Survival of juvenile Ecklonia radiata sporophytes after canopy loss

Journal of Experimental Marine Biology and Ecology 349 (2007) 170 – 182 www.elsevier.com/locate/jembe

Survival of juvenile Ecklonia radiata sporophytes after canopy loss Benjamin D. Toohey ⁎, Gary A. Kendrick School of Plant Biology, University of Western Australia, Crawley, 6009, WA, Australia Received 29 November 2006; received in revised form 9 May 2007; accepted 15 May 2007

Abstract The understorey beneath a canopy of the kelp Ecklonia radiata often contains juvenile sporophytes of the same species. When canopy disturbance occurs, these juvenile sporophytes are exposed to new environmental conditions. If these juvenile sporophytes survive these new conditions, then they become a ready source of kelps to rapidly form a new canopy. This study investigated the potential of preexisting juvenile sporophytes of E. radiata to survive post-disturbance conditions and contribute to the rapid formation of a new canopy. The potential of canopy recovery by recruitment of kelp from zoospores was also investigated. These processes were studied at different times during the summer and on reefs ranging in topographic complexity from simple, flat reefs to highly complex, rugose reefs. By tagging juvenile sporophytes after the adult kelp canopy was removed and monitoring them through time, it was demonstrated that most juveniles (N 50%) survived the change in conditions after canopy loss, with some juveniles going on to become members of a new canopy. Approximately 6–47% of tagged sporophytes died within 3–4 days after canopy removal possibly due to excessive photoinhibition and photostress as demonstrated by changes in photosynthetic performance (decreased alpha values) of juveniles. The potential contribution of juvenile sporophytes to the rapid formation of a new canopy appears to be dependent on the timing of canopy removal with late summer– autumn canopy loss favouring faster recovery. Topographically complex reefs had less short-term (7 days) survival of juvenile sporophytes than topographically simple reefs; however this difference was not carried through to the long-term (6 months) abundance of adult kelp in experimental clearings, which was greater on topographically complex reefs. Clearly, juvenile sporophytes in arrested development under existing canopies of the small kelp E. radiata are important for the rapid recovery of the kelp canopy once adults are lost through physical disturbance. © 2007 Elsevier B.V. All rights reserved. Keywords: Gap recovery; Kelp; Recruitment; Relief; Topography

1. Introduction Recovery of plant communities from disturbance is a central concept for ecology. In terrestrial forests, recovery from disturbance often involves growth of dormant tree seedlings to accelerate canopy recovery (Vleeshouwers et al., 1995) A similar process may occur in marine kelp

⁎ Corresponding author. Tel.: +61 8 64884733; fax: +61 8 64881001. E-mail address: [email protected] (B.D. Toohey). 0022-0981/$ - see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.jembe.2007.05.008

forests throughout the temperate world (Edwards, 2000). Algal assemblages in temperate southern and southwestern Australian waters are commonly made up of a canopy of kelp or fucalean algae with an understorey of red, green and brown foliose species. This understorey often contains juvenile kelp sporophytes (Wernberg et al., 2005). These juvenile sporophytes are not associated with the holdfasts of adults and persist in a state of arrested or slowed development (Kirkman, 1981; Kinlan et al., 2003, Edwards 2000), whereby they remain in a juvenile form until conditions are suitable for them to grow into an adult.

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These conditions usually require the loss of the associated canopy (Deysher and Dean, 1986; Graham, 1997). Disturbance in kelp beds often involves the removal of the adult canopy by either physical or biological means (Ebeling et al., 1985; Seymour et al., 1989; Dayton et al., 1992; Johnson and Mann, 1993). In Western Australia, Ecklonia radiata canopies are often disturbed by winter storms (Thomsen et al., 2004), creating a gap in the canopy which recovers through time (Kendrick et al., 2004). Growth of pre-existing juvenile sporophytes is one possible means by which kelp beds recover quickly from canopy disturbance. If these juvenile sporophytes are to contribute to the formation of a new canopy after disturbance, they must survive post-disturbance conditions (Kang et al., 2005). Once the canopy has been removed, the sporophytes are exposed to increased light, sediment deposition and possibly greater water motion (Eckman et al., 1989; Irving and Connell, 2002; Toohey et al., 2004; Wernberg et al., 2005). Canopy removal may also increase the level of grazing and sand abrasion experienced by the sporophytes. These post-disturbance conditions can be influenced by the time of year the canopy is lost. Greater downwelling irradiance can be expected in summer than in winter. Furthermore, sea conditions vary greatly between seasons. Experimental canopy disturbances made in summer months often have different recovery trajectories than similar disturbances made during winter months (Kennelly, 1987; Wood, 1987). Differences in recovery trajectory between disturbances made in different seasons may in part due to differences in post-disturbance conditions between seasons. Post-disturbance conditions are also affected by the topography of the reef on which the algae grow. Kelp beds in southwestern Australia are found on limestone reefs ranging in topographically complexity from complex, with an intricate system of channels, crevices and overhangs, to simple with only a flat pavement of reef, raised slightly above the seafloor (Harman et al., 2003). These two reef types have significantly different physical environments (Toohey, 2007), which may influence the survival of preexisting juvenile sporophytes. Topographically complex reefs have greater irradiance and more turbulent water motion than topographically simple reefs (Toohey, 2007). Topographically simple and complex reefs are sometimes referred to as low and high relief respectively [see Harman et al. (2003) and Watson et al. (2005)] as these terms have similar geomorphological definitions (Anon., 1997). Apart from development of pre-existing juvenile sporophytes, an alternative means by which the canopy recovers from disturbance is by the development of canopy species directly from zoospores that settle and develop in

