DOI 10.1515/bot-2012-0193 Botanica Marina 2013; 56(1): 3–14

Angelika Graiff , Ulf Karsten , Steffi Meyer , David Pfender , Fadia Tala and Martin Thiel * Seasonal variation in floating persistence of detached antarctica (Chamisso) Hariot a thalli

Abstract: Several large species are capable of long- Science , University of Bremen, Leobener Stra ß e NW2, D-28359 distance dispersal via rafting. However, seasonal changes Bremen, Germany in environmental conditions at the sea surface may vari- David Pfender: Facultad de Ciencias del Mar , Universidad Cat ó lica del Norte, Larrondo 1281, Coquimbo, ably affect the physiological status of the floating thalli; Fadia Tala: Facultad de Ciencias del Mar , Universidad Cat ó lica del challenging conditions during summer may accelerate dis- Norte, Larrondo 1281, Coquimbo, Chile ; and Centro de Investigaci ó n integration and cause rapid sinking. We used the bull kelp y Desarrollo Tecnol ó gico en Algas (CIDTA) , Larrondo 1281, from northern-central Chile (30 °S) to Coquimbo, Chile test seasonal variation in floating persistence. Experiments Martin Thiel: Centro de Estudios Avanzados en Zonas Á ridas (CEAZA), Larrondo 1281, Coquimbo, Chile with tethered specimens were conducted in all seasons to assess how variable environmental conditions influence the morphology and photosynthetic characteristics of floating D. antarctica . Floating specimens stayed afloat at the surface for more than 1 month during moderate envi- Introduction ronmental conditions that prevailed in winter, spring, and fall. However, higher water temperatures and intense Rafting on floating objects is an important dispersal mech- solar radiation in summer resulted in significant biomass anism for many aquatic organisms with limited autono- losses and rapid disintegration of the floating ; conse- mous dispersal capacity (Hobday 2000a , Thiel 2003 ). quently, they sank within < 1 month. These strong seasonal Floating are considered one of the most important effects were reflected in decreasing maximal quantum yield rafting vectors in all oceans (Helmuth et al. 1994 , Hobday as well as in maximum relative electron transport rates of 2000a , Vandendriessche et al. 2006 , Nikula et al. 2010 ). photosynthesis. Understanding physiological responses of Algal rafting appears to be advantageous for dispersal of floating algae is important because increasing global tem- some taxa and their associated fauna (Dayton peratures and shifts in solar radiation may strongly affect 1973 , Macaya et al. 2005 , Thiel and Gutow 2005 ). When positively buoyant algae become detached from the survival of floating algae, potentially reducing the dis- the benthic substratum, they can float to the sea surface tances and frequencies of rafting dispersal. where they may remain afloat for several weeks or even months (Harrold and Lisin 1989 , Ing ó lfsson 1998 , Hobday Keywords: Durvillaea antarctica ; floating persistence; 2000b , Hern á ndez-Carmona et al. 2006 ). Floating thalli of rafting; temperature; UV radiation. macroalgae act as long-distance dispersal vectors, thereby contributing to population connectivity and colonization a Supplementary material to this article is available online at of habitats (Fraser et al. 2009 , Hinojosa et al. 2010 ). Suc- http://www.degruyter.com/view/j/botm. cessful dispersal therefore largely depends on the avail- *Corresponding author: Martin Thiel, Facultad de Ciencias del Mar , ability of floating algae and on the persistence time of Universidad Cat ó lica del Norte, Larrondo 1281, Coquimbo, Chile , e-mail: [email protected] the thalli at the sea surface (Smith 2002 , Thiel and Gutow Angelika Graiff: Facultad de Ciencias del Mar , Universidad Cat ó lica 2005 ). del Norte, Larrondo 1281, Coquimbo, Chile ; and Institute of Upon detachment, whole buoyant algae are trans- Biological Sciences , Applied Ecology, University of Rostock, ferred to surface conditions where survival depends on Albert-Einstein-Stra ß e 3, D-18057 Rostock, Germany several biotic and abiotic factors that differ from those in Ulf Karsten: Institute of Biological Sciences , Applied Ecology, the benthos. The main factors influencing the persistence University of Rostock, Albert-Einstein-Stra ß e 3, D-18057 Rostock, Germany of floating algae at the sea surface are solar radiation, Steffi Meyer: Facultad de Ciencias del Mar , Universidad Cat ó lica del temperature, epibiont load and herbivory (Edgar 1987 , Norte, Larrondo 1281, Coquimbo, Chile ; and Department of Marine Hobday 2000a , Thiel and Gutow 2005 , Vandendriessche 4 A. Graiff et al.: Floating duration of kelps et al. 2007a , Rothä usler et al. 2009, 2011a). Previous offers protection against potential damage by the strong studies have recorded seasonal variations in the abun- waves in its natural habitat (Skottsberg 1941 , Santelices et dances of floating algae in particular areas (Yoshida al. 1980 , Hay 1994 , Koehl 1999 ). However, during periods 1963 , Hobday 2000c, Hirata et al. 2001 , Hinojosa et al. of strong waves, D. antarctica suffers