ICES Journal of Marine Science: Journal du Conseil

Malavenda, Sergey, S;Malavenda, Svetlana, V;Chovgan,, Olga

doi: 10.1093/icesjms/fsz076pmid: N/A

Abstract The mutual influence of the dominant macroalgae species inhabiting the intertidal zone of the Murman Coast was studied. Particularly, the proposed negative effect of Palmaria palmata on the growth of Fucus algae was tested. The interspecific interactions of the Fucus vesiculosus, F. distichus, F. serratus, and P. palmata were studied experimentally. The species were cultivated pairwise in the laboratory. A field experiment with species removal was performed in the intertidal zone of the Zelenetskaya Bay, the Barents Sea. The growth rate, algae biomass, and the content of chlorophyll pigments was measured. Fucus species affected positively the growth of P. palmata. No effect of the other species on F. vesiculosus was recorded under the experimental conditions. Palmaria palmata affected negatively the growth of F. serratus; its presence led to an increase in the pigment content in F. serratus and F. distichus. Introduction According to a number of researchers, the competitive relationships between species are the key factor in the formation of biocenoses; these relationships are the main selection force (Paine, 1990; Karez and Chapman, 1998; Choi and Norton, 2005; Scrosati, 2005; Nabivailo and Titlyanov, 2006). Epiphytes are mainly believed to have a direct negative influence on the host’s fitness because of competition for light and nutrients, decreasing its growth and reproductive efficiency, or by attracting grazers, which may cause tissue loss in the host alga (Karez et al., 2000; Rohde et al., 2008; Wiencke and Bischof, 2012). Epiphytes can suppress the growth of the algae due to allelopathy or by increasing the total biomass of their community, thus contributing to the detachment of the basophyte from the substrate (Harlin and Rice, 1987; Svirski et al., 1993). However, epiphytes may also enhance survival of basibionts by protecting them from biotic stress (i.e. being more palatable to grazers than their host and, thus, deflect grazing pressure) or from harsh abiotic conditions by offering shelter from UV-radiation and desiccation during emersion (Worm and Sommer, 2000; Longtin et al., 2009). Positive interactions between seaweeds, such as mutualism, commensalism, and protocooperation, are important in algal communities (Wiencke and Bischof, 2012; Bronstein, 2015). The interactions of key species of algae are of great interest due to the overall influence they finally have on the total community. Fucus vesiculosus L., Fucus distichus L., Fucus serratus L. (Fucaceae, Phaeophyceae, rockweeds), and Palmaria palmata (L.) F. Weber & D. Mohr (Palmariaceae, Rhodophyta, dulse) comprise >80% of the biomass of the intertidal communities at the Murman Coast of the Barents Sea, so they are the key species in this region. All these species are perennial, with a relatively complexly organized thallus; they are widespread, dominate in the intertidal communities, and have a commercial value. At the intertidal zone of the Murman Coast, P. palmata is a non-obligate epiphyte of Fucus algae, i.e. it grows on both the algae (F. vesiculosus, F. distichus, F. serratus, and on some other species from time to time) and boulder or rocky ground. Palmaria palmata is distributed along the entire coastline of the Murman Coast. Its biomass reaches up to 3 kg m−2 in the boulder–cobble areas of the littoral, in the zone protected from the surf (Shoshina, 2003). The study aims to search for allelopathic interactions between Fucus and Palmaria, as well as for competition between F. vesiculosus and P. palmata. Material and methods Allelopathy Algae—F. vesiculosus, F. distichus, F. serratus, and P. palmata—were collected in the Belokamennaya Inlet, the Kola Bay, the