The Role of Gametes of the Macroalgae Ascophyllum Nodosum (L.) Le Jolis and Fucus Vesiculosus L
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ISSN 00014370, Oceanology, 2010, Vol. 50, No. 2, pp. 198–208. © Pleiades Publishing, Inc., 2010. Original Russian Text © O.V. Maximova, A.F. Sazhin, 2010, published in Okeanologiya, 2010, Vol. 50, No. 2, pp. 218–229. MARINE BIOLOGY The Role of Gametes of the Macroalgae Ascophyllum nodosum (L.) Le Jolis and Fucus vesiculosus L. (Fucales, Phaeophyceae) in Summer Nanoplankton of the White Sea Coastal Waters O. V. Maximova and A. F. Sazhin Shirshov Institute of Oceanology, Russian Academy of Sciences, Moscow email: [email protected], [email protected] Received July 1, 2008; in final form November 14, 2008 Abstract—Studies of macrophytes in the coastal zone of the Artic Seas, including the White Sea, have shown the essential role of these algae in the activity of the coastal halflatitude ecosystems. In summer, during the macrophyte reproduction period, a great number of reproduction products are released into the water. For a short time, this considerably affects the ratio of the nanoplankton in the populations that inhibit the vast and shallow coastal areas. At different coastal sites in Chernorechenskaya Inlet, Kadalaksha Bay, during the period of intensive reproduction of Ascophyllum nodosum and Fucus vesiculosus, 42 plankton samples were collected in 2005. During this period the concentration of antherozoids in the water reached 55000 cells/ml (216 mg C/m3). The number of eggs was within the range of 0.05–0.7 cells/ml. The proportion of anthero zoids in the total biomass of nanoplankton varied at different coastal sites from 0.37 to 99%, with a mean of 46% for the reproduction period of A. nodosum, and only 7% for the reproduction period of F. vesiculosus. As was shown by counts of F. vesiculosus female gametes in sedimentation traps, 1 m2 of the macrophyte bed (assuming 100% coverage) produces 18000–108000 eggs per day (0.33–2 mg C). The calculated flux of the reproductive material from the brown algae beds to the coastal water shows good agreement with the sample counts. DOI: 10.1134/S0001437010020050 INTRODUCTION eggs (Sargassum) or 109 zoospores (Undaria, Lami naria) [46] and big thalloms of laminaria produce up The role of brown algae in coastal halflatitude × 12 ecosystems, including the White Sea, is extremely to 3.7 10 zoospores, which could give rise to × 12 high. They are edificators of littoral and upper sublit 1.85 10 new plants [7]. On one thallom of the Black toral phytocenosis, the main producers of the upper Sea brown algae Cystaceira barbata, up to 2200 recep phytal zone, and the basis of the coastal trophic web tacles are formed, in which up to 550000 oogonia are [4, 5, 10, 11]. The production characteristics of these developed and one egg is matured in each oogonium; commercial macrophytes (biomass, linear growth, in C. crinita up to 1400 receptacles and 400000 oogonia oxygen exchange, excretion) have been thoroughly are developed [9]. The number of eggs per receptacle is studied [1, 5, 7, 10, 12, 15, 17, etc.]. There are a num assessed for A. nodosum as 7 × 104, and during the repro ber of works devoted to the reproductive ecology of ductive period, an individual of average size produces brown algae [26, 28, 35, 40, 41]. But there are practi 6 × 107 eggs. The potential production of eggs by big cally no data on the amount of gametes released into A. nodosum may reach 2.5 × 109 per 1 m2 of brown algae the water. We know of only four publications in which during the reproduction period. This leads to the appear the potential production of algae eggs has been studied ance of 2 × 10–8 new plants [18]. The egg production of [18, 20, 42, 44] and only one work in which data on the F. distichus in the reproduction period is estimated at daily dynamics of the concentration of algae gametes 1.5 × 107 per 1 m2 of brown algae [20], of F. spiralis, 3 × 108 in the coastal waters are given [25]. [42], and for Sargassum sinclarii, 2 × 106 [44]. Gametes and zygotes, spores of different types, special vegetative “buds,” i.e., all kinds of devices for The thallom of the brown algae Rhodymenia per reproduction and dissemination, are collectively tusa with a length about 1 m produces 12000000 car called “propagules” [28]. Macroalgaes produce great pospores, and one tetrasporephyte of this algae pro amounts of propagules, which are an important source duces up to 10000000 tetraspores, which “form a part of of energy for different protozoa and other small inver the phytoplankton of the coastal sea zone” [3, p. 212]. tebrates and for the coastal ecosystems of the whole However, the majority of propagules do not germinate: sea in general [30]. According to the data of different “the more common destiny of algae propagules is to be authors, during one season one thallom produces 105 eaten” [30, p. 228]. 