Seasonal Module Dynamics of Turbinaria Triquetra (Fucales, Phaeophyceae) in the Southern Red Sea1

J. Phycol. 42, 990–1001 (2006) r 2006 by the Phycological Society of America DOI: 10.1111/j.1529-8817.2006.00258.x

SEASONAL MODULE DYNAMICS OF TURBINARIA TRIQUETRA (FUCALES, PHAEOPHYCEAE) IN THE SOUTHERN RED SEA1

Mebrahtu Ateweberhan Department of Marine Biology and Fisheries, University of Asmara, PO Box 1220, Asmara, Eritrea and Department of Marine Biology, University of Groningen, PO Box 14, 9750 AA Haren, The Netherlands J. Henrich Bruggemann Laboratoire d’Ecologie marine, Universite´ de La Re´union, B.P. 7151, 97715 Saint-Denis, La Re´union, France and Anneke M. Breeman2 Department of Marine Biology, University of Groningen, PO Box 14, 9750 AA Haren, The Netherlands

Module dynamics in the fucoid alga Turbinaria Key index words: density; growth rate; intraspecif- triquetra (J. Agardh) Ku¨tzing were studied on a ic competition; module density; module dynamics; shallow reef ﬂat in the southern Red Sea. Seasonal primary axes; reproduction; temperature; trade-off patterns in thallus density and size were determined, and the initiation, growth, reproduction, and shedding of modules were studied using a tag- Whole thalli of many fucoid species are long-lived ging approach. The effects of module density and and they adjust to heterogeneous environments module/thallus size on module initiation, growth, through phenotypic plasticity. This plasticity is ex- reproduction, and shedding were analyzed, and the pressed at the level of the modules. Modules are repet- occurrence of intraspecific competition among itive components of plants (genets), which may behave modules was examined. Seasonal variation oc- as physiologically independent units (Schmid 1990, curred mainly at the modular level. There was a re- Scrosati 2002). A modular construction provides devel- stricted period of new module formation in the opmentally, physiologically, and allometrically simple cooler season, followed by fast growth and repro- ways to vary life-history traits (Toumi and Vourisalo duction, massive shedding of modules from the end 1989, Collado-Vides 2002). Measurements of size, of the cooler season onward, and strongly reduced growth, and reproduction are, therefore, better con- biomass in summer. There was no evidence of sup- ducted at the level of modules than at the level of whole pressed growth in small modules due to intraspe- plants (Toumi and Vourisalo 1989, Sprugel et al. 1991). cific competition. Module density and thallus/ Studies at the modular level are scarce in macroal- module size had opposite effects on elongation gae (Santos 1995, Scrosati and DeWreede 1997, 1998, rates. High module densities enhanced maximum Scrosati 1998, Lazo and Chapman 1998, Scrosati and elongation rates (fastest-growing module per thal- Servie`re-Zaragoza 2000, Viejo and A˚berg 2001, Arenas lus), resulting in longer thalli. On the other hand, et al. 2002, Ateweberhan et al. 2005a) and have mainly elongation rates decreased and tissue loss increased concentrated on comparisons with terrestrial plants, with increasing module length. Reproduction had for which adverse effects of high densities on survival, no clear effect on elongation rates, indicating that growth, and reproduction have been well documented there was no direct trade-off between reproduction (Harper 1977, Westoby 1984, Weiner 1988). As is the and growth. The apparent size-dependence of re- case in higher plants, high module densities have been production was due to delayed fertility in young found to reduce new module formation in fucoid spe- modules. Module initiation and shedding were in- cies and clonal red algae (Scrosati and DeWreede 1997, dependent of module density. Shedding was also Lazo and Chapman 1998, Viejo and A˚berg 2001, Ate- independent of module size and reproductive sta- weberhan et al. 2005a). This is a mechanism to avoid tus. We conclude that seasonal changes in the envi- overcrowding in the population. Other mechanisms ronment affect module initiation, growth, regulating population biomass include the suppression reproduction, and shedding, whereas density and of growth of the smaller plants due to competition for size-dependent processes mainly affect growth light, and self-thinning (Westoby 1984, Hutchings rates. 1986, Weiner and Thomas 1986). In macroalgae, the effects of high densities may differ from those in 1Received 19 October 2005. Accepted 26 June 2006. higher plants. For instance, self-thinning appears 2Author for correspondence: e-mail [email protected]. to be lacking in clonal red algae (Scrosati and

