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Changes in drag and drag coefficient on small Sargassum horneri (Turner) C. Agardh individuals
Aquatic Botany 144 (2018) 61–64
Contents lists available at ScienceDirect
Aquatic Botany journal homepage: www.elsevier.com/locate/aquabot
Short communication
Changes in drag and drag coefficient on small Sargassum horneri (Turner) C. Agardh individuals
MARK
⁎
Min Xua,b, , Shuji Sasab, Takayoshi Otakib, Fu-xiang Huc, Tadashi Tokaic, Teruhisa Komatsub a
Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China Atmosphere and Ocean Research Institute, The University of Tokyo, Chiba 277-0882, Japan c Graduate School of Marine Science and Technology, Tokyo University of Marine Science and Technology, Tokyo 108-8477, Japan b
A R T I C L E I N F O
A B S T R A C T
Keyword: Sargassum horneri Drag Drag coefficient Cd Reynolds number Re
Sargassum horneri (Turner) C. Agardh is used to restore, create, and recreate seaweed beds along the coastlines of East Asia. Drag produced by waves is a bulk force that can detach thalli from substrata during the early growth stages from substrata. In this study we measured drag forces on small S. horneri thalli (10–40 cm long). Unidirectional steady flow was controlled from 20 to 130 cm s−1 in increments of 10 cm s−1 in a recirculating water tank. Drag force on individuals ranged from ∼0.3 N to ∼3 N. Drag (Fdrag) and water velocity (U) produced the following exponential empirical approximations: Fdrag = 0.0168 × U0.8925. The drag coefficient (Cd) was plotted as a function of Reynolds number (Re) as follows: Cd = 4744.7 × Re−0.93. Cd converged to 0.037 at Re of 105−6 suggesting that small thalli exhibit optimal morphological adaptations to withstand high current speeds.
1. Introduction
(Kjellman) in a large (100 cm height) water tunnel that generates undulatory flow. Assuming that large waves have a long wavelength that is far greater than the bottom depth, they measured fluid forces consisting of additional mass force proportional to acceleration and drag force proportional to speed. Under the long wave situation, drag was the prevalent force and additional forces could be neglected. When devising strategies for developing seaweed beds, it is important to study the balance between drag and attachment strength during early life stages. Drag (Fdrag) on thalli of any length is estimated by the drag coefficient (Cd) at a given water speed. Xu and Komatsu (2017) used the boat method (Utter and Denny, 1996) to evaluate Cd plotted as a function of Reynolds number (Re) of S. horneri thalli 40–270 cm long. A seaweed specimen was attached to one end of a nonstretching string, and its other end was attached to a spring scale running on low-friction wheels along a vertical steel bar attached to the side of the boat. The thallus was towed behind the boat at a constant speed while forces were read from the spring scale and recorded in a notebook. However, it is difficult to measure drag on small S. horneri thalli using the boat method, so in this study a recirculating water tunnel that can generate unidirectional steady flow was used to measure drag forces on S. horneri thalli ranging from 10 to 40 cm long. We investigated Fdrag and Cd of small S. horneri thalli at different water velocities ranging from 20 to 130 cm s−1 in increments of 10 cm s−1.
Sargassum horneri (Turner) C. Agardh is a subtidal seaweed species that belongs to the order Fucales (Class: Phaeophyceae; Order: Fucales; Family: Sargassaceae; Genus: Sargassum) (Yoshida et al., 1997). Sargassum horneri forms an underwater forest with a canopy height of 300–700 cm above the hard substrata and grows from near shore to a bottom depth of several meters (Komatsu et al., 2015). It is widely distributed along the coasts of northeast Asia from China to Russia through the Korean Peninsula and Japan, with the exception of Taiwan and the Ryukyu Archipelago (Komatsu et al., 2014). Sargassum horneri has spread aggressively throughout southern California, USA, and Baja California, Mexico since it was discovered in the eastern Pacific in 2003 and it poses a major threat to the sustainability of native marine ecosystems in this region (Cruz-Trejo et al., 2015; Marks et al., 2015). Scientists have been trying to restore, create, and recreate S. horneri beds with varying success in East Asia (Yamauchi, 1983; Hamaguchi et al., 1988; Sun et al., 2008; Zhang et al., 2013). Thus, it is important to understand the ecological processes such as survival, transport and dispersal of this species. Drag is a bulk hydrodynamic force that can dislodge seaweeds from substrata (Denny, 1995; Gaylord, 2000; Thomsen et al., 2004; Stewart, 2006). Sugawara et al. (1998) measured the fluid force on the brown seaweeds Eisenia bicyclis (Kjellman Setchell) and Ecklonia cava
⁎
Corresponding author at: Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China. E-mail address: [email protected] (M. Xu).
https://doi.org/10.1016/j.aquabot.2017.11.002 Received 2 March 2017; Received in revised form 26 October 2017; Accepted 8 November 2017 Available online 11 November 2017 0304-3770/ © 2017 Elsevier B.V. All rights reserved.
