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 deter- mined, 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 Ferna´ndez 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