Barents Sea (Figure 1a). Young thalli were sampled, Fucus species with three branches and P. palmata with two rows of proliferation. Testing for allelopathic effects was performed in August–September 2013 in the laboratory of Murmansk State Technical University, Murmansk. The algae were acclimated for 7 days in a phytotron at a temperature of 7°C and water salinity of 32, close to natural conditions (Mityaev, 2014), at 12/12 L/D illumination of 60 W m−2 (40 980 lux at 555 nm), and constant air agitation. Natural irradiance in the autumn in the intertidal zone of the Murmansk Coast varies between 50 and 80 W m−2 (34 150–54 640 lux at 555 nm); the species under study are well adapted to these conditions, and their light-harvesting complexes provide maximum absorption of energy (Makarov, 1999; Makarov et al., 2010; Makarov and Voskoboinikov, 2012). The experiment was performed in a climatic chamber. The water was changed daily. We tested the species in pairs: F. vesiculosus + F. distichus, F. distichus + P. palmata, and F. serratus + P. palmata. Each experimental pair comprised three treatments: species no. 1 (control), species no. 2 (control), species nos 1 + 2 (experiment). To compensate for the difference in size (and, therefore, weight) of a single thallus of a particular species, the flask volume and the number of thalli per flask varied to have a similar biomass in each of them (Table 1). There are two replicate flasks for each treatment. The experiment lasted for 7 weeks. Table 1. Experimental design and wet weight of the studied specimens at the start of the experiment. Treatment Mi, g Ni Ma/Vw, g l−1 Vw, l F. vesiculosus + F. distichus: 5 + 5 2  F. vesiculosus 0.479 ± 0.105 5 2.40 1  F. distichus 0.521 ± 0.274 5 2.61 1  F. vesiculosus (control) 0.501 ± 0.146 10 2.51 2  F. distichus (control) 0.518 ± 0.085 10 2.59 2 F. serratus + P. palmata: 7 + 8 4  F. serratus 0.885 ± 0.254 7 3.10 2  P. palmata 0.691 ± 0.349 8 2.77 2  F. serratus (control) 0.803 ± 0.325 15 3.01 4  P. palmata (control) 0.685 ± 0.267 15 2.57 4 F. distichus + P. palmata: 10 + 10 3  F. distichus 0.407 ± 0.231 10 2.71 1.5  P. palmata 0.434 ± 0.261 10 2.89 1.5  F. distichus (control) 0.407 ± 0.233 20 2.71 3  P. palmata (control) 0.394 ± 0.229 20 2.63 3 Treatment Mi, g Ni Ma/Vw, g l−1 Vw, l F. vesiculosus + F. distichus: 5 + 5 2  F. vesiculosus 0.479 ± 0.105 5 2.40 1  F. distichus 0.521 ± 0.274 5 2.61 1  F. vesiculosus (control) 0.501 ± 0.146 10 2.51 2  F. distichus (control) 0.518 ± 0.085 10 2.59 2 F. serratus + P. palmata: 7 + 8 4  F. serratus 0.885 ± 0.254 7 3.10 2  P. palmata 0.691 ± 0.349 8 2.77 2  F. serratus (control) 0.803 ± 0.325 15 3.01 4  P. palmata (control) 0.685 ± 0.267 15 2.57 4 F. distichus + P. palmata: 10 + 10 3  F. distichus 0.407 ± 0.231 10 2.71 1.5  P. palmata 0.434 ± 0.261 10 2.89 1.5  F. distichus (control) 0.407 ± 0.233 20 2.71 3  P. palmata (control) 0.394 ± 0.229 20 2.63 3 Ni is the number of specimens (experimental algae in one flask) in the treatment; Mi is the average wet weight of specimens per one experimental flask; Ma is the total weight of all specimens in particular treatment; Vw is water volume in the experimental flask. View Large Table 1. Experimental design and wet weight of the studied specimens at the start of the experiment. Treatment Mi, g Ni Ma/Vw, g l−1 Vw, l F. vesiculosus + F. distichus: 5 + 5 2  F. vesiculosus 0.479 ± 0.105 5 2.40 1  F. distichus 0.521 ± 0.274 5 2.61 1  F. vesiculosus (control) 0.501 ± 0.146 10 2.51 2  F. distichus (control) 0.518 ± 0.085 10 2.59 2 F. serratus + P. palmata: 7 + 8 4  F. serratus 0.885 ± 0.254 7 3.10 2  P. palmata 0.691 ± 0.349 8 2.77 2  F. serratus (control) 0.803 ± 0.325 15 3.01 4  P. palmata (control) 0.685 ± 0.267 15 2.57 4 F. distichus + P. palmata: 10 + 10 3  F. distichus 0.407 ± 0.231 10 2.71 1.5  P. palmata 0.434 ± 0.261 10 2.89 