Competitive interactions between two fucoid algae with different growth forms, Fucus serratus and Himanthalia elongata

Competitive interactions between two fucoid algae with different growth forms, Fucus serratus L. and Himanthalia elongata (L.) S.F. Gray were examined both in the laboratory and on a shore of the Isle of Man, Irish Sea. The growth of germlings of both species declined with increasing density, irrespective of whether they were with cohorts or rival species, indicating that intraand interspecific competition occurred between germlings. H. elongata suppressed the performance of F. serratus at the germling stage by virtue of its larger initial size, and at the ‘mushroom’ stage by forming a miniature canopy with the ‘caps’ of the adjacent plants. In a field experiment, the mortality of H. elongata juveniles generally increased in mixtures with F. serratus and was highest when F. serratus were 50% of the plants. At the juvenile stage, the negative effect of F. serratus onH. elongatawas more severe than the other way round. This was because F. serratus grows predominantly upwards, whereas H. elongata had already begun to expand laterally at the distal end. If F. serratus survives in sparse mixed stands with H. elongata juveniles, it can overgrow them and inhibit their subsequent survivorship and growth, probably by both shading and physical sweeping. H. elongata and F. serratus maintain their discrete monospecific stands because of the varying outcomes of mutual competitive exclusion resulting from their differing growth patterns. Thus it is possible for them to co-occur at a similar shore height. Introduction Fucus serratus and Himanthalia elongata are important components of the intertidal flora on NE Atlantic coasts (Lüning 1990). They colonize the shore andmaintain their populations by means of sexual reproduction by spores (Creed 1995; Creed et al. 1996a; Stengel et al. 1999). On the semi-exposed rocky shores of the Isle of Man, both species co-occur near the bottom of the littoral zone and have overlapping reproductive periods in the winter (Gibb 1937; Lewis 1964; Creed et al. 1996a). Reproductive effort, measured as the relative biomass allocated to the reproductive organs, is over 98% forH. elongata and between 38 and 50% for F. serratus (Norton 1991; Brenchley et al. 1996). Thus, mixed stands of juveniles of the two species are expected to be common on the shore, but mixed stands are rarer than monospecific stands of either species (Lewis 1964; Lüning 1990; Creed 1995). The formation of monospecific and mixed stands relates to the release time of gametes and their dispersal (Amsler et al. 1992; Pearson et al. 1998).H. elongata and F. serratus may release gametes in calm water conditions, resulting in the formation of monospecific stands near to the parent plants, as found in other fucoid species (Brawley 1992; Creed 1995; Pearson and Brawley 1996). However, on semi-exposed rocky shores the dispersal distance of zygotes may be far greater than the 5 m of F. serratus (Arrontes 1993). Indeed, H. elongata juveniles are often observed in algal turfs situated far away from the parent plants (Stengel et al. 1999). Therefore, the scarcity of mixed stands of juveniles of the two species is surprising, and the occurrence of competitive interactions between germlings before they become visible is likely (Amsler et al. 1992; Vadas et al. 1992). Intraspecific competition determines the performance of both germlings and juveniles in pure stands of each species (Creed 1995; Creed et al. 1996a, 1997; Stengel et al. 1999). In a mixture of F. serratus and H. elongata germlings, interspecific competition also occurs (Norton 1986), although other conditions that Communicated by O. Kinne, Oldendorf/Luhe H. G. Choi (&) Faculty of Biological Science and Research Institute for Basic Science, Wonkwang University, Iksan, 570-749 Chonbuk, Korea E-mail: [email protected] Fax: +82-63-8578837 T. A. Norton Port Erin Marine Laboratory, School of Biological Sciences, University of Liverpool, Port Erin, Isle of Man, IM9 6JA, UK Marine Biology (2005) 146: 283–291 DOI 10.1007/s00227-004-1441-4 may affect germling growth, such as the culture conditions, density and relative abundance of each species, were not reported. In mixed stands, the growth of plants may be influenced by the morphology of competing species, since a plant’s morphology influences its ability to obtain growth resources (reviews by Carpenter 1990; Olson and Lubchenco 1990). F. serratus is different in morphology and growth pattern from H. elongata (Creed 1995; Brenchley et al. 1996, 1997, 1998). F. serratus grows mainly upwards (Knight and Parke 1950) but H. elongata has four different growth patterns during its life span. The germling expands outward