ISSN 0001 4370, 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 e mail: [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 half latitude 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 half latitude × 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. Ascophyllum nodosum (June 20–21) and F. vesiculosus In summer during the period of intensive fruiting of (the end of July to the beginning of August). These brown algae, their gametes seriously change, though conditions for sample gathering were chosen because for a short time, the quantitative ratio of nano and the release of brown algae gametes occurs in warm and microplankton that inhabit vast regions with shallow calm weather [25, 39]. Thus, the weather on June 20– depths. The temporary change in the water color at the 21, 2005, was not windy and the air temperature time of release of male gametes by ascophyllum is vis reached 25°C; the subsurface water temperature was ible even to the naked eye. Nevertheless, no attempts 17°C. From July 30 to August 9, the air temperature were made to assess the quantity of gametes of brown ranged from 16.7 to 23°C, and the underwater temper algae in the structure of nanoplankton of the littoral ature (depth of 1 cm) ranged from 14.1 to 20.6°C and sublittoral zones during the period of their fruit (from the end of low tide to the beginning of high tide). ing. This deficiency was the main driving force for this The last samples in October were taken to deter research. In addition, we tried to estimate the distance mine whether gametes are encountered in plankton in of gametes settling from the parental tangles and bring this season.
OCEANOLOGY Vol. 50 No. 2 2010 200 MAXIMOVA, SAZHIN
°N 67
Kola Peninsula
K a n d a la k sh a G u lf 66
WHITE SEA
32 35 38°E
Cape Peschany 4 5 2
1 3 6
Olenevskii Island Pereima 1 km
Fig. 1. Index map of the study region. Numbers in brackets indicate the place of sample collection: (1) Cape Peschany (sample nos. 1–18, 22, 23, 28–42 and traps); (2) Olenevskii Island (sample nos. 24, 25); (3) Pereima (sample nos. 19, 20); (4) narrow channel of estuary (sample no. 24); (5) wide channel (sample no. 27); (6) lower rapids of the estuary (sample no. 21).
The samples were taken with sterile containers both fucus and ascophyllum with a projective coverage in tangles of brown algae and at a significant distance (PC) of 90–100%. The remaining area had tangles from them. In addition, we used a sedimentation trap with PC of approximately 60–65%. The traps were put from plastic food cylinders with size 18 × 7 cm fixed in under the bushes of fucus, one in the “thickest” parts the bottom for accumulation of gametes (primarily of tangles, the second in a group of stones overgrown female) going out into the water. The need for such a by fucus away from the main tangles, and the third in a double approach is explained by the differences in the sandy “meadow” with no plants. The water from traps behavior of female and male gametes after their release was gathered with a rubber bag. into the water: eggs sink fast, whereas antherozoids Water samples for determining the presence of spend more time in the water depth moving both with male gametes were gathered at different stages of the the current and actively. Motion and tidal currents tidal cycle. The takes were conducted in the tangles of may move eggs tens of meters away from the maternal brown algae at a distance of several meters from the plant. water’s edge during low tide, with the beginning of the For sample gathering and setting traps, we chose tide away from tangles and in the strait between the the littoral region, including Cape Peschany (Fig. 2). continent and Olenevskii Island at distances of about The area of this region was approximately 120 m2, and 100 and 300 m from the coast (Fig. 1). The water was approximately 20% of this area was mixed tangles of transported to the coastal laboratory (not more than
OCEANOLOGY Vol. 50 No. 2 2010 THE ROLE OF GAMETES OF THE MACROALGAE Ascophyllum nodosum (L.) 201
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5 m
Fig. 2. Index map of region of samples collection on Peschany Gulf. (1) Sand without vegetation; (2) fucoid tangles with PC up to 65%; (3) fucoid tangles with PC 90–100%; (4) boulders; (5) traps. an hour passed from the moment of collection), con CHARACTERISTICS OF THE STUDY REGION tainers were intensively shaken, and subsamples of The research was conducted in Chernorechenskaya 20 ml were put in scintillation bottle. Next, the sub Inlet of Kandalaksha Bay of the White Sea, in Cape sample was dyed with fluorochrome primuline and Peschany in the estuary of the Chernaya Rivier, and on then fixed in glutaric dialdehyde (final concentration Olenevskii Island (Fig. 1) during the White Sea coastal in the sample 1–2%). For precise identification of expedition of the Shirshov Institute of Oceanology, female and male gametes of Ascophyllum nodosum and Russian Academy of Sciences. Fucus vesiculosus, suspensions of eggs from nature Cape Peschany separates the top of Chernorechen receptacles of both algae in sterile seawater were made skaya Inlet from the estuary of the Chernaya River. as were suspensions of antheridia with