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disturbed areas. This process involves the settling of zoospores onto appropriate substratum, growth of gametophytes, successful fertilisation and finally growth and survival of the newly formed sporophyte (Santelices, 1990). All of these steps are strongly influenced by the environment (Vadas et al., 1992; Fredriksen et al., 1995; Huovinen et al., 2000) and only a very small percentage of zoospores ever become adult sporophytes (Kirkman, 1981; Camus, 1994; Berger et al., 2003). This study investigates the potential of pre-existing juvenile sporophytes of E. radiata to survive post-disturbance conditions and contribute to the rapid formation of a new canopy on topographically simple, planar and topographically complex, rugose reefs. The possible source of juvenile mortality from photophysiological and biomechanical damage was also quantified. The potential of canopy recovery by recruitment of kelp from zoospores was also investigated. 2. Methods This study was conducted in Hamelin Bay (34°22′S, 115°01′E), a coastal embayment approximately 350 km south of Perth, Western Australia (Fig. 1A). The bay has many limestone reefs ranging in topographic complexity from planar platforms (simple topography) to highly rugose reefs that rise N1 m from the seafloor (complex topography). Topographically complex reefs can be found both sea-ward and lee-ward of topographically simple reefs, forming a haphazard mosaic of topographically simple and complex reefs in Hamelin Bay. All research was conducted in kelp beds with a mono-specific canopy of E. radiata. 2.1. Juvenile sporophyte survivorship after canopy removal In this study, juvenile sporophytes were defined as macroscopic sporophytes with a thallus made up of a single blade between 2 and 40 cm in length (Kirkman, 1981). To measure the survivorship of pre-existing E. radiata juvenile sporophytes after canopy disturbance, the kelp canopy was cleared in 4 m2 circles on three topographically complex reefs and three topographically simple reefs (Fig. 1B). Reefs were between 30 and 75 m apart, with the study location approximately 1.5 km from shore. Topographically simple reefs were at depths of 5– 6 m while topographically complex reefs were at depths of 1–2 m. This difference in depth is inherent to the comparison of topographically simple and complex reefs within the same location. The canopy was cleared by cutting the stipes of adult kelps close to the holdfast. Care was taken not to disturb

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Fig. 1. (A) A map of Hamelin Bay (34°22′S, 115°01′E) showing the study location which was approximately 1.5 km from shore. (B) A schematic representation of the experimental design. Note: clearings where 3–5 m apart and haphazardly located with reefs. Reefs where positioned 30–75 m apart.

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the juvenile sporophytes during this process. Pilot studies indicated that the survival of juvenile sporophytes was heavily dependant on the timing of canopy removal and hence this experiment was repeated four times (start dates: 18/03/05 late summer/autumn; 17/11/ 05 early summer; 18/01/06 mid summer; 14/03/06 late summer/autumn) to assess the influence of timing on the survivorship of juvenile sporophytes. Different clearings were made each time, with clearings interspersed by old clearing from other times. Sampling was not conducted during winter as Hamelin Bay becomes inaccessible due to frequent storms and large ocean swells which prevent boating and scuba diving. Once the canopy was removed, 30 juvenile sporophytes distributed throughout each clearing (both centre and edge) were tagged by tying a small length of labelled nylon tape around the stipe. Pilot studies indicated that tag loss (without associated loss of juvenile) was extremely low, therefore no double tagging control procedure was undertaken. Initial recruit density was estimated in all clearings made in November 2005, January 2006 and March 2006, by haphazardly placing four 0.25 m2 quadrats in each clearing and counting all juvenile E. radiata. Average initial density was found to be 6.22 ± 0.78 juveniles per 0.25 m2 (mean and std error, n = 72), with no significant differences in initial juvenile density between dates of clearance or reef topography (data not shown). After tagging, survivorship of juvenile sporophytes was then monitored each day for seven days, and then once again 30 days and approximately 6 months after clearance of the adult canopy. Juvenile sporophytes were considered dead when they were either unable to be found after considerable searching or had significant damage to their thallus and meristem including loss of thallus pigments or tissue erosion. Sampling at approximately 6 months after clearance consisted of counting the total number of adult and juvenile E. radiata in four replicate 0.25 m2 quadrats as tags were no longer visible at this time. Juvenile sporophyte survivorship was analysed with a repeated measures ANOVA because the same tagged populations were monitored repeatedly over time. In the model, date of clearing (random), reef topography (fixed) and days since clearing (fixed) were crossed with one another and reefs was the repeated random factor nested within reef topography and date of clearing. Each population (30 tagged juveniles) within a given clearing served as a replicate in this model, such that we had three replicates per reef type. A consideration when using repeated measures ANOVA is that the days since clearing × reef interaction can not be tested and must be assumed to be non-significant. In addition to the repeated measures ANOVA, sigmoidal curves were fitted to the

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survivorship data as they had parameters with ecological meaning. For the approximately 6 month density counts, separate permutational multivariate ANOVA (Anderson, 2001; McArdle and Anderson, 2001) were used due the large number of zeros in the dataset. Bray–Curtis dissimilarity was used to compare samples. The model applied was reef topography (fixed) and date of clearing (random) crossed, with reefs nested within both factors. 2.2. Photophysiological and biomechanical measurements Canopy removal is associated with an increase in light levels (Pearse and Hines, 1979; Reed and Foster, 1984; Clark et al., 2004) and possibly an increase in turbulent water motion (Eckman et al., 1989; Mork, 1996; Wernberg et al., 2005). An increase in both of these factors has the potential to cause high mortality in the juvenile sporophytes. Higher light levels could lead to photoinhibition and greater water motion could dislodge juveniles from the reefs. If severe photoinhibition occurred we expected to observe a large decline in the photosynthetic parameters alpha and ETRmax (Ralph and Gademann, 2005). If frequent dislodgment of juveniles occurred, we expected to observe an increase in the average attachment force of the remaining juvenile as weakly attached individuals were removed first. Photophysiological and biomechanical measurements of juvenile sporophytes were made before and after canopy removal to measure changes in the sporophytes to the new conditions created by the removal of the canopy. Sampling was performed for the November 2005, January 2006 and March 2006 clearings only, as equipment was unavailable in March 2005. The photophysiological state in terms of the maximum rate of electron transport (ETRmax) and alpha values of three juvenile sporophytes per clearing was assessed before canopy removal, and then again 3, 7 and 30 days after canopy clearance. Alpha values represent the lightlimited rate of electron transport from photosystem II, while ETRmax represents the maximum rate of electron transport from photosystem II when saturated light is supplied. Changes in either of these variables indicate a modification of the alga's photosynthetic performance resulting from changes in the light climate after canopy removal. A significant decline in these variables represents photoinhibition (and/or photoacclimation) which may lead to death if light levels in excess of saturation are maintained. By measuring these variables, we were able to determine the extent of light stress applied to the kelp juveniles. ETRmax and alpha was measured from rapid light curves (RLCs) generated by a Pulse Amplitude Modulated