Aquatic Botany 144 (2018) 61–64
M. Xu et al.
2. Materials and methods Sargassum horneri thalli used for this experiment were collected from Nabeta Cove near Shimoda (34°39′58″N, 138°56′31″E) in the southernmost part of Izu Peninsula, Japan, on the morning of 29 January 2015 (Xu et al., 2016). Small sized (10–40 cm long) thalli (n = 21) including 3 individuals without vesicles were cropped with their holdfasts. Cropped individuals were immediately kept in an ice box and transported from Shimoda to Tokyo University of Marine Science and Technology in Shinagawa, Tokyo on the day of collection. A recirculating flow tank (150 cm long × 50 cm wide × 80 cm deep) that could generate unidirectional steady flow ranging from 20 to 130 cm s−1 was used for the experiment. The tank was filled with freshwater and was used to measure drag forces exerted on individual seaweed thalli at different speeds of water flow. Water speed was measured using a small electromagnetic current meter (VM-801HA, KENEK, Japan). Water temperatures measured on 29 and 30 January 2015 using a water temperature device (WTM-R, PIVOT, Japan) were 9.1 and 8.2 °C, respectively. The method used to measure drag on seaweeds was based on Utter and Denny (1996), who studied Macrocystis pyrifera (Linnaeus) C. Agardh. One end of a buckle was attached to the holdfast of an individual thallus. The other end of a buckle was attached to a strain gauge that measured force through a pulley located at the bottom of a cylindrical tube at a depth of 10 cm from the water surface in the working section of the tank and another pulley situated at the water surface. A wooden frame was placed on the experimental section of the tank to support the cylindrical tube and connect the end of a buckle to the strain gauge. Tension on the thread produced by drag on an individual thallus by water flow changed the resistance on the strain gauge. Drag force on only the thread projecting from the cylindrical tube in the experimental section of the tank filled with freshwater was measured under the tested speeds of water flow and subtracted from drag forces of individual thalli as an offset value. After the experiment, thallus length from the bottom of the holdfast to the top of the longest lateral branch (with an accuracy of ± 1 cm) was measured using a 30 cm ruler. A balance (CR-5000WP, Custom, Japan) was used to determine wet weights of thalli with the holdfast (with an accuracy of ± 2 g) after removing surface water with a paper towel. Surface area of one side of an individual was measured using ImageJ software (ver. 6.4; National Institutes of Health, Bethesda, MD, USA). We prepared five pictures of each individual that were corrected horizontally using image processing software (Photoshop CS, Adobe, USA). The area of a given thallus was based on the mean of five images of that thallus. Drag coefficient Cd was calculated using the following Eq. (1):
Fig. 1. Plots of drag force (N) against water flow speed (cm s−1) of thalli for thallus length of 10–40 cm. Upper regression line: F = 0.0151 × U1.0976; bottom regression line: F = 0.0024 × U1.0344.
for each thallus to calculate its Re at different values of U using Eq. (2). Pearson correlation was applied to evaluate relationships between Fdrag and U and between Cd and Re. 3. Results and discussion 3.1. Drag and drag coefficient Fig. 1 shows drag on thalli. The plot of U versus Fdrag produced the following exponential approximation:
Fdrag = 0.0168 × U 0.8925
for thalli with lengths of 10–40 cm (n = 21; R = 0.42, p < 0.05; 20 cm s−1 < U < 130 cm s−1). Fdrag in Eq. (3) shows that drag force was roughly proportional to the flow rate to the 0.9 power. The upper regression plot of U and Fdrag for a thallus with length of 35.6 cm resulted in
Fdrag = 0.0151 × U1.0976 2
ρ×
×A
U× L ν
−1
−1
(5)
< U < 130 cm s . with R = 0.865, p < 0.001; 20 cm s Cd of individuals was calculated as a function of Re (n = 21; R2 = 0.72, p < 0.001, SE = 0.053) as follows (Fig. 2):
(1)
where Fdrag, ρ, U, and A were drag exerted on a seaweed in a steady flow, freshwater mass density (at 8 °C on 30 January 2015 and at 9 °C on 29 January 2015, values were 0.99985 and 0.99978 g cm−3, respectively), fluid speed relative to a seaweed, and one side’s surface area of the seaweed, respectively. We measured Fdrag, ρ, U. Using these values, Cd of an individual at various speeds of water flow was estimated. To compare drag coefficients among different algae, Cd was plotted as a function of Re in the form of a Log–Log linear regression. Re was calculated as follows:
Re =
−1
Fdrag = 0.0024 × U1.0344
2 × Fdrag U2
(4) −1
< U < 130 cm s . with R = 0.984, p < 0.001; 20 cm s The lower regression plot of U and Fdrag for a thallus with length of 12.7 cm resulted in
2
Cd =
(3) 2
Cd = 4744.7 × Re−0.93
(6)
As speed of water flow increased, Cd converged to 0.037 at high Re values between 105 and 106. 3.2. Effect of drag on small versus large S. horneri and its ecological implications When subjected to a given water current speed, macrophytes experience a drag force 25 times higher than that of terrestrial plants exposed to a similar wind speed (Denny and Gaylord, 2002). Sargassum horneri inhabit a wave exposed subtidal environment, and they face possible detachment or breakage from the substrate to which they are attached. Holdfasts of individuals are torn from the substrate by drag produced by waves that exceed the attachment strength of the holdfast (Yoshida, 1963), and maximum dislodgement force represents the maximum drag force that fronds can resist.
(2)
where L and ν were the characteristic length of a thallus and the kinematic viscosity of a fluid (freshwater: 0.0139 cm2 s−1 at 8 °C and 0.0134 cm2 s−1 at 9 °C), respectively. We used the square root of one side’s surface area of each thallus as the characteristic length (L = A ) 62
Aquatic Botany 144 (2018) 61–64
M. Xu et al.
Fig. 2. Plots of drag coefficient (Cd) as a function of Reynolds number (Re) for high drag seaweed species (Ecklonia radiata [C. Agardh] J. Agardh (de Bettignies et al., 2013), Mastocarpus papillatus [C. Agardh] (Carrington, 1990) and Saccarina japonica (Kawamata, 2001)) and low drag seaweed species (Sargassum horneri with thalli 0–40 cm long with and without vesicles [upper panel] and 40–270 cm long [bottom panel] (Xu and Komatsu, 2017). Data for a rigid smooth flat plate oriented parallel to the flow (Schlichting, 1968) also are shown.