1.5  F. distichus (control) 0.407 ± 0.233 20 2.71 3  P. palmata (control) 0.394 ± 0.229 20 2.63 3 Treatment Mi, g Ni Ma/Vw, g l−1 Vw, l F. vesiculosus + F. distichus: 5 + 5 2  F. vesiculosus 0.479 ± 0.105 5 2.40 1  F. distichus 0.521 ± 0.274 5 2.61 1  F. vesiculosus (control) 0.501 ± 0.146 10 2.51 2  F. distichus (control) 0.518 ± 0.085 10 2.59 2 F. serratus + P. palmata: 7 + 8 4  F. serratus 0.885 ± 0.254 7 3.10 2  P. palmata 0.691 ± 0.349 8 2.77 2  F. serratus (control) 0.803 ± 0.325 15 3.01 4  P. palmata (control) 0.685 ± 0.267 15 2.57 4 F. distichus + P. palmata: 10 + 10 3  F. distichus 0.407 ± 0.231 10 2.71 1.5  P. palmata 0.434 ± 0.261 10 2.89 1.5  F. distichus (control) 0.407 ± 0.233 20 2.71 3  P. palmata (control) 0.394 ± 0.229 20 2.63 3 Ni is the number of specimens (experimental algae in one flask) in the treatment; Mi is the average wet weight of specimens per one experimental flask; Ma is the total weight of all specimens in particular treatment; Vw is water volume in the experimental flask. View Large Figure 1. View largeDownload slide (a) Study sites at the Murman Coast. (1) Kola Inlet (collection of algae for laboratory experiment), (2) Zelenetskaya Bay. (b) Schematic map of Zelenetskaya Bay. The areas of the experimental sites are depicted separately. Figure 1. View largeDownload slide (a) Study sites at the Murman Coast. (1) Kola Inlet (collection of algae for laboratory experiment), (2) Zelenetskaya Bay. (b) Schematic map of Zelenetskaya Bay. The areas of the experimental sites are depicted separately. The state of the algae taken for the experiment was assessed using the content of chlorophylls a and c (at the end of the experiment), the absolute and relative growth rates of the thallus length and wet weight (at the end of each week). Growth rate of macroalgae reliably characterizes their physiological state during the prolonged cultivation (Khailov and Burlakova, 1969; Khailov et al., 1978). The algae were weighed with 0.01-g accuracy after double superficial drying with filter paper; the length of the tallus was determined with 1-mm accuracy by the longest branch. The growth rates were calculated according to Shoshina (2003): GRl= Δl/Δt, (1) GRw= Δw/Δt, (2) RGRl=ln ΔlΔt, (3) RGRw=ln ΔwΔt, (4) where GRl is the absolute growth rate in length units (cm day−1); GRw is the absolute growth rate in weight units (g day−1); RGRl is the relative growth rate, length (%); RGRw is the relative growth rate, weight (%); l is the thalli length (cm); and W is the wet weight of thalli (g). The content of chlorophylls a and c was analysed according to the standard method (Shoaf and Lium, 1976; Chakchir and Aleksejeva, 2002): 95% ethanol was used as the solvent for brown algae; acetone (AR grade) for red algae (only chlorophyll a was measured). The reciprocal effect of the algae was assessed using two-way ANOVA (α = 0.05, an error of the mean was set as a confidence interval). Presence of another species and time of cultivation were the independent factors. Сompetition in the littoral The field experiment was performed in the Zelenetskaya Bay (69°7′15″N 36°5′11″E; Figure 1a and b). In August 2010, three experimental sites on two plots (1 m × 2 m) were set at the middle level of the intertidal zone, parallel to the water’s edge. The thalli of F. vesiculosus were completely removed from one site, P. palmata from the second site, while the third plot was designated as a control (no weeding performed). Quantitative samples were taken from the control site. It was assumed that the linear dimensions of the experimental sites allowed to avoid the influence of neighbouring intertidal zones that were not covered by the experiment. A year later, the algae were removed again from each plot: thalli of F. vesiculosus from the first plot, P. palmata from the second; at the third plot no weeding was