substantial hydro- 2010 ), which may be due either to differences in supply dynamic drag at the base of the stipe, resulting in detach- from benthic sources or to variable survival times of algal ment of thalli from the rocks with or without holdfasts rafts. Water temperature and solar radiation are particu- (Smith and Bayliss-Smith 1998, Garden and Smith 2011 , larly important factors that affect the floating persistence Garden et al. 2011 ). of algae (Hobday 2000b , Vandendriessche et al. 2007a , At present, little information is available on the Rothä usler et al. 2009, 2011b,c). The transfer of detached biology and survival of D. antarctica after detachment, to the sea surface may increase the risk of physi- although it is known that the potential to persist at the sea ological stress (Macaya et al. 2005 ). Additionally, micro- surface is a key factor in long-distance dispersal (Hobday bial degradation of the floating algae might be higher with 2000b , Thiel and Gutow 2005 ). Patagonian areas affected increasing temperatures, as has been shown for benthic by the Last Glacial Maximum have been repopulated by D. macroalgae (Kristensen et al. 1992 ). antarctica, and genetic analyses demonstrate that popula- Withstanding extreme solar radiation and high tem- tions from can be considered as the source perature requires an efficient physiological acclimation of of recolonization (Fraser et al. 2010b ). This reveals a high floating alga (Roth ä usler et al. 2011b ). This allows thalli potential for trans-oceanic dispersal in D. antarctica . to quickly recover from stress via adjustment of pigment However, the distance and commonly reported floating concentrations, dynamic photoinhibition and/or repair velocities of 0.5 – 1 km h-1 (Thiel and Gutow 2005 ) suggest mechanisms (Franklin and Forster 1997 , Bischof et al. that floating kelps coming from New Zealand would 1998a, 1999, G ó mez et al. 2004, Edwards and Kim 2010 ). require about 1 year before reaching the Chilean coast. It Thus, within the tolerance range of algae (e.g., during fall is thus important to understand the acclimation potential or spring conditions in many temperate regions), physio- of D. antarctica thalli floating at the sea surface. logical acclimation may operate efficiently (Eggert 2012 ), As yet, little is known about how seasonal changes in thereby enhancing the persistence of floating algae at the solar radiation and temperature affect the survival poten- sea surface. Each algal species has a specific temperature tial of floating macroalgae. We studied the floating per- range within which the expression of photoprotective sistence of detached D. antarctica thalli from continental mechanisms is most effective (H ä der and Figueroa 1997, Chile under different environmental conditions. We pos- Eggert 2012 ), thereby enhancing the possibility of persis- tulated that the survival time of D. antarctica at the sea tence for protracted periods at the sea surface. surface differs between the seasons. To test this postulate, Optimal conditions for dispersal of an algal species we conducted seasonal experiments to determine the might be found at different times and locations, depending floating persistence of tethered kelps, and we also exam- on the seasonal variation in water temperature (Wooster ined how variable environmental conditions during differ- and Sievers 1970 ) and solar radiation (Huovinen et al. ent seasons influence the morphology and photosynthetic 2006 ). However, the effects of seasonal variations in envi- physiology of floating D. antarctica thalli. ronmental parameters on the floating persistence of algae have not yet been examined. Algae from cold-temperate regions suffer at high temperatures and from solar irradi- Materials and methods ances, i.e., typical summer conditions (Vandendriessche et al. 2007a , Rothä usler et al. 2009), which suggests that Seasonal sampling of algae they may float significantly longer during winter months. An ideal candidate species to test this postulate is the Algae were collected in each season (winter: 5 August bull kelp Durvillaea antarctica (Chamisso) Hariot, which is 2011; spring: 28 October 2011; summer: 1 February frequently found floating in the (Smith 2002 ) 2012; fall: 6 May 2012) during low tide from the shore of and cold-temperate regions of the southern hemisphere Pichicuy, in the Province of Petorca, Chile (32 ° 20 ′ S, 71 ° 27 ′ (Hinojosa et al. 2010 ). It is also very abundant along the W). The sampling site is close to the northern distribution Chilean coast on exposed rocky shores (Westermeier et al. limit of the continental range of D. antarctica in central 1994 , Fraser et al. 2010a ). Furthermore, D. antarctica pos- Chile (Fraser et al. 2010b). Each season, 19 – 28 complete sesses a unique gas-filled honeycomb structure within the D. antarctica thalli (i.e., individuals with their holdfasts) blades, which gives strength and extreme buoyancy, and were detached from their natural habitat (Table 1 ). The A. Graiff et al.: Floating duration of kelps 5