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Fig. 2. Average (and std error) percentage survival of Ecklonia radiata juvenile sporophytes over time on topographically simple (white circles) and complex (black circles) reefs. Note the logarithmic scale for the x-axis. Non-linear regression fitted. See Table 2.

fluorometer (Diving PAM; WALZ, Germany), using standard procedures (Beer and Bjork, 2000; Beer et al., 2001; Franklin and Badger, 2001). Tissue samples were collected from the reefs in black, water-tight container and transported back to the laboratory, were they dark-adapted for a minimum of 30 min to allow reaction centres to oxidise. All RLCs were generated in a random order during the late morning (1000–1200 h) to minimise the influence of diurnal rhythms in photosynthetic performance (Sagert et al., 1997; Hader et al., 2001). An illumination interval of 30 s was used before each measurement in the RLC was taken. The actinic light intensity was set to achieve approximately five values

below the saturating irradiance. Since battery power strongly affects actinic light intensity produced by the PAM, the light intensities were re-calibrated after every five RLC recordings. ETR was calculated using individual thallus absorption values. These values were obtained by measuring the ratio of light transmitted to the Diving PAM's built in light sensor with and without the sample tissue covering the sensor and subtracting that ratio from one to give the fraction of light absorbed by the tissue, assuming minimal reflection of light from the tissue. RLCs were generated by plotting the electron transport rate (ETR) against the actinic light intensity. Non-linear curves were fitted using the software WinCurveFit 1.2.2

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(Raner, 1996), and the inverse tangential equation (Jassby and Platt, 1976). The ETRmax and alpha values were analysed separately using the same linear model as detailed for the survivorship data with an additional interaction term of days since clearing× reef (date of clearing × reef topography) included because individual juvenile sporophytes were the replicates in this model. Individual juvenile sporophytes were the replicates (rather than a population of 30 tagged juvenile as used in the survivorship analysis) because photophysiological state and biomechanical attachment are fundamentally characteristics of each individual juvenile kelp. To determine if canopy loss resulted in changes in the average biomechanical attachment properties of preexiting kelp juvenile sporophytes, the force required to dislodge juvenile sporophytes from the reefs was measured using a clamp and a spring scale. The clamp was attached to the thalli of the juvenile sporophytes and the spring scale (which was tied to the clamp) was pulled in one continuous vertical motion so that the force required to dislodge the sporophyte from the reefs could be recorded. A vertical direction of pull was used as juvenile sporophytes were clumped preventing a horizontal pull. If the thallus broke at the point of attachment to the clamp, the reading was discounted. Attachment force was measured for 3 juvenile sporophytes per clearing before canopy removal and then again 3, 7 and 30 days post canopy clearance. As well as with measuring the dislodgment force of the juvenile sporophytes, the surface area of all dislodged juvenile sporophytes was measured by tracing the outline of the sporophytes onto blank cardboard, that was then cut out and weighed. A regression of weight to known surface area for that cardboard (SA = 49.429 w, r2 = 0.999) was then used to determine the surface area of the cardboard cut-outs. The dislodgment data was analysed using the same ANOVA model as detailed for the photophysiological data but with surface area used as a co-variate to account for differences in the size of juvenile sporophytes sampled. 2.3. E. radiata recruitment onto primary substratum To measure kelp recruitment from zoospores, limestone plates were deployed onto topographically simple and complex reefs. Limestone plates were choose to replicate the nature eroded limestone which makes up the reefs in Hamelin Bay and allow primary colonisation to be documented. The plates were 450 mm long, 300 mm wide and 30 mm in profile. The limestone plates were randomly deployed in 2 m2 circular clearings in E. radiata canopy during late February

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2005 at three topographically complex and three topographically simple reefs that were between 100 and 450 m apart. The clearings in the canopy were experimentally made 6 months prior to the deployment of the tiles. One plate was anchored in the centre of each of five clearing per reef using a steel rod hammered into the substratum. Plates were left in-situ for 295 days, covering the austral autumn, winter, spring and most of summer. At the end of the deployment period, plates were collected and the number of E. radiata juvenile sporophytes present on each was recorded. This was considered to be effective recruitment as it encompassed both the settlement and post-settlement survival of kelps recruiting from zoospores. A one cm perimeter around the edge of the plates was not sampled to account for any edge effect (Foster, 1975). 3. Results 3.1. Juvenile sporophyte survivorship after canopy removal The majority of juvenile sporophytes survived the change in conditions associated with canopy loss. Canopy removal did have a significant negative effect on the survival of some juvenile sporophytes (Fig. 2, Table 1), as they lost all thallus pigmentation and eroded away, leaving only part of the stipe and a bleached holdfast. Almost all tagged juveniles were found on monitoring days indicating that tag loss without the associated loss of juvenile was extremely low in our study. After canopy removal, average survivorship across reef types dropped in a sigmoidal fashion with the greatest rate of decline often three to four days after canopy removal (Table 2, Fig. 2). This decline in survivorship was always significantly more pronounced on topographically complex reefs (Fig. 2, Table 1). The extent of this difference between reef types, however, was dependant on the date the canopy was removed (Table 1). Average survivorship of juvenile sporophytes was modelled well using a non-linear curve with r2 values all above 0.95 (Table 2). The sigmoidal nature of the curves indicates that after the initial mortality due to the change in conditions associated with canopy loss, the population of tagged juveniles stabilises and little more mortality occurs. The parameters of this model can describe many features of juvenile sporophyte survivorship. The Y0 parameter represents the percentage of the population which survives throughout time. It should be noted that this value is never less than 50% in all curves. The “a” parameter represents the percentage of the population that died during the transition to new conditions outside the canopy. The sum of Y0 and “a”