performed. In August 2012, three quantitative samples were taken using a 0.25-m2 frame from each plot, including the undisturbed part of the control plot. The biomass of each species, the share of P. palmata growing freely on the bottom and as epiphytes on Fucus spp., and the species ratio were assessed. The significance of changes between the years of observation at a certain site and between sites in particular year was assessed by paired two-sample t-test for medium. Results Allelopathy Initial level of chlorophyll content in F. vesiculosus was: Chl a 0.208 ± 0.099 mg g−1, Chl c 0.048 ± 0.023 mg g−1; in F. distichus, Chl a 0.283 ± 0.109 mg g−1, Chl c 0.056 ± 0.018 mg g−1. Chlorophyll content in acclimated thalli and thalli from the littoral was similar. The condition of thalli in the laboratory on the basis of this indicator was assessed as normal. The physiological parameters of F. vesiculosus did not differ in the presence of F. distichus and in the control; this species was characterized by a stable growth rate during the entire experiment (Table 2, Figure 2). There were also no changes in pigment content. When combined with F. vesiculosus, F. distichus grew slowly, but the content of chlorophylls a and c increased. Both species displayed stable growth rates and a constant content of chlorophyll pigments in their respective controls. Table 2. Effects of pairwise cultivation on the relative growth rate (ANOVA). Treatment Species RGRl, cm day−1 RGRw, g day−1 F Fcrit p-value F Fcrit p-value F. vesiculosus + F. distichus F. vesiculosus 4.17 4.20 No 1.97 4.20 No F. distichus 0.03 4.35 No 16.89 4.35 45% F. serratus + P. palmata F. serratus 9.49 4.13 22% 16.50 4.13 32% P. palmata – – – 55.26 4.04 53% F. distichus + P. palmata F. distichus 1.44 4.26 No 0.48 4.26 No P. palmata – – – 4.66 4.20 11% Treatment Species RGRl, cm day−1 RGRw, g day−1 F Fcrit p-value F Fcrit p-value F. vesiculosus + F. distichus F. vesiculosus 4.17 4.20 No 1.97 4.20 No F. distichus 0.03 4.35 No 16.89 4.35 45% F. serratus + P. palmata F. serratus 9.49 4.13 22% 16.50 4.13 32% P. palmata – – – 55.26 4.04 53% F. distichus + P. palmata F. distichus 1.44 4.26 No 0.48 4.26 No P. palmata – – – 4.66 4.20 11% View Large Table 2. Effects of pairwise cultivation on the relative growth rate (ANOVA). Treatment Species RGRl, cm day−1 RGRw, g day−1 F Fcrit p-value F Fcrit p-value F. vesiculosus + F. distichus F. vesiculosus 4.17 4.20 No 1.97 4.20 No F. distichus 0.03 4.35 No 16.89 4.35 45% F. serratus + P. palmata F. serratus 9.49 4.13 22% 16.50 4.13 32% P. palmata – – – 55.26 4.04 53% F. distichus + P. palmata F. distichus 1.44 4.26 No 0.48 4.26 No P. palmata – – – 4.66 4.20 11% Treatment Species RGRl, cm day−1 RGRw, g day−1 F Fcrit p-value F Fcrit p-value F. vesiculosus + F. distichus F. vesiculosus 4.17 4.20 No 1.97 4.20 No F. distichus 0.03 4.35 No 16.89 4.35 45% F. serratus + P. palmata F. serratus 9.49 4.13 22% 16.50 4.13 32% P. palmata – – – 55.26 4.04 53% F. distichus + P. palmata F. distichus 1.44 4.26 No 0.48 4.26 No P. palmata – – – 4.66 4.20 11% View Large Figure 2. View largeDownload slide Major parameters of the cultivated talli at the end of the experiment. (a) RGRl is the relative growth rate, length (%); (b) RGRw is the relative growth rate, weight (%); (c) the chlorophyll a content, mg g−1; and (d) the chlorophyll c content, mg g−1. Figure 2. View largeDownload slide Major parameters of the cultivated talli at the end of the experiment. (a) RGRl is the relative growth rate, length (%); (b) RGRw is the relative growth rate, weight (%); (c) the chlorophyll a content, mg g−1; and (d) the chlorophyll c content, mg g−1. When F. distichus and P. palmata were cultivated together, the growth rate of F. distichus did not differ from the control, but the content of chlorophylls a and c increased (Table 2, Figure 2). In the