198 THE ROLE OF GAMETES OF THE MACROALGAE Ascophyllum nodosum (L.) 199 Propagules of the majority species are distributed some seasonal aspects to light. We assessed the flow of from a single parental plant at a distance of only a few generative substances by our own data and from the meters (2–3 m for Sargassum muticum, up to 5 m for literature and compared the calculated results with Macrocystis pyrifera); the maximal detected distance is those obtained in the field. about 60 m for Fucus eggs [31, 47, 32]. It was shown in one of the first publications on this problem [46] by the example of species with different types of propagules MATERIALS AND METHODS (zygotes and zoospores of green Monostroma, aplano Both studied species are dioecious plants, i.e., male spores of red Gelidium and Pterocladia, monospores and female gametangia (antheridia and oogonia), are and carpospores of red Porphyra, anterozoids of Sar developed on different thalloms. Gametangia are gassum, and others) that all of them for a short period formed in special cavities, scaphidia and conceptacle, of time (in situ from 20 min up to two days, in vitro up which are concentrated on swollen apexes of genera to 4–11 days) retain the ability of free floating, react to tive branches called receptacles. The receptacles of light (positive or negative phototaxis), and sink in the A. nodosum can be clearly differentiated by color: male zone of the parents' growth. In calm water the average are bright orange and female are olive. The sex of speed of propagule settling is about 0.5 mm/s. Only F. vesiculosus may be distinguished only by optics: the few propagules (zoospores and antherozoids, which color variants of receptacles of this species are not have flagella) are able to move actively with speeds 80– connected with sex. Oogonia of brown algae contain 300 µm/s; the majority are spread passively by the coastal 8eggs and those of ascophyllum, 4. Eggs of brown current, the typical speed of which is 1–10 cm/s [38]. algae are big (they are visible to the naked eye) and The tangles of parental plants during fruiting pro motionless. In male gametangia (antheridia), duce a cloud of spores, especially in the case when the 64 microscopic movable antherozoids with 2 flagella release of gametes happens in the whole population are developed [8]. Surrounded by a membrane, oogo simultaneously. The spreading of this cloud increases nia and antheridia go out into the water and the covers the settling distance; for example, for Macrocystis it are destroyed outside the scaphidia and release the increases 14 times in comparison with single plants. gametes. Fertilization occurs in the water and takes The propagules of green algae were distributed furthest 30–120 min [27]. Several hours later the formed of all: they are more numerous than gametes of brown zygote sticks to the substrate with polysaccharide and red algaes in water samples taken away from the slime and immediately starts to form the organ of shore, even if the latter dominate in local bottom tangles. attachment, i.e., primary rhizoids. Less than one day This is due to both the high fertility of Chlorophyta and after fertilization, the seedling is formed. the fact that heavier eggs and zygotes of Phaeophyceae After the end of the active fruiting period, the and Rhodophyta sink in the nearest coastal zone. The receptacles fall off. They are never absolutely empty: propagules of Enteromorpha sp. (Chlorophyta) have been some quantity of oogonia and antheridia remains. detected at a distance of 35 km from the nearest fructif Both the release of gametes and dropping of recepta erous population, and a number of brown (Desmares cles of ascophyllum occur over several days in the tia Laminaria, Petalonia) and red (Phycodris) were whole population (at the end of June), and in fucus found at a distance of 5 km [38]. both processes are stretched out in time, from the end The release of gametes and the intensity of this pro of July until the end of September. Fallen receptacles, cess depend on many natural factors: temperature, which accumulate in the littoral puddles and in ejec illumination intensity, water motion, stages of the tidal tions, preserve viable gametes: under laboratory con cycle, and even the phase of the moon [19, 23, 45, ditions the gametes of F. vesiculosus form zygotes and etc.]. These and a number of other studies showed that germinate even at the end of October. gamete release is more intensive in warm, not windy, We chose 42 water samples of brown algae (Fig. 1). weather in the evening (after 16:00) and two days The samples were taken at the time of active fruiting of before the full moon or the new moon.