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

Car, Ana; Witkowski, Andrzej; Dobosz, Sławomir; Jasprica, Nenad; Ljubimir, Stijepo; Zgłobicka, Izabela

doi:10.2478/ohs-2019-0019

Figures & Tables

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) 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

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

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

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)

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

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
Taxa	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
Taxa	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

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

Figures & Tables

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

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

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)

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

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

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

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

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