cm). At a water speed of 85 cm s−1, we obtained Cd = 0.11314 following Eq. (6) and Fdrag =0.88 N following Eq. (1). These results show that the two methods estimated a similar drag force output. We also used method (2) to conduct back-calculations to calculate breaking speed created by waves to compare with attachment strength of 10–40 cm long S. horneri thalli collected in December 2014 and 2015 (Xu et al., 2016). Mean breaking speed classified by for thalli in the range of 10–40 cm were as follows: 10–20 cm long thalli, 403.3 ± 263.1 cm s−1, N = 23; 20–30 cm long thalli, 467.2 ± 243.0 cm s−1, N = 17; 30–40 cm long thalli, 904.0 ± 817.0 cm s−1, N = 10). Thomsen and Wernberg (2005) argued that thallus size was an important factor for scaling macroalgal break forces within and between species, and thus it might also be related to breaking velocity increasing with thallus size. He reported mean breaking speeds to be 40–120 cm s−1 for Ulva curvata, Gracilaria verrucosa, Gracilaria foliifera, Agardhiella subulata, Fucus vesiculosus, and Codium fragile. Sargassum species seem to have higher breaking speeds, probably due to their large biomass and habitation of wave-exposed areas. A given seaweed species regardless of its size uses the same strategy to go with the flow as waves pass in order to decrease Cd and eventually drag force by the water flow (Fig. 2). The presence of vesicles has little impact on the plot of Cd versus Re, and the plots for thalli with and
Xu and Komatsu (2017) used the same method implemented in this study to measure drag on S. horneri thalli 40–270 cm long. Drag forces on thalli 40–50 cm long were usually < 5 N. Drag forces on thalli 50–100 cm long were < 15 N, whereas most in the longest thallus group (100–270 cm) were < 20 N at 400 cm s−1 flow speeds. In the present study, drag forces on thalli < 20 cm long and those between 20 and 40 cm were less than ∼1.5 N and 1.5 to ∼3 N, respectively. Cd of algae generally decreases gradually as the Re increases through the range 104 to 106 (Vogel, 1981). Past studies of Cd of several seaweeds at high Re values under high flow speeds ranged from 0.01 to 0.05 at Re of 106 (Koehl, 2000; Kawamata, 2001; Thomsen, 2004). For S. horneri with thallus length varying from 0 to 50 cm to 200–300 cm, the Cd limit value decreased 10 times from 0.02 to 0.002 (Xu and Komatsu, 2017). The current study provides two ways to calculate drag on S. horneri thalli ranging in size from 10 to 40 cm. Using method 1, we estimated a drag force range at a certain water speed for S. horneri thalli ranging from 10 to 40 cm long, as shown in Fig. 1. For example, at water speed of 85 cm s−1, drag force on a 25-cm long S. horneri thallus ranged from 0.24 to 1.98 N following Eqs. (4) and (5). Drag force was 0.88 N following Eq. (3). Using method 2, thallus length of 25 cm was equivalent to 217 cm2 surface area (Unpublished data: One side surface area = 3.5168 × thallus length1.2805, R2 = 0.53, thallus length < 40
63
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without vesicles overlap (Fig. 2). The range of Cd values is similar for S. horneri thalli < 40 cm long and the intertidal small alga Mastocarpus papillatus (C. Agardh) (Carrington, 1990). The range of Cd values for larger S. horneri thalli (40–270 cm) is similar to those of a rigid smooth flat plate oriented parallel to the flow (Schlichting, 1968) and to Ecklonia radiata (C. Agardh) J. Agardh (de Bettignies et al., 2013) and Saccarina japonica of the high and low drag groups (Kawamata, 2001). The Cd of S. horneri obtained in the present study can be used to estimate drag force in a storm and to conduct back-calculations to estimate breaking velocities. Cd converged to 0.037 at Re of 105−6, suggesting that small thalli exhibit optimal morphological adaptations to withstand high current speeds. Studying the effects of drag and drag coefficient on the early life stages of S. horneri is important to understanding its survival, transport, and dispersal. In future studies we will need to incorporate other hydrodynamic forces, such as acceleration and break force, into the model in order to obtain a more comprehensive understanding of the biomechanics of Sargassum species.