presence of F. distichus, P. palmata had higher growth rates (both of length and weight), as well as higher content of chlorophyll a. In the control, both species had stable growth rates and a constant content of chlorophyll pigments. When cultivated F. serratus with P. palmata, Fucus specimens slowed down their linear growth rate, but gained more absolute weight. The content of chlorophylls a and c also increased in F. serratus. In the presence of F. serratus, P. palmata was characterized by higher growth rate (in terms of weight) and higher content of chlorophyll a. In the control, both species had stable growth and a constant content of chlorophyll pigments (Table 2, Figure 2). Therefore, the content of chlorophyll pigments increased during joint cultivation of F. distichus and F. serratus with P. palmata in all three species. The growth of P. palmata accelerated in the presence of F. distichus and F. serratus. No effect of P. palmata on the growth rate of F. distichus was detected. Fucus serratus grew slower in the presence of P. palmata. However, the increase in the concentration of chlorophylls or/and growth rate of P. palmata and F. distichus was not observed in the cultivation together. Competition in the littoral In the field experiment, most of the new germlings of Palmaria were found on Fucus, but the biomass of all other epiphyte species of Fucus has significantly reduced compared to the reference site and initial values. When F. vesiculosus was removed, the biomass and the proportion of P. palmata in the sample decreased significantly compared to the control. During the 2 years of observations, the total biomass of macrophytes in all experimental sites decreased, the biomass of F. distichus increased, and the percentage of epiphytes, including P. palmata, significantly decreased (Table 3, Figure 3). Table 3. The biomass of algae at the field experimental sites. Treatment BF. vesiculosus g m−2 BP. palmata g m−2 Bepiphytes g m−2 2010 2012 2010 2012 2010 2012 Removal of P. palmata 1092 ± 305 988 ± 168 0 108 ± 20 304 ± 50 119 ± 51 Removal of F. vesiculosus 0 530 ± 57 905 ± 279 320 ± 88 340 ± 61 71 ± 21 No weeding 1003 ± 402 676 ± 200 605 ± 300 300 ± 282 362 ± 58 327 ± 25 Treatment BF. vesiculosus g m−2 BP. palmata g m−2 Bepiphytes g m−2 2010 2012 2010 2012 2010 2012 Removal of P. palmata 1092 ± 305 988 ± 168 0 108 ± 20 304 ± 50 119 ± 51 Removal of F. vesiculosus 0 530 ± 57 905 ± 279 320 ± 88 340 ± 61 71 ± 21 No weeding 1003 ± 402 676 ± 200 605 ± 300 300 ± 282 362 ± 58 327 ± 25 View Large Table 3. The biomass of algae at the field experimental sites. Treatment BF. vesiculosus g m−2 BP. palmata g m−2 Bepiphytes g m−2 2010 2012 2010 2012 2010 2012 Removal of P. palmata 1092 ± 305 988 ± 168 0 108 ± 20 304 ± 50 119 ± 51 Removal of F. vesiculosus 0 530 ± 57 905 ± 279 320 ± 88 340 ± 61 71 ± 21 No weeding 1003 ± 402 676 ± 200 605 ± 300 300 ± 282 362 ± 58 327 ± 25 Treatment BF. vesiculosus g m−2 BP. palmata g m−2 Bepiphytes g m−2 2010 2012 2010 2012 2010 2012 Removal of P. palmata 1092 ± 305 988 ± 168 0 108 ± 20 304 ± 50 119 ± 51 Removal of F. vesiculosus 0 530 ± 57 905 ± 279 320 ± 88 340 ± 61 71 ± 21 No weeding 1003 ± 402 676 ± 200 605 ± 300 300 ± 282 362 ± 58 327 ± 25 View Large Figure 3. View largeDownload slide The biomass of algae on the experimental sites, g. Initial level—2010 year, other—2012. Figure 3. View largeDownload slide The biomass of algae on the experimental sites, g. Initial level—2010 year, other—2012. Changes in the structure of the plant community during the field experiment evidenced that the average biomass of Fucus species did not change significantly during the observation period. Regard must be paid to the variability of the ratio F. vesiculosus/F. distichus in a particular association, both in terms of space and time. In addition to Fucus and Palmaria, a number of