antherozoids. This region is protected by Olenevskii Island and char These samples were also dyed with primuline and fixed acterized by poorly shown wave activity (maximal in glutaric dialdehyde. Later at the Shirshov Institute water motion is about 2), the maximal speed of along of Oceanology, Russian Academy of Sciences, all sam coast flow is 0.4 m/s, and the speed of tidal–intertidal ples were precipitated on a nuclear filter with pore flows is 1–3 cm/s. The tidal cycle is a precise half day. diameter 0.4 µm. Preparations were made and exam The width of dried land during low tide is about 90 m, ined under a LYUMAM R8 luminance microscope and the soil is washed sand with numerous rocks. under magnification ×400–2500. Desalination due to the current of the Chernaya River Macrophyte gametes and organisms representing influences the entire shore near Cape Peschany, nanoplankton (2–20 µm) were taken into consider whereas the influence of fresh waters on the water area ation. We used the previously tested method of count around Olenevskii Island is insignificant. ing small plankton including flagellate forms [29, 34, The saltiness of the water near Cape Peschany fluc 37]. The volume of gametes and nanoplankton repre tuates depending on the season and wind direction: sentatives (2–20 µm) was estimated by the volume of from 8–10‰ (spring, after snow melting) to 19– the corresponding stereometric figures. The gamete 21‰ (summer). The temperature of both coastal water and nanoplankton organism biomass in carbohydrate and air is unstable even in warm periods. On the soil sur ° equivalent was assessed by the cell volume [36]. face, daily fluctuations may reach 20 С [2, 13, 16]. The shallow water near Peschany is characterized To make the biomass of brown algae more precise, by rich bottom plants. The most numerous plants in 10 quantitative takes (dimensional frames 25 × 25 cm, the literal and upper sublittoral zones are Fucus vesic i.e., 1/16 m2) were collected in the places of water ulosus and Ascophyllum nodosum. Common species are sample collection and near traps. For each thallom, Fucus vesiculosus f. edentatus, Chorda filum, Halosiphon the share of receptacle weight in the total thallom tomentosus, Chordaria flagelliformis, Desmarestia weight (%) was determined. Furthermore, the average aculeata (Phaeophyceae), and also seaweed Zostera number of scaphidia in receptacles and, respectively, marina and halophytes Ruppia maritima, Salicornia oogonia in them was assessed. The number of anthe europaea, Aster tripolium, etc. The projective coverage ridia was estimated from their volume and the volume (PC) of the bottom by two brown algae (mixed tangles of male receptacles (our own measures and published of both species) on the border of the littoral and sublit data). toral zones along Peschany Cape reached 90–100%.
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In the medium littoralzone, the PC of Fucus vesiculo range (60–110 µm), but the average diameter of cells sus is 25–30% in the low littoral zone; the PC of mixed in the study period is somewhat less at about 70 µm. tangles does not exceed 65–70%. The sublittoral zone Antherozoids of F. vesiculosus are also prolonged and is flat, the bottom is sandy, and at a distance of approx drop shaped (on average 7 × 2.5–3 µm) with a slightly imately 2 m from the water’s edge during the spring bent sharp end. The body of the antherozoid has 2 dif low tide, tangles of brown algae are replaced by ferently oriented flagella going from the middle of the thinned tangles of wrack (Zostera marina). body. The lengths of the flagella are 8–10 µm and 15– In the zone of brown algae, Mythilus edulis (both on 20 µm. The average volume of antherozoids is 20 µm3. the soil and on the thallom) develops in a mass and The average size of antheridia is close to that of rich settlements of polychaeta Arenicola marina are A. nodosum (50 × 15–20 µm or 2620 µm3). The aver detected. The epiphyton of brown algae is floristically age volume of eggs of F. vesiculosus is 180000 µm3. poor and is presented by filamentous algae Elachista The period of fruiting of Ascophyllum nodosum (sample fucicola (Phaeophyceae) and Cladophora sp. (Chloro nos. 1–8, June 20–21, 2005). The concentration of phyta). Red algae are presented only by epiphyte or antherozoids of A. nodosum in water in different places of unattached Polysiphonia fucoides. Among animals asso takes was from 91 to 55000 cells/ml (0.36–217 mg C/m3) ciated with fucoids prevail gasteropods (species from (table). The abundance of antheridia and eggs varied gena Littorina and Hydrobia) and crustaceans (Gam in the range 0.05–0.8 sp./ml and 0.05–0.6 sp./ml, maridae). respectively. Antherozoids were more abundant in the The estuary of the Chernaya River is about 2 km in lower littoral and upper sublittoral zone at the begin length. It consists of two widenings separated by rapid ning of high tide just when water covered the tangles of narrowings. The upper narrowing, called by natives that macrophyte. The lowest values were detected at Peresina (Fig. 1), is a border of the settling of Fucus high tide at a distance of 5 m from bushes of vesiculosus. Fucus plants here are small (not more