Japanese with English abstract). Kawamata, S., 2001. Adaptive mechanical tolerance and dislodgement velocity of the kelp Laminaria japonica in wave-induced water motion. Mar. Ecol. Progr. 211 (4), 89–104. Koehl, M.A.R., 2000. Mechanical design and hydrodynamics of blade like algae: Chondracanthus exasperates. In: Spatz, H.C., Speck, T. (Eds.), Third International Plant Biomechanics. Thieme Verlag, Stuttgart, pp. 295–308. Komatsu, T., Mizuno, S., Natheer, A., Kantachumpoo, A., Tanaka, K., Morimoto, A., Hsiao S.-t. Rothausler Eva, A., Shishidou, H., Aoki, M., Ajisaka, T., 2014. Unusual distribution of floating seaweeds in the East China Sea in the early spring of 2012. J. Appl. Phycol. 26 (2), 1169–1179. Komatsu, T., Ohtaki, T., Sakamoto, S., Sawayama, S., Hamana, Y., Shibata, M., Shibata, K., Sasa, S., 2011. Impact of the 2011 tsunami on seagrass and seaweed beds in otsuchi bay, sanriku coast, Japan. In: Ceccaldi, H.J., Hénocque, Y., Koike, Y., Komatsu, T., Stora, G., Tusseau-Vuillemin, M.-H. (Eds.), Marine Productivity: Perturbations and Resilience of Socio-Ecosystems. Springer International Publishing, Switzerland, Cham, pp. pp. 43–53. Marks, L.M., Salinas-Ruiz, P., Reed, D.C., Holbrook, S.J., Culver, C.S., Engle, J.M., et al., 2015. Range expansion of a non-native, invasive macroalga Sargassum horneri (Turner) C. Agardh, 1820 in the eastern Pacific. BioInvasions Rec. 4, 243–248. Schlichting, H., 1968. Boundary-Layer Theory, 6th edn. McGraw-Hill, New York. Stewart, H.-l., 2006. Morphological variation and phenotypic plasticity of buoyancy in the Macroalga Turbinaria ornate across a barrier reef. Mar. Biol. 149 (4), 721–730. Sugawara, A., Seto, M., Komatsu, T., 1998. Study on the zonation of macro algae: vertical distribution and current environments in Eisenia bicyclis Setchell and Ecklonia cava Kjellman. Proceedings of Civil Engineering in the Ocean 14, 29–34 (in Japanese with English abstract). Sun, J.-z., Chen, W.-d., Zhuang, D.-g., Zheng, H.-y., Lin, L., Pang, S.-j., 2008. In situ ecological studies of the subtidal brown alga Sargassum horneri (Turner) C. Agardh at Nanji Island of China. South China Fish. Sci. 4 (3), 58–63 (in Chinese with English abstract). Thomsen, M.S., Wernberg, T., 2005. Mini review: what affects the forces required to break or dislodge macroalgae? Eur. J. Phycol. 40, 139–148. Thomsen, M.S., Wernberg, T., Kendrick, G.A., 2004. The effect of thallus size, life stage, aggregation, wave exposure and substrate conditions on the forces required to break or dislodge the small kelp Ecklonia radiata. Bot. Mar. 47, 454–460. Thomsen, M.S., 2004. Species, thallus size and substrate determine macroalgal break force and break location in a low-energy soft bottom lagoon. Aquat. Bot. 80, 153–161. Utter, B., Denny, M., 1996. Wave-induced forces on the giant kelp Macrocystis pyrifera (Agardh): field test of a computational model. J. Exp. Biol. 199, 2645–2654. Vogel, S., 1981. Life in Moving Fluids. Willard Grant Press, Boston. Xu, M., Komatsu, T., 2017. Field measurements of drag force on Sargassum horneri (Turner) C. Agardh towed by a boat and estimation of drag coefficient. La mer 54, 77–86. Xu, M., Sakamoto, S., Komatsu, T., 2016. Attachment strength of the subtidal seaweed Sargassum horneri (Turner) C. Agardh varies among development stages and depths. J. Appl. Phycol. 28 (6), 3679–3687. Yamauchi, K., 1983. The formation of Sargassum beds on artificial substrata by transplanting seedlings of S. horneri (Turner) C. Agardh and S. muticum (Yendo) Fensholt. Bull. Japan. Soc. Sci. Fish. 50 (7), 1115–1123. Yoshida, G., Arai, S., Terawaki, T., 1997. Effects of irradiance and temperature on the germling growth of Sargassum macrocarpum (Phaeophyta) from Ohno-Seto strait, Hiroshima Bay. Bull. Nansei Nat. Fish. Res. Inst. 30, 137–145 (in Japanese with English abstract). Yoshida, T., 1963. Studies on the distribution and drift of the floating seaweed. Bull. Tohoku Reg. Fish. Res. Lab. 23, 141–186 (in Japanese with English abstract). Zhang, S.Y., Bi, Y.X., Wu, Z.L., 2013. Spatial distribution pattern of Sargassum horneri around Gouqi Island, Shengsi, China. J. Fish. China 37 (6), 884–893 (in Chinese with English abstract). de Bettignies, T., Wernberg, T., Lavery, P.S., 2013. Size, not morphology, determines hydrodynamic performance of a kelp during peak flow. Mar. Biol. 160, 843–851.
Acknowledgements The authors thank to Mr. Yasutaka Tsuchiya, Hideo Shinagawa and Toshihiko Sato of Shimoda Marine Research Center of Tsukuba University for their helps to field experiments and to members especially to Shingo Sakamoto of Laboratory of Behavior, Ecology and Observation Systems, Atmosphere and Ocean Research Institute, The University of Tokyo for their constructive discussions and encouragements. The first author thanks to Ministry of Education, Culture, Science and Sports of Japan (MEXT) for giving him Japanese Government (Monbukagakusho) Scholarship. This study was supported by Grant-in-Aid for Scientific Research (A), No. 22255010 from Japan Society for Promotion of Science and Japanese Association of Marine Biology (JAMBIO) of Shimoda Marine Research Center, Tsukuba University. References Carrington, E., 1990. Drag and dislodgment of an intertidal macroalga: consequences of morphological variation in Mastocarpus papillatus Kützing. J. Exp. Mar. Biol. Ecol. 139 (3), 185–200. Cruz-Trejo, G.I., Ibarra-Obando, S.E., Aguilar-Rosas, L.E., Poumian-Tapia, M., SolanaArellano, E., 2015. Presence of Sargassum horneri at Todos Santos Bay, Baja California, Mexico: its effects on the local macroalgae community. Am. J. Plant Sci. 6, 2693. Denny, M., Gaylord, B., 2002. The mechanics of wave-swept algae. J. Exp. Biol. 205 (10), 1355–1362. Denny, M., 1995. Predicting physical disturbance: mechanistic approaches to the study of survivorship on wave-swept shores. Ecol. Monogr. 65, 371–418. Gaylord, B., 2000. Biological implications of surf-zone flow complexity. Limnol. Oceanogr. 45 (45), 174–188. Hamaguchi, A., Iguchi, H., Yoshida, T., Hayama, S., Tanaka, Y., Ueda, S., Nezu, Y., 1988. Comparison of maricultural new material composite resin and vinylon for seedlings and growing of Sargassum horneri C. Agardh. Suisanzoshoku 36 (3), 171–182 (in
