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Epiphytic diatom assemblages on invasive Caulerpa taxifolia and autochthonous Halimeda tuna and Padina sp. seaweeds in the Adriatic Sea – summer/autumn aspect

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Figure 1

A) Caulerpa taxifolia, the Bay of Stari Grad, the Island of Hvar, 2 cm long cut-off upper part (photo by Tonči Dulčić). B) Padina sp. (arrow) in a dense patch of Caulerpa taxifolia, the Bay of Stari Grad, the Island of Hvar (photo by Tonči Dulčić)
A) Caulerpa taxifolia, the Bay of Stari Grad, the Island of Hvar, 2 cm long cut-off upper part (photo by Tonči Dulčić). B) Padina sp. (arrow) in a dense patch of Caulerpa taxifolia, the Bay of Stari Grad, the Island of Hvar (photo by Tonči Dulčić)

Figure 2

Map of the study site
Map of the study site

Figure 3

A) The number of epiphytic diatom taxa on Caulerpa taxifolia fronds, Padina sp. and Halimeda tuna from June to October 2010. B) Values of the Shannon– Wiener Diversity Index for epiphytic diatom samples on Caulerpa taxifolia, Padina sp. and Halimeda tuna in summer and autumn 2010 on the Island of Hvar. C) Contribution of individual Cocconeis taxa to the epiphytic diatom community on Caulerpa taxifolia in summer and autumn 2010
A) The number of epiphytic diatom taxa on Caulerpa taxifolia fronds, Padina sp. and Halimeda tuna from June to October 2010. B) Values of the Shannon– Wiener Diversity Index for epiphytic diatom samples on Caulerpa taxifolia, Padina sp. and Halimeda tuna in summer and autumn 2010 on the Island of Hvar. C) Contribution of individual Cocconeis taxa to the epiphytic diatom community on Caulerpa taxifolia in summer and autumn 2010

Figure 4

Average abundance of Cocconeis caulerpacola on Caulerpa taxifolia from the Island of Hvar is presented in relation to sea water temperature. N = 5
Average abundance of Cocconeis caulerpacola on Caulerpa taxifolia from the Island of Hvar is presented in relation to sea water temperature. N = 5

Figure 5

A) Relative percentage contribution of individual Mastogloia taxa on Caulerpa taxifolia fronds in June 2010. B) Relative percentage contribution of individual Mastogloia taxa on Caulerpa taxifolia fronds in July 2010
A) Relative percentage contribution of individual Mastogloia taxa on Caulerpa taxifolia fronds in June 2010. B) Relative percentage contribution of individual Mastogloia taxa on Caulerpa taxifolia fronds in July 2010

Figure 6

A) Abundance (%) of Mastogloia taxa on Caulerpa taxifolia fronds from June to October 2010. B) The number of Mastogloia taxa on Caulerpa taxifolia fronds. C) Abundance (%) of the genus Cocconeis on Caulerpa taxifolia fronds from June to October 2010. D) The number of Cocconeis taxa on Caulerpa taxifolia fronds
A) Abundance (%) of Mastogloia taxa on Caulerpa taxifolia fronds from June to October 2010. B) The number of Mastogloia taxa on Caulerpa taxifolia fronds. C) Abundance (%) of the genus Cocconeis on Caulerpa taxifolia fronds from June to October 2010. D) The number of Cocconeis taxa on Caulerpa taxifolia fronds

Figure 7

Abundance (%) of the genera Hyalosynedra, Nitzschia, Navicula, Amphora, Licmophora, Toxarium, Ardissonea and Berkeleya taxa on Caulerpa taxifolia fronds from June to October 2010
Abundance (%) of the genera Hyalosynedra, Nitzschia, Navicula, Amphora, Licmophora, Toxarium, Ardissonea and Berkeleya taxa on Caulerpa taxifolia fronds from June to October 2010

