1. bookVolume 48 (2019): Issue 3 (September 2019)
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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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23 Feb 2007
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English
Abstract

This study focuses on the taxonomy of epiphytic diatoms in the area of invasive macroalgae from the genus Caulerpa. Caulerpa species are characterized by the presence of secondary metabolites, such as caulerpenyne (CYN), the main function of which is a chemical defense mechanism against herbivores and epiphytes. Epiphytic diatoms were studied on fronds of Caulerpa taxifolia (“killer seaweed”) and, for comparison, on autochthonous macroalgae Padina sp. and Halimeda tuna at the eastern Adriatic Sea coast (Island of Hvar) in the summer and autumn of 2010. The qualitative analysis was performed with the use of light and scanning electron microscopy. The Shannon–Wiener Diversity Index determined for Caulerpa taxifolia showed a wide range of values (3.11–4.88), with a maximum in August and a minimum in October. While the number of taxa on Caulerpa taxifolia fronds increased from June (41) to August (88), it declined in autumn due to the high relative abundance of Cocconeis caulerpacola, which is a diatom typical for Caulerpa. On the other hand, the largest number of taxa on Padina sp. was observed in September (82). The detailed composition of epiphytic diatoms and seasonal dynamics in the area affected by the invasive macroalga Caulerpa taxifolia have been determined for the first time.

Key words

Introduction

The marine green macroalga Caulerpa taxifolia (M.Vahl) C.Agardh has pinnate, fern-like fronds (up to 25 cm long, 2 cm wide) that extend upward from horizontal stolons (Meinesz et al. 1995; Fig. 1). This alga outcompetes native seaweeds and seagrasses in the Mediterranean by forming dense carpets, leading to a loss of biodiversity. It is indigenous to tropical and subtropical seas worldwide, including Australia (Phillips & Price 2002) and has been widely used as a decorative plant in the marine aquarium trade. It was accidentally released from the Monaco Aquarium in 1984 (Meinesz & Hesse 1991), rapidly spread across the western Mediterranean basin (Meinesz et al. 2001) and became one of the most invasive species. In the eastern Adriatic, C. taxifolia was observed for the first time in 1994 in the Bay of Stari Grad (43°10’54”N, 16°35’00”E) on a hard, sandy and muddy substrate without vegetation or within meadows of Posidonia oceanica (L.) Delile (Žuljevic & Antolic 2002).

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)

Caulerpa species are characterized by the presence of secondary metabolites, such as caulerpenyne (CYN), the main function of which is as a chemical defense mechanism against herbivores and epiphytes (Box et al. 2008; Sureda et al. 2009). The maximum concentrations of CYN for the “aquarium-Mediterranean” strain of C. taxifolia were recorded in autumn and the minimum in spring, reaching values that are much higher than those observed in other Caulerpa species (Dumay et al. 2002). Caulerpa taxifolia has a marked seasonal biomass cycle with higher biomass corresponding to higher water temperatures (Meinesz et al. 1995). In summer and autumn, C. taxifolia can grow by nearly 2 cm per day (Meinesz 2002) and during this period fronds of C. taxifolia reach their maximum length (Meinesz & Hesse 1991; Meinesz et al. 1993; 1995). As the growth and toxicity of C. taxifolia vary greatly throughout the year (Amade & Lemée 1998; Thibaut et al. 2004), the chemical defense of this species may affect the settlement and development of different sessile organisms in invaded systems to varying degrees (Prado & Thibaut 2008). As the species turnover is known to be strictly controlled by seasonal variables of the host plant, such as leaf growth (e.g. Wittmann et al. 1981; Prado & Thibaut 2008), it is important to analyze epiphytic diatom assemblages throughout different seasons, which in the case of C. taxifolia means particularly in summer and autumn.