n Mass (g) Min Max Length (cm) Min Max

Winter 19 7445.8 ± 5367.1 1770.3 21,359.6 376.8 ± 131.0 209.4 676.3 Spring 20 6094.5 ± 4147.9 1720.1 17,730.9 331.8 ± 94.4 118.1 512.0 Summer 24 2931.7 ± 2289.4 590.2 11,420.4 272.3 ± 126.2 97.4 569.9 Fall 28 5938.9 ± 4504.8 1150.7 19,920.8 386.2 ± 147.0 194.6 696.5

Table 1 Durvillaea antarctica : mean wet mass and length ± SD of thalli on day 0 of individuals during different seasons. algae collected in summer were significantly smaller and Experimental design lighter than those collected in the other seasons [one-way analysis of variance (ANOVA) with post hoc Tukey ’ s test; The individual algae (winter: n = 19; spring: n = 20; summer: = = < = = wet mass: F 3,89 7.3; total length: F 3,89 5.2; p 0.001 for both n 24; fall: n 28) were tethered at the sea surface in the comparisons; Tables S1 and S2 ), but there was extensive relatively enclosed Bahia La Herradura, Coquimbo, Chile, overlap in the size distribution among all four seasons in their natural habitat. Durvillaea antarctica individuals sampled (Table 1). For logistical reasons, eight initial algae were randomly distributed and tied to a line of buoys 1 – 3 were detached slightly before each seasonal experiment m distance from one another, where they were maintained (winter: 15 July 2011; spring: 4 September 2011; summer: until their individual days of sinking. 17 January 2012; fall: 10 April 2012) to document the initial Each individual received an identification tag attached physiological status of these kelps in their native habitat. to its main stipe before being tethered to a single buoy by After sampling, the algae were immediately transported in a plastic cord. For tethering, a cable tie surrounded by coolers and tanks (protected from light and desiccation) sliced bicycle inner tubing was pulled through the loop to the marine laboratory at Universidad Cató lica del Norte, of a plastic cord to reduce the risk of physical damage to Bahí a La Herradura, Coquimbo, Chile (29° 57 ′ S, 71° 20 ′ W). the stipe. Throughout the experiments, we observed a The algae were kept overnight in flow-through seawater slight damage to the stipe due to the friction of the cable tanks (2000 l) before being measured and tethered in the tie in some seasons, but this did not lead to holdfast losses field (see below). despite substantial water movements during some seasons (e.g., winter 2011). The plastic cord had a loop at its other end that was fastened to the buoy using another cable tie. Environmental conditions during the study The algae were able to freely sway and float in the water. After the first 2 weeks of floating, the algae were Throughout the course of each experimental period, checked daily to ensure that their exact days of sinking surface water temperature (50 cm below the sea surface) and changes in thallus physical condition were recorded. was monitored every 3 min using the HOBO ® TidbiT v2 data The algae were considered as having sunk when they were logger (Onset computer corporation, Bourne, MA, USA). In completely submerged and no part remained above the addition, the incident ultraviolet B (UV B; 290– 340 nm) and water surface. ultraviolet A (UV A; 340 – 400 nm) radiation were meas- During the experiments, sea gulls (Larus dominicanus ured using the UV3pB and UV3pA sensors (Delta-T Devices Lichtenstein) and pelicans (Pelecanus thagus Molina) Ltd, Cambridge, UK) connected to a Li-Cor-1400 data logger pecked at the floating kelps. Most likely these seabirds (Li-Cor Bioscience, Lincoln, NE, USA). Whereas the UV B consume the organisms settling on or hiding under sensor slightly overestimated the defined UV B waveband the fronds of the algae, as reported from the Northeast [290– 315 nm according to the International Commission on Atlantic for various seabirds, which frequently associate Illumination (CIE) definition], the UV A sensor produced with patches of floating seaweeds (Vandendriessche et a corresponding underestimation (315 – 400 nm). In paral- al. 2007b ). This might have caused lesions on the thalli, lel, photosynthetically active radiation (PAR, 400 – 700 nm) enhancing the degradation process and leading to the data were obtained with a Li-190SA quantum sensor (Li-Cor sudden loss of larger frond pieces. Bioscience). Radiometers were placed free of physical interference, and ultraviolet and photosynthetically active irradiances were measured every 5 or 15 min throughout Measurement of D. antarctica responses the day from 07:00 to 19:00. This information was used to calculate the daily doses of ultraviolet radiation and PAR The morphological parameters and physiological by integrating instantaneous data (Table 2 ). responses of D. antarctica were measured on the eight 6 A. Graiff et al.: Floating duration of kelps

a Winter (° C) Spring (° C) Summer ( ° C) Fall (° C) 05 Aug – 19 Sept 2011 28 Oct – 14 Dec 2011 01 Feb – 02 Mar 2012 07 May – 29 Jun 2012

Mean ± SD 13.4 ± 0.4 16.0 ± 0.8 18.3 ± 0.7 14.3 ± 1.1 Min 12.2 13.6 15.7 13.0 Max 14.8 21.0 21.3 16.2

b Winter Spring Summer Fall 05 Aug – 19 Sept 2011 28 Oct – 14 Dec 2011 01 Feb – 02 Mar 2012 07 May – 29 Jun 2012