Figure 8

Scanning electron microscope (SEM) micrographs of epiphytic diatoms on the invasive Caulerpa taxifolia and autochthonous Halimeda tuna and Padina sp. macroalgae from the Adriatic Sea. Figs a–c. Cocconeis caulerpacola Witkowski, Car & Dobosz. Figs d, e. Cocconeis scutellum Ehrenberg var. scutellum, sternum valves. Fig. d. External view. Fig. e. Internal view. Figs f, g. Cocconeis molesta var. crucifera Grunow in Van Heurck, Sternum valves. Fig. f. External view; Fig. g. Internal view. Figs h, i. Mastogloia fimbriata (Brightwell) Cleve. Fig. h. External valve view. Fig. i. Internal valve view. Figs j, k. Mastogloia binotata (Grunow) Cleve. Fig. j. External valve view. Fig. k. Internal valve view. Figs l, m. Mastogloia cuneata (Meister) Simonsen. Fig. l. External valve view. Fig. m. Internal valve view. Fig. o. Mastogloia crucicula (Grunow) Cleve var. crucicula; internal view. Fig. p. Mastogloia crucicula var. alternans; internal view. Fig. q. Mastogloia pumila (Grunow) Cleve; internal view. Fig r. Mastogloia ovalis A. Schmidt; internal view. Fig. s. Mastogloia cyclops Voigt; internal valve view. Fig. t. Mastogloia corsicana Grunow in Cleve & Möller; external valve view. Fig. u. Amphora kolbei Aleem; internal view. Figs v, w, x. Navicula subagnita Proshkina-Lavrenko. Figs y, z, aa. Berkeleya scopulorum (Brébisson) Cox; internal views. Fig. ab Berkeleya rutilans (Trentepohl) Grunow; internal view. Figs ac, ad. Ardissonea fulgens (Greville) Grunow (SEM); external views. Fig. ae. Ardissonea crystallina (C.A. Agardh) Grunow; internal view. Scale bars = 100 μm (Fig. ac); 50 μm (Fig. y); 30 μm (Fig. ad); 20 μm (fig. i); 10 μm (Figs d, e, h, j, k, l, s, v); 5 μm (Figs a, b, f, g, m, o, p, q, r, t, u, z, ab, ae); 4 μm (Fig. aa); 3 μm (Fig. x); 1 μm (Fig. w); 500 nm (Fig. c)
Scanning electron microscope (SEM) micrographs of epiphytic diatoms on the invasive Caulerpa taxifolia and autochthonous Halimeda tuna and Padina sp. macroalgae from the Adriatic Sea. Figs a–c. Cocconeis caulerpacola Witkowski, Car & Dobosz. Figs d, e. Cocconeis scutellum Ehrenberg var. scutellum, sternum valves. Fig. d. External view. Fig. e. Internal view. Figs f, g. Cocconeis molesta var. crucifera Grunow in Van Heurck, Sternum valves. Fig. f. External view; Fig. g. Internal view. Figs h, i. Mastogloia fimbriata (Brightwell) Cleve. Fig. h. External valve view. Fig. i. Internal valve view. Figs j, k. Mastogloia binotata (Grunow) Cleve. Fig. j. External valve view. Fig. k. Internal valve view. Figs l, m. Mastogloia cuneata (Meister) Simonsen. Fig. l. External valve view. Fig. m. Internal valve view. Fig. o. Mastogloia crucicula (Grunow) Cleve var. crucicula; internal view. Fig. p. Mastogloia crucicula var. alternans; internal view. Fig. q. Mastogloia pumila (Grunow) Cleve; internal view. Fig r. Mastogloia ovalis A. Schmidt; internal view. Fig. s. Mastogloia cyclops Voigt; internal valve view. Fig. t. Mastogloia corsicana Grunow in Cleve & Möller; external valve view. Fig. u. Amphora kolbei Aleem; internal view. Figs v, w, x. Navicula subagnita Proshkina-Lavrenko. Figs y, z, aa. Berkeleya scopulorum (Brébisson) Cox; internal views. Fig. ab Berkeleya rutilans (Trentepohl) Grunow; internal view. Figs ac, ad. Ardissonea fulgens (Greville) Grunow (SEM); external views. Fig. ae. Ardissonea crystallina (C.A. Agardh) Grunow; internal view. Scale bars = 100 μm (Fig. ac); 50 μm (Fig. y); 30 μm (Fig. ad); 20 μm (fig. i); 10 μm (Figs d, e, h, j, k, l, s, v); 5 μm (Figs a, b, f, g, m, o, p, q, r, t, u, z, ab, ae); 4 μm (Fig. aa); 3 μm (Fig. x); 1 μm (Fig. w); 500 nm (Fig. c)

