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A survey of epiphytic organisms in cultured kelp Saccharina japonica in Korea

A survey of epiphytic organisms in cultured kelp Saccharina japonica in Korea A survey was conducted to investigate the presence of epiphytic organisms in four kelp Saccharina japonica farms in the coastal area of Korea from 2014 to 2015. Of 740 kelp samples that were taken, 208 exhibited six kinds of epiphytic organisms, including hydroid (detection rate: 11.6%), bryozoan (6.4%), polychaete (3.4%), algae (3.2%), caprellid (3%), and oyster (0.5%). The infestation rate for hydroid, bryozoan, and polychaete was significantly higher in the Wando farm, Busan farm, and Pohang farm, respectively. Epiphytic organisms were generally observed during May to September and not January to April, indicating that their infestation was significantly higher when the water had a higher temperature. The histopathogical examination revealed that hydroid and bryozoan organisms were attached on the cuticula of the thallus while some algae were attached on the cuticula of the thallus or had penetrated the epidermis. These results indicate that hydroid and bryozoan were the most predominant epiphytic organisms in Korean kelp farms, even though the infested thallus had not been broken. Keywords: Epiphytic organisms, Bryozoan, Hydroid, Kelp, Saccharina japonica Background epiphytic organisms (Gong et al., 2010; Park and Hwang, Within the last 30 years, seaweed cultivation has 2012). An infestation is characterized by the appearance attained large-scale production levels and has become a of numerous colonies on the thallus of the kelp, and major industry in China, Korea, and Japan. Korea had a therefore, the affected kelp appears unsightly and cannot harvest of 1,022,326 tons in 2012, which makes it the be sold. Although systematic research on fish disease fourth largest seaweed-producing country in the world has been conducted in Korea since the 1990s, seaweed (FAO, 2014). The economically important seaweed disease has not yet been systematically studied. There- species harvested in Korea are laver Porphyra spp., fore, little information is available on kelp disease. The wakame Undaria spp., kelp Laminaria spp., fusi- present study consists of a survey that was conducted to forme, Hizikia fusiformis, and green laver Monostroma investigate the presence of epiphytic organisms in spp. (KOSIS, 2015). Korean kelp farms. In addition, a histopathological Kelp Saccharina japonica cultivation was industrial- examination was conducted to understand the effect by ized in Korea in the 1970s, and from 2005, it has been epiphytic organisms on the thallus. extensively developed together with the abalone indus- try. During the 1970s to 1980s, kelp production reached Methods less than 12,000 tons, and production steadily increased Kelp samples and epiphytic organism examination since then with about 370,000 tons harvested in 2013 Kelp samples were obtained from four private farms in (KOSIS, 2015). Kelp production now accounts for about Wando (Southern Sea), Busan (Southern Sea), and 25% of all Korean seaweed cultivation (KOSIS, 2015). Pohang (Eastern Sea) during 2014 and 2015 (Table 1, However, the increase in production has also resulted in Fig. 1). Wando is the most popular area for kelp cultiva- kelp farms becoming severely infected by several tion, producing about 97% of the kelp crop of Korea. The kelps were randomly selected by a farmer, trans- * Correspondence: ohmj@Jnu.ac.kr ported on ice, and immediately subjected an examin- Department of Aqualife Medicine, Jeonnam National University, Yeosu ation of the epiphytic organisms. The total length (from 59626, South Korea Full list of author information is available at the end of the article apex to holdfast) of the thallus was measured, and the © The Author(s). 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Kim et al. Fisheries and Aquatic Sciences (2017) 20:1 Page 2 of 7 Table 1 Detection of epiphytic organisms in four kelp farms in Korea Place Farm Date Water temperature Mean thallus Detection rate of epiphytic organisms % (detection no./total no.) (°C) length (cm) Hydroid Bryozoan Polychaete Algae Caprellid Oyster Wando WDA Apr 2014 11.5 340 (200–380) 0 (0/10) 0 (0/10) 0 (0/10) 0 (0/10) 0 (0/10) 0 (0/10) May 2014 15.5 260 (260–270) 0 (0/2) 0 (0/2) 0 (0/2) 0 (0/2) 0 (0/2) 0 (0/2) Jun 2014 17.4 NT 20 (1/5) 0 (0/5) 0 (0/5) 0 (0/5) 20 (1/5) 0 (0/5) Jul 2014 21.7 190 (100–240) 100 (6/6) 50 (3/6) 0 (0/6) 100 (6/6) 0 (0/6) 0 (0/6) Aug 2014 23 200 (100–240) 71.4 (5/7) 57.1 (4/7) 0 (0/7) 71.4 (5/7) 71.4 (5/7) 0 (0/7) Sep 2014 22.1 120 (90–160) 57.1 (4/7) 71.4 (5/7) 0 (0/7) 14.3 (1/7) 0 (0/7) 57.1 (4/7) Jan 2015 9 41 (20–71) 0 (0/71) 0 (0/71) 0 (0/71) 0 (0/71) 0 (0/71) 0 (0/71) Jan 2015 8.3 82 (39–122) 0 (0/75) 0 (0/75) 0 (0/75) 0 (0/75) 0 (0/75) 0 (0/75) Apr 2015 11 236 (200–280) 0 (0/30) 0 (0/30) 0 (0/30) 0 (0/30) 0 (0/30) 0 (0/30) Total detection rate in WDA 7.5 (16/213) 5.6 (12/213) 0 (0/213) 5.6 (12/213) 2.8 (6/213) 0.9 (4/213) WDB May 2014 15.4 220 (100–330) 0 (0/14) 0 (0/14) 0 (0/14) 0(0/14) 0 (0/14) 0 (0/14) Jun 2014 21 260 (180–320) 57.1 (4/7) 0 (0/7) 0 (0/7) 28.6 (2/7) 0 (0/7) 0 (0/7) Jul 2014 21.5 160 (130–200) 100 (14/14) 0 (0/14) 35.7 (5/14) 0 (0/14) 7.1 (1/14) 0 (0/14) Sep 2014 21.6 130 (60–230) 100 (15/15) 33.3 (5/15) 0 (0/15) 13.3 (2/15) 0 (0/15) 0 (0/15) Feb 2015 9 57 (30–100) 0 (0/100) 0 (0/100) 0 (0/100) 0 (0/100) 0 (0/100) 0 (0/100) Mar 2015 11 97 (50–180) 0 (0/73) 0 (0/73) 0 (0/73) 0 (0/73) 0 (0/73) 0 (0/73) Apr 2015 12.5 127 (90–190) 0 (0/30) 0 (0/30) 0 (0/30) 0 (0/30) 0 (0/30) 0 (0/30) Total detection rate in WDB 13 (33/253) 2 (5/253) 2 (5/253) 1.6 (4/253) 0.4 (1/253) 0 (0/253) Busan BS Apr 2014 11 170 (50–270) 0 (0/10) 10 (1/10) 0 (0/10) 30 (3/10) 0 (0/10) 0 (0/10) May 2014 14.5 230 (130–280) 100 (9/9) 88.9 (8/9) 0 (0/9) 0 (0/9) 0 (0/9) 0 (0/9) Jun 2014 21 220 (180–300) 100 (7/7) 71.4 (5/7) 0 (0/7) 71.4 (5/7) 0 (0/7) 0 (0/7) Jul 2014 20.4 160 (120–180) 100 (10/10) 90 (9/10) 0 (0/10) 0 (0/10) 100 (10/10) 0 (0/10) Feb 2015 11.5 76 (26–175) 0 (0/58) 0 (0/58) 0 (0/58) 0 (0/58) 0 (0/58) 0 (0/58) Feb 2015 12 143 (80–219) 0 (0/37) 0 (0/37) 0 (0/37) 0 (0/37) 0 (0/37) 0 (0/37) Mar 2015 12.5 182 (110–260) 0 (0/70) 0 (0/70) 0 (0/70) 0 (0/70) 0 (0/70) 0 (0/70) Apr 2015 13 203 (120–270) 0 (0/35) 0 (0/35) 0 (0/35) 0 (0/35) 0 (0/35) 0 (0/35) 11 (26/236) 9.7 (23/236) 0 (0/236) 3.4 (8/236) 4.2 (10/236) 0 (0/236) Total detection rate in BS Pohang PH Jul 2014 20.5 140 (50–220) 28.6 (4/14) 7.1 (1/14) 28.6 (4/14) 0 (0/14) 0 (0/14) 0 (0/14) Aug 2014 23.4 110 (80–150) 50 (5/10) 60 (6/10) 20 (2/10) 0 (0/10) 0 (0/10) 0 (0/10) Sep 2014 23.1 70 (30–110) 14.3 (2/14) 0 (0/14) 100 (14/14) 0 (0/14) 0 (0/14) 0 (0/14) Total detection rate in PH 28.9 (11/38) 18.4 (7/38) 52.6 (20/38) 0 (0/38) 0 (0/38) 0 (0/38) Total detection rate in 4 farms 11.6 (86/740) 6.4 (47/740) 3.4 (25/740) 3.2 (24/740) 3 (22/740) 0.5 (4/740) NT not tested surfaces of the specimens were examined macroscopic- were photographed and identified according to their ally and microscopically for the presence of epiphytic morphological characteristics (Gong et al., 2010; Kim organisms. The detection rate of the epiphytic organisms and Lee, 1975; Lee, 1994; Park, 2010; 2011; Saunders was measured by calculating the percentages of the kelp and Metaxas, 2009; Schwaninger, 1999; The Korean infested by epiphytic organisms, and their infestation Society of Systematic Zoology, 2014). area was calculated as the percentage of the thallus that had been colonized. The number of caprellid was Histology measured in a 2 × 2 cm kelp area infected with hy- The epiphytic organisms attached to the thallus were re- droid because their infestation area cannot be calcu- moved and immediately fixed in 10% neutral buffered lated. The epiphytic organisms that were obtained formalin. After fixation, standard histological procedures Kim et al. Fisheries and Aquatic Sciences (2017) 20:1 Page 3 of 7 Fig. 1 Location of the aquaculture farms (stars) were used for tissue dehydration and paraffin embed- The infestation areas for hydroid, bryozoan, and algae ding. The tissue sections were then stained with were 10 to 85%, 0.3 to 17%, and 20 to 30%, respectively hematoxylin and eosin. (Table 2). Two and eight caprellids were observed in theJune sampleand in theAugust sample of 2014, Results respectively. Detection of epiphytic organisms Two hundred fifty-three samples were examined in Table 1 shows the results of the detection of epiphytic the Wando B farm (Table 1). Hydroid, bryozoan, organisms. Of the 740 kelp samples, 208 had six kinds of polychaete, algae, and caprellid were detected in 13% epiphytic organisms attached, including hydroid, bryo- (33/253), 2% (5/253), 2% (5/253), 1.6% (4/253), and 0.4% zoan, polychaete, algae, caprellid, and oyster (Fig. 2). Of (1/253) kelp, respectively, and these organisms were ob- these, hydroid, bryozoan, polychaete, algae, and caprellid served from June to September in 2014. 57.1 to 100% were frequently observed and were detected in the kelp were found to be hydroid-positive, and 33.3, 35.7, and samples with rates of 11.6% (86/740), 6.4% (47/740), 3.4% 13.3 to 28.6% were bryozoan-positive, polychaete- (25/740), 3.2% (24/740), and 3% (22/740), respectively. positive, and algae-positive, respectively. The caprellid Two hundred thirteen samples were examined in the (7.1%) was observed on the hydroids in the July 2014 Wando A farm (Table 1). Hydroid, bryozoan, algae, sample. No epiphytic organisms were observed in the caprellid, and oyster were detected in 7.5% (16/213), kelp in May 2014 and from February to April 2015. The 5.6% (12/213), 5.6% (12/213), 2.8% (6/213), and 0.9% infestation areas for hydroid gradually increased from 10 (4/213) kelp, respectively, and these organisms were only to 55% as the water temperature increased, but these observed during the period from June to September in were lower than those of the Wando A farm (Table 2). 2014. Twenty to 100% were found to be hydroid-positive, The infestation areas for bryozoan, polychaete, and algae 50 to 71.4% were bryozoan-positive, and 14.3 to 100% were observed in 0.13% (0.06–0.5%) in the September were algae-positive. Twenty and 71.4% of the caprellid sample, 3% (1–5%) in the July sample, and 5% (3–6%) in were observed on hydroids, but not on kelp. The oyster the June sample, 2014, respectively. Two caprellids were (57.1%) was observed in the September 2014 sample. observed in the July 2014 sample. Epiphytic organisms were not observed among the kelp Two hundred thirty-six samples were examined in the during April to May in 2014 and January to April in 2015. Busan farm (Table 1). Hydroid, bryozoan, algae, and Kim et al. Fisheries and Aquatic Sciences (2017) 20:1 Page 4 of 7 Fig. 2 Photos of epiphytic organisms on cultured kelp. Hydroid (a), bryozoan (c), polychaete (e), algae (g), and caprellid (i) encrusting blades of kelp. Magnification of hydroid (b), bryozoan (d), polychaete (f), algae (h), and caprellid (j). Bar = 100 μm(b, h, and j) and 1000 μm(d, f) caprellid were detected in kelp with an incidence rate of were bryozoan-positive and algae-positive, respectively. 