45 days 16 days 15 days 53 days

PAR Maximum range (μ mol photons m -2 s-1 ) 508.2 – 2238.6 1024.5 – 2879.6 2077.9 – 2942.2 356.6 – 1364.4 Mean ± SD (μ mol photons m-2 s-1 ) 625.5 ± 221.3 969.6 ± 273.0 1202.9 ± 186.1 449.4 ± 153.5 Daily dose (kJ m-2 ) 6158.0 ± 2515.9 9316.8 ± 2570.0 11,338.3 ± 1731.2 3915.1 ± 1350.4 UV A Maximum range (W m-2 ) 3.4 – 18.5 8.5 – 23.7 16.1 – 21.8 1.98 – 10.2 Mean ± SD (W m-2 ) 5.1 ± 1.9 7.5 ± 2.2 8.9 ± 1.4 3.1 ± 1.1 Daily dose (kJ m-2 ) 232.6 ± 95.6 335.8 ± 94.1 387.2 ± 60.5 122.5 ± 45.7 UV B Maximum range (W m-2 ) 2.1 – 5.1 3.2 – 6.6 6.2 – 8.4 2.0 – 7.9 Mean ± SD (W m-2 ) 1.7 ± 0.4 2.5 ± 0.7 3.2 ± 0.5 1.3 ± 0.1 Daily dose (kJ m-2 ) 74.7 ± 22.3 123.0 ± 29.3 140.0 ± 21.4 51.1 ± 5.1

Table 2 Average, minimum, and maximum seawater temperatures (a) and range of maximum values, average, and daily dose of PAR, UV A (340 – 400 nm), and UV B (290 – 340 nm) radiation (b) in the different seasons. UV A, Ultraviolet A; UV B, Ultraviolet B. initial individuals and on the experimental thalli on their sensitive indicator of photosynthetic performance and, day of sinking. Maximum length and total wet mass of hence, of the viability of algae, which might be affected all experimental algae were measured at day 0 and on by high photon fluence rates or stress exposure in general. the respective days of sinking. The total wet mass and For estimation of the relative PSII electron transport rate, maximum length measured at the start of the experi- each sample disc was irradiated individually with increas- ment and on the day of sinking were used to calculate the ing photon fluence rates of PAR (0– 1299 μ mol photons biomass and length loss for each experimental alga. m-2 s-1 ) provided by a light-emitting diode lamp of the PAM The within-individual biomass distribution of D. ant- device, as described in Schreiber et al. (1994) . For each PAR arctica was determined by destructive sampling. There- range, the absorptance of light and the effective quantum fore, only the initial individuals and the algae that had yield (Fv ′ /Fm ′ ) of the samples were determined. The electron sunk could be dissected into holdfasts, stipes and fronds. transport rate (ETR) parameters, such as ETR max and satu-

The length of each frond was measured, and wet masses ration irradiance (Ik ), were estimated by using the effective of holdfasts, stipes and fronds determined. quantum yield, the photon fluence rate and the absorptance In order to assess the physiological performance of of the individual sample (G ó mez et al. 2004, see also Hanelt the D. antarctica individuals in the initial samples and on et al. 1997a,b and Bischof et al. 1998a,b ). The photosynthe- the day of sinking, the chlorophyll a fluorescence of pho- sis-irradiance characteristics were fitted to photosynthesis tosystem II (PSII), i.e., the maximal quantum yield (F v /Fm ), models without (Webb et al. 1974 ) or with photoinhibition and the relative electron transport rate were measured. (Platt et al. 1980 ). Additionally, the non-photochemical In vivo chlorophyll fluorescence of PSII was determined quenching (NPQ) capacity of the algal samples was calcu- with a portable pulse modulation fluorometer (PAM 2500, lated according to Govindjee (1995) . Walz, Effeltrich, Germany). Three blade samples were taken with a cork borer from the frond of the main stipe of the eight initial D. antarctica individuals and on the day Statistical analyses of sinking for each thallus. The samples were cleaned of epibionts with seawater. They were incubated for 20 min Floating persistence was analyzed using Kaplan-Meier in darkness and measured six times for maximal quantum survival analysis. The different Kaplan-Meier survival yield (Fv /Fm ). The maximal quantum yield represents a curves were compared with the Peto-Wilcoxon test. A. Graiff et al.: Floating duration of kelps 7