The specific composition of diatom communities of C. taxifolia has not been thoroughly examined, despite the potentially important role of epiphytic diatoms in the functioning of ecosystems influenced by C. taxifolia. The only studies of benthic diatoms from areas of invasive C. taxifolia in the Adriatic were those related to epiphytic diatoms of C. taxifolia and focused on the morphology and description of valve ultrastructure of a new marine diatom, Cocconeis caulerpacola (Car et al. 2012), and the study of epilithic diatom communities from areas of invasive Caulerpa species (Car et al. 2019). The analysis of epiphytic diatoms of another taxa from the genus Caulerpa, Caulerpa racemosa, on the Pacific coast

of Japan was primarily focused on the morphology of taxa from genus Cocconeis (Suzuki et al. 2001). In the Mediterranean Sea, the genus Cocconeis was thoroughly researched when a fine-scale analysis of diatoms associated with Posidonia oceanica was carried out to investigate the composition and diversity of epiphytic communities, with special reference to the most common and abundant genus – Cocconeis (Majewska et al. 2014). The epiphytic diatom communities of the endemic Mediterranean seagrass Posidonia oceanica are among the most frequently analyzed (Mazzella et al. 1994; De Stefano et al. 2000; Majewska et al. 2014). Unlike the Posidonia communities, there are few studies of diatom communities associated with the green macroalga Padina sp. and the brown macroalga Halimeda tuna (J. Ellis & Solander) J. V. Lamouroux in the Mediterranean (e.g. Belegratis & Economou-Amilli 2002).

In general, the majority of previous studies on benthic diatoms in the Adriatic were conducted in the northern Adriatic and estuaries, and seasonal fouling by diatoms was studied on artificial substrates (e.g. Buric et al. 2004; Totti et al. 2007; Caput Mihalić et al. 2008; Levkov et al. 2010; Mejdandžić et al. 2015; Nenadović et al. 2015). Limited information is available on the composition of diatom assemblages growing on either natural or artificial substrates in marine coastal waters of the eastern Middle and South Adriatic, e.g. diatoms from stones in the oligotrophic Bay of Neum in Bosnia and Herzegovina (Hafner et al. 2018a,b) and along the Albanian coastal wetlands (Miho & Witkowski 2005).

The main objective of this study was to describe the dynamics of diatoms on the invasive macroalga Caulerpa taxifolia during a monthly sampling over summer and autumn and to compare the structure of epiphytic diatom assemblages of the investigated invasive macroalgae with the taxonomic composition of epiphytic diatoms on autochthonous brown (Padina sp.) and green (Halimeda tuna) algae in the area inhabited by C. taxifolia in the Adriatic. Due to differing thallus architecture, it was expected that the taxonomic composition of epiphytic diatoms on the investigated macroalgae would vary. In addition, the diversity of dominant diatom genera found in this area is thoroughly described. The results of the analysis of the epiphytic diatom community and its succession on macroalgae on a fine time scale in an area affected by invasive C. taxifolia in the Adriatic Sea are described for the first time.

Materials and methods
Study Area

Thalli of Caulerpa taxifolia were sampled during summer and autumn 2010 by SCUBA diving in the Bay of Stari Grad, the Island of Hvar, the Central Adriatic, Croatia (Fig. 2). The Bay of Stari Grad is a semi-enclosed bay with the prevailing cyclonic currents driven mainly by seasonal winds (Cvitkovic et al. 2017). The sampling site is one of the sunniest areas in Croatia (Zaninović & Matzarakis 2007). It is characterized by Mediterranean climate and is exposed to anthropogenic impact (tourism) limited to the summer season. The sampling site of C. taxifolia was quite shallow (maximum depth of 8 m) and water temperature ranged from 20 to 25°C. Specimens of C. taxifolia were carefully detached from the seafloor at a depth of ca. 5–8 m in three replicates without damaging the fronds and avoiding the dispersal of fragments. In order to conduct a detailed analysis of epiphytic diatom assemblages occurring on fronds of C. taxifolia and to describe their dynamics on a fine time scale, the younger 2 cm tips of C. taxifolia fronds were cut and prepared for diatom analysis. Sampling was carried out from June to October 2010.

Figure 2

Map of the study site

To compare the epiphytic diatom community on Caulerpa taxifolia with communities reported in previous studies and to provide information about host dependence, particularly due to the existence of toxins characteristic for Caulerpa species, sampling of the autochthonous brown alga Padina sp. and the autochthonous green alga Halimeda tuna was conducted at the same time from the same localities. Replicates of three different specimens of each macroalga collected simultaneously were selected. While all five samples of Padina sp. were collected in three replicates between June and October 2010, only three samples of H. tuna were collected in three replicates in June, July and September.

Sample preparation

Immediately after the macroalgal samples were collected, they were fixed in 4% formaldehyde solution in seawater. Organic material was removed from samples prior to light (LM) and electron microscopy (EM) observations by boiling with 30% H2O2 and adding 10% HCl to remove CaCO3. They were then rinsed with deionized water, pipetted onto ethanol-cleaned coverslips and left to air dry before mounting in Naphrax®.