990 SEASONAL MODULE DYNAMICS TURBINARIA 991

Servie`re-Zaragoza 2000), and biomass–density combi- level of whole thalli (McCourt 1984, 1985, Ang 1992, nations lie considerably above the conventional self- A˚berg 1996, Gillespie and Critchley 2001). Little is thinning line in some fucoid species (Karez 2003). known about possible trade-offs at the modular level. Studies on the effects of density on growth rate have Seasonal cycles in the initiation, growth, reproduc- yielded conflicting results in seaweeds (Schiel and tion, and shedding of modules are still largely unex- Choat 1980, Cousens and Hutchings 1983, Schiel plored (De Ruyter van Steveninck and Breeman 1987, 1985, Creed et al. 1996, 1998, Lazo and Chapman Arenas et al. 2002, Ateweberhan et al. 2005a). This is 1998, Viejo and A˚berg 2001, Arenas et al. 2002). Elon- an important aspect because direct environmental or gation rates may be enhanced by high thallus or mod- endogenous control of the seasonal cycle (Lu¨ning and ule densities but negative effects on growth have also tom Dieck 1989) may result in temporal changes, e.g. been reported (Viejo and A˚berg 2001). Contradictory in density- or size-dependent effects. In this study, we results have even been reported for the same species. investigate module dynamics in the fucoid alga Turbin- In Ascophyllum nodosum, Lazo and Chapman (1998) aria triquetra in the southern Red Sea, a highly seasonal, found that high module densities promoted module tropical environment. In this species, thalli consist of a elongation rates, whereas Viejo and A˚berg (2001) holdfast system formed by branched haptera, from found a decrease in growth rate with increasing thallus which primary axes arise (the modules). T. triquetra oc- density. The results of the former study are in contrast curs in the Red Sea and along the Djibouti and Somalia with the general pattern in higher plants (Harper coasts of the western Indian Ocean; there are also 1977), again suggesting that macroalgae may behave uncertain records from the Andaman and Nicobar in a fundamentally different way, as proposed earlier Islands (Silva et al. 1996, Lipkin and Silva 2002). The by Schiel and Choat (1980) and Schiel (1985). southern Red Sea is characterized by strong seasonal In dense stands of higher plants, only one or a few variation, which is driven by the Indian Ocean mon- modules per plant may reach full size; the remainder soon system (Morcos 1970, Edwards 1987, Sheppard are stunted due to competition for light (Westoby 1984). et al. 1992, Sheppard 2000). Although seawater tem- This results in highly skewed size frequency distribu- peratures fall within the normal tropical range during tions. Highly skewed distributions have been found at the cooler season (oceanic isotherms: approximately the level of whole thalli in fucoid species (Arenas and 261 C–281 C), they are higher than recorded elsewhere Fernańdez 2000) but the development and underlying in the tropics during the warmer months (oceanic causes of such distributions have yet to be examined at isotherms up to 321 C; Morcos 1970, Lu¨ning 1990). the modular level (Lazo and Chapman 1998; but see Relatively high surface chl concentrations occur Rivera and Scrosati 2006). Skewed distributions could throughout the year in this region, indicating that sea- be the result of growth inhibition in small modules and/ sonal nutrient limitation is unlikely (Van Couwelaar or enhanced elongation rates in the longer ones, and 1997, Wiebinga et al. 1997, Medio et al. 2000). the effects would be expected to be density dependent. Recent studies on module dynamics and density/ In fact, Viejo and A˚berg (2001) found that the growth of size-dependent effects in fucoid algae have been based short shoots was negatively affected by density in A. on manipulative experiments (Lazo and Chapman nodosum, but not the growth of long shoots, and Arenas 1998, Viejo and A˚berg 2001, Arenas et al. 2002). In et al. (2002) found that high densities caused changes in this study, we use a correlative approach, based on the the morphology of Sargassum muticum, with the longer natural variation occurring among established thalli shoots becoming more elongated at high densities. and their modules. Module dynamics were assessed by Growth rates appear to be negatively size-dependent tagging all modules on individual thalli and following at the level of whole thalli in fucoid species (A˚berg 1996, their development from initiation to shedding. Al- Creed et al. 1998), but few studies have examined size- though no seasonal variation in thallus density had dependent effects at the modular level (Lazo and Chap- been detected in an earlier study (Ateweberhan 2004), man 1998, Viejo and A˚berg 2001, Arenas et al. 2002, thallus densities were also determined. We addressed Ateweberhan et al 2005a). the following specific questions: (1) What is the course The close relationship between the seasonal cycles of the seasonal cycle of module initiation, growth, of growth, reproduction, and senescence in macroal- reproduction, and shedding in T. triquetra? (2) Do gae has been taken as an indicator of the presence of module density and/or thallus/module size affect growth-reproduction and survival-reproduction trade- new module initiation, growth, reproduction, and offs (McCourt 1984, 1985, Ang 1992, A˚berg 1996, Gill- shedding, and is there any evidence of intraspecific espie and Critchley 2001). Based on the assumption of competition among the modules? (3) Is there evidence resource trade-off, De Wreede and Klinger (1988) pre- of growth-reproduction or survival-reproduction dicted that: (1) an organism must attain a certain size in trade-offs at the modular level? order to begin reproduction; (2) a reduction or cessation of growth would be likely at the onset of repro- MATERIALS AND METHODS duction because of partitioning of resources; and (3) an Study site. The study was conducted at Sheikh Said Island organism would be more likely to die after having (also called Green Island; 15135.60N, 39129.10E; Fig. 1) near reproduced. Growth-reproduction and survival-repro- Massawa, Eritrea, in the southern Red Sea. On the subtidal duction trade-offs have mainly been investigated at the reef flat of Sheikh Said Island, three distinct algal zones are 992 MEBRAHTU ATEWEBERHAN ET AL.

FIG. 2. Monthly variation in seawater temperature. The bar above indicates the general cycle of monsoon winds in the southern Red Sea: SSE during the cooler season (NE monsoon), NNW during the hot season (SW monsoon), v, transition period with variable wind directions.