Algae wet mass and length at day 0, as well as float- with the curves of the other seasons, and the fall curve ing persistence, were analyzed with one-way ANOVA. The compared to the winter curve, revealed significant differ- biomass and length loss while floating were log-trans- ences (Peto-Wilcoxon test, Table S3 ). The floating persis- formed before being analyzed with a one-way ANOVA. The tence in summer (22 ± 4.6 days; median ± SD) with higher comparisons between the initial wet mass of holdfasts, water temperature and stronger solar radiation (Table 1) stipes and fronds (per season n = 8), and the final wet was significantly reduced compared to the other seasons mass of holdfasts, stipes and fronds on the day of sinking (winter: 33 ± 5.7 days; spring: 38 ± 5.4 days; fall: 41 ± 6.1 days; (winter: n = 19; spring: n = 21; summer: n = 24; fall: n = 28) median ± SD) (one-way ANOVA with post hoc Tukey ’ s test, = < were done with a two-way ANOVA. The two factors were F 3,68 27.0, p 0.0001; Table S4 ). Comparison was done only season (winter, spring, summer and fall) and type of alga for the central range of alga masses (2000 – 14,000 g); in (initial algae, sunk algae). Correlation of total algal mass at this range, there were no seasonal differences in algal = = day 0 with floating persistence was analyzed with a Pear- weight at day 0 (one-way ANOVA, F 3,68 2.495, p 0.05; son ’ s correlation test for each season. Data were tested for Figure 2 , see gray bar). normality with the Shapiro-Wilk test and for homogene- There was no relationship between total algal weight ity with the Levene’ s test and transformed, if necessary, at day 0 and floating persistence in winter, spring and to comply with requirements. When the ANOVA revealed fall (Pearson correlation: winter: r = 0.066, n = 19, p = 0.789; significant differences, a post hoc Tukey ’ s honest signifi- spring: r = 0.23, n = 20, p = 0.923; fall: r = 0.03, n = 28, p = 0.88), cant difference test was applied. Data were analyzed using but there was a correlation in summer (Pearson correla- the R software (R Development Core Team 2011 ) and SPSS tion, summer: r = 0.542, n = 24, p = 0.006; Figure 2). Statistics 20 (IBM, Armonk, NY, USA). Sinking of thalli was linked to a strong change in biomass distribution, and the total length of the frond was considerably reduced (Figure 3 ). The algae lost 80 – 81 % Results of their total lengths from day 0 to the day of sinking in all seasons. The mass of the stipes and holdfasts did not differ between the initial individuals and the experimen- Floating persistence and morphological tal algae on their days of sinking (two-way ANOVA, stipe: changes = = = = F1,122 0.02, p 0.887; holdfast: F 1,122 2 . 6 , p 0.111; Table S5 ). However, the masses of the fronds differed considerably In spring and fall, 85– 100 % of the floating kelps survived (86 – 91 % ) between the initial algae and the experimental for 30 or more days. In winter, 68% survived for ≥ 30 days, algae on their days of sinking (two-way ANOVA, source of but in summer no alga survived until day 30 and the first thallus sank by day 9 (Figure 1 ). The floating persistence of D. antarctica was significantly different between the χ2 = < seasons (Peto-Wilcoxon test, 3 108, p 0.001). In detail, 60 the summer survival curve of D. antarctica in comparison Winter Spring 50 Summer Fall Winter Spring Summer Fall 40 100

30 80 40

20 60 20 Floating persistence (days) 40 10 0 0 5000 10,000 15,000

Floating algae (%) 20 0 0 5000 10,000 15,000 20,000 25,000 Total weight day 0 (g) 0 0 10 20 30 40 50 60 Days of floating Figure 2 Durvillaea antarctica : relation between wet mass of exper- imental individuals on day 0 and floating persistence (winter: n = 19, Figure 1 Durvillaea antarctica : survival of floating individuals September; spring: n = 20, November/December; summer: n = 24, during different seasons (winter: n = 19, September; spring: n = 20, February/March; fall: n = 28, June). The gray bar represents the November/December; summer: n = 24, February/March; fall: n = 28, central range of algal masses (2000 – 14,000 g). The small inserted June). panel shows summer-only data (y = 0.0015x + 17.401; n = 24). 8 A. Graiff et al.: Floating duration of kelps

12,000 A

600 10,000

8000 400 6000 Fronds (g)

Total length (cm) Total 4000 200

2000

0 0 Day 0 sinking Day 0 sinking Day 0 sinking Day 0 sinking B Winter Spring Summer Fall

Figure 3 Durvillaea antarctica: total lengths of experimental algae 600 on day 0 (winter: n = 19, August; spring: n = 20, October; summer: n = 24, February; fall: n = 28, May) and on their days of sinking (winter: n = 19, September; spring: n = 20, November/December; summer: 400 n = 24, February/March; fall: n = 28, June). Horizontal lines represent the median; boxes, the interquartile range; whiskers, 1.5 × of inter- quartile range; circles, the outliers; and squares, extreme values. Stipe (g) 200

= < variation: initial vs. final frond mass F 1,122 165.5, p 0.001; Figure 4 and Table S5). 0 The daily biomass and length losses were 2% in winter, spring and fall (Figure 5 ). However, in summer, the losses 2000 C were almost 4 % and significantly higher than during the other seasons (one-way ANOVA with post hoc Tukey ’ s test, = = < 1500 biomass loss: F 3,89 22.1; length loss: F3,89 20.1, p 0.001 for both comparisons; Figure 5).

1000

Photosynthetic characteristics Holdfast (g)

500 The initial algae from winter, spring and fall had the highest relative maximal electron transport rates (ETR max ). The PI curve of the initial individuals from summer was 0 lower than that of individuals from the other seasons Initial sinking Initial sinking Initial sinking Initial sinking Winter Spring Summer Fall (Figure 6 ). Light-saturated photosynthesis (ETRmax ) varied between the initial algae and the experimental algae on Figure 4 Durvillaea antarctica: wet masses of fronds (A), stipes (B) their days of sinking but only slightly between the seasons and holdfasts (C) of the initial algae (initial: n =8 in winter, spring, = (Table 3 and Figure 6). The comparison of ETRmax between summer and fall) and those on their days of sinking (winter: n 19, initial status and day of sinking showed that it declined in September; spring: n =20, November/December; summer: n =24, = winter and summer by about 50 % , but in spring and fall February/March; fall: n 28, June). Horizontal lines represent the median; boxes, the interquartile range; whiskers, 1.5 × of interquar- it was only slightly reduced. The initial individuals from tile range; circles, the outliers; and squares, extreme values. summer had lower ETRmax values than those from winter, spring and fall (Figure 6).