Light microscopy

Slides and the prepared material were deposited in the diatom collection (SZCZ) of the Institute of Marine Sciences, University of Szczecin (Poland). The abundance of diatoms was calculated from three replicate slides per sampling date and substrate to confirm the average relative abundance (RA) of diatoms. The RA of individual taxa and taxa richness in the assemblages were estimated on the basis of at least 300 diatom valves counted per glass slide. As the surface (or weight) of thalli fragments was not measured before the cleaning procedure, the actual abundance (cells cm−2 or cells g−1) could not be calculated. Our method was designed for qualitative analysis and the abundance of diatom taxa expressed as RA can be found in many papers dealing with diatom communities (Vilbaste et al. 2000; Cunningham & McMinn 2004; Çolak Sabanci 2011; 2012; Çolak Sabanci et al. 2011 etc.).

Identifications were carried out following Witkowski et al. (2000). Terminology follows Round et al. (1990). Nomenclature of the identified taxa follows AlgaeBase (Guiry & Guiry, 2018). Some taxa reported here could not be clearly assigned to the species level (assigned as “sp.”) and they will be subjected to further taxonomic investigations.

For the structural analysis of the diatom communities, the identified taxa were categorized according to their growth form into one of the following groups: adnate (cells growing with the valve face strongly adherent to the substrate and having a limited motility), erect (cells attached to the substrate by stalks, pads or peduncles), motile (biraphid cells moving on the substrate surface), and tube-dwelling (raphid forms living in mucilage tubes produced by themselves; Majewska et al. 2013; 2014; 2016; Round et al. 1990; Totti et al. 2007).

The results of the analysis of epiphytic diatoms were gathered according to the seasons: summer (June, July, August) and autumn (September, October).

Electron microscopy

Ultrastructural analysis was performed with the use of scanning electron microscopy (SEM). A drop of a cleaned sample was air-dried overnight on aluminum stubs and coated with Au/Pd using Precision Etching Coating System Model 682 (Gatan, USA), a coating thickness of 10 nm. SEM observations were primarily conducted at the Warsaw University of Technology, the Faculty of Materials Science and Engineering, using Hitachi S-3500, SU-70 and SEM/ STEM S-5500 (Hitachi, Tokyo, Japan).

Statistical analysis

To analyze the diversity of epiphytic diatom assemblages from different substrates over different months, the Shannon–Wiener Diversity Index (SWDI) was computed (Krebs 1999).

Multidimensional scaling (MDS) ordination and hierarchical clustering (CLUSTER) together with the SIMPROF test, which highlights significantly different (p < 0.05) groups, were used to display differences in communities associated with the substrates and were based on the standardized RA data of all recorded diatom taxa. Data used to perform MDS and Cluster analyses to assess differences between invasive C. taxifolia and autochthonous Padina sp. and H. tuna, and between sampling months, were organized in a matrix of 254 taxa over 13 samples collected during the period of 5 months (June–October 2010). Species abundance data were square root transformed prior to the analysis to normalize the data. A resemblance matrix of the data was generated using Bray Curtis analysis. The dissimilarity percentage analysis (SIMPER; Clarke & Warwick 1994) was used to identify the taxa that contributed most to the differences between the observed clusters.

The analysis of similarities (ANOSIM) was used to determine whether there were any significant differences in the growth form structure and species composition of diatom communities among the selected substrates (macroalgae) and seasons. Adnate diatom taxa belong to the genera Cocconeis, Amphora, and Halamphora, while erect diatoms belong to the genera Grammatophora, Licmophora, Ardissonea, Striatella, Synedra, Fragilaria, Tabularia, and Achnanthes, the motile diatoms belong to the genera Navicula, Nitzschia, Tryblionella and Pleurosigma, and the tube-dwelling diatom taxa to the genera Berkeleya and Parlibellus.

Canonical analysis of principal coordinates (CAP) was used to summarize the structure of diatom assemblages and to characterize epiphytic communities along the months and substrates.

All statistical analyses were performed using the PRIMER v6 software (Clarke & Gorley, 2006) and Statistica 7.0 (StatSoft, Inc. 2004).

Results

Altogether, 137 diatom taxa belonging to 42 diatom genera were identified as epiphytes on the upper 2 cm part of C. taxifolia fronds. The genus with the largest number of taxa was Mastogloia (29), followed by Amphora (18), Nitzschia (14), Cocconeis (9) and Navicula (7).