11% (26/236), 9.7% (23/236), 3.4% (8/236), and 4.2% No epiphytic organisms were observed among the kelp (10/236), respectively, and these organisms were ob- from February to April 2015. The infestation areas of the served from April to July 2014. One hundred percent hydroid were 14.4 to 37%, which are lower than those of of the samples were found to be hydroid-positive the two farms in Wando (Table 2). In contrast, the infest- from May to July 2014. Ten to 90% and 30 to 71.4% ation areas for bryozoan were of 0.04 to 37.9%, which were Kim et al. Fisheries and Aquatic Sciences (2017) 20:1 Page 5 of 7 Table 2 Infestation areas for epiphytic organisms in kelp Place Farm Date Water temperature Mean thalli Mean infection area of epiphytic organisms % (epiphytic area/total area) (°C) length (cm) a Hydroid Bryozoan Polychaete Algae Caprellid Oyster Wando WDA Apr 2014 11.5 340 (200–380) 0 0 0 0 0 0 May 2014 15.5 260 (260–270) 0 0 0 0 0 0 Jun 2014 17.4 NT 10 (5–20) 0 0 0 2 (1–5) 0 Jul 2014 21.7 190 (100–240) 85 (70–100) 4 (0.8–7.9) 0 30 (20–50) 0 0 Aug 2014 23 200 (100–240) 81 (60–95) 0.3 (0.2–0.6) 0 20 (10–35) 8 (3–17) 0 Sep 2014 22.1 120 (90–160) NT 17 (0.2–48.7) 0 0 0 2.35 (0.4–4.3) Jan 2015 9 41 (20–71) 0 0 0 0 0 0 Jan 2015 8.3 82 (39–122) 0 0 0 0 0 0 Apr 2015 11 236 (200–280) 0 0 0 0 0 0 WDB May 2014 15.4 220 (100–330) 0 0 0 0 0 0 Jun 2014 21 260 (180–320) 10 (5–25) 0 0 5 (3–6) 0 0 Jul 2014 21.5 160 (130–200) 41.8 (10–80) 0 3 (1–5) 0 2 (1–5) 0 Sep 2014 21.6 130 (60–230) 55 (20–90) 0.13 (0.06–0.5) 0 0 0 0 Feb 2015 9 57 (30–100) 0 0 0 0 0 0 Mar 2015 11 97 (50–180) 0 0 0 0 0 0 Apr 2015 12.5 127 (90–190) 0 0 0 0 0 0 Busan BS Apr 2014 11 170 (50–270) 0 0.04 (0.04) 0 0 0 0 May 2014 14.5 230 (130–280) 14.4 (5–30) 7.3 (1.8–14.1) 0 0 0 0 Jun 2014 21 220 (180–300) 34 (10–60) 2.8 (0.03–11.6) 0 34.1 (5–70) 0 0 Jul 2014 20.4 160 (120–180) 37 (20–60) 37.9 (1.1–86) 0 0 3 (1–5) 0 Feb 2015 11.5 76 (26–175) 0 0 0 0 0 0 Feb 2015 12 143 (80–219) 0 0 0 0 0 0 Mar 2015 12.5 182 (110–260) 0 0 0 0 0 0 Apr 2015 13 203 (120–270) 0 0 0 0 0 0 Pohang PH Jul 2014 20.5 140 (50–220) 3.3 (3–5) 0.5 (0.5) 9.5 (3–20) 0 0 0 Aug 2014 23.4 110 (80–150) 5.3 (1–10) 1.2 (0.2–3.6) 50 (40–60) 0 0 0 Sep 2014 23.1 70 (30–110) 3 (2–4) 0 90 (80–95) 0 0 0 NT not tested Mean number of caprellid the highest in the four farms. 34.1% of the algae were ob- bryozoan were attached to the cuticula of the thallus but served in June 2014, and three caprellids were observed in did not penetrate into the thallus (Fig. 3a–d). In con- July 2014. trast, some of the algae penetrated the epidermis and In the Pohang farm, hydroid, bryozoan, and polychaete attached to the cuticula of thallus (Fig. 3e, f). were detected in kelp with rates of 28.9% (11/38), 18.4% (7/38), and 52.6% (20/38), respectively, from July to Discussion September 2014 (Table 1). The infestation areas for hy- Korean farms have been cultivating kelp since the 1970s, droid and bryozoan were less than 5.5%, which were the but to date, no systematic research on their disease has lowest in the four farms (Table 2). In contrast, the infest- been conducted. In this study, we investigated the pres- ation areas for polychaete were 9.5 to 90%, which were ence of epiphytic organisms in four kelp farms in the the highest of the four farms. coastal area of Korea. Of the 740 kelp samples, 208 sam- ples had epiphytic organisms attached, including hy- Histopathology droid, bryozoan, polychaete, algae, caprellid, and oyster. The hydroid, bryozoan, and algae that were attached to The predominant epiphytic organisms were hydroid the thallus were examined (Fig. 3). The hydroid and (detection rate: 11.6%) followed by bryozoan (6.4%), Kim et al. Fisheries and Aquatic Sciences (2017) 20:1 Page 6 of 7 Fig. 3 Histological section of kelp infected with hydroid (a, b), bryozoan (c, d), and algae (e, f). The arrows indicate the epiphytic organisms. Bar =20 μm(b, e), 50 μm(c, d, and f), 100 μm(a) polychaete (3.4%), algae (3.2%), and caprellid (3%), as ob- the Gulf of Maine (USA) (Berman et al., 1992; Saunders served from May to September. No epiphytic organisms and Metaxas, 2008; Scheibling and Gagnon, 2009). The were observed among the kelp from January to April, ex- calcified Membranipora zooids present a firm mechanical cept for one sample from Busan. These results indicate barrier on epidermal tissue. This barrier can affect ex- that at least six kinds of epiphytic organisms were ob- change processes such as mineral nutrient uptake between served in kelp farms in Korea, and their infestation was kelp epidermis and surrounding seawater (Hurd et al., significantly higher in water with a higher temperature. 