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Table 1 Repeated measures ANOVA on survivorship of juvenile sporophytes of Ecklonia radiata Levene's test

0.79, p = 0.871

Source

df

Date of clearing Days since clearing Reef topography [RT] Reef (Date of clearing, RT) Date of clearing ⁎ RT Date of clearing ⁎ days since clearing Days since clearing ⁎ RT Date of clearing ⁎ days since clearing ⁎ RT Residual

MS

F

p

3 8 1 16 3 24

209.02 118.25 682.67 20.78 155.86 13.12

1.29 9.01 4.38 9.94 6.01 1.81

0.412 b0.001 0.127 b0.001 0.004 0.077

8 24

34.42 7.27

4.74 3.48

0.001 b0.001

128

2.09

The exact error mean square can not be calculated for the test of date of clearing or date of clearing ⁎ reef topography. The Levene's test is for factors of date of clearing, reef topography and days only. RT = reef topography. All significant p-values (b0.05) are shown in bold.

equals 100 (approximately) because by definition at the beginning of the experiment (x = 0) there was 100% survivorship. The X0 and “b” parameters define the nature of mortality due to canopy removal. The X0 parameter describes the point in time with the highest rate of mortality (i.e. the position of the inflection point on the x-axis). The average X0 across all dates and reef types was four and a half days after canopy removal (4.61 ± 0.58, mean ± std error, n = 8). The “b” parameter describes the rate at which the mortality rate increases and decreases over time with high values of “b” being associated with a rapid increase and decrease in the death of juveniles (in units of % mortality per day2). The values of all these parameters are summarised in Table 2 and strongly supports the hypothesis that the date of canopy removal and reef topography strongly influence the nature of juvenile sporophyte survivorship after canopy removal. Approximately six months after canopy removal, all clearings made for the survivorship experiment had significant canopy recovery, except for those made during November 2005. There were significant differences between reef types and dates of canopy clearance for the density of adult E. radiata (Fig. 3, Table 3). There appeared to be a trend between the extent of canopy recovery and the season in which the clearances were made (Fig. 3), with clearances made earlier in summer having recovered less than those made later in summer (March 2005 and November 2005, November 2005 and January 2006, November 2005 and March 2006; p b 0.001 in pairwise comparisons of adult E. radiata density 6 months after clearance). In the November 2005 clearings, no adult

kelp thalli were present approximately six months after canopy removal but significantly higher abundances of juvenile sporophytes (Fig. 4, Table 3). In the January 2006 clearance, some canopy recovery was evident, however the greatest amount of recovery within approximately 6 months of canopy removal occurred in the March clearances of 2005 and 2006 (Fig. 3) Topographically complex reefs had significantly higher adult kelp densities approximately six months after clearance than topographically simple reefs (Fig. 3, Table 3). 3.2. Photophysiological and biomechanical measurements There was a significant change in the photosynthetic state of E. radiata juvenile sporophytes after canopy removal, with alpha values declining for surviving juvenile sporophytes (Fig. 5, Table 4). This decline was associated with changes in thallus pigmentation, with juvenile sporophytes shifting in colour from dark brown to yellow-brown. The decline in alpha values was evident three days after canopy removal in November 2005, January and March 2006 indicating a change in the number of antenna pigments with canopy loss. Differences in ETRmax occurred between different dates of canopy clearance (Table 5) with average ETRmax increasing from 17.88 ± 0.95 in November 2005 to 34.83 ± Table 2 Regression of survivorship of juvenile sporophytes of Ecklonia radiata (reef-averaged) on topographically simple and complex reefs Equation used: Y ¼ Y0 þ ½1þ

a b

Date of clearing

Reef a topography

X X0

 b

X0

Y0

R2

F, pvalue

March 2005

Complex 19.79 17.75 5.71 78.66 0.99 259.70; reef b0.001 Simple reef 13.52 27.81 6.99 85.56 0.99 296.29; b0.001 November Complex 28.29 14.22 3.68 70.39 0.98 96.00; 2005 reef b0.001 Simple reef 14.08 3.38 4.33 85.04 0.95 33.34; 0.001 January Complex 17.29 2.24 4.38 83.30 0.96 45.11; 2006 reef b0.001 Simple reef 6.75 4.02 6.32 93.29 0.97 70.17; b0.001 March Complex 47.47 4.88 2.00 53.27 0.99 1581.85; 2006 reef b0.001 Simple reef 8.73 3.63 3.46 91.54 0.98 98.93; b0.001 Four parameter logistic regression used. F and p values are from an ANOVA for the regression, df= 3, 8. a = percentage of population that die (%). b = the rate at which the mortality rate increases and decreases (% mortality per day2). X0 = the time of highest mortality rate (in days since canopy removal). Y0 = percentage of population that survives throughout time (%). All significant p-values (b0.05) are shown in bold.

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Fig. 3. Density of Ecklonia radiata adults (kelps. 0.25 m2) approximately six months after canopy removal for the March 2005, November 2005, January 2006 and March 2006 clearances on topographically simple and complex reefs. Mean and standard error shown, n = 12. Note dates ordered by extent of summer exposure rather than chronological order.

3.3. E. radiata recruitment onto primary substratum

1.38 in March 2006 (mean ± std error, n = 72). Therefore the numbers of photosynthetic units in juvenile sporophytes increased as the summer progressed. Canopy removal had no significant effect on the average force required to dislodge an E. radiata juvenile sporophyte. Although some significant differences between reefs were detected, there was no significant difference between reef types, dates of canopy clearance or days since clearing on dislodgment force (Table 6). Our sampling did detect a significant regression between dislodgment force and the surface area of juvenile sporophytes (Table 6), with greater surface area being associated with a greater force to dislodge the juvenile.