FIG. 1. Map of Massawa and location of the study area at selected along a 50 m transect. Quadrats were marked with Sheikh Said Island (arrow). The solid lines indicate the perim- concrete steel nails at their corners and colored synthetic eter of the shallow reef flats; the dotted lines indicate the parti- ropes were attached to the nails for easy retracing. Thallus tion between intertidal and subtidal zones of the reef flats. densities were monitored at monthly intervals from Septem- ber 1999 to August 2000, December 2000 to April 2001, and in July 2001. Thallus and module parameters. The dynamics of T. triquetra distinguished. The canopy alga Sargassum ilicifolium forms a were studied by monitoring tagged thalli and modules. In conspicuous belt at the transition between the intertidal and September 1999, 30 thalli were randomly selected along the the subtidal parts of the reef flat (Ateweberhan et al. 2005a). transect and marked by nailing numbered tags close to their In the subtidal, the lowest zone of the reef flat is dominated holdfast. Thalli that were interconnected by haptera were by the canopy-forming alga T. triquetra, which forms a 10– considered as one individual. Lost thalli were replaced at 15 m wide belt adjacent to the coral-dominated fore reef, every census by labeling new ones. Out of the 30 thalli that which starts at about 1.5 m depth. In the cooler season, the were tagged in September 1999, a total of seven was lost: four foliose brown algae Dictyota cervicornis and Stoechospermum in October 1999, one in June 2000, and two in July 2000. polypodioides dominate in the zone between the Sargassum Of each thallus, all modules of 2 cm long were tagged by and Turbinaria belts, with S. polypodioides extending into the tying individually numbered tie-wraps around their lower upper part of the Turbinaria zone (Ateweberhan et al. 2005b). parts. As all modules were tagged and each one was identified Environmental parameters. Seawater temperature was by its own serial number, older modules that had lost their measured to the nearest 0.21 C on the fore reef at 2.5 m tags could be easily identified because of the missing serial depth (slightly deeper than the Tu r b i n a r i a zone) at 2-h inter- number. Tag losses were low, occurring in just a single mod- vals from September 1999 to July 2001, using underwater ule in some of the thalli at any census. Lost tags were re- temperature loggers (Onset Optic Stow-Away, Onset Com- placed immediately. Each month, the length, biomass, and puter Cooperation, Pocasset, MA, USA; Guillaume et al. number of modules were determined for each thallus. The 2000). Monthly mean values ranged from 27.71 Cinwinter length and the presence of receptacles were recorded for (January) to 33.51 C in summer (August) (Fig. 2). Monthly each module. At each census, newly appearing modules were means of daily maxima ranged from 28.41 C to 34.11 C, and tagged. The tagged thalli and modules were monitored means of daily minima from 26.51 C to 32.51 C. The highest at monthly intervals from September 1999 to August 2000, temperatures of the month exceeded 34.51 Cinsummer December 2000 to April 2001, and in July 2001. In addition, (July–September) and the lowest temperatures of the month 30 thalli in roughly the same size range as the tagged ones were below 251 C in winter (January–March). In the context were haphazardly selected from the Turbinaria zone at each of the Indian Ocean monsoon system, the period from census (referred to as ‘‘selected thalli’’ hereafter) to check for November to April is referred to in this study as the cooler possible adverse effects of tagging. Thallus size (length and season (north-eastern monsoon) and the period from May biomass), the number of modules on each thallus, and the to October as the hot season (south-western monsoon) presence of receptacles on each module were recorded. (Edwards 1987; Fig. 2). Thallus biomass was estimated using a non-destructive Thallus density. In an earlier study (Ateweberhan 2004), method as described by A˚berg (1990). Thallus length (L, hold- no significant temporal variation in thallus density was de- fast to tip of the longest branch) and maximum circumference tected during bimonthly monitoring of randomly placed (C) were measured in the field for each thallus. Maximum cir- quadrats (1998–2000). In the present study, thallus densities cumference was measured as described in A˚berg (1990), always were monitored more closely using permanent quadrats. In by the same investigator (M. Ateweberhan). LC2 (a crude meas- September 1999, 10 quadrats (0.5 0.5 m2)wererandomly ure of volume) was calculated. Thallus biomass (ash-free dry SEASONAL MODULE DYNAMICS TURBINARIA 993 matter, AFDM) was estimated using the relationship between growth parameters. Detailed results are presented only for se- ln LC2 and lnAFDM as determined from a destructively sam- lected parameters where the relationships showed a consistent pled set of calibration thalli, collected at bimonthly intervals pattern. Significant P-values are given, as well as the sign of between September 1998 and October 2000 (n 5 1105; Ate- correlation coefficients that were not significant but confirmed weberhan 2004). As no seasonal variation was detected the general trend (for P-values <0.10 and for P-values <0.40). in the calibration thalli (analysis of covariance [ANCOVA] Analyses at the level of the modules were based on pooled of lnAFDM by month with ln LC2 as a covariate, interaction data for all tagged thalli. Newly formed modules were exclud- term: F5, 1039 5 0.57, P 5 0.722), the following equation was ed from the analyses because they behaved differently from the used for all months: lnAFDM (g) 5 ln LC2 (0.998)–7.947 older modules. They showed little apical growth but went (R2 5 0.983, P<0.0001). through an early phase of differentiation, forming many short Data analysis. Temporal variation in thallus density and spur branches (Ateweberhan 2004). The effects of module in all thallus and module parameters of the tagged thalli length on elongation rates (positive growth only) and on size was analyzed with repeated measures analysis of variance reduction (negative growth) were investigated with linear re- (ANOVA) (RMA), using the Greenhouse–Geisser correction gression. The effects of module length on the occurrence of to accommodate violation of the sphericity assumption tissue loss, survivorship and reproduction were analyzed with (Stevens 2002). Thallus length, estimated AFDM, and the Mann–Whitney U-tests (persistently heterogeneous variances mean number (total and new) and length of the modules in some months). The effect of reproductive status on module were determined for each thallus. In addition, the percent- elongation rate was analyzed with ANCOVA, taking length as a age of fertile modules, the percentage of modules sustaining covariate. Only modules with positive growth were included. tissue loss (decrease in length at the following census), and The effects of reproductive status on the occurrence of tissue the percentage of modules that was shed between censuses loss and on module survivorship were analyzed with Chi- were determined for each thallus. Size frequency distribu- square tests. The analyses on survivorship were restricted to tions of modules were determined, based on pooled data for the months between April and July when reproduction coin- all thalli, distinguishing between sterile and fertile modules. cided with mean