species grew on the experimental sites, the list of which is given below. Among the epiphytes, the weight of Pylaiella littoralis was dominant: its share in total biomass was more 50% (Table 4). Table 4. Species composition and biomass (g m−2) of Fucus’ epiphytes and related species on experimental sites. Species 2010 average 2012 No weeding Removal of F. vesiculosus Removal of P. palmata Epiphytes of Fucus P. palmata (Linnaeus) F. Weber & D. Mohr 52 ± 5 55 ± 6 52 ± 4 11 ±1 P. littoralis (Linnaeus) Kjellman 298 ± 10 213 ± 29 46 ± 28 62 ± 6 Elachista fucicola (Velley) Areschoug 11 ± 2 28 ± 6 14 ± 1 18 ± 6 Dictyosiphon foeniculaceus (Hudson) Greville 1 ± 1 31 ± 2 11 ± 1 28 ± 2 On ground P. palmata 853 ± 45 245 ± 10 320 ± 21 97 ± 11 Acrosiphonia arcta (Dillwyn) Gain 21 ± 5 68 ± 15 8 ± 3 8 ± 2 Blidingia minima (Nägeli ex Kützing) Kylin − − + + Devaleraea ramentacea (Linnaeus) Guiry + 24 ± 14 + + Monostroma grevillei (Thuret) Wittrock + − + − Porphyra umbilicalis Kützing − + 9 ± 0 16 Pseudothrix groenlandica (J. Agardh) Hanic & S. C. Lindstrom − − + − Rhizoclonium riparium (Roth) Harvey + − − + Scytosiphon lomentaria (Lyngbye) Link − − + − Ulvaria obscura (Kützing) Gayral ex Bliding − − − + Vertebrata fucoides (Hudson) Kuntze − + − − Species 2010 average 2012 No weeding Removal of F. vesiculosus Removal of P. palmata Epiphytes of Fucus P. palmata (Linnaeus) F. Weber & D. Mohr 52 ± 5 55 ± 6 52 ± 4 11 ±1 P. littoralis (Linnaeus) Kjellman 298 ± 10 213 ± 29 46 ± 28 62 ± 6 Elachista fucicola (Velley) Areschoug 11 ± 2 28 ± 6 14 ± 1 18 ± 6 Dictyosiphon foeniculaceus (Hudson) Greville 1 ± 1 31 ± 2 11 ± 1 28 ± 2 On ground P. palmata 853 ± 45 245 ± 10 320 ± 21 97 ± 11 Acrosiphonia arcta (Dillwyn) Gain 21 ± 5 68 ± 15 8 ± 3 8 ± 2 Blidingia minima (Nägeli ex Kützing) Kylin − − + + Devaleraea ramentacea (Linnaeus) Guiry + 24 ± 14 + + Monostroma grevillei (Thuret) Wittrock + − + − Porphyra umbilicalis Kützing − + 9 ± 0 16 Pseudothrix groenlandica (J. Agardh) Hanic & S. C. Lindstrom − − + − Rhizoclonium riparium (Roth) Harvey + − − + Scytosiphon lomentaria (Lyngbye) Link − − + − Ulvaria obscura (Kützing) Gayral ex Bliding − − − + Vertebrata fucoides (Hudson) Kuntze − + − − +, species were coupons in the samples, but their biomass was <1 g m−1; −, the species is not detected. View Large Table 4. Species composition and biomass (g m−2) of Fucus’ epiphytes and related species on experimental sites. Species 2010 average 2012 No weeding Removal of F. vesiculosus Removal of P. palmata Epiphytes of Fucus P. palmata (Linnaeus) F. Weber & D. Mohr 52 ± 5 55 ± 6 52 ± 4 11 ±1 P. littoralis (Linnaeus) Kjellman 298 ± 10 213 ± 29 46 ± 28 62 ± 6 Elachista fucicola (Velley) Areschoug 11 ± 2 28 ± 6 14 ± 1 18 ± 6 Dictyosiphon foeniculaceus (Hudson) Greville 1 ± 1 31 ± 2 11 ± 1 28 ± 2 On ground P. palmata 853 ± 45 245 ± 10 320 ± 21 97 ± 11 Acrosiphonia arcta (Dillwyn) Gain 21 ± 5 68 ± 15 8 ± 3 8 ± 2 Blidingia minima (Nägeli ex Kützing) Kylin − − + + Devaleraea ramentacea (Linnaeus) Guiry + 24 ± 14 + + Monostroma grevillei (Thuret) Wittrock + − + − Porphyra umbilicalis Kützing − + 9 ± 0 16 Pseudothrix groenlandica (J. Agardh) Hanic & S. C. Lindstrom − − + − Rhizoclonium riparium (Roth) Harvey + − − + Scytosiphon lomentaria (Lyngbye) Link − − + − Ulvaria obscura (Kützing) Gayral ex Bliding − − − + Vertebrata fucoides (Hudson) Kuntze − + − − Species 2010 average 2012 No weeding Removal of F. vesiculosus Removal of P. palmata Epiphytes of Fucus P. palmata (Linnaeus) F. Weber & D. Mohr 52 ± 5 55 ± 6 52 ± 4 11 ±1 P. littoralis (Linnaeus) Kjellman 298 ± 10 213 ± 29 46 ± 28 62 ± 6 Elachista fucicola (Velley) Areschoug 11 ± 2 28 ± 6 14 ± 1 18 ± 6 Dictyosiphon foeniculaceus (Hudson) Greville 1 ± 1 31 ± 2 11 ± 1 28 ± 2 On ground P. palmata 853 ± 45 245 ± 10 320 ± 21 97 ± 11 Acrosiphonia arcta (Dillwyn) Gain 21 ± 5 68 ± 15 8 ± 3 8 ± 2 