64
Contents lists available at ScienceDirect
Aquatic Botany journal homepage: www.elsevier.com/locate/aquabot
Short communication
Changes in drag and drag coefficient on small Sargassum horneri (Turner) C. Agardh individuals
MARK
⁎
Min Xua,b, , Shuji Sasab, Takayoshi Otakib, Fu-xiang Huc, Tadashi Tokaic, Teruhisa Komatsub a
Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China Atmosphere and Ocean Research Institute, The University of Tokyo, Chiba 277-0882, Japan c Graduate School of Marine Science and Technology, Tokyo University of Marine Science and Technology, Tokyo 108-8477, Japan b
A R T I C L E I N F O
A B S T R A C T
Keyword: Sargassum horneri Drag Drag coefficient Cd Reynolds number Re
Sargassum horneri (Turner) C. Agardh is used to restore, create, and recreate seaweed beds along the coastlines of East Asia. Drag produced by waves is a bulk force that can detach thalli from substrata during the early growth stages from substrata. In this study we measured drag forces on small S. horneri thalli (10–40 cm long). Unidirectional steady flow was controlled from 20 to 130 cm s−1 in increments of 10 cm s−1 in a recirculating water tank. Drag force on individuals ranged from ∼0.3 N to ∼3 N. Drag (Fdrag) and water velocity (U) produced the following exponential empirical approximations: Fdrag = 0.0168 × U0.8925. The drag coefficient (Cd) was plotted as a function of Reynolds number (Re) as follows: Cd = 4744.7 × Re−0.93. Cd converged to 0.037 at Re of 105−6 suggesting that small thalli exhibit optimal morphological adaptations to withstand high current speeds.
1. Introduction
(Kjellman) in a large (100 cm height) water tunnel that generates undulatory flow. Assuming that large waves have a long wavelength that is far greater than the bottom depth, they measured fluid forces consisting of additional mass force proportional to acceleration and drag force proportional to speed. Under the long wave situation, drag was the prevalent force and additional forces could be neglected. When devising strategies for developing seaweed beds, it is important to study the balance between drag and attachment strength during early life stages. Drag (Fdrag) on thalli of any length is estimated by the drag coefficient (Cd) at a given water speed. Xu and Komatsu (2017) used the boat method (Utter and Denny, 1996) to evaluate Cd plotted as a function of Reynolds number (Re) of S. horneri thalli 40–270 cm long. A seaweed specimen was attached to one end of a nonstretching string, and its other end was attached to a spring scale running on low-friction wheels along a vertical steel bar attached to the side of the boat. The thallus was towed behind the boat at a constant speed while forces were read from the spring scale and recorded in a notebook. However, it is difficult to measure drag on small S. horneri thalli using the boat method, so in this study a recirculating water tunnel that can generate unidirectional steady flow was used to measure drag forces on S. horneri thalli ranging from 10 to 40 cm long. We investigated Fdrag and Cd of small S. horneri thalli at different water velocities ranging from 20 to 130 cm s−1 in increments of 10 cm s−1.
Sargassum horneri (Turner) C. Agardh is a subtidal seaweed species that belongs to the order Fucales (Class: Phaeophyceae; Order: Fucales; Family: Sargassaceae; Genus: Sargassum) (Yoshida et al., 1997). Sargassum horneri forms an underwater forest with a canopy height of 300–700 cm above the hard substrata and grows from near shore to a bottom depth of several meters (Komatsu et al., 2015). It is widely distributed along the coasts of northeast Asia from China to Russia through the Korean Peninsula and Japan, with the exception of Taiwan and the Ryukyu Archipelago (Komatsu et al., 2014). Sargassum horneri has spread aggressively throughout southern California, USA, and Baja California, Mexico since it was discovered in the eastern Pacific in 2003 and it poses a major threat to the sustainability of native marine ecosystems in this region (Cruz-Trejo et al., 2015; Marks et al., 2015). Scientists have been trying to restore, create, and recreate S. horneri beds with varying success in East Asia (Yamauchi, 1983; Hamaguchi et al., 1988; Sun et al., 2008; Zhang et al., 2013). Thus, it is important to understand the ecological processes such as survival, transport and dispersal of this species. Drag is a bulk hydrodynamic force that can dislodge seaweeds from substrata (Denny, 1995; Gaylord, 2000; Thomsen et al., 2004; Stewart, 2006). Sugawara et al. (1998) measured the fluid force on the brown seaweeds Eisenia bicyclis (Kjellman Setchell) and Ecklonia cava
⁎
Corresponding author at: Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China. E-mail address: [email protected] (M. Xu).
https://doi.org/10.1016/j.aquabot.2017.11.002 Received 2 March 2017; Received in revised form 26 October 2017; Accepted 8 November 2017 Available online 11 November 2017 0304-3770/ © 2017 Elsevier B.V. All rights reserved.