There was very little observed recruitment of E. radiata onto plates after 10 months of deployment. The number of replicate plates was reduced to 3 plates per reef due to loss of 1–2 plates per reef. All the observed recruitment did occur on topographically simple reefs with 1, 1 and 3 juvenile sporophytes observed on each of the reefs respectively. No E. radiata juvenile sporophytes were observed on plates deployed on topographically complex reefs. At the end of deployment, the plates supported a large assemblage of algae other than E. radiata (1–2 kg wet weight) suggesting the plates were suitable surfaces to algal to colonise.

Table 3 PERMANOVA of Ecklonia radiata density (kelps. 0.25 m2) approximately 6 months after canopy removal for the clearances made in March 2005, November 2005 January 2006 and March 2006 Adults

Juveniles

Source

df

MS

F

p

MS

F

p

Date of clearing Reef topography [RT] Reef (Date of clearing, RT) Date of clearing ⁎ RT Residual

3 1 16 3 72

34550.20 5708.85 1486.79 1062.54 1826.23

23.24 5.37 0.81 0.71

b0.001 0.008 0.714 0.584

7176.77 14800.78 2416.23 5784.47 2478.17

2.97 2.55 0.98 2.39

0.019 0.121 0.492 0.053

RT = Reef topography. All significant p-values (b0.05) are shown in bold.

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4. Discussion The key finding of this research is that the majority of juvenile sporophytes under the adult canopies of E. radiata survived the change in conditions associated with canopy loss, although some juvenile sporophytes were negatively affected by canopy loss. The extent of the negative influence of canopy loss was dependant on the date of clearance and the topography of the reef in which it occurred. Pre-existing E. radiata juvenile sporophytes had higher initial survivorship on topographically simple reefs after canopy loss and survivorship varied between clearings made at different times of the year. The timing of canopy loss and survivorship of juvenile sporophytes have important implications for the speed of canopy recovery. 4.1. Canopy recovery after disturbance Survival of pre-existing juvenile sporophytes is one means by which a new canopy is rapidly formed. For a new kelp canopy to form after disturbance, new kelps must occupy the disturbed area and grow to adult size. Our results suggest that survival of pre-existing juvenile sporophytes plays a major role in the rapid establishment of a new canopy. In this study, after the initial mortality associated with canopy loss, over 50% of juvenile sporophytes persisted for up to 30 days in the clearances. Canopy removal caused a significant change in the photosynthetic state of the surviving juvenile sporophytes

with decreases in alpha, consistent with photoacclimation from a shade-tolerant to a sun-adapted state (Gantt, 1990; Fairhead and Cheshire, 2004a,b). Photoacclimation is a likely explanation for why survivorship of kelp juvenile sporophytes was never less than 50% of the tagged population. Such persistence will allow these juveniles to contribute to the rapid development of a new canopy. Of these persisting juveniles, some of them grew to adult-size thalli within approximately six months of the previous canopy being lost. Personal observations when conducting the density counts of E. radiata approximately six months after canopy removal revealed the remains of tags were still present around the stipes of adult kelps occupying the March 2005, January 2006 and March 2006 clearings, demonstrating that these adult kelps were part of the tagged population of juvenile sporophytes 6 months earlier. The potential for pre-existing juvenile sporophytes to generate a new canopy after disturbance is dependant on the timing or season in which canopy removal occurs. The effect of timing of canopy loss on the response of the algal assemblage to disturbance has been observed in other algal assemblages (Wood, 1987; Kennelly, 1987, Schiel and Nelson, 1990). Clearings made at the end of summer–early autumn (i.e. March 2005) resulted in the rapid recovery of the E. radiata canopy; whereas clearing made during or at the start of summer (i.e. November 2006) resulted in slow canopy recovery. The recovery of large (314 m2) canopy clearances made in

Fig. 4. Density of Ecklonia radiata juveniles (kelps. 0.25 m2) approximately 6 months after canopy removal for the March 2005, November 2005, January 2006 and March 2006 clearances. Mean and standard error shown, n=24. Note dates ordered by period of summer rather than chronological order.

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Table 4 ANOVA of alpha of juvenile sporophytes of Ecklonia radiata before and after canopy clearance Levene's test

0.79, p = 0.868

Source

df

Date of clearing Days since clearing Reef topography [RT] Reef (Date of clearing, RT) Date of clearing ⁎ days since clearing Date of clearing ⁎ RT Days since clearing ⁎ RT Days since clearing ⁎ reef (Date of clearing, RT) Date of clearing ⁎ days since clearing ⁎ RT Residual

MS

F

p

2 3 1 12 6

0.214 0.080 b0.001 0.004 0.010

28.72 8.26 0.01 1.25 2.00

0.020 0.015 0.914 0.290 0.210

2 3 36

0.003 0.005 0.003

0.47 1.12 1.02

0.647 0.411 0.442

6

0.005

1.57

0.185

144

0.003

Non-exact F-tests for all tests except days since clearing ⁎ reef (date of clearing, RT). RT = reef topography. All significant p-values (b0.05) are shown in bold.

Hamelin Bay during late summer resulted in the initial formation of a extensive canopy of Sargassum subgenus Anthrophycus followed by a slower recovery of the kelp E. radiata over 2–3 years (Toohey et al., in press). The presence of a Sargassum canopy during the recovery process of clearances made in summer may slow the development of pre-existing juvenile sporophytes into a new kelp canopy via canopy shading. It is interesting to note that short-term differences in the survivorship of juvenile sporophytes between reefs with simple and complex topography were reversed in the adult kelp density approximately six months later suggesting that Table 5 ANOVA of ETRmax of juvenile sporophytes of Ecklonia radiata before and after canopy clearance

Fig. 5. Alpha of Ecklonia radiata juveniles before (black bars) and after (white bars) canopy removal. Mean and standard error shown (n = 18).