Blidingia minima (Nägeli ex Kützing) Kylin − − + + Devaleraea ramentacea (Linnaeus) Guiry + 24 ± 14 + + Monostroma grevillei (Thuret) Wittrock + − + − Porphyra umbilicalis Kützing − + 9 ± 0 16 Pseudothrix groenlandica (J. Agardh) Hanic & S. C. Lindstrom − − + − Rhizoclonium riparium (Roth) Harvey + − − + Scytosiphon lomentaria (Lyngbye) Link − − + − Ulvaria obscura (Kützing) Gayral ex Bliding − − − + Vertebrata fucoides (Hudson) Kuntze − + − − +, species were coupons in the samples, but their biomass was <1 g m−1; −, the species is not detected. View Large At the intertidal zone protected from the wave action, the biomass of P. palmata was higher in the presence of F. vesiculosus, while the reverse effect was not observed (Table 3). The reliability of epiphyte biomass decrease was confirmed by t-statistic values: 45.8 when comparing the control site with the removal of P. palmata, 11.8—with the removal of the F. vesiculosus with a t-critical 2.92. On the site, which was not subjected to selective removal of species, the change in epiphyte biomass was not significant: t-statistics 1.84 with t-critical 2.92. Discussion Searching for the effect one algal species has on another appears to be a complex issue. The influence of abiotic factors can be studied more easily and the conclusions may be drawn quite firmly. When one is assessing the impact of a particular algal species on the other members of the phytocenose, the experimental design as well as the field observations may easily bring contradictory results. To minimize the effect of most of the factors and to focus on studying possible allelopathic interactions, the algae that were cultured in laboratory flasks were free floating, so they did not compete for the light. Their thalli were moved under the air action and mixing, so both sides were illuminated. However, such conditions do not necessarily exclude competition for nutrients. It is known that Palmaria has a higher rate of absorption of nutrients than Fucus species do. Competition for nutrients was minimized by changing the water daily, so that each algal species received enough nutrients. Although we did not measure the concentration of main nutrients (such as nitrates), the combination of flask volume and exposed algal biomass allows us to consider no nutrient limitation during the laboratory experiment, since the growth rates of all the species fit the natural range. Therefore, all the observed changes in the growth rate compared to the control can primarily be explained by the influence of thalli of one species on another. Cultivating different species together has another effect on their parameters. In particular, not only the growth rate was affected, but the concentration of chlorophyll pigments also. Chlorophyll content usually serves as an indicator of the plant and alga fitness (Khailov and Burlakova, 1969; Khailov et al., 1978). The content of chlorophyll pigments increased in the thalli of F. distichus, F. serratus, and P. palmata cultivated together. In F. vesiculosus, there were no changes in the chlorophyll content, when it was cultivated with F. distichus. On one hand, an increase in photosynthetic activity may be used to cover the energy needs for growing and thus evidences on favourable cultivation conditions. On the other hand, no statistically significant changes in chlorophyll content indicate stable conditions. However, bringing together growth rates and chlorophyll content allows us to draw an overall picture of interspecific interactions: No effects of F. distichus and P. palmata on F. vesiculosus were found. Fucus vesiculosus, F. distichus, and F. serratus favourably influenced the growth of P. palmata. Palmaria palmata did not affect the growth and content of pigments in F. distichus. Palmaria palmata negatively affected F. serratus. The results obtained in