1994; 2000), or it can interfere with the photophysiology Moreover, encrusting hydroid and bryozoan were the of the host alga (Oswald et al., 1984; Cancino et al., 1987; most predominant form of infestation in kelp farms, Muñoz et al., 1991). In this study, even though the effect even though their infestation rates were different among of the bryozoan on kelp is unknown, Korean kelp farm is the kelp farms. Encrusting by hydroid has been reported suffered from infestation by bryozoan. to be abundant on farmed kelp in Korea at higher water It is unclear how the epiphytic organisms attach to the temperatures (Park and Hwang, 2012). The infestation thallus tissue. A histopathogical examination revealed rate from May to July was of about 97%, and it was that hydroid and bryozoan were attached on the cuticula below 26% from February to April. These results are of thallus while some algae attached to the cuticula of similar to the results of the present study. Encrusting by the thallus or penetrated the epidermis. These results in- bryozoan (Membranipora) has been reported to be abun- dicate that kelp tissue can be broken by some algae, but dant on kelp blades in Atlantic Nova Scotia (Canada) and not by hydroid and bryozoan. Kim et al. Fisheries and Aquatic Sciences (2017) 20:1 Page 7 of 7 The cultivation period for kelp in Korea had tradition- Department, National Fisheries Research and Development Institute, Busan 46083, South Korea. ally spanned from December to July, with a harvest of thalli occurring between June and July for use with ed- Received: 29 August 2016 Accepted: 10 January 2017 ible marine vegetable food. Recently, the harvest season has been shortened from March to May due to the pres- References ence of these epiphytic organisms. Moreover, kelp that is Berman J, Harris L, Lambert W, Buttrick M, Dufresne M. Recent invasions of severely infected by hydroid and bryozoan is used as theGulfofMaine:three contrastingecological histories. Conserv Biol. 1992;6:435–41. abalone feed during the summer, even though their ef- Cancino JM, Muñoz J, Muñoz M, Orellana MC. Effects of the bryozoan fect on abalone remains. In addition, there are many en- Membranipora tuberculata (Bosc.) on the photosynthesis and growth of vironmental factors that can affect the prevalence of the Gelidium rex Santelices et Abbott. J Exp Mar Biol Ecol. 1987;113:105–12. FAO (Food and Agriculture Organization of the United Nations). The state of epiphytes on kelps. Therefore, further studies are neces- world fisheries and aquaculture. Rome: Food and Agriculture Department. sary to elucidate which environmental factors are related Food and Agriculture Organization of the United Nations; 2014. to the epiphytic organisms’ infestation, to understand Gong YG, Hwang IG, Ha DS, Hwang MS, Hwang EK, Lee SY, Park EJ. Study on the Saccharina culture technique for abalone feed, Report of National Fisheries how to prevent the epiphytic organisms from infesting Research & Development Institute. 2010. p. 42–9. kelp farms and to assess their effect when used as aba- Hurd CL, Durante KM, Chia FS, Harrison PJ. Effect of bryozoan colonization on lone feed. inorganic nitrogen acquisition by the kelps Agarum fimbriatum and Macrocystis integrifolia. Mar Biol. 1994;121:167–73. Hurd CL, Durante KM, Harrison PJ. Influence of bryozoan colonization on the Conclusion physiology of the kelp Macrocystis integrifolia (Laminariales, Phaeophyta) In conclusion, we investigated the presence of epiphytic from nitrogen-rich and -poor sites in Barkley Sound, British Columbia, Canada. Phycologia. 2000;39:435–40. organisms in four kelp Saccharina japonica farms in the Kim HS, Lee KS. Faunal studies on the genus Caprella (Crustacea: Amphipoda, coastal area of Korea from 2014 to 2015. The infestation Caprellidae) in Korea. Kor J Zool. 1975;18:115–26. rate for hydroid, bryozoan, and polychaete was signifi- KOSIS (Korean statistical information service). 2015. Fishery production survey: statistics by type of fishery and species. Retrieved from http://kosis.kr/eng/ cantly higher in the Wando farm, Busan farm, and statisticsList/statisticsList_01List.jsp?vwcd=MT_ETITLE&parmTabId=M_01_ Pohang farm, respectively. Epiphytic organisms were 01#SubCont. On March 2016. generally observed during May to September. The histo- Lee CM. A systematic study on Korean Caprellids (Crustacea, Amphipoda) in the east sea. Yongin: Thesis for Master’s degree. Dan Kook University; 1994 pathogical examination revealed that hydroid and bryo- Muñoz J, Cancino JM, Molina MX. Effect of encrusting bryozoans on the zoan organisms were attached on the cuticula of the physiology of their algal substratum. J Mar Biol Assoc UK. 1991;71:877–82. thallus. These results indicate that hydroid and bryozoan Oswald RC, Telford N, Seed R, Happey-Wood CM. The effect of encrusting bryozoans on the photosynthetic activity of Fucus serratus L. Estuar Coast were the most predominant epiphytic organisms in Ko- Shelf Sci. 1984;19:697–702. rean kelp farms. Park JH. Invertebrate fauna of Korea. Athecates. National institute of biological resources ministry of environment; 2011 Acknowledgements Park JH. Invertebrate fauna of Korea. Thecates. National institute of biological This study was supported by the National Fisheries Research and resources ministry of environment; 2010 Development Institute (R2016069). Park CS, Hwang EK. Seasonality of epiphytic development of the hydroid Obelia geniculata on cultivated Saccharina japonica (Laminariaceae, Phaeophyta) in Funding Korea. J Appl Phycol. 2012;24:433–9. This study was supported by the National Fisheries Research and Saunders M, Metaxas A. High recruitment of the introduced bryozoan Development Institute (R2016069). Membranipora membranacea is associated with kelp bed defoliation in Nova Scotia, Canada. Mar Ecol Prog Ser. 2008;369:139–51. Availability of data and materials Saunders M, Metaxas A. Effects of temperature, size, and food on the growth of All datasets in this study are available from the corresponding author on Membranipora membranacea in laboratoy and field studies. Mar Biol. reasonable request. 