than A. nodosum (sample nos. 4, 5), but at low tide at a dis 25–30 cm in length), dark, and abundantly branching. tance of 10 m the concentration of antherozoids was Small, often ugly receptacles develop on them, which, quite high—6279 cells/ml (sample no. 7). It is neces however, have quite viable gametangia developed in sary to point out that, in sample no. 4 situated at the them. Thalloms are practically always in the water, the growth line of ascophyllum tangles, the number of saltiness of which changes twice a day from null (at low antherozoids is twice as high as in sample no. 5 taken tide) to 9–17‰ (at high tide) [13, 16]. at the same distance from the coast but away from the The water area around Olenevskii Island practi tangles (202 and 91 cells/ml, respectively). cally does not undergo desalination (the saltiness is In the study period, the concentration of nanoplankton 22–24‰), the soil is represented mainly by boulder in the coastal zone changed in the range 46–6464 cells/ml placer, for this reason the algoflora is much richer: (1.46–124 mg C/m3); i.e., its abundance was signifi laminaria and brown fucus algae are abundantly repre cantly lower than the abundance of antherozoids of sented. Fucoids on Olenevskii Island are much bigger A. nodosum and the biomass was comparable with than on Peschany, and their tangles are characterized those of male gametes that are formally referred to by high values of PC (75–100%) and biomass (up to nanoplankton. The share of antherozoids in the total 20 kg/m2 and more). Samples were gathered on the biomass of nanoplankton varied in different sites of the north half open shore on the border of the littoral and coastal zone from 11 to 99% and was 46%, on average, sublittoral zones, where the PC of fucoids was 90–100%. for A. nodosum in this period. The absolute prevalence of male gametes in nanoplankton was detected for macrophytes, lower values were typical for the waters RESULTS away from tangles and bushes of A. nodosum. A signif Gametangia and gametes characterization Asco icant share in the nanoplankton biomass was held by dia phyllum nodosum. Mature eggs of this macrophytum toms Skeletonema costatum (average cell size 15 × 4 µm are globelike with a crumbly, slightly granular surface and by formal features it is referred to nanoplankton). without a clear internal structure. The egg diameter On the other hand, this algae practically always forms fluctuated from 60 to 110 µm, and the average value in long colonies and belongs to the group of microplank the study period was 80 µm. Antherozoids are elon ton algae (20–200 µm). If we exclude S. castatum from gated, drop shaped (on average 6 × 3 µm) with two dif nanoplankton, the share of antherozoids in the total ferently oriented flagella, one from the end and the biomass of this group of algae in different parts of the other from the middle of the body. The longer flagel coastal zone on average for the period of fruiting of lum goes from the edge end of the antherozoid’s body. A. nodosum will be 65%. The average volume of antherozoids is 22 µm3. The aver Period of fruiting of F. vesiculosus (sample nos. 9–18, age size of antheridia is 50 × 20 µm, volume 2620 µm3. July 30–31, 2005, and nos. 19–37, August 6–9, 2005). The average egg volume is 268000 µm3. The concentration of antherozoids was much lower Fucus vesiculosus. Eggs do not practically differ than during the fruiting of A. nodosum, i.e., not more from that of A. nodosum: spherical with a crumbly than 1880 cells/ml (6.77 mg C/m3, table). This maxi granular surface. The size of eggs varies in the same mal value was detected in sample no. 10 gathered on
OCEANOLOGY Vol. 50 No. 2 2010 THE ROLE OF GAMETES OF THE MACROALGAE Ascophyllum nodosum (L.) 203
3 3 Abundance (N, cells/ml) and biomass (Ba mg C/m ) of antherozoids in water and biomass of nanoplankton (Bn mg C/m ) and the share of male gametes of fucoids in the total biomass of nanoforms (%) in the fruiting period of Ascophyllum nodosum and Fucus vesiculosus Location Fucoid species Tangles of fucoids Away from tangles of fucoids of sample collection Ascophyllum nodosum Antherozoids N, cells/ml 9229–55216 202–6279 3 Ba, mgC/m 36.32–217.30 0.79–24.71 3 Nanoplankton Bn, mgC/m 1.46–4.77 2.54–124.42 The share of antherozoids in the total biomass 88–99 11–17 of nanoforms, % Average: 46 Fucus vesiculosus Antherozoids N, cells/ml 10–1882 0–101 3 Ba, mgC/m 0.04–6.77 0–0.26 3 Nanoplankton Bn, mgC/m 0.30–26.40 3.12–21.90 The share of antherozoids in the total biomass 0.4–33 0–7 of nanoforms, % Average: 7