the field experiment are somewhat different from that of the laboratory experiment performed with the young thalli of these species. When testing Fucus germlings cultivated together, the growth rate was the highest in F. distichus, followed by F. vesiculosus, and the lowest, in F. serratus (Karez, 2003). Therefore, these reported facts and original data support our suggestions about the species interaction. When P. palmata or F. vesiculosus were removed, a change in the community structure was revealed, namely, a decrease in the biomass of epiphytes. The most obvious reason lies in the loss of growth substrate. The bulk of epiphytes in these communities, according to our observations, as in this case, is P. littoralis. This species grows on both the ground and algae, mainly Fucus. Fucus vesiculosus is the most resistant Fucus species to abiotic factors (Chapman 1995; Davison and Pearson, 1996; Wahl et al., 2011), and its distribution in the intertidal zone cannot be explained solely by a combination of external environmental factors of a particular biotope. The combination of external environmental factors (temperature, salinity) and the presence of large beds of F. vesiculosus in the intertidal zone may be the reason for the frequent absence of the areas covered by F. distichus, or inhabiting inner parts of the inlets of the Barents Sea, where it does not form large beds (Blinova, 1969; Shoshina, 2003). The competitive advantage of F. vesiculosus over other Fucus species is supported experimentally in this study. This is probably one of the reasons why F. vesiculosus comprises almost 50% by biomass of all the fucoids on the Murman Coast (Blinova, 1969; Malavenda, 2018). In the Barents Sea, red alga P. palmata grows on the lower level of the intertidal zone, often as the epiphyte of F. serratus. Palmaria palmata grew better in the presence of all three Fucus species, but had a negative effect only on F. serratus. It can be assumed that this case belongs to the kind of the epiphyte–basiphyte interaction, when the epiphyte reduces the basiphyte metabolism via allelopathic substances (Harlin and Rice, 1987; Svirski et al., 1993; Kübler and Raven, 1995; Potin, 2012). During our experiments, we potentially observed the manifestation and positive interspecific interaction, namely the beneficial effect of Fucus species on P. palmata, i.e. the accelerated growth of the latter. It has been found earlier that dense beds of red algae inhibit the growth of Fucus germlings (Brawley and Johnson, 1991). Red algae also produce substances that inhibit the growth of other algae. High absorption rate of nitrates and phosphates by P. palmata may possibly explain this phenomenon. Palmaria palmata and F. vesiculosus are characterized by the highest absorption rates in the group of species we have studied. Palmaria palmata is even recommended as a species for bioremediation in eutrophicated waters (Sanderson et al., 2012; Tremblay-Gratton et al., 2018; Grote, 2019). Complex interspecific interactions were observed between the dominant macroalgae species of the intertidal zone of the Murman Coast. Palmaria palmata is an active and aggressive dominant, effectively competing with Fucus species for space, which is confirmed by the distribution of the studied species in the intertidal zone (Blinova, 1969; Shoshina, 1998, 2003; Malavenda, 2018). Conclusions In the experiments performed both in the laboratory and at the intertidal zone, P. palmata grew better in the presence of Fucus species; F. distichus slowed down its growth rate in the presence of F. vesiculosus, and F. serratus, in the presence of P. palmata. In the thalli of F. distichus, F. serratus, and P. palmata, the content of chlorophyll increased in the presence of representatives of different species. 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