Figure 9

Cluster analysis and multidimensional scaling (MDS) ordination on Bray–Curtis similarity matrices of square root transformed species-abundance data of epiphytic diatom assemblages collected from all three substrates (Caulerpa taxifolia, Halimeda tuna, Padina sp.) during a period of 5 months from June to October 2010 (taxa relative abundance data). All recorded diatom taxa were used in the ordination analysis. Group average similarity values of clusters with significant differences from CLUSTER analysis were superimposed on the MDS plot (SIMPROF; p < 0.05). Top: Cluster analysis. Red lines indicate homogeneous clusters of taxa detected by SIMPROF. Bottom: MDS. Numbers correspond to the same main clusters detected by SIMPROF. Letters A, B, C and D indicate sub-clusters within the main clusters. Symbols Ctax (Caulerpa taxifolia), Hal (Halimeda tuna), Pad (Padina sp.); Jun (June); Jul (July); Aug (August); Sep (September); Oct (October). N(Ctax) = 5; N(Hal) = 3; N(Pad) = 5
Cluster analysis and multidimensional scaling (MDS) ordination on Bray–Curtis similarity matrices of square root transformed species-abundance data of epiphytic diatom assemblages collected from all three substrates (Caulerpa taxifolia, Halimeda tuna, Padina sp.) during a period of 5 months from June to October 2010 (taxa relative abundance data). All recorded diatom taxa were used in the ordination analysis. Group average similarity values of clusters with significant differences from CLUSTER analysis were superimposed on the MDS plot (SIMPROF; p < 0.05). Top: Cluster analysis. Red lines indicate homogeneous clusters of taxa detected by SIMPROF. Bottom: MDS. Numbers correspond to the same main clusters detected by SIMPROF. Letters A, B, C and D indicate sub-clusters within the main clusters. Symbols Ctax (Caulerpa taxifolia), Hal (Halimeda tuna), Pad (Padina sp.); Jun (June); Jul (July); Aug (August); Sep (September); Oct (October). N(Ctax) = 5; N(Hal) = 3; N(Pad) = 5

Figure 10

Canonical Analysis of Principal Coordinates (CAP; Primer+PERMANOVA, UK). CAP biplot showing months and vectors of diatom relative abundance (%) data (arrows). The group of 11 diatom taxa, which contribute the most (cumulatively 51%) to the variance between invasive and autochthonous algae, was selected according to SIMPER analysis. Codes for the diatom taxa are as follows:Ccaul = Cocconeis caulerpacola Witkowski, Car & DoboszCcfsc = Cocconeis cf. scutellum EhrenbergCmolcr = Cocconeis molesta var. crucifera Grunow in Van HeurckCscsc = Cocconeis scutellum Ehrenberg var. scutellumHyla = Hyalosynedra laevigata (Grunow) Williams & RoundMade = Mastogloia decipiens HustedtMapu = Mastogloia pusilla (Grunow) Cleve var. pusillaNaar = Navicula arenaria Donkin var. arenariaNara = Navicula ramosissima (Agardh) CleveNian = Nitzschia angularis W. SmithNifu = Nitzschia fusiformis Grunow
Canonical Analysis of Principal Coordinates (CAP; Primer+PERMANOVA, UK). CAP biplot showing months and vectors of diatom relative abundance (%) data (arrows). The group of 11 diatom taxa, which contribute the most (cumulatively 51%) to the variance between invasive and autochthonous algae, was selected according to SIMPER analysis. Codes for the diatom taxa are as follows:Ccaul = Cocconeis caulerpacola Witkowski, Car & DoboszCcfsc = Cocconeis cf. scutellum EhrenbergCmolcr = Cocconeis molesta var. crucifera Grunow in Van HeurckCscsc = Cocconeis scutellum Ehrenberg var. scutellumHyla = Hyalosynedra laevigata (Grunow) Williams & RoundMade = Mastogloia decipiens HustedtMapu = Mastogloia pusilla (Grunow) Cleve var. pusillaNaar = Navicula arenaria Donkin var. arenariaNara = Navicula ramosissima (Agardh) CleveNian = Nitzschia angularis W. SmithNifu = Nitzschia fusiformis Grunow