The number of taxa on C. taxifolia fronds increased from June to August, with the smallest number in June (41) and the largest one in August (88). The largest number of taxa on Padina sp. was observed in September (82; Fig. 3a).

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

The widest (3.11–4.88) range of the Shannon– Wiener Diversity Index was determined for C. taxifolia, with the maximum in August and the minimum in October (Fig. 3b). The reason for the low value of the Shannon–Wiener Diversity Index in June and October 2010 was the high RA (> 40%) of the genus Cocconeis that occurred with a small number of taxa. Cocconeis molesta var. crucifera and Cocconeis scutellum

var. scutellum, which were initially the main fouling components occurring as patches, declined in July to be replaced by Cocconeis caulerpacola, the latter species being dominant in autumn (Fig. 3c). Due to the high RA of C. caulerpacola in September, the maximum abundance of taxa observed on C.taxifolia that month was replaced by the maximum abundance of taxa on Padina sp. The maximum RA of C .caulerpacola of over 40% was observed in October. No correlation between the abundance of C. caulerpacola and sea water temperature was confirmed (Fig. 4).

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

In June, the taxa richness on Padina sp. and H. tuna was higher than on C. taxifolia and in both cases the value of the Shannon–Wiener Diversity Index was almost the same and amounted to about 4.5. In July, the taxa richness of both autochthonous algae declined (Fig. 3b). While the taxa richness on H. tuna remained unchanged throughout the autumn, the taxa richness on Padina sp. increased in August and the Shannon–Wiener Diversity Index remained at the highest level observed in this study (4.95–4.96) over the next months.

Table 1 lists 22 dominant taxa, which were most abundant in the epiphytic diatom assemblage on C. taxifolia fronds. They dominated in terms of both frequency of occurrence (> 40%) and RA in the total number of samples (> 1%). When combined together in a single sample, these 22 dominant taxa contribute from 70 to 87% of RA. The following taxa, characteristic of summer and autumn on C. taxifolia fronds, occurred in all five samples with an average RA>1%: Cocconeis caulerpacola, Hyalosynedra laevigata, Cocconeis molesta var. crucifera, Cocconeis scutellum var. scutellum, Nitzschia lanceolata var. minima, Nitzschia panduriformis var. panduriformis, Mastogloia crucicula var. crucicula, Mastogloia crucicula var. alternans, Toxarium undulatum, Ardissonea fulgens and Nitzschia angularis.

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

Colonization of diatoms on C. taxiofolia fronds in summer indicated, however, that taxa of the genus Mastogloia belong to the dominant taxa in the fouling community. In July and August 2010, Mastogloia spp. occurred with high RA (> 20%) and with a large number of taxa, thus contributing to the high value of the Shannon–Wiener Diversity Index. Of the 19 Mastogloia taxa identified in July 2010, the most abundant was Mastogloia crucicula var. crucicula, followed by Mastogloia crucicula var. alternans and Mastogloia cuneata (Table 2, Fig. 5). Although Mastogloia binotata occurred in all five samples of Caulerpa taxifolia fronds, with the highest RA (1%) observed in July, the average abundance was only 0.6% and therefore M. binotata is not included on the list of the dominant taxa of C.taxifolia fronds. In June 2010, only three taxa of Mastogloia, i.e. M. crucicula var. crucicula, M. crucicula var. alternans and M. cuneata, together accounted for 73% of the total abundance of Mastogloia taxa, thus contributing to the low value of the Shannon–Wiener Diversity Index.

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

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

The distribution of the relative abundance of the dominant genera over time showed that the majority of these genera reached the high RA in July and August (Figs 6a, 7). The exception was Cocconeis with the lowest RA in July and August and the highest value in October (Fig. 6c). The average abundance of Hyalosynedra declined from 25% in June to 8% in October, whereas Amphora showed an increase in the abundance at the beginning of autumn. No significant difference in RA of Navicula taxa was observed during this study period.

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

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

The analysis of the succession of diatoms colonizing C.taxiofolia fronds in summer and autumn by LM and SEM (Fig. 8) showed that colonial tube dwelling forms, e.g. Berkeleya taxa, belonged to the dominant taxa of the fouling community. In the case of the Berkeleya taxa, an interesting switch in the species composition was observed in August and September. The relative abundance of Berkeleya scopulorum, initially the only fouling component representing Berkeleya, decreased in late summer and was replaced by Berkeleya rutilans in early autumn.