Peschany at the water’s edge in the thickest tangles of from 0.37 to 33% and was, on average, for the period fucoids (PC 100%), just near receptacles in the lowest of fruiting of F. vesiculosus only 7%. Naturally, the water level (syzygies). Sample no. 9 taken simultaneously maximal share of male gametes in the total nano in the sublittoral water (depth at low tide 10 cm) among plankton biomass was in regions with tangles of mac the same algae contained 538 cells/ml. The concen rophytes of this species. tration of eggs was 0.1 sp/ml in sample no. 9 and Three samples were taken on August 6, 2005, in the 0.7 cells/ml in sample no. 10. The next day these takes estuary of the Chernaya River: two (nos. 19–20) on were repeated at the same stage of the tidal cycle (sam Pereima and one (no. 21) in the region of lower rapids. ples nos. 17–18), but the concentration of antherozo All samples were taken at the beginning phase of high ids had fallen by one–two degrees and was only 41 and tide. The concentration of antherozoids was very sim 30 cells/ml, respectively. The concentration of eggs ilar: sample no. 19 had 81 cells/ml, no. 20 had did not change so significantly: 0.05 and 0.25 cells/ml. 71 cells/ml, and no. 21 had 61 cells/ml. Sample no. 19 The temperature conditions of both days of material was taken in fucus tangles in a relatively calm place; collection were similar (air temperature 15–17°C, sample no. 20 in a heavy water current at a distance of water temperature 14°C) but the second day was very 20–30 cm from bushes of fucus from which it washed. windy and during the sample gathering it began to It is interesting that in spite of the significantly lower rain. It was apparently a “signal” to stop gamete biomass of fucus on Pereima and clearly oppressed release. condition of thalloms in the upper border of its settling The abundance of eggs of F. vesiculosus did not in the estuary, the concentration of male gametes is exceed 7 cells/ml. Antheridia were encountered in quite comparable (and even higher!) with data on plankton quite rarely. In the middle of the day between Cape Peschany (table) and even on Olenevskii Island the continent and Olenevskii Island at a distance of (samples nos. 25–26, 51 and 1001 cells/ml, respec 100 m from both shores, the concentration of gametes tively). in the water was very low: antherozoids 30 cells/ml, According to data of sedimentation traps, which and eggs 0.5 cells/ml. The sample was taken in the take into consideration female gametes of F. vesiculo final stage of low tide, which indicates that even heavy sus, 18000–108000 eggs are released in 1 day in 1 m2 eggs may be moved by currents such distances. At 300 m in the macrophyte tangles (under 100% projective from shore, there were no antherozoids or eggs in the coverage). This makes 0.33–2 mg C under quite a plankton. large size of female gametes of fucoids. It is necessary During the fruiting of F. vesiculosus, the concentration to point out that the data from traps gave unpredict of nanoplankton varied in the range 99–2353 cells/ml able results: the concentration of gametes in traps in (0.3–26.4 mg C/m3). In most cases the abundance the sandy “meadow” were higher than in the two oth and biomass of typical nanoplankton forms was higher ers: in this trap after one day of exposure, there were than the abundance of F. vesiculosus antherozoids. 560 cells/ml of antherozoids and 0.6 cells/ml of eggs, The share of antherozoids in the total biomass of nan whereas in the two other traps, the amounts were 152 oplankton varied at different points of the coastal zone and 0.3 (lower littoral) and 31 and 0.1 (middle littoral)
OCEANOLOGY Vol. 50 No. 2 2010 204 MAXIMOVA, SAZHIN cells/ml, respectively. It is likely that the fucus thallom Bay, the Solovetskii islands), this value fluctuates from covered the entrance to the traps, which preventedga 9 to 44% but, on average, is also 22.1% (Maximova, metes from entering. More detailed investigation should own data). Older plants always prevail by mass (espe be done to determine the gamete concentration more pre cially before release of receptacles), whereas the young cisely. However, we wanted only to obtain rough data to prevail by number. compare with data on water samples. According to our data for the study region, the Quantitative characteristics of fucoids. Kandalak share of receptacles in the total mass of both species in sha Bay holds the second place by biomass of F. vesic the period of maximal maturity fluctuates from 4– ulosus after the narrow entrance to the White Sea: it 10% in young thalloms, which have just reached varies here from 2.9 to 26.8 kg/m2 and is, on average, reproductive age, and up to 70–80% in older plants. 20.5 kg/m2 (the maximal biomass in the narrow The average value in the population is 45.2%. entrance is 40.8 kg/m2) [11]. For A. nodosum in Kan Assessment of flow of the generative material from dalaksha Bay, the same authors give the values 24.1– the fucoid tangle in coastal water. We assessed the 33.7 kg/m2, and the maximal biomass for the White quantity of fucoid gametes that entered the coastal Sea is 52–60 kg/m2. Vozzhinskaya [5] gives signifi water according to our data and that from the litera cantly lower numbers: for F. vesiculosus, 3.3–8.8 (on ture by the quantitative characteristics of populations average 6) kg/m2, and maximum is more than of the two species studied. 10 kg/m2; for A. nodosum, on average, 8 kg/m2, maxi 2 According to measurement data on the linear size mally 34 kg/m . According to our data of the 1970s, of 105 receptacles of F. vesiculosus (length, width, the biomass of F. vesiculosus in Kandalaksha Bay var thickness), their volume was assessed by the volume ied from 7 to 19.5 kg/m2 and that of A. nodosum was 2 formula of a spin ellipsoid [33]. The volume of one 24–25 kg/m (all data represents the raw mass). receptacle varies from 3.9 to 0.02 cm3 and is, on aver The fucoid biomass in the period of our investiga age, 0.6 ± 0.14 cm3. Differences in the values of the tion in Cape Peschany was, on average, about receptacles of the two species are unauthentic and in 13 kg/m2 (raw mass) and varied from 27.3 kg/m2 on the further assessments we took them as similar and the border of the littoral and sublittoral zones up to equal to 0.6 cm3. 