2009;156:2267–76. Scheibling RE, Gagnon P. Temperature-mediated outbreak dynamics of the Authors’ contributions invasive bryozoan Membranipora membranacea in Nova Scotian kelp beds. JOK, WSK, HNJ, and SJC carried out the experiments. JOK and WSK Mar Ecol Prog Ser. 2009;390:1–13. participated to write the manuscript. MJO conceived of the study and Schwaninger H. Population structure of the widely dispersing marine bryozoan participated in its design. JSS and MAP analyzed the data. All authors read Membranipora membranacea (Cheilostomata): implications for population and approved the final manuscript. history, biogeography, and taxonomy. Mar Biol. 1999;135:411–23. The Korean Society of Systematic Zoology. Seoul: Zoological taxonomy. Competing interests Jiphyupsa; 2014 The authors declare that they have no competing interests. Consent for publication Not applicable. Ethics approval and consent to participate Not applicable. Author details Department of Aqualife Medicine, Jeonnam National University, Yeosu 59626, South Korea. Algae Research Institute, JeollaNamdo, Wando 59146, South Korea. Aquatic Life Disease Control Division, Fundamental Research http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Fisheries and Aquatic Sciences Springer Journals

A survey of epiphytic organisms in cultured kelp Saccharina japonica in Korea

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Springer Journals
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Copyright © 2017 by The Author(s)
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Life Sciences; Fish & Wildlife Biology & Management; Marine & Freshwater Sciences; Zoology; Animal Ecology
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10.1186/s41240-017-0046-z
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Abstract

A survey was conducted to investigate the presence of epiphytic organisms in four kelp Saccharina japonica farms in the coastal area of Korea from 2014 to 2015. Of 740 kelp samples that were taken, 208 exhibited six kinds of epiphytic organisms, including hydroid (detection rate: 11.6%), bryozoan (6.4%), polychaete (3.4%), algae (3.2%), caprellid (3%), and oyster (0.5%). The infestation rate for hydroid, bryozoan, and polychaete was significantly higher in the Wando farm, Busan farm, and Pohang farm, respectively. Epiphytic organisms were generally observed during May to September and not January to April, indicating that their infestation was significantly higher when the water had a higher temperature. The histopathogical examination revealed that hydroid and bryozoan organisms were attached on the cuticula of the thallus while some algae were attached on the cuticula of the thallus or had penetrated the epidermis. These results indicate that hydroid and bryozoan were the most predominant epiphytic organisms in Korean kelp farms, even though the infested thallus had not been broken. Keywords: Epiphytic organisms, Bryozoan, Hydroid, Kelp, Saccharina japonica Background epiphytic organisms (Gong et al., 2010; Park and Hwang, Within the last 30 years, seaweed cultivation has 2012). An infestation is characterized by the appearance attained large-scale production levels and has become a of numerous colonies on the thallus of the kelp, and major industry in China, Korea, and Japan. Korea had a therefore, the affected kelp appears unsightly and cannot harvest of 1,022,326 tons in 2012, which makes it the be sold. Although systematic research on fish disease fourth largest seaweed-producing country in the world has been conducted in Korea since the 1990s, seaweed (FAO, 2014). The economically important seaweed disease has not yet been systematically studied. There- species harvested in Korea are laver Porphyra spp., fore, little information is available on kelp disease. The wakame Undaria spp., kelp Laminaria spp., fusi- present study consists of a survey that was conducted to forme, Hizikia fusiformis, and green laver Monostroma investigate the presence of epiphytic organisms in spp. (KOSIS, 2015). Korean kelp farms. In addition, a histopathological Kelp Saccharina japonica cultivation was industrial- examination was conducted to understand the effect by ized in Korea in the 1970s, and from 2005, it has been epiphytic organisms on the thallus. extensively developed together with the abalone indus- try. During the 1970s to 1980s, kelp production reached Methods less than 12,000 tons, and production steadily increased Kelp samples and epiphytic organism examination since then with about 370,000 tons harvested in 2013 Kelp samples were obtained from four private farms in (KOSIS, 2015). Kelp production now accounts for about Wando (Southern Sea), Busan (Southern Sea), and 25% of all Korean seaweed cultivation (KOSIS, 2015). Pohang (Eastern Sea) during 2014 and 2015 (Table 1, However, the increase in production has also resulted in Fig. 1). Wando is the most popular area for kelp cultiva- kelp farms becoming severely infected by several tion, producing about 97% of the kelp crop of Korea. The kelps were randomly selected by a farmer, trans- * Correspondence: ohmj@Jnu.ac.kr ported on ice, and immediately subjected an examin- Department of Aqualife Medicine, Jeonnam National University, Yeosu ation of the epiphytic organisms. The total length (from 59626, South Korea Full list of author information is available at the end of the article apex to holdfast) of the thallus was measured, and the © The Author(s). 