loss rates (per thallus) of more than 10%. Frequency distributions for the same months of the 2 years of Levene’s test of homogeneity of variances was performed to monitoring were compared with Kolmogorov–Smirnov tests. check the assumptions of parametric statistics in ANOVA. In Growth rates of large fucoid algae have been documented case of persistently heterogeneous variances in part of the data variously as absolute and as relative growth rates (RGR), both set, non-parametric tests were used for all months. All statistical at the thallus and module levels (De Ruyter van Steveninck and analyses were performed in accordance with Sokal and Rohlf Breeman 1987, Schaffelke and Klumpp 1997, Lazo and Chap- (1995) and Stevens (2002) using SPSS for Windows 11.0 man 1998, Viejo and A˚berg 2001). In most cases, changes in (2001). length have been presented but some authors have used changes in thallus biomass (Lazo and Chapman 1998). For comparison, we therefore calculated growth rates both in ab- RESULTS solute terms and as RGR for length as well as biomass. Seasonal patterns are documented here based on elongation rates and Seasonal patterns. Thallus density showed signifi- RGR (length) of whole thalli and as the means of all modules cant temporal variation (RMA: F5, 73 5 4.65, (per thallus). Growth in terms of absolute rates of biomass in- P 5 0.001; Fig. 3a). Mean densities were the lowest crease was included in the analyses on the effects of module inthesecondhalfofthecoolerseason(March–April) density and thallus size on growth rates. In addition, maximum and the highest at the onset of the hot season growth rates (RGR and elongation rate of the fastest growing module per thallus) are presented. This measure gives a better (May–July). Thallus length, thallus biomass (estimat- estimate of the seasonal variation in growth potential than ed AFDM), and the number and length of the mean values for all modules, which are more strongly affected modules varied strongly with season (RMAs: thallus by tissue loss. Absolute growth rates were calculated as the length F6, 69 5 216.06, P<0.0001; thallus biomass difference in length or biomass between two consecutive F6, 42 5 24.86, P<0.0001; mean module length F6, 49 measurements (cm/mo; g AFDM/mo). RGRs (RGR-length) 5 201.95, P<0.0001; module numbers: F2, 83 5 were calculated using the formula 62.86, P<0.0001; Fig. 3, b–d). Values were the low- RGR ¼flnðlength at t2Þlnðlength at t1Þg=ft2 t1g est in the hot season from July to October, increased quickly from November onwards, peaked between and expressed as %d 1 of the initial length. Temporal variation in growth rate was analyzed with RMA as described above. February and May, and declined sharply in June. Data for the August–December 2000 interval were The size frequency distributions of the modules are excluded from the analyses on growth rates and on the pro- shown in Figure 4. In September 1999, virtually all portion of modules sustaining tissue loss because few thalli modules fell into the smallest size class (10 cm). From had persisting modules over that interval. October onward, size distributions gradually shifted Possible relationships between various thallus and module toward the larger size classes. However, until April, parameters were investigated. All analyses were carried out for each month separately because relationships between param- small modules in the first size class(es) were also eters may change with season. Moreover, data on tagged mod- present. The individual history of these small modules ules are not independent over time. At the level of whole thalli, was checked, and it was confirmed that they were new- the following analyses were performed. Possible effects of mod- ly formed (Fig. 5a) and grew into larger size classes in ule density (number of modules per thallus) on thallus length the following months. From May onwards, size distri- were tested with linear regression analysis. Similarly, the effects butions shifted downward and in the middle of the hot of module density, thallus length, and thallus biomass were tested on: (1) the number of new modules formed in the fol- season (August) all modules were less than 20 cm long. lowing month, (2) the proportion of modules that was shed in In the 2 years of monitoring, size distributions were the following month, (3) the proportion of fertile modules, (4) similar in all months (Kolmogorov–Smirnov tests: the proportion of modules sustaining tissue loss, and (5) all P 0.05), except in December and January, when 994 MEBRAHTU ATEWEBERHAN ET AL. there were more very small modules in the first than in tion of fertile modules decreased in June and repro- the second year (Kolmogorov–Smirnov tests: duction had ended by August, although some fertile P<0.0001) (Fig. 4). modules remained in this month on the selected thalli Reproduction was strictly seasonal and the propor- (Fig. 3e). During most months, reproductive modules tion of fertile modules per thallus showed significant occurred only in the larger size classes (Fig. 4, white temporal variation during the reproductive season bars). Small fertile modules were only present in June (RMA: F4, 89 5 44.56, P<0.0001; Fig. 3e). Fertile mod- and July, representing older modules that had lost api- ules first appeared in February; between March and cal tissue but were still fertile, and young ones formed May, about 70%–80% were reproductive. The propor- during the last months of new module initiation. The initiation of new modules on the holdfast was restricted to the months between October/November and April, and showed significant temporal variation during this period (RMA: F5, 71 5 13.10, P<0.0001; Fig. 5a). Initiation had probably just started in Octo- ber (low number of new modules); the main peak occurred between November and January. In Febru- ary–April, formation decreased to about one module per thallus and no new modules were formed between May and August. Loss rates of modules were also strongly seasonal (RMA: F4, 79 5 9.62, P<0.0001; Fig. 5e); they were low during the main growth season between December and February, increased from March onward, and remained relatively high to the end of the hot season (September). At the start of the next cooler season (December 2000 data), only approximately 5% of the previous year’s modules remained. Growth rates (RGR-length and elongation rates) showed strong seasonal variation, both at the thallus and module level (RMAs: RGR thalli F3, 83 5 24.97, P<0.0001; mean RGR modules F3, 91 5 22.54, P<0.0001; maximum RGR modules F5, 29 5 13.65, P<0.0001; elongation rate thalli F5, 69 5 39.86, P<0.0001; mean elongation rate modules F4, 19 5 38.95, P<0.0001; maximum elongation rate modules F3, 58 5 24.61, P<0.0001; Fig. 5, b and c). RGRs reached high values earlier in the year than did elongation rates, related to the size-dependence of RGR and the smaller module/thallus sizes early in the growth season (Figs. 3b, and 5b and c). Seasonal patterns in the maximum growth rates (RGR and elongation rate) were different from those based on the means for all modules and whole thalli. Maximum growth rates remained high until March/April, several months after mean growth rates had started to decline. The proportion of modules sustaining tissue loss varied over time (RMA: F5, 86 5 32.81, P<0.0001) and increased strongly during this period (Fig. 5d). Max- imum elongation rates were high, reaching peak values of approximately 90 cm/mo (Fig. 5c). In most