SIMPER analysis of diatom taxa contributing (% cumulative = 51%) to dissimilarities between Padina sp. and Halimeda tuna habitats

Taxa Padina sp. Halimeda tuna
Av. Abund Av. Abund Av. Diss Contrib. % Cum. %
Cocconeis scutellum Ehrenberg var. scutellum 2.12 12.89 5.40 9.65 9.65
Nitzschia fusiformis Grunow 10.41 0.90 4.76 8.50 18.15
Navicula ramosissima (Agardh) Cleve 9.71 14.37 2.60 4.65 22.80
Navicula sp.1 0.00 4.64 2.32 4.15 26.95
Nitzschia angularis W. Smith 3.81 6.86 1.91 3.42 30.37
Mastogloia decipiens Hustedt 3.60 0.24 1.73 3.09 33.46
Amphora acutiuscula Kützing 0.70 3.72 1.51 2.70 36.17
Mastogloia pusilla (Grunow) Cleve var. pusilla 3.16 1.39 1.29 2.30 38.47
Mastogloia cuneata (Meister) Simonsen 3.60 1.25 1.28 2.29 40.76
Mastogloia ignorata Hustedt 3.12 0.65 1.27 2.27 43.02
Rhopalodia pacifica Krammer 2.79 0.33 1.27 2.26 45.29
Tabularia ktenoides Kuylenstierna 0.76 2.88 1.09 1.94 47.23
Hyalosynedra laevigata (Grunow) Williams & Round 5.20 6.68 1.02 1.82 49.05
Berkeleya rutilans (Trentepohl) Grunow 2.22 0.50 1.01 1.81 50.87

SIMPER analysis of diatom taxa contributing (% cumulative = 51%) to dissimilarities between invasive C. taxifolia and coexisting autochthonous (Padina sp. + Halimeda tuna) macroalgae

Taxa Invasive alga Autochthonous algae
Av. Abund Av. Abund Av. Diss Contrib% Cum.%
Cocconeis caulerpacola Witkowski, Car & Dobosz 16.31 0.03 8.23 11.87 11.87
Navicula ramosissima (Agardh) Cleve 0.93 11.45 5.30 7.64 19.51
Hyalosynedra laevigata (Grunow) Williams & Round 14.44 5.75 4.36 6.29 25.80
Nitzschia fusiformis Grunow 0.33 6.85 3.31 4.77 30.57
Cocconeis molesta var. crucifera Grunow in Van Heurck 9.01 3.27 3.16 4.56 35.13
Cocconeis scutellum Ehrenberg var. scutellum 5.47 6.16 3.00 4.33 39.46
Cocconeis cf. scutellum Ehrenberg 5.00 0.00 2.53 3.65 43.11
Nitzschia angularis W. Smith 1.37 4.96 1.82 2.63 45.74
Navicula arenaria Donkin var. arenaria 2.70 0.16 1.31 1.89 47.63
Mastogloia decipiens Hustedt 0.16 2.34 1.16 1.67 49.30
Mastogloia pusilla (Grunow) Cleve var. pusilla 0.35 2.50 1.13 1.64 50.94

Occurrence of different taxa from the genus Mastogloia on Caulerpa taxifolia fronds from June to October 2010 (“+” indicates the presence and “ ” the absence of a taxon in the sample)