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Kim et al. Fisheries and Aquatic Sciences (2017) 20:1 Page 2 of 7 Table 1 Detection of epiphytic organisms in four kelp farms in Korea Place Farm Date Water temperature Mean thallus Detection rate of epiphytic organisms % (detection no./total no.) (°C) length (cm) Hydroid Bryozoan Polychaete Algae Caprellid Oyster Wando WDA Apr 2014 11.5 340 (200–380) 0 (0/10) 0 (0/10) 0 (0/10) 0 (0/10) 0 (0/10) 0 (0/10) May 2014 15.5 260 (260–270) 0 (0/2) 0 (0/2) 0 (0/2) 0 (0/2) 0 (0/2) 0 (0/2) Jun 2014 17.4 NT 20 (1/5) 0 (0/5) 0 (0/5) 0 (0/5) 20 (1/5) 0 (0/5) Jul 2014 21.7 190 (100–240) 100 (6/6) 50 (3/6) 0 (0/6) 100 (6/6) 0 (0/6) 0 (0/6) Aug 2014 23 200 (100–240) 71.4 (5/7) 57.1 (4/7) 0 (0/7) 71.4 (5/7) 71.4 (5/7) 0 (0/7) Sep 2014 22.1 120 (90–160) 57.1 (4/7) 71.4 (5/7) 0 (0/7) 14.3 (1/7) 0 (0/7) 57.1 (4/7) Jan 2015 9 41 (20–71) 0 (0/71) 0 (0/71) 0 (0/71) 0 (0/71) 0 (0/71) 0 (0/71) Jan 2015 8.3 82 (39–122) 0 (0/75) 0 (0/75) 0 (0/75) 0 (0/75) 0 (0/75) 0 (0/75) Apr 2015 11 236 (200–280) 0 (0/30) 0 (0/30) 0 (0/30) 0 (0/30) 0 (0/30) 0 (0/30) Total detection rate in WDA 7.5 (16/213) 5.6 (12/213) 0 (0/213) 5.6 (12/213) 2.8 (6/213) 0.9 (4/213) WDB May 2014 15.4 220 (100–330) 0 (0/14) 0 (0/14) 0 (0/14) 0(0/14) 0 (0/14) 0 (0/14) Jun 2014 21 260 (180–320) 57.1 (4/7) 0 (0/7) 0 (0/7) 28.6 (2/7) 0 (0/7) 0 (0/7) Jul 2014 21.5 160 (130–200) 100 (14/14) 0 (0/14) 35.7 (5/14) 0 (0/14) 7.1 (1/14) 0 (0/14) Sep 2014 21.6 130 (60–230) 100 (15/15) 33.3 (5/15) 0 (0/15) 13.3 (2/15) 0 (0/15) 0 (0/15) Feb 2015 9 57 (30–100) 0 (0/100) 0 (0/100) 0 (0/100) 0 (0/100) 0 (0/100) 0 (0/100) Mar 2015 11 97 (50–180) 0 (0/73) 0 (0/73) 0 (0/73) 0 (0/73) 0 (0/73) 0 (0/73) Apr 2015 12.5 127 (90–190) 0 (0/30) 0 (0/30) 0 (0/30) 0 (0/30) 0 (0/30) 0 (0/30) Total detection rate in WDB 13 (33/253) 2 (5/253) 2 (5/253) 1.6 (4/253) 0.4 (1/253) 0 (0/253) Busan BS Apr 2014 11 170 (50–270) 0 (0/10) 10 (1/10) 0 (0/10) 30 (3/10) 0 (0/10) 0 (0/10) May 2014 14.5 230 (130–280) 100 (9/9) 88.9 (8/9) 0 (0/9) 0 (0/9) 0 (0/9) 0 (0/9) Jun 2014 21 220 (180–300) 100 (7/7) 71.4 (5/7) 0 (0/7) 71.4 (5/7) 0 (0/7) 0 (0/7) Jul 2014 20.4 160 (120–180) 100 (10/10) 90 (9/10) 0 (0/10) 0 (0/10) 100 (10/10) 0 (0/10) Feb 2015 11.5 76 (26–175) 0 (0/58) 0 (0/58) 0 (0/58) 0 (0/58) 0 (0/58) 0 (0/58) Feb 2015 12 143 (80–219) 0 (0/37) 0 (0/37) 0 (0/37) 0 (0/37) 0 (0/37) 0 (0/37) Mar 2015 12.5 182 (110–260) 0 (0/70) 0 (0/70) 0 (0/70) 0 (0/70) 0 (0/70) 0 (0/70) Apr 2015 13 203 (120–270) 0 (0/35) 0 (0/35) 0 (0/35) 0 (0/35) 0 (0/35) 0 (0/35) 11 (26/236) 9.7 (23/236) 0 (0/236) 3.4 (8/236) 4.2 (10/236) 0 (0/236) Total detection rate in BS Pohang PH Jul 2014 20.5 140 (50–220) 28.6 (4/14) 7.1 (1/14) 28.6 (4/14) 0 (0/14) 0 (0/14) 0 (0/14) Aug 2014 23.4 110 (80–150) 50 (5/10) 60 (6/10) 20 (2/10) 0 (0/10) 0 (0/10) 0 (0/10) Sep 2014 23.1 70 (30–110) 14.3 (2/14) 0 (0/14) 100 (14/14) 0 (0/14) 0 (0/14) 0 (0/14) Total detection rate in PH 28.9 (11/38) 18.4 (7/38) 52.6 (20/38) 0 (0/38) 0 (0/38) 0 (0/38) Total detection rate in 4 farms 11.6 (86/740) 6.4 (47/740) 3.4 (25/740) 3.2 (24/740) 3 (22/740) 0.5 (4/740) NT not tested surfaces of the specimens were examined macroscopic- were photographed and identified according to their ally and microscopically for the presence of epiphytic morphological characteristics (Gong et al., 2010; Kim organisms. The detection rate of the epiphytic organisms and Lee, 1975; Lee, 1994; Park, 2010; 2011; Saunders was measured by calculating the percentages of the kelp and Metaxas, 2009; Schwaninger, 1999; The Korean infested by epiphytic organisms, and their infestation Society of Systematic Zoology, 2014). area was calculated as the percentage of the thallus that had been colonized. The number of caprellid was Histology measured in a 2 × 2 cm kelp area infected with hy- The epiphytic organisms attached to the thallus were re- droid because their infestation area cannot be calcu- moved and immediately fixed in 10% neutral buffered lated. The epiphytic organisms that were obtained formalin. After fixation, standard histological procedures Kim et al. Fisheries and Aquatic Sciences (2017) 20:1 Page 3 of 7 Fig. 1 Location of the aquaculture farms (stars) were used for tissue dehydration and paraffin embed- The infestation areas for hydroid, bryozoan, and algae ding. The tissue sections were then stained with were 10 to 85%, 0.3 to 17%, and 20 to 30%, respectively hematoxylin and eosin. (Table 2). Two and eight caprellids were observed in theJune sampleand in theAugust sample of 2014, Results respectively. Detection of epiphytic organisms Two hundred fifty-three samples were examined in Table 1 shows the results of the detection of epiphytic the Wando B farm (Table 1). Hydroid, bryozoan, organisms. Of the 740 kelp samples, 208 had six kinds of polychaete, algae, and caprellid were detected in 13% epiphytic organisms attached, including hydroid, bryo- (33/253), 2% (5/253), 2% (5/253), 1.6% (4/253), and 0.4% zoan, polychaete, algae, caprellid, and oyster (Fig. 2). Of (1/253) kelp, respectively, and these organisms were ob- these, hydroid, bryozoan, polychaete, algae, and caprellid served from June to September in 2014. 57.1 to 100% were frequently observed and were detected in the kelp were found to be hydroid-positive, and 33.3, 35.7, and samples with rates of 11.6% (86/740), 6.4% (47/740), 3.4% 13.3 to 28.6% were bryozoan-positive, polychaete- (25/740), 3.2% (24/740), and 3% (22/740), respectively. positive, and algae-positive, respectively. The caprellid Two hundred thirteen samples were examined in the (7.1%) was observed on the hydroids in the July 2014 Wando A farm (Table 1). Hydroid, bryozoan, algae, sample. No epiphytic organisms were observed in the caprellid, and oyster were detected in 7.5% (16/213), kelp in May 2014 and from February to April 2015. The 5.6% (12/213), 5.6% (12/213), 2.8% (6/213), and 0.9% infestation areas for hydroid gradually increased from 10 (4/213) kelp, respectively, and these organisms were only to 55% as the water temperature increased, but these observed during the period from June to September in were lower than those of the Wando A farm (Table 2). 