FIG.3. Turbinaria triquetra. Seasonal variation in density, thallus size, and module length, number, and reproduction. (a) Thallus density in permanent quadrats (no. 0.25 m 2; n 5 10). (b) Thallus length ( , ) and mean module length (per thallus) (&). (c) Estimated thallus ash-free dry matter (AFDM). (d) Mean number of modules (per thallus). (e) Mean proportion of fertile modules (per thallus). (b–e) Data based on tagged (open symbols) and selected (closed symbols) thalli (both n 5 30); nd, no data; the error bars indicate standard error of the mean. SEASONAL MODULE DYNAMICS TURBINARIA 995

1999 and July 2000 and between January 2001 and April 2001), indicating a decrease in elongation rate with increasing module length. Relationships between thallus and module parameters. Thallus length showed a significant positive correlation with module density (number of modules per thallus) in most months and correlation coefficients were positive also in nearly all other months (Table 1). In general, the proportion of fertile modules (per thallus) was independent of module density. A significant positive correlation was found only in January 2000 (linear regression: F1, 28 5 12.50, P 5 0.001). In both years, fertile modules were significantly longer than sterile ones during the first months of the reproductive season (February to April/May) (Mann– Whitney U-tests: P<0.05). However, this effect was caused by a delay in the onset of reproduction until the modules were 2 months old. Reproduction was independent of size in older modules (Mann–Whit- ney U-tests: P 0.05). Reproduction was not inhib- ited in the young modules because of their small size because modules formed late in the growth season (April) started to reproduce (in June) when they were only approximately 23 cm long. Module initiation was independent of module density and thallus biomass in all months (linear regressions: P 0.05) but a significant positive correlation with thallus length was found in February 2001 (linear regression: F1, 28 5 6.18, P 5 0.019) and April 2001 (linear regression: F1, 28 5 7.98, P 5 0.009). Module survivorship was generally independent of module density (linear regression: P 0.05 in most months). A significant negative correlation was found only in May 2000 (linear regression: F1, 28 5 7.87, P 5 0.009), when loss rates were the highest (Fig. 5e). Module survivorship was generally independent of module length (ANOVAs: P 0.05 in all months except December 1999 [F1, 35 5 9.18, P 5 0.005], when persisting modules were longer than those that were lost). Module survivorship was also independent of reproductive status (Chi-square tests: P 0.05 in all months). Effects of module density, thallus size, module length, and reproduction on growth rates. Module density as well as thallus size affected absolute growth rates but in different ways (Table 1). High module densities appeared to have a positive effect on the maximum module elongation rate (fastest growing module per thallus). A significant positive correlation was found in several months and correlation coefficients were also positive in most other months (Table 1). The mean elongation rate of modules (per thallus), the FIG.4. Turbinaria triquetra. Size frequency distribution of elongation rate of whole thalli, and the absolute rate modules by stage. Total number of modules indicated; based of thallus biomass increase did not show such density on pooled data for 30 tagged thalli. dependence. These growth parameters generally showed a significant negative correlation with thallus months, the mean length of the modules with the length/biomass (Table 1). In addition, the proportion highest elongation rate (per thallus) was significantly of modules sustaining tissue loss generally increased below the overall mean for all modules (Mann–Whit- with thallus length (Table 1). Significant effects of ney U-tests, P<0.05 in all months between November module density and thallus size were found not only 996 MEBRAHTU ATEWEBERHAN ET AL. during the main growth season but also during (Table 2). Size reduction (modules with negative months when mean growth rates had fallen below growth) increased with increasing module length zero (Table 1, Fig. 5c). (Table 2). Moreover, the probability of tissue loss in- Analyses at the module level, based on pooled data creased with increasing module length (Table 2). The for all thalli (Table 2), showed that both a decrease in effects of size were significant for much of the periods apical growth and an increase in the amount of tissue of growth and degeneration (Table 2), when mean loss were responsible for the strong size-dependence of module lengths varied strongly (Fig. 3b). elongation rates. Elongation rates (modules with pos- Reproductive status had no clear effect on module itive growth) decreased with increasing module length elongation rates. ANCOVA on elongation rate (positive growth only) by reproductive status with length as a covariate generally showed no effects of reproductive status (Prepro 0.05 in most months), only of length (see Table 2). Significant effects of reproductive status were found only in April 2000 (ANCOVA: F1, 63 5 5.60, Prepro 5 0.021) and March 2001 (ANCOVA: F1, 124 5 6.43, Prepro 5 0.012) but y-intercepts and slopes of linear regressions for fertile and sterile modules were not significantly different (based on 95% confidence intervals). Reproductive status had no significant effect on the occurrence of tissue loss either (Chi-square tests: P 0.05 in all months).