Levene's test

0.70, p = 0.950

Source

df

Date of clearing Days since clearing Reef topography [RT] Reef(Date of clearing, RT) Date of clearing ⁎ days since clearing Date of clearing ⁎ RT Days since clearing ⁎ RT Days since clearing ⁎ reef (Date of clearing, RT) Date of clearing ⁎ days since clearing ⁎ RT Residual

MS

F

p

2 3 1 12 6

5238.52 526.65 100.54 62.06 177.50

23.78 2.97 0.85 0.70 2.34

0.008 0.119 0.455 0.742 0.163

2 3 36

118.77 55.12 88.79

2.41 0.73 1.30

0.327 0.573 0.145

6

75.96

0.86

0.536

144

68.51

Non-exact F-tests for all tests except days since clearing ⁎ reef(date of clearing, RT). RT = reef topography. All significant p-values (b0.05) are shown in bold.

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Table 6 ANCOVA of dislodgment force in newtons of Ecklonia radiata sporophytes before and after canopy removal Levene's test

0.43, p = 1.00

Source

df

Surface area 1 Date of clearing 2 Days since clearing 3 Reef topography [RT] 1 Reef (Date of 12 clearing, RT) Date of clearing ⁎ days 6 since clearing Date of clearing ⁎ RT 2 Days since clearing ⁎ RT 3 Days since clearing ⁎ reef 36 (Date of clearing, RT) Date of clearing ⁎ days 6 since clearing ⁎ RT Residual 143

MS

F

758.47 47.78 15.84 5.58 47.50

38.56 b0.001 2.22 0.598 1.13 0.412 0.13 0.750 2.65 0.012

14.10

0.41

0.849

41.65 12.71 17.89

0.66 0.37 0.91

0.538 0.778 0.618

34.50

1.93

0.103

19.67

S = 452.089

R2 = 0.5034

Term

Coefficient SE coefficient T

Constant Surface area

8.32 0.10

p

R2(adj) = 0.2534

0.77 0.02

p

10.86 b0.001 6.21 b0.001

Surface area of sporophytes used a co-variate in the model. Not exact F-tests for all tests except days since clearing ⁎ reef (date of clearing, RT). RT =reef topography. All significant p-values (b0.05) are shown in bold.

topographically complex reefs were better environments for growth of juveniles into adults once acclimation after canopy loss had occurred. Given that an E. radiata canopy has a significant negative effect on species richness (Kendrick et al., 1999; Kendrick et al., 2004; Toohey et al., 2004; Wernberg et al., 2005), survivorship of juvenile sporophytes after canopy loss has implications for macroalgal diversity through its influence on the rate and pattern of canopy recovery. If canopy recovery is slow, for instance when clearings are made during summer, then species rich canopy gaps remain present for a longer time period. If clearings are made during late summer/winter, rapid recovery of the canopy from juvenile sporophytes will suppress species richness. By varying the rate of canopy recovery, differences in the survivorship of juvenile sporophytes after canopy loss do contribute to the high local-scale alpha diversity seen in the macroalgal assemblage of South-Western Australia (Wernberg et al., 2003; Kendrick et al., 2004). 4.2. Mortality of juvenile sporophytes after canopy loss The survival of E. radiata juvenile sporophytes after canopy loss may be inversely related to changes in light climate associated with canopy removal. As canopy

forming thalli block up to 98% of the downwelling light (Gerard, 1984; Wood, 1987; Wernberg et al., 2005), their removal causes a rapid and sudden increase in the level of light to which the juvenile sporophytes are exposed. This increase in light can lead to mortality by photoinhibition, evident as thallus bleaching in this study (Hanelt et al., 1997; Hader et al., 2001; Altamirano et al., 2004). Bleaching of crustose corallines is commonly observed after canopy removal (Figueiredo et al., 2000; Irving et al., 2004; Irving et al., 2005). Light levels after canopy loss may be related to the timing of canopy removal. During sunny weather conditions, such as during March 2006 (pers. obs.), higher light levels were associated with increased short-term mortality. Wood (1987) found that removal of E. radiata canopy during summer lead to great ultra-violet damage to juvenile kelp than removal of the canopy during winter. Water clarity at the time of canopy removal may also influence the magnitude of the change in light levels. Furthermore, the extent of the increase in light levels caused by the removal of the canopy was also dependant on the topography of the reef in which the clearing was made. We believe that the lower light levels on topographically simple reefs (Toohey, 2007) lead to greater survivorship of juveniles. Increases in light levels after canopy loss are greater on topographically complex reefs as these reefs have more downwelling light than their topographically simple counterparts (Toohey, 2007). Mortality of E. radiata juvenile sporophytes after canopy removal does not appear to be due to biomechanical dislodgement of juvenile sporophytes, nor do sporophytes appear to alter their biomechanical attachment properties when the canopy is removed. Of those sporophytes which died, very few disappeared entirely (i.e. lost by dislodgment), with the majority of dead juvenile sporophytes leaving behind a bleached stipe and holdfast with the tag still attached. Juvenile sporophytes in the clearings appeared to sway with the passing of swells across the reefs, bending at their stipe to reduce the drag produced by their thalli (Biedka et al., 1987; Friedland and Denny, 1995). These observations lend credence to an underlying assumption of this research; that during storm events, juvenile kelps are often left attached to the reefs while adult thalli are lost. 5. Conclusions This research lends support to the idea that juvenile sporophytes present in the understorey before disturbance can act as a mechanism for rapid recovery of the canopy. By photoacclimating to the new conditions after disturbance, a large percentage of the juvenile sporophytes survive and