2 6.8 kg/m in the middle littoral (mixed tangles of both The unit weight of receptacles is approximately species). The maximal biomass of fucus was 3 2 2 0.8 g/cm . The weight of one receptacle varies in the 15.1 kg/m and that of ascophyllum was 12.2 kg/m . range from 2.1 g to 0.01 g and is, on average, about 0.5 g. The density of mixed tangles varied from 704 to 2976 sp/m2 (not taking into consideration the young Scaphidia (or conceptacles) have a spherical form of the current year and plants up to one year old). The and are located in the depth of receptacles close to its mass of fruiting plants was 70–80% (up to 83.3%) of surface. According to our data, the number of the total biomass of the sample. scaphidia in one receptacle in both species of fucoids varies from 30 to 237 and is, on average, 121, which The biomass of F. vesiculosus in the Pereima region 2 actually agrees with published data: for ascophyllum it did not exceed 0.6 kg/m (PC was 30–50%). is 90–97 scaphidia in one receptacle; for F. vesiculosus On Olenevskii Island samples were taken only in it ranges from 55 to 198 [11], for the Baltic F. vesiculo the period of fruiting of F. vesiculosus and its biomass sus it is, on average, 169 ± 12 [19]. There is no signifi there reached 20 kg/m2 and more; PC was 75–100%. cant dependence of the scaphidia number on the Young thalloms of fucoids have some receptacles, and receptacle volume. the number grows with each year; in plants of 5–7 years In the period of maximal maturity, the diameter of old, it reaches several hundred (the maximum number one scaphidium reaches 0.05–0.1 cm and its volume in our samples was on 8 year old thalloms of F. vesic is, on average, 2.2 × 10–4 cm3. According to our assess ulosus). The fertility index according to our data is ment, the volume of all scaphidia in one receptacle of from 0.51 to 0.61. It matches the data from the North fucus is from 2 to 20% of its total volume and is, on Atlantic being 0.64 while that from the Baltic is 0.53 [22]. average, 8%. It may be regarded that the share of the According to published data, the share of recepta total mass of scaphidia in the mass of the receptacle is cle weight in the total mass of the thallom in the period in the same range. of maximal maturity in the White Sea is up to 80–85% According to our data, in one female scaphidium of for F. vesiculosus, up to 50–60% in F. distichus, up to ascophyllum about 30–50 oogonia are formed, that of 30% in F. serratus, and up to 84% of the mass of the fucus ranges from 10 (and less) to 30–40. Practically whole thalom in A. nodosum [5, 6]. In the Barents Sea all scaphidia of ascophyllum are formed simulta (East Murman), the share of receptacles in the total neously; the period of fruiting of fucus is extended in mass of plant reaches 22% for fucus and up to 50% for time, which is why gametangia maturation happens ascophyllum (East Murman) [12]. Vozzhinskaya [5] gradually and different plants from one population gives a close number for the White Sea: 22.03% for (even from one stone) may “mature” with a time shift fucus and 42.3% for ascophyllum. For F. vesiculosus of 2–4 weeks. Thus, about 10–20 mature oogonia are from different areas of the White Sea (Kandalaksha present mostly in scaphidia of fucus, practically the
OCEANOLOGY Vol. 50 No. 2 2010 THE ROLE OF GAMETES OF THE MACROALGAE Ascophyllum nodosum (L.) 205 same number of maturing oogonia, and dozens of their total mass in the basin is 135000 tons. Assuming forming oogonia. that the sex ratio in populations is 1 : 1, we will get that The diameter of mature oogonia of fucoids is about unisexual plants make up 675000 tons. If there is 0.015 cm, its volume is 1.8 × 10–6 cm3. The total vol according to our assessments 20000–25000 eggs, then ume of oogonia in scaphidium of ascophyllum varies the total production in the basin will be 1.7 × 1012 from 6 × (10–5–10–4) cm3, and their share in the oocytes or about 500 tons. Apparently the total pro scaphidium volume is, on average, 32%. Conse duction of male gametes is comparable with this value. quently, the share of oogonia in the mass of one recep tacle is, on average, 2.6%. The weight of receptacles in the total weight of the population is about 45%, with DISCUSSION the sex ratio 1 : 1, the share of oogonia in the total bio Quantitative assessments of the fucoid gamete role mass is 0.58%. The average biomass of ascophyllum in in the coastal plankton are obtained for the first time; Cape Peschany is 6 kg of raw mass per 1 m2, and the there is no such data in the world literature. There is total area of the region of mixed tangles is about only one work [25] devoted to reproductive activity of 120 m, with a length of 25 m. During the reproduction F. vesiculosus (Man, United States) in the tidal cycle. period (7–10 days), ascophyllum releases in this area Water samples were taken every 30 minutes with a about 4.15 kg of raw mass of oogonia and antherozoids pump. Eggs were calculated under a microscope, and or 0.31 kg per tidal cycle. If the width of the littoral for the determination of antherozoid concentration, zone is 90 m, the tidal height is 2 m, and the speed of the monoclonal antibodies method was used to take the along shore current is 0.4 cm/s, about 2500 m3 of into consideration precisely antherozoids of this spe water will go through the studied area. Then, the con cies and separate them from other small flagellant centration of male and female gametes is 120 mg of forms. The obtained data were recalculated by 1 l of raw mass at 1 m3 or, recalculating by carbohydrates, water. It was shown that female and male gametes 33.54 mg C/m3 (under the condition of its even distri enter into the water simultaneously, which increases bution in this volume, which does not conform to the the probability of fertilization, and it occurs most natural situation). The total mass of antherozoids and intensively during the flow. Maximal values of propagule eggs of ascophyllum, which we assessed in terms of concentration were obtained in a salty locality (oogonia, carbohydrates was 78.37 mg C/m3 (average for all up to 1500 pcs/l; eggs, up to 2400 pcs/l; antherozoids, gathering points). Such an excess of the calculated up to 11000 pcs/l when the averages are respectively value by more than two times may be due to the fact 750, 1500, and 8000 pieces per 1 l) in comparison with that part of the samples were taken just after fucoids the estuary (oogonia, up to 375 pcs/l, eggs, up to were covered by the incoming tidal water, in the cloud 350 pcs/l; antherozoids, up to 1300 pcs/l when the aver of propagules. In the range of gametes, the concentra ages are, respectively, 175, 220, and 900 pieces per 1 l). tion is naturally significantly higher than in coastal According to our data, the concentrations of anthero water in general. zoids of fucus in fully salted and estuary conditions Due to the extended reproductive period of practically do not differ. F. vesiculosus, such assessments for this species are quite Other studies of propagules of marine macroalgae relative because the speed of gamete release depends on in the water column did not include its direct calcula the weather and is very uneven. During the reproductive tion: water samples were filtered and filters were incu period (2 months) of focus, about 50 oogonia are devel bated up to appearance of the first shoots. Then, by the oped in each scaphidium, which makes up about 40% shoots the species range of propagules was determined of the scaphidium volume or 0.72% of the total fucus [21, 47]. biomass. For the studied littoral region at Cape Pesch Strangely, there are not a lot of quantitative data on any (total biomass is 7 kg raw mass/m2), the release of generative production of fucoids. Usually researchers male and female gametes is 43 g per tidal cycle, which limited themselves to determination or correlation of corresponds to an average egs and antherozoid con receptacles mass and the total mass of plankton fertil centration 17 mg of raw mass in 1 m3 or in terms of ity index [22]. Evidently, the great amount of recepta carbohydrates 4.81 mg C/m3 in total. The total mass of cles, which are released yearly, plays a great role in antherozoids and eggs of F. vesiculosus, which we dendrite formation: annually after fucoid fruiting in assessed, in terms of carbohydrate is 3.12 mg C/m3 the dendrite, the food chain is supplied with from 2 to (average by all gathering points). 6.2 kg of vegetable mass from 1 m2 of tangles [5]. But Thus, our calculated data correlate well with data this mass does not strictly speaking belong to genera obtained as a result of sample processing. tive production: eggs and antherozoids make up only a The reserve of fucoids in the White Sea is 250000– small part of the receptacle mass, as we have shown, as 350000 tons raw mass [5, 7, 14]. It may be assumed the values given along with receptacles include the that for the two studied species there are 300000 tons, mass of moribund generative branches. if we compare the others to other fucoids species (pel In a number of studies more concrete data is given. vetia, F. serratus, F. distichus), which have a lesser role in Thus, the density of gametangia in 1 mm2 of scaphidia coastal ecosystems. Then, with a receptacle share of 45%, section is determined: for dioecious F. vesiculosus
OCEANOLOGY Vol. 50 No. 2 2010 206 MAXIMOVA, SAZHIN