2014. Twenty to 100% were found to be hydroid-positive, The infestation areas for bryozoan, polychaete, and algae 50 to 71.4% were bryozoan-positive, and 14.3 to 100% were observed in 0.13% (0.06–0.5%) in the September were algae-positive. Twenty and 71.4% of the caprellid sample, 3% (1–5%) in the July sample, and 5% (3–6%) in were observed on hydroids, but not on kelp. The oyster the June sample, 2014, respectively. Two caprellids were (57.1%) was observed in the September 2014 sample. observed in the July 2014 sample. Epiphytic organisms were not observed among the kelp Two hundred thirty-six samples were examined in the during April to May in 2014 and January to April in 2015. Busan farm (Table 1). Hydroid, bryozoan, algae, and Kim et al. Fisheries and Aquatic Sciences (2017) 20:1 Page 4 of 7 Fig. 2 Photos of epiphytic organisms on cultured kelp. Hydroid (a), bryozoan (c), polychaete (e), algae (g), and caprellid (i) encrusting blades of kelp. Magnification of hydroid (b), bryozoan (d), polychaete (f), algae (h), and caprellid (j). Bar = 100 μm(b, h, and j) and 1000 μm(d, f) caprellid were detected in kelp with an incidence rate of were bryozoan-positive and algae-positive, respectively. 11% (26/236), 9.7% (23/236), 3.4% (8/236), and 4.2% No epiphytic organisms were observed among the kelp (10/236), respectively, and these organisms were ob- from February to April 2015. The infestation areas of the served from April to July 2014. One hundred percent hydroid were 14.4 to 37%, which are lower than those of of the samples were found to be hydroid-positive the two farms in Wando (Table 2). In contrast, the infest- from May to July 2014. Ten to 90% and 30 to 71.4% ation areas for bryozoan were of 0.04 to 37.9%, which were Kim et al. Fisheries and Aquatic Sciences (2017) 20:1 Page 5 of 7 Table 2 Infestation areas for epiphytic organisms in kelp Place Farm Date Water temperature Mean thalli Mean infection area of epiphytic organisms % (epiphytic area/total area) (°C) length (cm) a Hydroid Bryozoan Polychaete Algae Caprellid Oyster Wando WDA Apr 2014 11.5 340 (200–380) 0 0 0 0 0 0 May 2014 15.5 260 (260–270) 0 0 0 0 0 0 Jun 2014 17.4 NT 10 (5–20) 0 0 0 2 (1–5) 0 Jul 2014 21.7 190 (100–240) 85 (70–100) 4 (0.8–7.9) 0 30 (20–50) 0 0 Aug 2014 23 200 (100–240) 81 (60–95) 0.3 (0.2–0.6) 0 20 (10–35) 8 (3–17) 0 Sep 2014 22.1 120 (90–160) NT 17 (0.2–48.7) 0 0 0 2.35 (0.4–4.3) Jan 2015 9 41 (20–71) 0 0 0 0 0 0 Jan 2015 8.3 82 (39–122) 0 0 0 0 0 0 Apr 2015 11 236 (200–280) 0 0 0 0 0 0 WDB May 2014 15.4 220 (100–330) 0 0 0 0 0 0 Jun 2014 21 260 (180–320) 10 (5–25) 0 0 5 (3–6) 0 0 Jul 2014 21.5 160 (130–200) 41.8 (10–80) 0 3 (1–5) 0 2 (1–5) 0 Sep 2014 21.6 130 (60–230) 55 (20–90) 0.13 (0.06–0.5) 0 0 0 0 Feb 2015 9 57 (30–100) 0 0 0 0 0 0 Mar 2015 11 97 (50–180) 0 0 0 0 0 0 Apr 2015 12.5 127 (90–190) 0 0 0 0 0 0 Busan BS Apr 2014 11 170 (50–270) 0 0.04 (0.04) 0 0 0 0 May 2014 14.5 230 (130–280) 14.4 (5–30) 7.3 (1.8–14.1) 0 0 0 0 Jun 2014 21 220 (180–300) 34 (10–60) 2.8 (0.03–11.6) 0 34.1 (5–70) 0 0 Jul 2014 20.4 160 (120–180) 37 (20–60) 37.9 (1.1–86) 0 0 3 (1–5) 0 Feb 2015 11.5 76 (26–175) 0 0 0 0 0 0 Feb 2015 12 143 (80–219) 0 0 0 0 0 0 Mar 2015 12.5 182 (110–260) 0 0 0 0 0 0 Apr 2015 13 203 (120–270) 0 0 0 0 0 0 Pohang PH Jul 2014 20.5 140 (50–220) 3.3 (3–5) 0.5 (0.5) 9.5 (3–20) 0 0 0 Aug 2014 23.4 110 (80–150) 5.3 (1–10) 1.2 (0.2–3.6) 50 (40–60) 0 0 0 Sep 2014 23.1 70 (30–110) 3 (2–4) 0 90 (80–95) 0 0 0 NT not tested Mean number of caprellid the highest in the four farms. 34.1% of the algae were ob- bryozoan were attached to the cuticula of the thallus but served in June 2014, and three caprellids were observed in did not penetrate into the thallus (Fig. 3a–d). In con- July 2014. trast, some of the algae penetrated the epidermis and In the Pohang farm, hydroid, bryozoan, and polychaete attached to the cuticula of thallus (Fig. 3e, f). were detected in kelp with rates of 28.9% (11/38), 18.4% (7/38), and 52.6% (20/38), respectively, from July to Discussion September 2014 (Table 1). The infestation areas for hy- Korean farms have been cultivating kelp since the 1970s, droid and bryozoan were less than 5.5%, which were the but to date, no systematic research on their disease has lowest in the four farms (Table 2). In contrast, the infest- been conducted. In this study, we investigated the pres- ation areas for polychaete were 9.5 to 90%, which were ence of epiphytic organisms in four kelp farms in the the highest of the four farms. coastal area of Korea. Of the 740 kelp samples, 208 sam- ples had epiphytic organisms attached, including hy- Histopathology droid, bryozoan, polychaete, algae, caprellid, and oyster. The hydroid, bryozoan, and algae that were attached to The predominant epiphytic organisms were hydroid the thallus were examined (Fig. 3). The hydroid and (detection rate: 11.6%) followed by bryozoan (6.4%), Kim et al. Fisheries and Aquatic Sciences (2017) 20:1 Page 6 of 7 Fig. 3 Histological section of kelp infected with hydroid (a, b), bryozoan (c, d), and algae (e, f). The arrows indicate the epiphytic organisms. Bar =20 μm(b, e), 50 μm(c, d, and f), 100 μm(a) polychaete (3.4%), algae (3.2%), and caprellid (3%), as ob- the Gulf of Maine (USA) (Berman et al., 1992; Saunders served from May to September. No epiphytic organisms and Metaxas, 2008; Scheibling and Gagnon, 2009). The were observed among the kelp from January to April, ex- calcified Membranipora zooids present a firm mechanical cept for one sample from Busan. These results indicate barrier on epidermal tissue. This barrier can affect ex- that at least six kinds of epiphytic organisms were ob- change processes such as mineral nutrient uptake between served in kelp farms in Korea, and their infestation was kelp epidermis and surrounding seawater (Hurd et al., significantly higher in water with a higher temperature. 