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)

The most striking differences in the species composition of the epiphytic diatom community were observed between invasive C. taxifolia on the one hand and the autochthonous green and brown macroalgae on the other (Fig. 9). The cluster analysis performed on the species RA data revealed two groups of significantly different assemblages of epiphytic diatoms inhabiting different hosts (group 1 – Halimeda tuna and Padina sp. and group 2 – Caulerpa taxifolia). The similarity between the two groups, one group consisting of samples of invasive Caulerpa and the other group consisting of autochthonous algae, was less than 40%.

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

As revealed by the cluster analysis, the type of macroalgae has a greater impact on the diatom community structure than monthly changes.

According to the cluster analysis, the shorter initial period (June–July) was clearly separated from the later sampling (August–September–October) for invasive C. taxifolia and Padina sp. No separation related to the month of sampling has been demonstrated for H. tuna.

In addition to clusters 1 and 2, SIMPROF analysis also distinguished sub-clusters A, B, C, and D. Sub-cluster A contained diatom samples of H. tuna, sub-cluster B contained samples of Padina sp. Cluster 2 contained C. taxifolia samples from June and July (sub-cluster C) and samples from August, September and October (sub-cluster D). The highest similarity was observed between samples of Padina sp. from August, September and October.

The SIMPER analysis identified the group of taxa contributing the most (cumulatively 51%) to the variance between invasive and autochthonous algae: Cocconeis caulerpacola, Navicula ramosissima, Hyalosynedra laevigata, Nitzschia fusiformis, Cocconeis molesta var. crucifera, Cocconeis scutellum var. scutellum, Cocconeis cf. scutellum, Nitzschia angularis, Navicula arenaria var. arenaria, Mastogloia decipiens and Mastogloia pusilla var. pusilla (Table 3).

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

Altogether, 158 taxa from 46 genera were identified as epiphytes on the investigated brown macroalga Padina sp. between June and October 2010. Genera with the largest number of taxa were Mastogloia (39), Amphora (21), Nitzschia (13), Diploneis (12), Licmophora (7) and Cocconeis (7). The diatom assemblage of the brown alga was characterized by high RA of taxa belonging to Mastogloia (Table 4). Of the 30 dominant taxa, 12 taxa represented Mastogloia. The average abundance of M. binotata, M. crucicula var. alternans, M. cuneata, M. decipiens, M. ignorata, M. pseudolatecostata and M. pusilla var.

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

pusilla was higher than 2%. The average abundance of M. decipienson Padina sp. was 4.5%, reaching up to 8.4% in August 2010. The diatom assemblage on Padina sp. in June and July 2010 was dominated by Nitzschia fusiformis with RA of 13.48% and 26.25%, respectively. In August, September and October, diatom assemblages were dominated by Navicula ramosissima with RA of 11%, 7.5% and 13% respectively.

In general, epiphytic diatom assemblages of Halimeda tuna are different from those hosted by Padina sp. As revealed by the SIMPER analysis, Cocconeis scutellum var. scutellum, Nitzschia fusiformis, Navicula ramosissima, Navicula sp.1, Nitzschia angularis, Mastogloia decipiens, Amphora acutiuscula, Mastogloia pusilla var. pusilla, Mastogloia cuneata, Mastogloia ignorata, Rhopalodia pacifica, Tabularia ktenoides, Hyalosynedra laevigata and Berkeleya rutilans contributed the most (cumulatively 51%) to the variance between assemblages (Table 5).

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

Altogether, 115 diatom taxa representing 34 genera were recorded as epiphytes on H. tuna from the Hvar sampling site. H. tuna hosted diatom assemblages dominated by taxa belonging to Mastogloia (20), (C. taxifolia, Padina sp., Halimeda tuna). The highest Global R (0.85) value was obtained in the analysis of similarity between diatom communities associated with the type of different macroalgal species (invasive/autochthonous; Table 7). The same test performed on the species RA data indicated that the difference between diatom communities over different sampling seasons was not significant (p >0.05). In terms of growth forms, no significant differences were found between the diatom communities on different macroalgal host species (Table 7).