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become an immediate supply of kelps to make up the new canopy. The extent to which this source of ready sporophytes contributes to canopy recovery varies with the timing of canopy removal. Short-term differences in juvenile sporophyte survival between topographically simple and complex reefs were not carried into the abundance of adults and juveniles kelps 6 months after disturbance. The sporophyte mortality which does occur after canopy removal is most likely due to high light levels causing thallus bleaching. Acknowledgements For providing help in the field, we would to thank Dave Abdo, Cain Delacy, Patrick Toohey, Emyrs Casali, Ben Saunders; George Shedrawi; Di Waston; Eloise Brown; Kylie Cook; Melissa White and Dave Gull. For supplying research funds, we thank the Australia Research Council and the University of Western Australia. For comments which improved this manuscript, we thank Robert Anderson, Thomas Wernberg and three anonymous reviewers. [RH] References Altamirano, M., Murakami, A., Kawai, H., 2004. High light stress in the kelp Ecklonia cava. Aquat. Bot. 79, 125–135. Anderson, M.J., 2001. A new method for non-parametric multivariate analysis of variance. Austral. Ecol. 26, 32–45. Anon., 1997. In: Jackson, J.A. (Ed.), Glossary of Geology. American Geological Institute, Virginia, p. 669. Beer, S., Bjork, M., 2000. Measuring rates of photosynthesis of two tropical seagrasses by pulse amplitude modulated (PAM) fluorometry. Aquat. Bot. 66, 69–76. Beer, S., Biork, M., Gademann, R., Ralph, P., 2001. Measurement of photosynthetic rates in seagrasses. In: Short, F.T., Coles, R.G., Short, C.A. (Eds.), Global Seagrass Research Methods. Elsevier Science B.V., Amsterdam, pp. 190–198. Berger, R., Henriksson, E., Kautsky, L., Malm, T., 2003. Effects of filamentous algae and deposited matter on the survival of Fucus vesiculosus L. germlings in the Baltic Sea. Aquat. Ecol. 37, 1–11. Biedka, R.F., gosline, J.M., De Wreede, R.E., 1987. Biomechanical analysis of wave-induced mortality in the marine alga Pterygophora californica. Mar. Ecol. Prog. Ser. 36, 163–170. Camus, P.A., 1994. Recruitment of the intertidal kelp Lessonia nigrescens Bory in northern Chile: successional constraints and opportunities. J. Exp. Mar. Biol. Ecol. 184, 171–181. Clark, R.P., Edwards, M.S., Foster, M.S., 2004. Effects of shade from multiple kelp canopies on an understory algal assemblage. Mar. Ecol. Prog. Ser. 267, 107–119. Dayton, P.K., Tegner, M.J., Parnell, P.E., Edwards, P.B., 1992. Temporal and spatial patterns of disturbance and recovery in kelp forest community. Ecol. Monogr. 62 (3), 421–445. Deysher, L.A.E., Dean, T.A., 1986. In situ recruitment of sporophytes of giant kelp, Macrocystis pyrifera (L.) C. A. Agardh: effects of physical factors. J. Exp. Mar. Biol. Ecol. 103, 41–63.

181

Ebeling, A.W., Laur, D.R., Rowley, R.J., 1985. Severe storm disturbances and reversal of community structure in a southern California kelp forest. Mar. Biol. 84, 287–294. Eckman, J.E., Duggins, D.O., Sewell, A.T., 1989. Ecology of understory kelp enviroment I. effects of kelps on flow and particle transport near the bottom. J. Exp. Mar. Biol. Ecol. 129, 173–187. Edwards, M.S., 2000. The role of alternative life history stages of marine macroalga: a seed bank analogue? Ecology 81 (9), 2404–2415. Fairhead, V.A., Cheshire, A.C., 2004a. Rates of primary productivity and growth in Ecklonia radiata measured at different depths, over an annual cycle, at West Island, South Australia. Mar. Biol. 145, 41–50. Fairhead, V.A., Cheshire, A.C., 2004b. Seasonal and depth related variation in the photosynthesis-irradiance response of Ecklonia radiata (Phaeophyta, Laminariales) at West Island, South Australia. Mar. Biol. 145, 415–426. Figueiredo, M.Ad.O., Kain (Jones), J.M., Norton, T.A., 2000. Responses of crustose corallines to epiphyte and canopy cover. J. Phycol. 36, 17–24. Foster, M.S., 1975. Regulation of algal community development in a Macrocystis pyrifera forest. Mar. Biol. 32, 331–342. Franklin, L.A., Badger, M.R., 2001. A comparison of photosynthetic electron transport rates in macroalgae measured by pulse amplitude modulated chlorophyll fluorometry and mass spectrometry. J. Phycol. 37, 756–767. Fredriksen, S., Sjotun, K., Eiliv Lein, T., Rueness, J., 1995. Spore dispersal in Laminaria hyperborea (Laminariales, Phaeophyceae). Sarsia 80, 47–54. Friedland, M.T., Denny, M.W., 1995. Surviving hydrodynamic forces in a wave-swept environment: Consequences of morphology in the feather boa kelp, Egregia menziesii (Turner). J. Exp. Mar. Biol. Ecol. 190, 109–133. Gantt, E., 1990. Pigmentation and photoacclimation. In: Cole, K.M., Sheath, R.G. (Eds.), Biology of Red Algae. Cambridge University Press, Cambridge, pp. 203–219. Gerard, V.A., 1984. The light environment in a giant kelp forest: influence of Macrocystis pyrifera on spatial and temperal variability. Mar. Biol. 84, 189–195. Graham, M.H., 1997. Factors determing the upper limit of giant kelp, Macrocystis pyrifera Agardh, along the Monterey Peninsula, central California. J. Exp. Mar. Biol. Ecol. 218, 127–149. Hader, D.P., Porst, M., Lebert, M., 2001. Photoinhibition in common atlantic macroalgae measured on site in Gran Canaria. Helgol. Mar. Res. 55, 67–76. Hanelt, D., Christian, W., Karsten, U., Nultsch, W., 1997. Photoinhibition and recovery after high light stress in different developmental and lifehistory stages of Laminaria saccharina (Phaeophyta). J. Phycol. 33, 387–395. Harman, N., Harvey, E.S., Kendrick, G.A., 2003. Differences in fish assemblages from different reef habitats at Hamelin Bay, southwestern Australia. Mar. Freshw. Res. 54, 177–184. Huovinen, P.S., Oikari, A.O.J., Soimasuo, M.R., Cherr, G.N., 2000. Impact of UV radiation on the early development of the giant kelp (Macrocystis pyrifera) gametophytes. Photochem. Photobiol. 72 (3), 308–313. Irving, A.D., Connell, S.D., 2002. Sedimentation and light penetration interact to maintain heterogeneity of subtidal habitats: algal versus invertebrate dominated assemblages. Mar. Ecol. Prog. Ser. 245, 83–91. Irving, A.D., Connell, S.D., Elsdon, T.S., 2004. Effects of kelp canopies on bleaching and photosynthetic activity of encrusting coralline algae. J. Exp. Mar. Biol. Ecol. 310, 1–12. Irving, A.D., Connell, S.D., Johnston, E.L., Pile, A.J., Gillanders, B.M., 2005. The response of encrusting coralline algae to canopy loss: an