1677 ± 42 antheridia and 47.32 ± 1.73 oogonica and for In the fruiting period of fucoids, high concentra monoecious F. spiralis 162 ± 13 antheridia and 36.41 ± tions of antherozoids in places of mass growing of 2.13 oogonia [26]. It was shown that the intensity of A. nodosum and F. vesiculosus are not utilized in gamete release of F. vesiculosus depends on water plankton poor with consumers and are mainly used by motion and the time of day: under calm conditions the numerous epiphytic and benthos forms, which are intensity of gametes release is 5–6 times more than able to consume (grasp, filter) sinking male gametes. under high waves and at night gametes are practically These are first of all mollusks (mainly mussels) and not released [41]. Under calm conditions over several infusoria. hours 1220–1400 occytes are released per 1 g of raw The concentration of eggs of A. nodosum and mass of receptacle and under active waves this value F. vesiculosus, which is relatively low in comparison decreases to 300. The fucoid Pelvetia compressa over with the concentration of antherozoids of these spe 11 hours releases 48720 ± 5937 eggs per 1 g of raw mass of ± cies and representatives of nano and microplankton, receptacules under calm conditions and only 306 161 did not influence significantly the carbohydrate flow under energetic waves [40]. It was shown that male and in the ecosystem of water depth. Fucoids are an excep female gametes of F. vesiculosus are released simulta tion to the law that says that organisms with external neously, which increases successfulness of fertilization fertilization produce a colossal excess of gametes, the and mainly in the evening (after 16:00); in the peak most part of which is dispersed in the water, consumed moments of gametes release, their number in 1 g of by consumers, or dies. Thus, for example, only 29–78 receptacle (raw mass) varies for eggs from 1500 to 10000 7 8 and 42–54% respectively of carpogons of red algae and for antherozoids from 10 to 10 over 8 hours [45]. (fresh water Batrachospermum boryanum, marine Pol All these results were obtained under laboratory ysiphonia lanosa) are fertilized [43]. conditions, which do not always adequately reflect the natural situation. For fucoids this is correct only for antherozoids: the ratio of male and female gametes in the period of For the Baltic F. vesiculosus, two peaks of reproduc active release of gametes fluctuates from 10 : 1 to 70 : 1, tion are revealed: some plants fruit in May–June, oth and practically all eggs (95–100%) are fertilized and ers in September–November; these differences are sprout [28, 25]. Not propagules but shoots of fucoids apparently fixed genetically. In terms of thallom mass, have a great contribution in the functioning of food “summer” plants produce more relatively small eggs chains. In the beginning period of germination of × 4 (21 10 pcs/g, diameter 0.067 mm) during the repro zygotes of F. vesiculosus (middle to end of August), the duction period and “autumn” plants produce fewer big density of shoots may reach more than 650 pcs/cm2 × 4 ger ones (8.9 10 pcs/g, diameter 0.07 mm) [24]. and on average 80–230 pcs/cm2. This abundance is Recount of our data on 1 g of thallom mass (on the quickly lowered by periwinkles, which actively con assumption that per receptacle there are 121 scaphidia, sume these shoots: by 2–4 times a month (Maximova, each produces 50 oogonia for the season, i.e., 400 eggs) own data). gave the value about 2–2.5 × 104 eggs; i.e., the degree of values coincides. The average sizes of eggs in our study Our data on the seasonal distribution of fucoid (0.07 mm) fully agree with such for the “autumn” Bal gametes in the coastal plankton of course are not com tic fucus. plete. But it is clear that by the beginning of October Summarizing everything, we may conclude that in the gamete release stops despite the fact that recepta summer in the period of fucoid fruiting antherozoids cles with mature gametangia are left on plants: of A. nodosum and F. vesiculosus, the two most numer “empty” sample no. 40 was taken October 3, 2005, on the border of the littoral and sublittoral zones of Cape ous species of littoral macrophytobenthos of the White ° Sea, may play an important role in the coastal plank Peschany on a sunny and relatively warm day (15 C) ton. The share of antherozoids of fucoids in the total just near the bush of F. vesiculosus, which had nonde biomass of nanoplankton may vary in different regions stroyed male receptacles. Simultaneously, samples of the coast filled with tangles of A. nodosum and taken from traps also gave empty results. F. vesiculosus from 0.1% to 99%, which comprises according to our data 46% on average for A. nodosum CONCLUSIONS in the fruiting period and, for the fruiting period of F. vesiculosus, it is about 7%. If we take into consider (1) The concentration of antherozoids of A. nodosum ation microplankton (20–200 µm), the share of in different points of gathering ranged from 91 to antherozoids will naturally be lower. According to our 55000 cells/ml (0.36–217 mg C/m3); the concentration results, in the littoral zone it is not so evident; plankton of eggs varied in range 0.05–0.6 pcs/ml. For F. vesiculosus, microalgae and inusoria here are not so abundant. In analogous values were not more than 1880 cells/ml the sublittoral zone, the situation may be the reverse. (6.77 mg C/m3) and 0.1—0.7 pcs/ml, respectively. Numerous and diverse representatives of microplank According to data of sedimentation traps for one day at ton even in the period of intensive fruiting of fucoids 1 m2 in tangles of F. vesiculosus (under 100% projec form practically 100% of the total biomass of organ tive coverage) from 18000 to 108000 eggs are released, isms in the size range from 2 to 200 µm. which makes from 0.33 to 2 mg C.