Values of the maximal quantum yield (Fv /Fm ) were seasons coinciding with the onset of stronger solar radia- reduced on the day of sinking in comparison to the initial tion and higher water temperatures in summer (Table 2). status of the algae (Figure 7 ). This effect was particularly In the initial individuals, Fv /Fm was higher in winter than strong in summer. There were differences between the in the other seasons (Figure 7). A. Graiff et al.: Floating duration of kelps 9

A Winter Spring Summer Fall 0 Light saturation points (Ik ) varied between the seasons from 109 to 185 μmol photons m -2 s -1 for the -1 initial algae and from 89 to 165 μ mol photons m-2 s -1 for the experimental algae on their days of sinking. -2 The values of I k were lower on the day of sinking in com- a parison to the initial status of D. antarctica individuals a -3 a and lower in summer compared to the other seasons (Table 3). Biomass loss per day (%) -4 The initial algae in fall and summer had higher values

b of NPQ than those in winter and spring. This photo- -5 protective mechanism via heat dissipation was lower on the day of sinking than at the outset in all seasons, but B Winter Spring Summer Fall 0 especially so in summer and fall (Table 3).

-1

-2 Discussion a a -3 a Floating D. antarctica individuals persisted at the sea surface for more than 1 month during the moderate envi- -4 Length change per day (%) ronmental conditions (cool water temperature and low solar radiation) prevailing in winter, spring and fall. -5 b Higher water temperatures and solar radiation in summer were correlated with significant biomass losses and rapid Figure 5 Durvillaea antarctica : loss of biomass (A) and length (B) destruction of the floating kelps. The floating potential of per day in floating individuals from the start of the experiment to the D. antarctica appears to be strongly influenced by these day of sinking (winter: n = 19, September; spring: n = 20, November/ December; summer: n = 24, February/March; fall: n = 28, June); values environmental factors. At the study site, all kelp rafts are means ± SD. Different lowercase letters indicate significantly dif- degraded over time, albeit more rapidly during some ferent means (p < 0.05; one-way ANOVA with post hoc Tukey’ s test). seasons than during others.

120 120 Winter Spring

100 100

80 80

60 60 rETR rETR 40 40

20 20

0 0 120 Summer120 Fall

100 100

80 80

60 60 rETR rETR 40 40

20 20

0 0 0 500 1000 1500 0 500 1000 1500 PFD (μmol m-2 s-1) PFD (μmol m-2 s-1)

Figure 6 Durvillaea antarctica : photosynthesis-irradiance curves (relative electron transport rate as a function of increasing photon fluence rates) of the initial kelp individuals (open symbols: n = 8 in winter, spring, summer and fall) and experimental thalli on their day of sinking (filled symbols: winter: n = 19, September; spring: n = 20, November/December; summer: n = 24, February/March; fall: n = 28, June) in the different experimental seasons. Data expressed as the mean for every thallus. 10 A. Graiff et al.: Floating duration of kelps

Photosynthesis-irradiance Non-photochemical in microbial degradation might occur, resulting in exten- Curve parameters quenching sive tissue losses. Additionally, high water temperature μ μ accelerates herbivore consumption of rafts (Rothä usler ETRmax ( mol I k ( mol e m-2 s-1 ) photons m-2 s-1 ) et al. 2011c), but this was not observed for D. antarctica , which seems to suffer less from grazing impacts and epi- Winter Initial 95.5 ± 23.3 184.6 ± 51.8 3.1 ± 1.3 biont load than other floating algal species. In temper- Sinking 50.8 ± 44.9 123.9 ± 112.1 1.2 ± 0.7 ate regions, floating macroalgae appear to survive best Spring in waters with temperatures ranging from 5° C to 20° C. In Initial 88.5 ± 28.7 145.9 ± 52.3 2.8 ± 0.8 microcosm experiments, the floating persistence of tem- ± ± ± Sinking 74.6 66.5 164.8 129.8 2.4 2.1 perate Ascophyllum nodosum (L.) Le Jolis and Fucus vesic- Summer ulosus L. from the southwestern North Sea was reduced at Initial 71.1 ± 19.6 109.4 ± 19.5 3.5 ± 0.6 ° Sinking 36.4 ± 41.5 89.3 ± 66.9 0.3 ± 0.1 temperatures of 15 – 18 C (Vandendriessche et al. 2007a ). Fall These algae lose their floating capacity when subjected Initial 107.9 ± 31.1 140.2 ± 34.7 3.5 ± 1.0 to thermal stress by floating into warmer regions. Conse- Sinking 76.9 ± 75.2 138.5 ± 129.2 0.7 ± 0.5 quently, high water temperatures seem to be responsible for the rapid demise and sinking of floating algae in tem- Table 3 Durvillaea antarctica : physiological responses of initial perate regions. individuals (initial; n = 8) and those on the day of sinking (winter: n = 19, September; spring: n = 20, November/December; summer: Additionally, the influence of intense solar radiation n = 24, February/March; fall: n = 28, June). in summer might have further suppressed the floating Values are shown as means ± SD. persistence in D. antarctica. A comparison between irra- diations in summer and winter along a geographic gradi- ent in shows that, at least during summer Algae exposed at the sea surface at any given location, all organisms are exposed to a gen- erally high effectively damaging UV radiation (Vernet The conditions at the sea surface affected the physiological et al. 2009 ). However, employing various photoprotec- performance of floating D. antarctica during all seasons. tive mechanisms, some floating algae can acclimate to The higher water temperatures in summer apparently the stressful conditions of extreme irradiance at the sea contributed to the reduced persistence of kelp rafts. High surface and even continue to grow. For example, Macro- temperatures often result in metabolic deficiencies and cystis pyrifera (L.) C. Ag. responds to high solar irradi- destroyed tissue. In these damaged tissues, an increase ance by reducing pigment contents and protecting the photosynthetic apparatus against excessively absorbed radiation by energy dissipation via heat (Roth ä usler et al. 2011a,b ). At low latitudes, these photoacclimation 100 responses were costly for M. pyrifera, as reflected in an overall diminished growth response and reduced repro- 80 ductive investment (see also Macaya et al. 2005 ). These data imply a lower persistence of floating algae due to 60 combined effects of high water temperatures and high radiation (Rothä usler et al. 2011b). 40 Our data on the photosynthetic performance of D. antarctica are in agreement with those of G ó mez 20 and Huovinen (2011). This infralittoral kelp had low Relative maximal quantum yield (%)