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

Canonical Analysis of Principal Coordinates CAP (Fig. 10) showed that the samples from sub-cluster A (H. tuna) correlated with Navicula ramosissima and Nitzschia angularis, samples from sub-cluster B (Padina sp.) with taxa of the genus Mastogloia (M. decipiens and M. pusilla var. pusilla) together with Nitzschia fusiformis, while samples from sub-cluster D (C. taxifolia; August, September and October) correlated with the abundance of Cocconeis caulerpacola and Cocconeis cf. scutellum.

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 & Dobosz

Ccfsc = Cocconeis cf. scutellum Ehrenberg

Cmolcr = Cocconeis molesta var. crucifera Grunow in Van Heurck

Cscsc = Cocconeis scutellum Ehrenberg var. scutellum

Hyla = Hyalosynedra laevigata (Grunow) Williams & Round

Made = Mastogloia decipiens Hustedt

Mapu = Mastogloia pusilla (Grunow) Cleve var. pusilla

Naar = Navicula arenaria Donkin var. arenaria

Nara = Navicula ramosissima (Agardh) Cleve

Nian = Nitzschia angularis W. Smith

Nifu = Nitzschia fusiformis Grunow

Amphora (19), Nitzschia (13), Cocconeis (11) and Navicula (8). Of the 30 dominant taxa, six taxa represented Amphora (Table 6), of which Amphora acutiuscula showed the maximum RA of 6% in July. The diatom assemblage on H. tuna in July 2010 was also dominated by N. ramosissima and C. scutellum var. scutellum with RA of 10% and 23%, respectively. In September, diatom assemblages were dominated by the genus Navicula.

ANOSIM indicated that the diatom communities differed significantly depending on the substrate

Discussion

Due to the scarcity of information on benthic diatoms in the Adriatic, particularly from the area affected by the invasive macroalga Caulerpa taxifolia, the results of this study were compared with the literature data from different seas worldwide and the comparison was not limited to the investigated host (macroalga).

The data in this study confirmed the expected differences in the taxonomic composition and abundance of epiphytic diatoms among the investigated macroalgae. This may be explained, at least partly, by different physical, chemical and biological requirements of hosts and their ecological conditions.

In this study, Cocconeis taxa were the dominant epiphytic diatoms on C. taxifolia fronds. This is consistent with the findings of Majewska et al. (2014) for Posidonia oceanica leaves in the Mediterranean. In the case of the latter host, C. scutellum was the dominant taxon. Tanaka (1986) found that diatom taxa having higher adhesive strength (Cocconeis, Achnanthes) may be abundant on various macroalgae and tolerate adverse hydrodynamic conditions such as wave action.

In addition, Al-Yamani & Saburova (2011) showed that the epiphytic diatom assemblage on intertidal macroalgae, including Padina sp. from Kuwait, was largely dominated by Cocconeis taxa and constituted a continuous, almost monospecific layer. In our case, despite the high taxa richness on Padina sp., the epiphytic diatom C. caulerpacola was absent on specimens of this taxon, while it was frequently found on fronds of C. taxifolia.

Epiphytic diatom assemblages on Padina sp. were different from those hosted by Halimeda tuna. Although this study showed the presence of a smaller number of diatom taxa growing on H. tuna compared to Padina sp., the number of the analyzed samples (three on H. tunavs and five on Padina) could not be ignored. In the case of H. tuna, the Amphora taxa could be considered as frequent. The diversity of Mastogloia (>39 taxa) on Padina was much higher than on the two other macroalgae studied, and with the high frequency of occurrence the taxon significantly contributed to the high value of the Shannon–Wiener Diversity Index.