OCEANOLOGY Vol. 50 No. 2 2010 THE ROLE OF GAMETES OF THE MACROALGAE Ascophyllum nodosum (L.) 207
(2) In the period of intensive fruiting of fucoids, 8. A Course in Lower Plants), Ed. by M. V. Gorlenko antherozoids of A. nodosum and F. vesiculosus may (Vysshaya shkola, Moscow, 1981) [in Russian]. play a significant role in coastal plankton. Their share 9. A. A. Kalugina Gutnik, Phytobenthos of the White Sea in the total biomass of nanoplankton may vary from (Naukova dumka, Kiev, 1975) [in Russian]. 0.1 to 99% and, on average, for the fruiting period of 10. A. N. Kamnev, Structure and Functions of Brown Algae A. nodosum is 46% and for the fruiting period of (Mosk. Gos. Univ., Moscow, 1989) [in Russian]. F. vesiculosus is 7%. 11. V. V. Kuznetsov, The White Sea and the Biological Char (3) The obtained real and calculated values of the acteristics of Its Flora and Fauna (Akad. Nauk SSSR, biomass of fucoid gametes (in terms of carbohydrates) Moscow, 1960) [in Russian]. have the same degree but differ by one and a half to 12. L. L. Kuznetsov and E. V. Shoshina, Phytocenoses of the two times. For ascophyllum real values exceed the cal Barents Sea (Physiological and Structural Characteris culated values. This may be explained by the fact that tics) (Izd. KNTs RAN, Apatity, 2003) [in Russian]. a part of the samples were gathered directly in the 13. Yu. A. Mazei, Organization of the Microbenthos Commu propagules cloud. nity in the Zone of Mixing of River and Marine Waters, Candidate’s Dissertation in Biology (Mosk. Gos. (4) The obtained data confirm the fact that settle Univ., Moscow, 2002) [in Russian]. ment in new locality, which is at a distance more than 14. O. A. Pronina, “Raw Resources and Harvest of Algae in 100 m from places of fucoid growth, may occur due to the White Sea,” Rybnoe Khozyaistvo, No. 4, 44–47 cut off by storms and movement of fertile thalloms by (2002). currents. At a distance of 300 m from the shore, there 15. Z. P. Tikhovskaya, “Primary Production of Fucoids in were neither eggs nor antheridia in the samples. Bays of Eastern Murman,” Tr. Murmansk. Biol. Stan tsii 1, 164–188 (1948). ACKNOWLEDGMENTS 16. A. A. Udalov, V. O. Mokievskii, and E. S. Chertoprud, “Influence of the Salinity Gradient on the Distribution The authors are very grateful to Dr. A.I. Azovskii of Meiobenthos in the Chernaya River Estuary (White for active participation in field studies and candidate Sea),” Okeanologiya 45 (5), 719–727 (2005) [Ocean of biological sciences N.V. Kucherik for help in assess ology 45 (5), 680–688 (2005)]. ments and also to Dr. M.B. Flint for support and orga 17. K. M. Khailov, A. V. Prazukin, S. A. Kovardakov, and nization of the White Sea coastal expedition. V. E. Rygalov, Functional Morphology of Marine Multi cellular Algae (Naukova dumka, Kiev, 1992) [in Rus This research was supported by the Presidium of the sian]. Russian Academy of Sciences and the Russian Founda tion for Basic Research (project no. 07 05 00294). 18. P. Aberg and H. 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