DISCUSSION Seasonal patterns. The development of T. triquetra shows a highly seasonal and predictable pattern (Fig. 6). Although the data reported in this paper refer to a single site, they are supported by data for 1998– 2000, when thallus sizes were measured in randomly chosen quadrats at two replicate sites (Ateweberhan 2004). Rapid vegetative growth and build-up of biomass in the cooler season are offset by tissue loss and senescence of modules at the start of the hot season. Thalli survive the hot season as small clumps with pros- trate or short erect primary axes attached to the per- sistent holdfasts. Interpretation of the seasonal pattern of growth depends on the choice of growth parameter. The mean module elongation rate and the elongation rate of whole thalli decline earlier in the year than the maximum elongation rate (fastest-growing module per thallus). As this early decline is due to an increase in tissue loss (which depends on module size), seasonal patterns are best evaluated based on maximum elongation rates. The maximum elongation rate increases sharply in No- vember–December, following a decline in temperature during the previous month. A strong decline takes place

FIG.5. Turbinaria triquetra. Seasonal variation in module initiation, growth, tissue loss, and module loss. (a) Mean number of new modules (per thallus). (b) Relative growth rate (RGR) of whole thalli, and mean and maximum RGR of modules (per thallus). (c) Elongation rate of whole thalli, and mean and maximum elongation rate of modules (per thallus). Maximum values refer to the fastest-growing module per thallus. For periods when growth was not monitored at monthly intervals, values are placed in the middle and connected by dashed lines. The dashed horizontal lines indicate zero growth. (d) Percentage of modules sustaining tissue loss (per thallus). (e) Percentage of lost modules (per thallus). Data based on tagged thalli; number of thalli used for calculation of growth rates (bearing modules) shown on top; nd: no data; error bars indicate standard error of the mean. SEASONAL MODULE DYNAMICS TURBINARIA 997

TABLE 1. Turbinaria triquatra. (A) Relationships between module density (number of modules per thallus) and thallus length and maximum module elongation rate. (B) Relationships between thallus length and thallus elongation rate, mean module elongation rate, and the proportion of modules sustaining tissue loss. (C) Relationship between thallus biomass and the absolute rate of biomass increase.

Sep (1) Oct (1) Nov (1) Dec (2) Jan (2) Feb (2) Mar (2) Apr (2) May (1) Jun (1) Jul (2)a Aug (1) (A) Module density vs. Thallus length ( þ ) 0.005 <0.0001 <0.0001 ( þþ)(þ ) 0.022 0.007 ( þþ) 0.024 (17 mo þ ) ND ND ND 0.014 0.001 <0.0001 0.022 ND ND ( )ND Maximum module 0.034 0.044 ( þ )(þ )(þ ) 0.013 elongation rate ND ND ND 0.003 <0.0001 0.046 ND ND ND ND (16 mo þ ) (B) Thallus length vs. Thallus elongation ( ) 0.047 0.015 0.010 <0.0001 <0.0001 <0.0001 <0.0001 ( ) <0.0001 <0.0001 <0.0001 rate (18 mo ) ND ND ND ( )( ) <0.0001 0.002 <0.0001 ND ND ND Mean module 0.018 0.032 0.023 ( ) 0.007 <0.0001 0.003 <0.0001 ( ) <0.0001 <0.0001 ( ) elongation ND ND ND <0.0001 0.012 ( ) ND ND ND ND rate (16 mo ) % modules with tissue ( þþ) 0.021 ( þþ) 0.001 ( þ ) <0.0001 ( þ ) <0.0001 <0.0001 loss (14 mo þ ) ND ND ND <0.0001 ( þ )( )NDNDNDND (C) Thallus biomass vs. Abs. rate biomass ( ) 0.001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 increase (16 mo ) ND ND ND 0.001 <0.0001 <0.0001 <0.0001 ND ND ND ND

Summary of linear regression analyses: P-values in regular type indicate significant positive correlation (P<0.05); P-values in italics indicate significant negative correlation (P<0.05); ( þþ) ( ), sign of correlation coefﬁcients with 0.05

TABLE 2. Turbinaria triquetra. Effects of module length on elongation rate, size reduction, and the occurrence of tissue loss.

Elongation rate vs. length Size reduction vs. length Length þ / growth (linear regression) (linear regression) (Mann–Whitney U-test)

Month df FP df FP PLength (cm) Sep 99a 1.27 0.76 0.391 Not enough cases 0.019 5/11 Oct 99b 1.23 8.57 0.008 Not enough cases 0.065 NS Nov 99b 1.23 12.37 0.002 1,9 5.53 0.043 0.041 26/34 Dec 99b 1.82 28.24 <0.0001 Not enough cases 0.031 26/57 Jan 00b 1.88 94.35 <0.0001 1,25 2.59 0.120 <0.0001 49/84 Feb 00b 1.113 152.73 <0.0001 1,38 15.58 <0.0001 <0.0001 53/104 Mar 00b 1.97 120.79 <0.0001 1,67 18.31 <0.0001 <0.0001 66/114 Apr 00b 1.65 116.17 <0.0001 1,88 29.17 <0.0001 <0.0001 65/108 May 00 1.21 3.56 0.073 1,102 104.41 <0.0001 0.003 56/81 Jun 00 1.35 13.11 0.001 1,43 1858.31 <0.0001 <0.0001 4/59 Jul 00 1.5 0.10 0.767 1,43 48.96 <0.0001 0.001 7/14 Aug 00 1.10 2.53 0.143 All increased in size (4-month interval) Dec 00a 1.144 20.68 <0.0001 Not enough cases 0.813 NS Jan 01b 1.98 32.79 <0.0001 1,45 20.47 <0.0001 <0.0001 66/88 Feb 01b 1.123 123.21 <0.0001 1,61 22.82 <0.0001 <0.0001 58/108 Mar 01b 1.126 154.92 <0.0001 1,87 34.69 <0.0001 <0.0001 61/107 Apr 01b No cases (3 month interval) 1,57 1363.53 <0.0001