Mastogloia species: June 2010 July 2010 August 2010 September 2010 October 2010
Mastogloia baldjikiana Grunow +
Mastogloia binotata (Grunow) Cleve + + + + +
Mastogloia borneensis Hustedt + +
Mastogloia cf. cyclops Voigt +
Mastogloia cf. laminaris Grunow + +
Mastogloia cf. varians Hustedt +
Mastogloia corsicana Grunow in Cleve & Möller + + +
Mastogloia crucicula (Grunow) Cleve var. crucicula + + + + +
Mastogloia crucicula var. alternans Zanon + + + + +
Mastogloia cuneata (Meister) Simonsen + + + +
Mastogloia cyclops Voigt + + +
Mastogloia decipiens Hustedt + + +
Mastogloia delicatissima Hustedt +
Mastogloia emarginata Hustedt + + +
Mastogloia erythraea Grunow var. erythraea +
Mastogloia fimbriata (Brightwell) Cleve + + +
Mastogloia hovarthiana Grunow + + + +
Mastogloia ignorata Hustedt + + +
Mastogloia inaequalis Cleve +
Mastogloia linearis Simonsen +
Mastogloia pisciculus Cleve +
Mastogloia pseudoexigua Cholnoky +
Mastogloia pseudolatecostata Yohn & Gibson + + + +
Mastogloia pumila (Grunow) Cleve +
Mastogloia pusilla (Grunow) Cleve var. pusilla + + + +
Mastogloia regula Hustedt +
Mastogloia similis Hustedt + + +
Mastogloia spec. 1 (Ico.Diat.Vol.7, Pl. 75 Fig. 7-9) + + + +
Mastogloia spec. 2 (Ico.Diat.Vol.7, Pl. 82 Fig. 13, 14) +
TOTAL : 8 19 18 17 10

Dominant diatom taxa on Padina sp. with average relative abundance (Avg. RA) > 1% and frequency of occurrence (Freq.) > 20% in summer and autumn 2010. N = 5

Padina sp. – dominant taxa: Freq. (%) Avg. RA (%)
Amphora helenensis Giffen 100.00 1.54
Ardissonea crystallina (C.A. Agardh) Grunow 80.00 1.34
Auricula sp. 1 20.00 1.93
Berkeleya rutilans (Trentepohl) Grunow 100.00 2.22
Berkeleya scopulorum (Brébisson) Cox 100.00 1.66
Cocconeis molesta var. crucifera Grunow in Van Heurck 100.00 3.17
Cocconeis scutellum Ehrenberg var. scutellum 100.00 2.12
Cyclophora tenuis Castracane 1878 40.00 1.12
Hyalosynedra laevigata (Grunow) Williams & Round 100.00 5.20
Mastogloia binotata (Grunow) Cleve 100.00 2.16
Mastogloia corsicana Grunow in Cleve & Möller 100.00 1.05
Mastogloia crucicula (Grunow) Cleve var. crucicula 100.00 1.87
Mastogloia crucicula var. alternans Zanon 100.00 2.30
Mastogloia cuneata (Meister) Simonsen 100.00 3.60
Mastogloia decipiens Hustedt 80.00 4.50
Mastogloia ignorata Hustedt 100.00 3.12
Mastogloia inaequalis Cleve 60.00 1.40
Mastogloia ovalis A. Schmidt 80.00 1.17
Mastogloia pseudolatecostata Yohn & Gibson 100.00 2.09
Mastogloia pusilla (Grunow) Cleve var. pusilla 100.00 3.16
Mastogloia spec. 1 (Ico.Diat.Vol.7, Pl. 75 Figs 7-9) 100.00 1.50
Navicula ramosissima (Agardh) Cleve 100.00 9.71
Nitzschia angularis W. Smith 100.00 3.81
Nitzschia fusiformis Grunow 100.00 10.41
Nitzschia lanceolata var. minima Grunow 100.00 3.14
Nitzschia panduriformis Gregory var. panduriformis 100.00 2.51
Nitzschia scalpelliformis Grunow 20.00 1.47
Opephora pacifica (Grunow) Petit 100.00 1.05
Rhopalodia pacifica Krammer 100.00 2.79
Toxarium undulatum Bailey 80.00 1.06

Dominant diatom taxa on Halimeda tuna with average relative abundance (Avg. RA) > 1% and frequency of occurrence (Freq.) > 33% in summer and autumn 2010. N = 3

