha valida (Cladophoraceae, Chlorophyta)
J. Appl. Phycol.
24
927 -
933
DOI : 10.1007/s10811-011-9713-0
Eklöf J. S.
,
de la Torre Castro M.
,
Adelsköld L.
,
Jiddawi N. S.
,
Kautsky N.
2005
Differences in macrofaunal and seagrass assemblages in seagrass beds with and without seaweed farms
Estuar. Coast. Shelf Sci.
63
385 -
396
DOI : 10.1016/j.ecss.2004.11.014
Fletcher R. T.
,
Schramm W.
,
Nienhuis P. H.
1996
Marine Benthic Vegetation: Recent Changes and the Effects of Eutrophication
Springer Verlag
Berlin
The occurrence of ‘green tide’
7 -
43
Floreto E. A. T.
,
Hirata H.
,
Yamasaki S.
,
Castro S. C.
1994
Effect of salinity on the growth and fatty acid composition of Ulva pertusa Kjellman (Chlorophyta)
Bot. Mar.
37
151 -
155
Geertz-Hansen O.
,
Sand-Jensen K.
,
Hansen D. F.
,
Christiansen A.
1993
Growth and grazing control of abundance of the marine macroalga, Ulva lactuca L. in a eutrophic Danish estuary
Aquat. Bot.
46
101 -
109
DOI : 10.1016/0304-3770(93)90039-Y
Han T.
,
Han Y. -S.
,
Kain J. M.
,
Häder D. -P.
2003
Thallus differentiation of photosynthesis, growth, reproduction, and UV-B sensitivity in the green alga Ulva pertusa (Chlorophyceae)
J. Phycol.
39
712 -
721
DOI : 10.1046/j.1529-8817.2003.02155.x
Han T.
,
Kang S. -H.
,
Park J. -S.
,
Lee H. -K.
,
Brown M. T.
2008
Physiological responses of Ulva pertusa and U. armoricana to copper exposure
Aquat. Toxicol.
86
176 -
184
DOI : 10.1016/j.aquatox.2007.10.016
Hauxwell J.
,
McClelland J.
,
Behr P. J.
,
Valiela I.
1998
Relative importance of grazing and nutrient controls of macroalgal biomass in three temperate shallow estuaries
Estuaries
21
347 -
360
DOI : 10.2307/1352481
Kim C.
,
Kim Y. S.
,
Choi H. G.
,
Nam K. W.
2014
New records of three endophytic green algae from Grateloupia spp. (Rhodophyta) in Korea
Algae
29
127 -
136
DOI : 10.4490/algae.2014.29.2.127
Kim J. -H.
,
Kang E. J.
,
Park M. G.
,
Lee B. -G.
,
Kim K. Y.
2011
Effects of temperature and irradiance on photosynthesis and growth of a green-tide-forming species (Ulva linza) in the Yellow Sea
J. Appl. Phycol.
23
421 -
432
DOI : 10.1007/s10811-010-9590-y
Lubchenco J.
1983
Littornia and Fucus: effects of herbivores, substratum heterogeneity, and plant escapes during succession
Ecology
64
1116 -
1123
DOI : 10.2307/1937822
Mann K. H.
2000
Ecology of coastal waters: with implications for management
2nd ed
Blackwell Scientific
Oxford
432 -
Mantri V. A.
,
Singh R. P.
,
Bijo A. J.
,
Kumari P.
,
Reddy C. R. K.
,
Jha B.
2011
Differential response of varying salinity and temperature on zoospore induction, regeneration and daily growth rate in Ulva fasciata (Chlorophyta, Ulvales)
J. Appl. Phycol.
23
243 -
250
DOI : 10.1007/s10811-010-9544-4
Martins I.
,
Leite N.
,
Constantino E.
2014
Consumption and feeding preference of Echinogammarus marinus on two different algae: Fucus vesiculosus and Ulva intestinalis
J. Sea Res.
85
443 -
446
DOI : 10.1016/j.seares.2013.07.017
Menge B. A.
1978
Predation intensity in a rocky intertidal community: effect of an algal canopy, wave action and desiccation on predator feeding rates
Oecologia
34
17 -
35
DOI : 10.1007/BF00346238
Morand P.
,
Briand X.
1996
Excessive growth of macroalgae: a symptom of environmental disturbance
Bot. Mar.
39
491 -
516
Park C. S.
,
Park K. Y.
,
Baek J. M.
,
Hwang E. K.
2008
The occurrence of pinhole disease in relation to developmental stage in cultivated Undaria pinnatifida (Harvey) Suringar (Phaeophyta) in Korea
J. Appl. Phycol.
20
485 -
490
DOI : 10.1007/s10811-008-9329-1
Sokal R. R.
,
Rohlf F. J.
1995
Biometry: the principles and practices of statistics in biological research
3rd ed
W. H. Freeman
NY
887 -
Taylor R.
,
Fletcher R. L.
,
Raven J. A.
2001
Preliminary studies on the growth of selected ‘green tide, algae in laboratory culture: effects of irradiance, temperature, salinity and nutrients on growth rate
Bot. Mar.
44
327 -
336
Terawaki T.
,
Hasegawa H.
,
Arai S.
,
Ohno M.
2001
Management-free techniques for restoration of Eisenia and Ecklonia beds along the central Pacific coast of Japan
J. Appl. Phycol.
13
13 -
17
DOI : 10.1023/A:1008135515037
Zavodnik N.
1975
Effects of temperature and salinity variations on photosynthesis of some littoral seaweeds of the North Adriatic Sea
Bot. Mar.
18
245 -
250