Linear regression analyses on the effect of module length on elongation rate (growth 40; all significant regression coefﬁcients were negative) and size reduction (growth <0; all significant regression coefﬁcients were positive). aAll modules, new ones unknown in these months. bNewly formed modules not included; Mann–Whitney U-tests compare lengths of modules with positive growth and size reduction over the following month; mean lengths of the two groups indicated. Significant P-values in bold type; based on pooled data for all thalli. df, degrees of freedom; F, ANOVA F-statistic; P, probability. 998 MEBRAHTU ATEWEBERHAN ET AL.

the stand. In Ascophyllum nodosum (Lazo and Chap- man 1998, Viejo and A˚berg 2001), several Sargassum species (Arenas et al. 2002, Ateweberhan 2004, Ate- weberhan et al. 2005a) and in the clonal red alga Mazzaella cornucopiae (Scrosati and DeWreede 1997) new module formation decreased with increasing density. Adverse effects of large thallus sizes have also been reported (e.g. in S. subrepandum;Ate- weberhan 2004). In T. triquetra, there is no evidence that high module densities or large thallus sizes coun- teract new module formation. In this species, the modules (primary axes) arise from an extended system of branched haptera rather than a discoid holdfast,asisthecaseinAscophyllum, Sargassum,and Mazzaella. Thus, the modules are more dispersed and may function more as independent units.