1994; 2000), or it can interfere with the photophysiology Moreover, encrusting hydroid and bryozoan were the of the host alga (Oswald et al., 1984; Cancino et al., 1987; most predominant form of infestation in kelp farms, Muñoz et al., 1991). In this study, even though the effect even though their infestation rates were different among of the bryozoan on kelp is unknown, Korean kelp farm is the kelp farms. Encrusting by hydroid has been reported suffered from infestation by bryozoan. to be abundant on farmed kelp in Korea at higher water It is unclear how the epiphytic organisms attach to the temperatures (Park and Hwang, 2012). The infestation thallus tissue. A histopathogical examination revealed rate from May to July was of about 97%, and it was that hydroid and bryozoan were attached on the cuticula below 26% from February to April. These results are of thallus while some algae attached to the cuticula of similar to the results of the present study. Encrusting by the thallus or penetrated the epidermis. These results in- bryozoan (Membranipora) has been reported to be abun- dicate that kelp tissue can be broken by some algae, but dant on kelp blades in Atlantic Nova Scotia (Canada) and not by hydroid and bryozoan. Kim et al. Fisheries and Aquatic Sciences (2017) 20:1 Page 7 of 7 The cultivation period for kelp in Korea had tradition- Department, National Fisheries Research and Development Institute, Busan 46083, South Korea. ally spanned from December to July, with a harvest of thalli occurring between June and July for use with ed- Received: 29 August 2016 Accepted: 10 January 2017 ible marine vegetable food. Recently, the harvest season has been shortened from March to May due to the pres- References ence of these epiphytic organisms. Moreover, kelp that is Berman J, Harris L, Lambert W, Buttrick M, Dufresne M. Recent invasions of severely infected by hydroid and bryozoan is used as theGulfofMaine:three contrastingecological histories. Conserv Biol. 1992;6:435–41. abalone feed during the summer, even though their ef- Cancino JM, Muñoz J, Muñoz M, Orellana MC. Effects of the bryozoan fect on abalone remains. In addition, there are many en- Membranipora tuberculata (Bosc.) on the photosynthesis and growth of vironmental factors that can affect the prevalence of the Gelidium rex Santelices et Abbott. J Exp Mar Biol Ecol. 1987;113:105–12. FAO (Food and Agriculture Organization of the United Nations). The state of epiphytes on kelps. Therefore, further studies are neces- world fisheries and aquaculture. 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National institute of biological This study was supported by the National Fisheries Research and resources ministry of environment; 2010 Development Institute (R2016069). Park CS, Hwang EK. Seasonality of epiphytic development of the hydroid Obelia geniculata on cultivated Saccharina japonica (Laminariaceae, Phaeophyta) in Funding Korea. J Appl Phycol. 2012;24:433–9. This study was supported by the National Fisheries Research and Saunders M, Metaxas A. High recruitment of the introduced bryozoan Development Institute (R2016069). Membranipora membranacea is associated with kelp bed defoliation in Nova Scotia, Canada. Mar Ecol Prog Ser. 2008;369:139–51. Availability of data and materials Saunders M, Metaxas A. Effects of temperature, size, and food on the growth of All datasets in this study are available from the corresponding author on Membranipora membranacea in laboratoy and field studies. Mar Biol. reasonable request. 2009;156:2267–76. Scheibling RE, Gagnon P. Temperature-mediated outbreak dynamics of the Authors’ contributions invasive bryozoan Membranipora membranacea in Nova Scotian kelp beds. JOK, WSK, HNJ, and SJC carried out the experiments. JOK and WSK Mar Ecol Prog Ser. 2009;390:1–13. participated to write the manuscript. MJO conceived of the study and Schwaninger H. Population structure of the widely dispersing marine bryozoan participated in its design. JSS and MAP analyzed the data. All authors read Membranipora membranacea (Cheilostomata): implications for population and approved the final manuscript. history, biogeography, and taxonomy. Mar Biol. 1999;135:411–23. The Korean Society of Systematic Zoology. Seoul: Zoological taxonomy. Competing interests Jiphyupsa; 2014 The authors declare that they have no competing interests. Consent for publication Not applicable. Ethics approval and consent to participate Not applicable. Author details Department of Aqualife Medicine, Jeonnam National University, Yeosu 59626, South Korea. Algae Research Institute, JeollaNamdo, Wando 59146, South Korea. Aquatic Life Disease Control Division, Fundamental Research

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Fisheries and Aquatic SciencesSpringer Journals

Published: Jan 31, 2017

References