Halimeda tuna - dominant taxa: Freq. (%) Avg. RA (%)
Amphora acutiuscula Kützing 100.00 3.72
Amphora cf. marina Witkowski, Lange-Bertalot & Metzeltin 100.00 2.02
Amphora helenensis Giffen 100.00 1.48
Amphora kolbei Aleem 66.67 1.69
Amphora sp.1 33.33 1.54
Amphora sp. 2 33.33 1.10
Ardissonea crystallina (C.A. Agardh) Grunow 100.00 1.18
Bacillaria socialis (Gregory) Ralfs 33.33 1.28
Berkeleya scopulorum (Brébisson) Cox 33.33 2.56
Cocconeis cf. krammeri Lange-Bertalot & Metzeltin 33.33 3.09
Cocconeis costata Gregory var. costata 66.67 1.12
Cocconeis molesta var. crucifera Grunow in Van Heurck 100.00 3.45
Cocconeis scutellum Ehrenberg var. scutellum 100.00 12.89
Cyclophora tenuis Castracane 1878 33.33 2.31
Diploneis vacillans (A. Schmidt) Cleve var. vacillans 100.00 1.66
Fragilaria investiens (W. Smith) Cleve-Euler 100.00 2.16
Hyalosynedra laevigata (Grunow) Williams & Round 100.00 6.68
Licmophora remulus Grunow 33.33 1.03
Mastogloia crucicula var. alternans Zanon 100.00 2.40
Mastogloia cuneata (Meister) Simonsen 100.00 1.25
Mastogloia pusilla (Grunow) Cleve var. pusilla 66.67 2.09
Navicula ramosissima (Agardh) Cleve 100.00 14.37
Navicula sp.1 66.67 6.96
Navicula subagnita Proschkina-Lavrenko 100.00 1.81
Nitzschia angularis W. Smith 100.00 6.86
Nitzschia lanceolata var. minima Grunow 66.67 2.99
Nitzschia panduriformis Gregory var. panduriformis 100.00 1.34
Nizschia lanceolata var. minima Grunow 33.33 1.69
Seminavis sp. 1 100.00 1.12
Tabularia ktenoides Kuylenstierna 100.00 2.88

Results of the ANOSIM test performed on species and growth form relative abundance data. S– species; GF – growth form

Substrate (C. taxifolia, Padina sp., H. tuna) Type of macroalga (invasive/autochthonous) Months Season (summer/autumn) Sea temperature
S GF S GF S GF S GF S GF
p 0.001 >0.05 0.001 >0.05 >0.05 >0.05 >0.05 >0.05 >0.05 >0.05
Global R 0.717 0.518 0.850 0.463 −0.251 −0.335 0.049 −0.022 −0.214 −0.138

Dominant diatom taxa on upper 2 cm of Caulerpa taxifolia fronds with average relative abundance (Avg. RA) > 1% and frequency of occurrence (Freq.) > 40% in summer and autumn 2010. N = 5

Caulerpa taxifolia fronds – dominant taxa: Freq. (%) Avg. RA (%)
Amphora helenensis Giffen 60.00 2.05
Ardissonea fulgens (Greville) Grunow 100.00 1.54
Berkeleya scopulorum (Brébisson) Cox 80.00 1.13
Cocconeis caulerpacola Witkowski, Car & Dobosz 100.00 16.31
Cocconeis cf. scutellum Ehrenberg 80.00 6.25
Cocconeis molesta var. crucifera Grunow in Van Heurck 100.00 9.01
Cocconeis scutellum Ehrenberg var. scutellum 100.00 5.47
Hyalosynedra laevigata (Grunow) Williams & Round 100.00 14.44
Licmophora remulus Grunow 80.00 1.88
Mastogloia crucicula (Grunow) Cleve var. crucicula 100.00 2.59
Mastogloia crucicula var. alternans Zanon 100.00 2.02
Mastogloia cuneata (Meister) Simonsen 80.00 1.69
Mastogloia pseudolatecostata Yohn & Gibson 80.00 3.23
Mastogloia spec. (Ico.Diat.Vol.7, Pl. 75 Figs 7-9) 80.00 1.52
Navicula arenaria Donkin var. arenaria 80.00 3.38
Navicula ramosissima (Agardh) Cleve 60.00 1.55
Navicula subagnita Proschkina-Lavrenko 40.00 1.88
Nitzschia angularis W. Smith 100.00 1.37
Nitzschia lanceolata var. minima Grunow 100.00 2.96
Nitzschia panduriformis Gregory var. panduriformis 100.00 2.61
Opephora pacifica (Grunow) Petit 60.00 1.57
Tabularia ktenoides Kuylenstierna 40.00 1.21
Toxarium undulatum Bailey 100.00 1.57
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