0 to moderate light requirements for photosynthesis, as Initial sinking Initial sinking Initial sinking Initial sinking reflected in the initial values for light saturation of the Winter Spring Summer Fall = μ -2 -1 initial individuals (I k 110 – 185 mol photons m s ). In Figure 7 Durvillaea antarctica : relative maximal quantum yields addition, at the beginning of each experiment, D. antarc- of the initial kelp individuals (n = 8 in winter, spring, summer and tica had high F v /Fm and NPQ values, which substantially fall) and of the experimental thalli on the days of sinking (winter: decreased until sinking, suggesting advanced degrada- n = 19, September; spring: n = 20, November/December; summer: n = 24, February/March; fall: n = 28, June) in the different experimen- tion. Although the use of the maximal quantum yield tal seasons. The means and SDs of the measured values of winter as a “ health indicator ” for photosynthetic organisms is = initial individuals (F v /Fm 0.72) were normalized to 100% . widespread in ecophysiological studies (Maxwell and A. Graiff et al.: Floating duration of kelps 11

Johnson 2000 ), this parameter may be influenced by Influence of seasonal environmental various physiological and environmental conditions variations on floating algae (Nitschke et al. 2010 ). Non-photochemical quenching regulation data may therefore better reflect the actual The acclimation potential to changing environmental physiological state under stress. influences (Bischof et al. 2002 ) may produce varying While floating at the sea surface in summer with physiological responses between the seasons of floating high solar radiation, some parts of the fronds of algae at the sea surface. Additionally, the seasonal repro- D. antarctica developed red-brown necrotic areas, ductive pattern of the algae might influence the acclima- which turned soft and morbid. These probably sun- tion and floating potential of kelp rafts. Durvillaea antarc- burnt thallus parts caused substantial tissue losses in tica is primarily reproductive during the winter months the floating fronds. Similar observations of sunburn (Santelices et al. 1980 , Collantes et al. 2002 ), and during had been reported for the fronds of floating Hormosira that time period, the alga allocates a large part of its energy banksii (Turner) Decne, which become dark brown in to reproduction. This might explain the observed decrease color and then dry and brittle (McKenzie and Bellgrove in ETRmax during winter and the slightly lower survival 2008 ). In the latter species, phlorotannins deposited in of kelp rafts during that season compared to spring and the peripheral tissue of the thallus are photo-oxidized fall. For Sargassum species, Yatsuya (2008) found that, under high insolation leading to the change in color with progressing reproductive stage, the floating ability described (Schoenwaelder 2002 ). Individuals of Asco- of these species decreases. However, Yatsuya’ s study did phyllum nodosum that had been transplanted to the not examine the influence of seasonal variations in extrin- upper shore during summer also showed similar sun- sic factors, which play an important role in the longevity burnt lesions and died faster than individuals trans- of floating D. antarctica thalli. In addition, the seasonal planted during the winter (Stengel and Dring 1997 ). growth and recruitment rhythms of the benthic popula- Generally in algae damaged by strong solar radiation, tions during summer result in smaller thalli, which have the sunburn only penetrates the superficial cell layers reduced photosynthetic efficiency. However, these young (Schoenwaelder 2002 ), but this can influence the thalli grow at higher daily rates during summer than during reproductive output. Over the summer period, intense the other seasons (Santelices et al. 1980 ). Therefore, this insolation and heating probably alter the reproductive seasonally variable investment in growth or reproduction ability of floating H. banksii because tissue surrounding might result in different responses of the algae between the conceptacles is severely damaged (McKenzie and winter and summer. These intrinsic differences are proba- Bellgrove 2008 ). This would then substantially reduce bly enforced by extrinsic factors such as seasonal changes the dispersal potential of these floating algae, because in water temperature and solar radiation. photosynthetically active tissues, which provide energy Over the seasons, the photosynthetic performance for physiological acclimation, are destroyed. The red- and acclimation potential to stress conditions (e.g., NPQ) brown necrotic parts observed in D. antarctica may of D. antarctica varied, probably in relation to growth also be promoted by desiccation and high water tem- and physiological conditions. The length and mass of peratures, but this probably depends on the degree of D. antarctica individuals on day 0 differed between the buoyancy of the alga. If exposure of the algae at the sea seasons, which may have influenced the floating persis- surface causes desiccation and tissues pass beyond a tence in summer. However, similarly sized plants survived critical cellular water content, non-reversible damage for shorter times during summer than during the other occurs (Dring and Brown 1982 ). However, in Fucus seasons (Figure 2), suggesting that the smaller sizes of serratus L., desiccated thalli are less sensitive to light individuals from summer did not affect the seasonal vari- and thus inhibitory effects on photosynthesis are only ations in the survival of floating thalli. In all seasons, the minor (Huppertz et al. 1990 ). Therefore, desiccation photosynthetic activity of the floating algae on the day of might counteract the deleterious effects of excessive sinking was dramatically reduced compared to the initial irradiation to a certain extent, as also reported for the algae. On their days of sinking, the algae were dying, as red alga Porphyra perforata J. Agardh (Ö quist and Fork reflected in low values of maximal quantum yield, NPQ