In this study, the dominant taxa on C. taxifolia fronds, in addition to Mastogloia taxa, were those characterized by the high motility (e.g. Navicula and Nitzschia), capable of moving on the substrate to find optimal conditions. Totti et al. (2009) concluded that adnate diatoms, including mostly Cocconeis taxa, appear to be more affected by the structure of the host surface and their abundance increases on thalli that offer a more complex microarchitecture for colonization, while they were absent in soft thalli with smooth surface. Monoraphid Cocconeis tightly adhere along their raphe, but as organisms capable of slow motility they are also able to migrate to areas with the greatest availability of light and nutrients or the least chance of desiccation due to tidal fluctuations (Mitbavkar & Anil 2004), which are generally the areas that provide the most suitable and productive environmental conditions (Edgar & Pickett-Heaps 1984). The chemical defense of C. taxifolia may reduce the settlement rate and the development of sessile organisms in invaded systems (Prado & Thibaut 2008). Preliminary studies of secondary metabolites from macroalgae showed biological activity against epiphytes (Phillips & Towers 1982; de Nys et al. 1991; 1995). Organisms can produce different types and rates of metabolites such as wastes, nutrients and toxins, depending on the season, grazing pressure, developmental stage and biological cycles of individuals. Production and exudation may also vary among different organs of the same individual. Successful colonizers must have either a large tolerance range or settle during phases when – or on organs where – the composition and quantities of exudates are not harmful (Wahl 1989). For the Mediterranean strain of C. taxifolia, the maximum concentrations of caulerpenyne were recorded in autumn and the minimum in spring (Dumay et al. 2002). In our case, high summer and autumn values of toxic substances could be the cause of reduced diversity of diatoms and contribution of C. caulerpacola. In fact, this can be explained by the targeted chemical defense of macroalgae against particular taxa.

Defense and epibiosis may vary among different macroalgae parts. Jennings and Steinberg (1997) reported the greatest epiphyte abundance on the oldest tissue and the lowest on the youngest one. They also found that the epiphyte abundance was strongly correlated with the age of different parts of the thallus of the sublittoral kelp Ecklonia radiata (C.Agardh) J.Agardh. In the case of C. taxifolia, despite the fact that it grows nearly 2 cm per day throughout the summer and autumn (Meinesz 2002), it seems that C. taxifolia grows simultaneously with C. caulerpacola.

The research of Nenadovic et al. (2015) on 11 different artificial substrates exposed to the marine environment in the eastern Middle Adriatic in spring and on shoots of P. oceanica showed differences in quantitative and qualitative composition of diatoms among newly colonized surfaces and implied the preference of diatoms for specific substrates. Nitzschia, Cocconeis and Navicula taxa, which can be considered pioneer epiphytic diatoms regardless of the colonized substrate (Railkin 2004; Nenadovic et al. 2015), were frequently found on all substrates alongside the dominant diatom taxa, Cylindrotheca closterium and Amphora. Our results are consistent with those of Nenadovic et al. (2015) and Navarro et al. (1989), who also found abundant taxa of the genera Mastogloia, Navicula and Nitzschia on diverse marine substrates (organic or inorganic) in the tropical region of Puerto Rico. In addition, research on P.oceanica leaves showed that the diatom community structure is also affected by the seasonal cycle of the plant, the depth of the meadow, the age of leaves, and the grazing pressure exerted by herbivores (Mazzella 1983; Mazzella & Spinoccia 1992; Mazzella et al. 1994; De Stefano et al. 2000).

The results of the presented study clearly showed differences in the diatom species distribution pattern between the selected autochthonous macroalgae and invasive C. taxifolia. This may be explained, at least partly, by varying thallus architecture of the studied species, given that Padina sp. and H. tuna have calcified thalli. In addition, multiple environmental factors reflecting the seasonal and site-specific conditions could also be manifested in the structure and species composition of algal communities. For this reason, the results of the present study imply only that an epiphytic diatom community is affected by macroalgae, especially those containing toxins. The lack of samples of younger parts cut from indigenous algae does not allow us to draw definite conclusions about succession and seasonal specificity or distribution of epiphytic diatoms on macroalgal hosts. It can be assumed that differences between invasive and autochthonous algae would also be noticeable at an early stage of life and exposure of macroalgae to benthic diatoms. Obviously, in order to increase the accuracy of predictions, further long-term studies of dynamics of epiphytic diatoms on different macroalgae and other substrates, as well as effects of various environmental factors on the growth of epiphytic diatoms are necessary.

In summary, this study presents the epiphytic diatom species composition on the invasive macroalga Caulerpa taxifolia distributed along the coast of Croatia and the effects of lifespan and seasons on diatom assemblages. The diatom community on C. taxifolia fronds is dominated by Cocconeis taxa. The succession of diatom assemblages showed remarkable variations over the months of summer and autumn. We confirmed the hypothesis of host specificity of Cocconeis caulerpacola in relation to Caulerpa by showing the total absence of C. caulerpacola on Halimeda tuna and Padina sp. collected at the same time and at the same sites as in the case of the invasive Caulerpa. Knowledge of the diatom community structure in these areas is important for studies of toxic effects of the host and enables a better understanding of the functioning of ecosystems dominated by invasive C. taxifolia.

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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