FIG. 6. Summary of the seasonal dynamics of Turbinaria The loss of whole modules in T. triquetra is generally triquetra. Bar widths represent different categories relative to independent of module density and size. However, the maximum for each parameter, except for thallus density high module densities may offer some protection as where they are expressed relative to the range of variation: 0% loss rates correlated negatively with module density (no bar); 40%–25% (thin bar); 26%–75% (intermediate bar); and 76%–100% (thick bar). Data from Fig. 3a (thallus density), Fig. 5a during the month with the highest losses (May 2000 (module initiation), Fig. 5c (maximum elongation rate; no bar if data). T. triquetra thalli survive the hot season as hold- values not significantly 40), Fig. 3c (thallus ash-free dry matter fast clumps, sometimes with short erect axes, thereby [AFDM]), Fig. 3b (thallus length), Fig. 3e (reproduction), Fig. 5d minimizing metabolic demands. Module survivorship (tissue loss), and Fig. 5e (module loss). The bar above indicates is also seasonally controlled and independent of size in the general cycle of monsoon winds in the southern Red Sea: SSE during the cooler season (NE monsoon), NNW during the S. ilicifolium (Ateweberhan et al. 2005a) and S. sub- hot season (SW monsoon), v 5 transition period with variable repandum (Ateweberhan 2004) in the southern Red wind directions. Sea. In contrast to T. triquetra, loss rates are low during the hot season in these species. Sargassum spp. have a small discoid holdfast, and maintaining some mod- roalga, Sargassum ilicifolium (Ateweberhan et al. 2005a) ules would facilitate re-growth and would also provide and S. subrepandum (Ateweberhan 2004), also from the self-shading, which would be secured by the more southern Red Sea. The strategy is well known for mac- extensive holdfast system in T. triquetra. roalgae from temperate regions, where many species Density- and size-dependent regulation of growth. As show a strategic annual rhythm, with temperature and mentioned above, conflicting results have been re- day length acting as seasonal cues (Lu¨ning and tom ported with regard to the effects of crowding on Dieck 1989, Lu¨ning 1990). New module initiation is a growth rates in modular macroalgae. Some studies key process in the seasonal cycle of T. triquetra; it occurs showed growth inhibition under crowded conditions, only between October/November and April. Environ- as in modular higher plants, others showed increas- mental control of module formation can be investi- ing growth rates at higher module or thallus densities gated only through controlled experiments. However, (Lazo and Chapman 1998, Scrosati and Servie`re- direct temperature control seems unlikely. Over the Zaragoza 2000, Viejo and A˚berg 2001, Arenas et al. October/November interval, when initiation peaks, 2002). Our results on T. triquetra may provide an ex- temperatures are still higher than in April, when ini- planation for these contradictory results. We found tiation ceases. Module initiation could be regulated by that high module densities and large thallus sizes sharply defined photoperiodic cues, such as reported have opposite effects on elongation rates. High mod- for erect axis formation in S. muticum, which occurs ule densities enhance the maximum module elonga- mainly in short days (Hwang and Dring, 2002). At our tion rate (fastest-growing module per thallus), study site (151350 N), day length varies between about resulting in longer thalli. On the other hand, in- 11 and 13 h in the course of the year. A photoperiodic creased thallus and module lengths reduce the short day response with a sharply defined critical day- mean elongation rate and enhance the amount of length of about 12 h, such as found in tropical higher tissue loss. Similar results were obtained in modular- plants (rice; Thomas and Vince-Prue 1997), could ex- level studies of two other large canopy algae from plain why new modules are formed only from October southern Red Sea reef flats: Sargassum ilicifolium to April. The timing of reproduction and module (Ateweberhan et al. 2005a) and S. subrepandum shedding may also be under direct environmental or (Ateweberhan 2004). Thus, the same processes ap- endogenous control (Lu¨ning and tom Dieck 1989). pear to operate on different, unrelated species in the Possible effects of density and size on module initiation same environment. The balance between the coun- and shedding. The rate of module formation is often teracting effects of module density and thallus size on dependent on module density and/or the density of elongation rates may depend on environmental con- SEASONAL MODULE DYNAMICS TURBINARIA 999 ditions and/or biotic interactions, accounting for the recruitment could be expected to occur early in the conflicting results reported in the literature. hot season in T. triquetra, accounting for the higher Faster elongation rates at higher thallus or module densities. We have no clue as to the resistance of densities have also been reported for other large canopy propagules and recruits to the extreme temperature algae (Hart 1982, Schiel 1985, Lazo and Chapman 1998, and irradiation levels during the hot season. The Arenas et al. 2002). Within dense macroalgal stands, light decrease in thallus density during the main growth levels below the top of the canopy are low and would season could be due to some recruit mortality but decrease with increasing module density. These low light mayalsoberelatedtocoalescenceofhorizontallyex- levels could stimulate growth, as has been reported for panding haptera of neighboring thalli. In an earlier stipe elongation in some laminarian seaweeds (Hurd study, in which all thalli were monitored in randomly 1916, Duncan 1973, Hart 1982). The response may be chosen quadrats, we found no clear evidence of similar to the ‘‘shade avoidance responses’’ (Smith 1982) intraspecific competition at the population level. of terrestrial plants and may be mediated by photorecep- There were no small, suppressed thalli during peak tor pigments (Duncan and Foreman 1980). development (Ateweberhan 2004). The probability that modules sustain tissue loss in- In dense stands of terrestrial plants, only one or a creases strongly with module length. Grazing is often few modules per plant may reach full size (Westoby an important cause of biomass loss in tropical canopy 1984). This results in strongly skewed size frequency algae (Lewis 1985, McCook 1996, 1997). Although distributions. There is no evidence of growth inhibi- field observations indicate that T. triquetra is the cano- tion in the smaller modules of T. triquetra. In the mid- py alga least grazed upon by fish (M. Ateweberhan, dle of the growth season, size frequency distributions personal observation), invertebrate grazing may dam- are sometimes bimodal, with one of the modes falling age fronds, making them more vulnerable to wave into the smallest size class. However, when checking action. Mechanical abrasion may be expected because the individual history of these small modules, we found of breaking waves on the outer edge of the reef flat, that they were newly formed and grew rapidly into the and the vulnerability to wave action increases with size larger size classes in the following months. These re- (Gaylord et al. 1994). Adverse effects of module length sults show the importance of using tagged modules were also found in modules with positive growth. when interpreting the underlying causes of changing Thus, growth is probably partly redirected toward size frequency distributions. We conclude that there is the formation and elongation of secondary branches, no evidence of intraspecific competition at the modular instead of apical growth of the primary axes. More- level. Instead of suppressed growth in small modules, over, photosynthetic products could be dissipated in elongation rates actually decreased with increasing producing and maintaining non-photosynthetic struc- module length, as outlined above. tural elements (Norton 1991). Reproduction and possible trade-offs. In many sea- Growth rates of large canopy algae have been quan- weeds, the onset of reproduction is preceded by a pe- tified in terms of increases in thallus length or biomass riod of rapid vegetative growth (De Wreede 1976, (Lazo and Chapman 1998, Schaffelke and Klumpp Prince and O’Neal 1979, McCourt 1984, Martin-Smith 1997), and sometimes in the length of isolated modules 1993). This has been interpreted as the need for thalli (Schaffelke and Klumpp 1997). Estimates based on to reach a certain size before they can reproduce. Dur- RGR are less appropriate than those based on absolute ing the first months of the reproductive season, fertile rates of increase because growth occurs in apical meri- modules of T. triquetra are, indeed, longer than sterile stematic regions in fucoid species (Van den Hoek et al. ones, as has been reported for whole thalli of other 1995). Moreover, our data show that estimates of fucoid algae (e.g. Ascophyllum nodosum; Lazo and Chap- absolute rates of increase based on whole thalli or iso- man 1998, Viejo and A˚berg 2001). However, the lated modules result in a strong underestimation of the apparent size-dependence in T. triquetra is caused by maximum growth potential. For instance, during the fact that modules have to be at least 2 months old the period of peak development, the mean thallus before being able to reproduce. In the older modules, sizes are relatively constant and growth estimates based reproductive status is independent of module size, and on whole thalli are low. Yet, elongation rates of the fast- modules formed at the end of the growth season start- est growing module per thallus are still very high dur- ed to reproduce when still only approximately 23 cm ing this time of the year. Estimates of elongation rates long. Thus, conclusions about the possible size- based on isolated modules would also underestimate dependence of reproduction need to take possible growth potential because fast elongation may depend age-dependent ontogenetic control of module on photomorphogenetic responses induced by shading development into consideration. in the intact canopy. A cessation of growth has often been reported at the Possible intraspecific competition. Temporal variation onset of reproduction, and this has been interpreted in thallus density is usually related to recruitment as evidence of a trade-off between reproduction and peaks (Kendrick and Walker 1994) and density-re- growth (McCourt 1985, Ang 1992, A˚berg 1996, Gill- lated mortality of small plants caused by intraspecific espie and Critchley 2001). We found no clear evidence competition (Creed et al. 1998). Considering the that elongation rates are lower in fertile than in sterile peak in reproduction at the end of the cooler season, modules. Elongation rates depend on size, rather than 1000 MEBRAHTU ATEWEBERHAN ET AL. on reproductive status as such. Among the algae, re- Arenas, F., Viejo, R. M. & Fernańdez, C. 2002. Density-dependent production may be cost-free or cost-reduced because regulation in an invasive seaweed: responses at plant and reproductive structures are photosynthetic (McLa- modular levels. J. Ecol. 90:820–29. Ateweberhan, M. 2004. 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