for a few days after settlement to form the hat-like ‘syncytial stage’ (Moss 1969; Ramon 1973). It then grows upwards to the so-called ‘button stage’ and later expands laterally (‘mushroom stage’) in the vegetative stage (Gibb 1937; Creed 1995). Finally,H. elongata produces thong-like receptacles (‘receptacle stage’) from the center of the mushroom-like plant (Gibb 1937; Creed 1995). The self-sustaining receptacles again grow vertically, up to a length of 2 m (Brenchley et al. 1996, 1997). These are held more or less erect when submerged, but flop over when out of the water. F. serratus andH. elongata are ideal species to test the following hypotheses: 1. the monospecific stands of juveniles of either species are the consequence of competitive exclusion between germlings of the two species; and 2. the differing growth patterns of the two species affect the outcome of interspecific competition. To test these hypotheses, competition experiments were performed on both the germling and juvenile stages, in which H. elongata grows outwards. Here, juvenile plants are defined as the mushroom stage in H. elongata (ca. 2 cm in height and ca. 0.6 cm in diameter) and small (3–6 cm tall) plants of F. serratus lacking reproductive organs. Three experimental designs were applied: the additive, modified additive and replacement series designs. Additive and modified additive designs were used to examine the occurrence of interspecific competition and the relative intensity of intraand interspecific competition at the germling stage. The replacement series design was used to investigate the relative importance of intraand interspecific competition on the performance of plants at the juvenile stage. There has been criticism of the replacement series design (Silvertown and Lovett Doust 1993), but it remains useful for examining the effect of species proportion on the growth of plants, and the results can be analyzed statistically (Cousens 1996). Materials and methods Irradiance and competition between germlings in culture Ten fertile females and one male plant of both F. serratus and H. elongata were collected from Port St. Mary ledges (54 0¢N, 4 44¢W) on 23 November 1999. Propagules of F. serratus and H. elongata were released as described by Creed et al. (1996b) and Gibb (1937), respectively, to provide suspensions of propagules. In all laboratory experiments, the effects of irradiance on the germlings were examined at 60 and 120 lmol m 2 s , which is the light saturation point of F. serratus germlings (McLachlan 1974). Temperature (10±1 C) and photoperiod (16:8 h L:D) were kept constant. For each treatment, two Petri dishes, each containing eight glass slides (2.5·2.0 cm) and 30 ml of autoclaved seawater, were prepared. After inoculating zygote suspensions, Petri dishes were left 24 h for settlement. From each Petri dish, four slides on which germlings were most evenly distributed were chosen. The culture medium was renewed weekly over 17 days. Each treatment was replicated four times. Additive experimental design The interspecific competition between H. elongata and F. serratus was examined in experiments in which the density of one species was held constant in all treatments and the density of a second species varied (Cousens 1991). The density of the original zygote suspensions was 1,000 zygotes ml 1 for F. serratus and 700 zygotes ml 1 for H. elongata. First, 5 ml of F. serratus suspension was inoculated into four treatments and then three different amounts (5, 10 and 20 ml) of H. elongata suspension were added to each of three treatments. The settlement density of F. serratus was ca. 100 zygotes cm 2 in four treatments (monoculture and three different mixtures with H. elongata) and that of H. elongata was 0, 75, 150 and 300 zygotes cm . Modified additive experimental design Three suspensions of F. serratus zygotes with different concentrations (1,000, 2,500 and 5,000 zygotes ml ) and one H. elongata suspension with 700 zygotes ml 1 were prepared. To make three different monospecific densities, 5 ml of each F. serratus zygote suspension and 5, 10 and 20 ml of the H. elongata zygote suspension were inoculated into six Petri dishes. Three mixed cultures were obtained by mixing the zygote suspensions of the two species. Thus, a total of nine treatments were made and the density of germlings in each treatment is shown in Table 1 and the experimental design in Table 2. Measurements and analyses Initial settlement density of propagules was determined in four random 6 mm areas on each of four replicate slides. The mortality of germlings was estimated at the end of experiment, and the lengths of a total of 25 germlings were measured on each of four replicate slides for both species. The widths of H. elongata germlings 284