Aquatic Botany 144 (2018) 61–64
M. Xu et al.
2. Materials and methods Sargassum horneri thalli used for this experiment were collected from Nabeta Cove near Shimoda (34°39′58″N, 138°56′31″E) in the southernmost part of Izu Peninsula, Japan, on the morning of 29 January 2015 (Xu et al., 2016). Small sized (10–40 cm long) thalli (n = 21) including 3 individuals without vesicles were cropped with their holdfasts. Cropped individuals were immediately kept in an ice box and transported from Shimoda to Tokyo University of Marine Science and Technology in Shinagawa, Tokyo on the day of collection. A recirculating flow tank (150 cm long × 50 cm wide × 80 cm deep) that could generate unidirectional steady flow ranging from 20 to 130 cm s−1 was used for the experiment. The tank was filled with freshwater and was used to measure drag forces exerted on individual seaweed thalli at different speeds of water flow. Water speed was measured using a small electromagnetic current meter (VM-801HA, KENEK, Japan). Water temperatures measured on 29 and 30 January 2015 using a water temperature device (WTM-R, PIVOT, Japan) were 9.1 and 8.2 °C, respectively. The method used to measure drag on seaweeds was based on Utter and Denny (1996), who studied Macrocystis pyrifera (Linnaeus) C. Agardh. One end of a buckle was attached to the holdfast of an individual thallus. The other end of a buckle was attached to a strain gauge that measured force through a pulley located at the bottom of a cylindrical tube at a depth of 10 cm from the water surface in the working section of the tank and another pulley situated at the water surface. A wooden frame was placed on the experimental section of the tank to support the cylindrical tube and connect the end of a buckle to the strain gauge. Tension on the thread produced by drag on an individual thallus by water flow changed the resistance on the strain gauge. Drag force on only the thread projecting from the cylindrical tube in the experimental section of the tank filled with freshwater was measured under the tested speeds of water flow and subtracted from drag forces of individual thalli as an offset value. After the experiment, thallus length from the bottom of the holdfast to the top of the longest lateral branch (with an accuracy of ± 1 cm) was measured using a 30 cm ruler. A balance (CR-5000WP, Custom, Japan) was used to determine wet weights of thalli with the holdfast (with an accuracy of ± 2 g) after removing surface water with a paper towel. Surface area of one side of an individual was measured using ImageJ software (ver. 6.4; National Institutes of Health, Bethesda, MD, USA). We prepared five pictures of each individual that were corrected horizontally using image processing software (Photoshop CS, Adobe, USA). The area of a given thallus was based on the mean of five images of that thallus. Drag coefficient Cd was calculated using the following Eq. (1):
Fig. 1. Plots of drag force (N) against water flow speed (cm s−1) of thalli for thallus length of 10–40 cm. Upper regression line: F = 0.0151 × U1.0976; bottom regression line: F = 0.0024 × U1.0344.
for each thallus to calculate its Re at different values of U using Eq. (2). Pearson correlation was applied to evaluate relationships between Fdrag and U and between Cd and Re. 3. Results and discussion 3.1. Drag and drag coefficient Fig. 1 shows drag on thalli. The plot of U versus Fdrag produced the following exponential approximation:
Fdrag = 0.0168 × U 0.8925
for thalli with lengths of 10–40 cm (n = 21; R = 0.42, p < 0.05; 20 cm s−1 < U < 130 cm s−1). Fdrag in Eq. (3) shows that drag force was roughly proportional to the flow rate to the 0.9 power. The upper regression plot of U and Fdrag for a thallus with length of 35.6 cm resulted in
Fdrag = 0.0151 × U1.0976 2
ρ×
×A
U× L ν
−1
−1
(5)
< U < 130 cm s . with R = 0.865, p < 0.001; 20 cm s Cd of individuals was calculated as a function of Re (n = 21; R2 = 0.72, p < 0.001, SE = 0.053) as follows (Fig. 2):
(1)
where Fdrag, ρ, U, and A were drag exerted on a seaweed in a steady flow, freshwater mass density (at 8 °C on 30 January 2015 and at 9 °C on 29 January 2015, values were 0.99985 and 0.99978 g cm−3, respectively), fluid speed relative to a seaweed, and one side’s surface area of the seaweed, respectively. We measured Fdrag, ρ, U. Using these values, Cd of an individual at various speeds of water flow was estimated. To compare drag coefficients among different algae, Cd was plotted as a function of Re in the form of a Log–Log linear regression. Re was calculated as follows:
Re =
−1
Fdrag = 0.0024 × U1.0344
2 × Fdrag U2
(4) −1
< U < 130 cm s . with R = 0.984, p < 0.001; 20 cm s The lower regression plot of U and Fdrag for a thallus with length of 12.7 cm resulted in
2
Cd =
(3) 2
Cd = 4744.7 × Re−0.93
(6)
As speed of water flow increased, Cd converged to 0.037 at high Re values between 105 and 106. 3.2. Effect of drag on small versus large S. horneri and its ecological implications When subjected to a given water current speed, macrophytes experience a drag force 25 times higher than that of terrestrial plants exposed to a similar wind speed (Denny and Gaylord, 2002). Sargassum horneri inhabit a wave exposed subtidal environment, and they face possible detachment or breakage from the substrate to which they are attached. Holdfasts of individuals are torn from the substrate by drag produced by waves that exceed the attachment strength of the holdfast (Yoshida, 1963), and maximum dislodgement force represents the maximum drag force that fronds can resist.
(2)
where L and ν were the characteristic length of a thallus and the kinematic viscosity of a fluid (freshwater: 0.0139 cm2 s−1 at 8 °C and 0.0134 cm2 s−1 at 9 °C), respectively. We used the square root of one side’s surface area of each thallus as the characteristic length (L = A ) 62
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Fig. 2. Plots of drag coefficient (Cd) as a function of Reynolds number (Re) for high drag seaweed species (Ecklonia radiata [C. Agardh] J. Agardh (de Bettignies et al., 2013), Mastocarpus papillatus [C. Agardh] (Carrington, 1990) and Saccarina japonica (Kawamata, 2001)) and low drag seaweed species (Sargassum horneri with thalli 0–40 cm long with and without vesicles [upper panel] and 40–270 cm long [bottom panel] (Xu and Komatsu, 2017). Data for a rigid smooth flat plate oriented parallel to the flow (Schlichting, 1968) also are shown.