1982). Considering the wave-exposed natural habitat of and ETRmax , but during the days before sinking the algae D. antarctica , it is likely that positive desiccation effects had viable tissues, suggesting a high dispersal potential (if they exist in this species) are likely of only very short as long as they stay afloat. duration, rapidly becoming highly detrimental for the Some studies report an increase in relative abun- alga. dance of floating seaweed species during particular 12 A. Graiff et al.: Floating duration of kelps seasons (Yoshida 1963 , Kingsford 1992 , Ing ó lfsson 2000 , correspondence of genetic disjunctions in D. antarctica Hirata et al. 2001 , Hinojosa et al. 2010 ). The presence of indicates that habitat discontinuity drives genetic isola- floating seaweeds seems to be closely linked to intrinsic tion among established kelp populations (Fraser et al. seasonal reproductive and growth cycles and especially 2010b ). The present study was conducted at the northern to the maximum growth in benthic populations of the distribution limit of D. antarctica (Fraser et al. 2010b ), species. For example, in Sargassum muticum (Yendo) yet, in all seasons, some or all kelp rafts survived for Fensholt, breakage and floating of reproductive thalli are 1 month or more at the sea surface. These findings imply considered an integral part of its life cycle contributing to that within the central part of the geographic distribu- the dispersal and invasion success of this species (Arenas tion of this species the probability of persistence at the and Fern á ndez 2000 , Harries et al. 2007 ). Additionally, sea surface is likely much higher. Therefore, we suggest physical factors such as storms and wave action, which that in southern Chile detached D. antarctica individuals are season dependent, cause algal detachment and lead might be able to stay afloat for several months without the to a higher supply of floating thalli in certain seasons. strong seasonal effects that we observed. Consequently, these seasonal variations in abundances of In the face of climate change and increasing global floating algae are probably due to a combination of physi- temperatures, understanding of the physiological ological and abiotic parameters. responses of floating algae is important in order to predict The seasonal differences in floating persistence of their dispersal potential (Macreadie et al. 2011 ). In many D. antarctica at the sea surface were most likely due to the areas of the world’ s oceans, sea surface temperatures variation in solar radiation and water temperatures. For have substantially increased over the past decades and example, UV radiation in southern Chile (39° S) has strong are thought likely to continue increasing in the future seasonal variation and the risk of damaging UV exposure (Lima and Wethey 2012 ). This, together with shifts in solar is 37 times higher in summer than in winter (Huovinen et radiation, might strongly affect the survival of floating al. 2006 ). Further factors with strong seasonal changes are algae, potentially reducing the distances and frequencies wind, water movement and cloudiness. Winds and clear of rafting dispersal. Studies on other floating algae are skies are more frequent in summer and strongly coupled needed to better evaluate these changes and their impli- with increased solar radiation, but seasonal variability is cations on a global scale. high for all these environmental factors (Herná ndez et al. 2012 ). Acknowledgements: We gratefully thank German Penna, Freddy Gonz á lez, Lorena Jorquera, Andr é -Philippe Drapeau Picard, Miguel Penna, Jose Pantoja and David Implications Jofre for their invaluable help and assistance in the field and during the experiments. This research was supported Durvillaea antarctica is one of the most common float- by FONDECYT grant 1100749 to FT and MT. AG and SM are ing seaweeds in the southern hemisphere. This species grateful for the financial support by the fellowship pro- occurs in the SE Pacific along the Chilean coast (Hay grams PROMOS and RISE, respectively, from the German 1994 , Macaya et al. 2005 , Hinojosa et al. 2007 , 2011) and Academic Exchange Service (DAAD). Finally, we thank around Tasmania and New Zealand (Edgar 1987 , Kingsford two anonymous reviewers who helped to improve this 1992 ). The wide distribution of D. antarctica appears to manuscript. reflect the unique buoyancy of the blades that allow this species to float over long distances and colonize unoccu- Received 15 August, 2012; accepted 22 September, 2012; online first pied habitats (Hay 1994 ). However, in central Chile, the 19 October, 2012

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