182

B.D. Toohey, G.A. Kendrick / Journal of Experimental Marine Biology and Ecology 349 (2007) 170–182

independant test of predictions on an Antarctic coast. Mar. Biol. 147, 1075–1083. Jassby, A.D., Platt, T., 1976. Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnol. Oceanogr. 21 (4), 540–547. Johnson, C.R., Mann, K.H., 1993. Rapid succession in subtidal understorey seaweeds during recovery from overgrazing by sea urchins in Eastern Canada. Bot. Mar. 36, 63–77. Kang, R.S., Park, H.S., Won, K.S., Kim, J.M., Levings, C., 2005. Competition as a determinant of the upper limit of the subtidal kelp Ecklonia stolonifera Okamura in the southern coast of Korea. J. Exp. Mar. Biol. Ecol. 314, 41–52. Kendrick, G.A., Harvey, E., Wernberg, T., Harman, N., Goldberg, N., 2004. The role of disturbance in maintaining diversity of benthic macroalgal assemblages in southern Australia. Jap. J. Phycol. 52, 5–9 (Supplement). Kendrick, G.A., Lavery, P.S., Phillips, J.C., 1999. Influence of Ecklonia radiata kelp canopy on structure of macro-algal assemblages in Marmion Lagoon, Western Australia. Hydrobiologia 399, 275–283. Kennelly, S.J., 1987. Physical disturbances in an Australian kelp community. I. Temporal effects. Mar. Ecol. Prog. Ser. 40, 145–153. Kinlan, B.P., Graham, M.H., Sala, E., Dayton, P.K., 2003. Arrested development of giant kelp (Macrocystis pyrifera, Phaeophyceae) embryonic sporophytes: a mechanism for delayed recruitment in perennial kelps? J. Phycol. 39, 47–57. Kirkman, H., 1981. The first year in the life history and the survival of juvenile marine macrophyte, Ecklonia radiata (Turn.) J. Agardh. J. Exp. Mar. Biol. Ecol. 55, 243–254. McArdle, B.H., Anderson, M.J., 2001. Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82 (1), 290–297. Mork, M., 1996. The effect of kelp in wave damping. Sarsia 80, 323–327. Pearse, J.S., Hines, A.H., 1979. Expansion of central California kelp forest following the mass mortality of sea urchins. Mar. Biol. 51, 83–91. Ralph, P.J., Gademann, R., 2005. Rapid light curves: a powerful tool of assess photosynthetic activity. Aquat. Bot. 82, 222–237. Raner, K., 1996. WinCurve Fit version 1.2.2. Reed, M.S., Foster, D.C., 1984. The effects of canopy shading on algae recruitment and growth in a giant kelp forest. Ecology 65 (3), 937–948. Sagert, S., Forster, R.M., Feuerpfeil, P., Schubert, H., 1997. Daily course of photosynthesis and photoinhibition in Chondrus crispus (Rhodophyta) from different shore levels. Eur. J. Phycol. 32, 363–371.

Santelices, B., 1990. Patterns of reproduction, dispersal and recruitment in seaweeds. Oceanogr. Mar. Biol. Ann. Rev. 28, 177–276. Schiel, D.R., Nelson, W.A., 1990. The harvesting of macroalgae in New Zealand. Hydrobiologia 204/205, 25–33. Seymour, R.J., Tegner, M.J., Dayton, P.K., Parnell, P.E., 1989. Storm wave induced mortality of gain kelp, Macrocystis pyrifera, in Southern California. Estuar. Coast. Shelf Sci. 28, 277–292. Thomsen, M.S., Wernberg, T., Kendrick, G.A., 2004. The effect of thallus size, life stage, aggregation, wave exposure and substratum conditions on the forces required to break or dislodge the small kelp Ecklonia radiata. Bot. Mar. 47, 454–460. Toohey, B.D., 2007. The relationship between physical variables on topographically simple and complex reefs and algal assemblage structure beneath an Ecklonia radiata canopy. Estuar. Coast. Shelf Sci. 71, 232–240. Toohey, B.D., Kendrick, G.A., Wernberg, T., Phillips, J.C., Malkin, S., Prince, J., 2004. The effects of light and thallus scour from Ecklonia radiata canopy on an associated foliose algal assemblage: the importance of photoacclimation. Mar. Biol. 144, 1019–1027. Toohey, B.D., Kendrick, G.A., Harvey, E.S., in press. Disturbance and reef topography maintain high local diversity in Ecklonia radiata kelp forests. Oikos. doi:10.1111/j.2007.0030-1299.15689.x. Vadas, R.L., Johnson, S., Norton, T.A., 1992. Recruitment and mortality of early post-settlement stages of benthic algae. Br. Phycol. J. 27, 331–351. Vleeshouwers, L.M., Bouwmeester, H.J., Karssen, C.M., 1995. Redefining seed dormancy: an attempt to integrate physiology and ecology. Ecology 83, 1031–1037. Watson, D., Harvey, E.S., Anderson, M.J., Kendrick, G.A., 2005. A comparison of temperate reef fish assemblage recorded by three underwater stereo–video techniques. Mar. Biol. 148, 415–425. Wernberg, T., Kendrick, G.A., Phillips, J.C., 2003. Regional differences in kelp-associated algal assemblages on temperate limestone reefs in southern Australia. Divers. Distrib. 9, 427–441. Wernberg, T., Kendrick, G.A., Toohey, B.D., 2005. Modification of physical environment by an Ecklonia radiata (Laminariales) canopy and its implications for associated foliose algae. Aquat. Ecol. 39, 419–430. Wood, W.F., 1987. Effect of solar ultra-violet radiation on the kelp Ecklonia radiata. Mar. Biol. 96, 143–150.