cm). At a water speed of 85 cm s−1, we obtained Cd = 0.11314 following Eq. (6) and Fdrag =0.88 N following Eq. (1). These results show that the two methods estimated a similar drag force output. We also used method (2) to conduct back-calculations to calculate breaking speed created by waves to compare with attachment strength of 10–40 cm long S. horneri thalli collected in December 2014 and 2015 (Xu et al., 2016). Mean breaking speed classified by for thalli in the range of 10–40 cm were as follows: 10–20 cm long thalli, 403.3 ± 263.1 cm s−1, N = 23; 20–30 cm long thalli, 467.2 ± 243.0 cm s−1, N = 17; 30–40 cm long thalli, 904.0 ± 817.0 cm s−1, N = 10). Thomsen and Wernberg (2005) argued that thallus size was an important factor for scaling macroalgal break forces within and between species, and thus it might also be related to breaking velocity increasing with thallus size. He reported mean breaking speeds to be 40–120 cm s−1 for Ulva curvata, Gracilaria verrucosa, Gracilaria foliifera, Agardhiella subulata, Fucus vesiculosus, and Codium fragile. Sargassum species seem to have higher breaking speeds, probably due to their large biomass and habitation of wave-exposed areas. A given seaweed species regardless of its size uses the same strategy to go with the flow as waves pass in order to decrease Cd and eventually drag force by the water flow (Fig. 2). The presence of vesicles has little impact on the plot of Cd versus Re, and the plots for thalli with and
Xu and Komatsu (2017) used the same method implemented in this study to measure drag on S. horneri thalli 40–270 cm long. Drag forces on thalli 40–50 cm long were usually < 5 N. Drag forces on thalli 50–100 cm long were < 15 N, whereas most in the longest thallus group (100–270 cm) were < 20 N at 400 cm s−1 flow speeds. In the present study, drag forces on thalli < 20 cm long and those between 20 and 40 cm were less than ∼1.5 N and 1.5 to ∼3 N, respectively. Cd of algae generally decreases gradually as the Re increases through the range 104 to 106 (Vogel, 1981). Past studies of Cd of several seaweeds at high Re values under high flow speeds ranged from 0.01 to 0.05 at Re of 106 (Koehl, 2000; Kawamata, 2001; Thomsen, 2004). For S. horneri with thallus length varying from 0 to 50 cm to 200–300 cm, the Cd limit value decreased 10 times from 0.02 to 0.002 (Xu and Komatsu, 2017). The current study provides two ways to calculate drag on S. horneri thalli ranging in size from 10 to 40 cm. Using method 1, we estimated a drag force range at a certain water speed for S. horneri thalli ranging from 10 to 40 cm long, as shown in Fig. 1. For example, at water speed of 85 cm s−1, drag force on a 25-cm long S. horneri thallus ranged from 0.24 to 1.98 N following Eqs. (4) and (5). Drag force was 0.88 N following Eq. (3). Using method 2, thallus length of 25 cm was equivalent to 217 cm2 surface area (Unpublished data: One side surface area = 3.5168 × thallus length1.2805, R2 = 0.53, thallus length < 40
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without vesicles overlap (Fig. 2). The range of Cd values is similar for S. horneri thalli < 40 cm long and the intertidal small alga Mastocarpus papillatus (C. Agardh) (Carrington, 1990). The range of Cd values for larger S. horneri thalli (40–270 cm) is similar to those of a rigid smooth flat plate oriented parallel to the flow (Schlichting, 1968) and to Ecklonia radiata (C. Agardh) J. Agardh (de Bettignies et al., 2013) and Saccarina japonica of the high and low drag groups (Kawamata, 2001). The Cd of S. horneri obtained in the present study can be used to estimate drag force in a storm and to conduct back-calculations to estimate breaking velocities. Cd converged to 0.037 at Re of 105−6, suggesting that small thalli exhibit optimal morphological adaptations to withstand high current speeds. Studying the effects of drag and drag coefficient on the early life stages of S. horneri is important to understanding its survival, transport, and dispersal. In future studies we will need to incorporate other hydrodynamic forces, such as acceleration and break force, into the model in order to obtain a more comprehensive understanding of the biomechanics of Sargassum species.
Japanese with English abstract). Kawamata, S., 2001. Adaptive mechanical tolerance and dislodgement velocity of the kelp Laminaria japonica in wave-induced water motion. Mar. Ecol. Progr. 211 (4), 89–104. Koehl, M.A.R., 2000. Mechanical design and hydrodynamics of blade like algae: Chondracanthus exasperates. In: Spatz, H.C., Speck, T. (Eds.), Third International Plant Biomechanics. Thieme Verlag, Stuttgart, pp. 295–308. Komatsu, T., Mizuno, S., Natheer, A., Kantachumpoo, A., Tanaka, K., Morimoto, A., Hsiao S.-t. Rothausler Eva, A., Shishidou, H., Aoki, M., Ajisaka, T., 2014. Unusual distribution of floating seaweeds in the East China Sea in the early spring of 2012. J. Appl. Phycol. 26 (2), 1169–1179. Komatsu, T., Ohtaki, T., Sakamoto, S., Sawayama, S., Hamana, Y., Shibata, M., Shibata, K., Sasa, S., 2011. Impact of the 2011 tsunami on seagrass and seaweed beds in otsuchi bay, sanriku coast, Japan. In: Ceccaldi, H.J., Hénocque, Y., Koike, Y., Komatsu, T., Stora, G., Tusseau-Vuillemin, M.-H. (Eds.), Marine Productivity: Perturbations and Resilience of Socio-Ecosystems. Springer International Publishing, Switzerland, Cham, pp. pp. 43–53. Marks, L.M., Salinas-Ruiz, P., Reed, D.C., Holbrook, S.J., Culver, C.S., Engle, J.M., et al., 2015. Range expansion of a non-native, invasive macroalga Sargassum horneri (Turner) C. Agardh, 1820 in the eastern Pacific. BioInvasions Rec. 4, 243–248. Schlichting, H., 1968. Boundary-Layer Theory, 6th edn. McGraw-Hill, New York. Stewart, H.-l., 2006. Morphological variation and phenotypic plasticity of buoyancy in the Macroalga Turbinaria ornate across a barrier reef. Mar. Biol. 149 (4), 721–730. Sugawara, A., Seto, M., Komatsu, T., 1998. Study on the zonation of macro algae: vertical distribution and current environments in Eisenia bicyclis Setchell and Ecklonia cava Kjellman. Proceedings of Civil Engineering in the Ocean 14, 29–34 (in Japanese with English abstract). Sun, J.-z., Chen, W.-d., Zhuang, D.-g., Zheng, H.-y., Lin, L., Pang, S.-j., 2008. In situ ecological studies of the subtidal brown alga Sargassum horneri (Turner) C. Agardh at Nanji Island of China. South China Fish. Sci. 4 (3), 58–63 (in Chinese with English abstract). Thomsen, M.S., Wernberg, T., 2005. Mini review: what affects the forces required to break or dislodge macroalgae? Eur. J. Phycol. 40, 139–148. Thomsen, M.S., Wernberg, T., Kendrick, G.A., 2004. The effect of thallus size, life stage, aggregation, wave exposure and substrate conditions on the forces required to break or dislodge the small kelp Ecklonia radiata. Bot. Mar. 47, 454–460. Thomsen, M.S., 2004. Species, thallus size and substrate determine macroalgal break force and break location in a low-energy soft bottom lagoon. Aquat. Bot. 80, 153–161. Utter, B., Denny, M., 1996. Wave-induced forces on the giant kelp Macrocystis pyrifera (Agardh): field test of a computational model. J. Exp. Biol. 199, 2645–2654. Vogel, S., 1981. Life in Moving Fluids. Willard Grant Press, Boston. Xu, M., Komatsu, T., 2017. Field measurements of drag force on Sargassum horneri (Turner) C. Agardh towed by a boat and estimation of drag coefficient. La mer 54, 77–86. Xu, M., Sakamoto, S., Komatsu, T., 2016. Attachment strength of the subtidal seaweed Sargassum horneri (Turner) C. Agardh varies among development stages and depths. J. Appl. Phycol. 28 (6), 3679–3687. Yamauchi, K., 1983. The formation of Sargassum beds on artificial substrata by transplanting seedlings of S. horneri (Turner) C. Agardh and S. muticum (Yendo) Fensholt. Bull. Japan. Soc. Sci. Fish. 50 (7), 1115–1123. Yoshida, G., Arai, S., Terawaki, T., 1997. Effects of irradiance and temperature on the germling growth of Sargassum macrocarpum (Phaeophyta) from Ohno-Seto strait, Hiroshima Bay. Bull. Nansei Nat. Fish. Res. Inst. 30, 137–145 (in Japanese with English abstract). Yoshida, T., 1963. Studies on the distribution and drift of the floating seaweed. Bull. Tohoku Reg. Fish. Res. Lab. 23, 141–186 (in Japanese with English abstract). Zhang, S.Y., Bi, Y.X., Wu, Z.L., 2013. Spatial distribution pattern of Sargassum horneri around Gouqi Island, Shengsi, China. J. Fish. China 37 (6), 884–893 (in Chinese with English abstract). de Bettignies, T., Wernberg, T., Lavery, P.S., 2013. Size, not morphology, determines hydrodynamic performance of a kelp during peak flow. Mar. Biol. 160, 843–851.
Acknowledgements The authors thank to Mr. Yasutaka Tsuchiya, Hideo Shinagawa and Toshihiko Sato of Shimoda Marine Research Center of Tsukuba University for their helps to field experiments and to members especially to Shingo Sakamoto of Laboratory of Behavior, Ecology and Observation Systems, Atmosphere and Ocean Research Institute, The University of Tokyo for their constructive discussions and encouragements. The first author thanks to Ministry of Education, Culture, Science and Sports of Japan (MEXT) for giving him Japanese Government (Monbukagakusho) Scholarship. This study was supported by Grant-in-Aid for Scientific Research (A), No. 22255010 from Japan Society for Promotion of Science and Japanese Association of Marine Biology (JAMBIO) of Shimoda Marine Research Center, Tsukuba University. References Carrington, E., 1990. Drag and dislodgment of an intertidal macroalga: consequences of morphological variation in Mastocarpus papillatus Kützing. J. Exp. Mar. Biol. Ecol. 139 (3), 185–200. Cruz-Trejo, G.I., Ibarra-Obando, S.E., Aguilar-Rosas, L.E., Poumian-Tapia, M., SolanaArellano, E., 2015. Presence of Sargassum horneri at Todos Santos Bay, Baja California, Mexico: its effects on the local macroalgae community. Am. J. Plant Sci. 6, 2693. Denny, M., Gaylord, B., 2002. The mechanics of wave-swept algae. J. Exp. Biol. 205 (10), 1355–1362. Denny, M., 1995. Predicting physical disturbance: mechanistic approaches to the study of survivorship on wave-swept shores. Ecol. Monogr. 65, 371–418. Gaylord, B., 2000. Biological implications of surf-zone flow complexity. Limnol. Oceanogr. 45 (45), 174–188. Hamaguchi, A., Iguchi, H., Yoshida, T., Hayama, S., Tanaka, Y., Ueda, S., Nezu, Y., 1988. Comparison of maricultural new material composite resin and vinylon for seedlings and growing of Sargassum horneri C. Agardh. Suisanzoshoku 36 (3), 171–182 (in
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