Distribution of aerophilous diatom communities associated with terrestrial green macroalgae in the South Shetland Islands, Maritime Antarctica

Juliana Ferreira da Silva; Maria Angélica Oliveira Linton; Raylane Ribeiro da Anunciação; Eduardo Pereira da Silva; Rodrigo Paidano Alves; Adriano Luis Schünemann; Filipe de Carvalho Victoria; Margéli Pereira de Albuquerque; Antônio Batista Pereira

doi:10.1371/journal.pone.0226691

. 2019 Dec 30;14(12):e0226691. doi: 10.1371/journal.pone.0226691

Distribution of aerophilous diatom communities associated with terrestrial green macroalgae in the South Shetland Islands, Maritime Antarctica

Juliana Ferreira da Silva ^1,^#, Maria Angélica Oliveira Linton ^2,^#, Raylane Ribeiro da Anunciação ^3,^‡, Eduardo Pereira da Silva ^1,^‡, Rodrigo Paidano Alves ^4,^#, Adriano Luis Schünemann ^1,^‡, Filipe de Carvalho Victoria ^1,^*,^#, Margéli Pereira de Albuquerque ^1,^5,^‡, Antônio Batista Pereira ^1,^#

Editor: Jinzhuang Xue⁶

PMCID: PMC6936843 PMID: 31887164

Abstract

The establishment of diatom communities depends on environmental factors such as the type of substrate and geographic conditions that influence the dispersal processes of these organisms. The main goal of this study was to evaluate the similarity between diatom communities associated with the macroalgae Prasiola crispa (Lightfoot) Kützing in relation to spatial distance from six sampled sites located in the South Shetland Islands, Maritime Antarctica. The diatom flora associated with Prasiola crispa was represented by 23 species distributed in 15 genera. Pinnularia australoschoenfelderi Zidarova, Kopalová & Van de Vijver, Luticola austroatlantica Van de Vijver, Kopalová, S.A.Spaulding & Esposito, Luticola amoena Van der Vijver, Kopalová, Zidarova & Levkov, Pinnularia austroshetlandica (Carlson) Cleve-Euler and Psammothidium papilio (D.E. Kellogg et al.) Kopalová & Zidarova were the most abundant species in our samples, together they represented 68% of the total number of individuals collected. There was great similarity and abundance of the diatom communites among the sampled points, which resulted in the absence of a linear relationship pattern with distance between sampling points. We conclude that distance was not a factor of differentiation of Antarctic diatom communities associated with terrestrial green macroalgae. This suggests that Antarctic environments may have unique characteristics with homogeneous abiotic factors, at least in relation to this substrate.

Introduction

The diatom species diversity of the Antarctic is limited by extreme conditions, and studies have led to the conclusion that not all Antarctic islands share a similar flora, although the overall diversity of this flora on the continent is limited compared to tropical and subtropical regions [1]. Furthermore, many of the diatom taxa recently described are endemic to Antarctica and not cosmopolitan [2,3]. Regarding the study of diatom communities, in recent years, a more refined taxonomy has revealed a large number of new species in Antarctica [4–16].

Among biological substrates where microalgal communities may grow, terrestrial macroscopic algae, though unexpected at first, may be included. The class Trebouxiophyceae includes a group of morphologically heterogeneous eukaryotic green algae that occur mainly in soil and continental waters. The genus Prasiola Meneghini belongs to this class and includes marine, terrestrial and continental species. Prasiola crispa (Lightfoot) Kützing is a terrestrial species of Antarctica, which usually grows on moist soils that are fertilized by bird guano, being more abundant inside and around penguin colonies. These macroalgae tolerate repeated cycles of freezing and thawing during the year, as well as high levels of UV radiation during the summer [17]. At the micro-scale level, the substrate of periphytic communities may provide more than an inert surface, since its physical and chemical characteristics can influence the composition of the community and algal biomass [18–20].

Studies that address distribution patterns often document a decrease in species similarity as spatial distance increases between communities [21–23]. This reduction of similarity is attributed to some major factors such as environmental conditions and species dispersal processes. The influence of spatial distance can be summarized as follows: the larger the distance between sites, the larger are the environmental variations and, therefore, the difference between species tends to be also larger. Spatial distance is a factor that influences the displacement of species across smaller distances, once that this factor increases the chances of survival, and therefore is different from migration which applies over greater distances [21]. The main goal of this study was to evaluate the similarity between diatom communities associated with P. crispa spatially distributed in six sites located in the South Shetland Islands, Antarctica. The proposed hypothesis is that the larger the spatial distance between sampling points, the smaller the similarity of diatom communities associated with P. crispa.

Material and methods

During the Brazilian Antarctic Expeditions XXXIII (2014–2015) and XXXIV (2015–2016) (Fig 1), samples of P. crispa where obtained from Ardley Island, Halfmoon Island and King George Island (Copacabana, Punta Plaza, Steinhouse and Voureal), in the Maritime Antarctica (Table 1). All collections were authorized by the Secretariat of the Interministerial Commission for Sea Resources (SECIRM) and endorsed by the Brazilian Government’s Ministry of the Environment, under the activities regulated by the Brazilian Antarctic Program (PROANTAR).

Table 1. Sample site coordinates.

Sample Site	Latitude	Longitude
Ardley Island	62°12'40.40"S	058°55'38.70"W
Halfmoon Island	62°35'41.5"S	059°55'10.1"W
King George Island: Copacabana	62°10'38.4"S	058°26'57.3"W
King George Island: Punta Plaza	62°5'14.69"S	058°23'35.21"W
King George Island: Steinhouse	62°04'18.9"S	058°22'28.2"W
King George Island: Voureal	62°10'2.6"S	058°17’52.0"W

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The samples of P. crispa were stored in sealed plastic bags and frozen for further analysis in the Laboratory of Phycology of the Federal University of Santa Maria (UFSM), Rio Grande do Sul, Brazil. To prepare the material, cell contents and organic matter of the samples were removed by oxidation with hydrogen peroxide (H₂O₂) and potassium permanganate (KMnO₄) [24]. After washing with distilled water, permanent slides were mounted using Naphrax (refractive index of 1.74, Brunel Microscopes Ltd, Chippenham, Wiltshire, United Kingdom), Qualitative and quantitative analyses were carried out under a Leica DM750 optical microscope. The quantitative analyses were performed with approximately 80 valves for each sample, because the abundance is very small in the substrate. Thus, it was necessary to prepare several permanent slides to make observations under this criterion. Species represented by only one or two valves in each sample were excluded from the study to avoid potential contaminants [25–27]. A specific bibliography for identification of polar diatoms was used [1, 8–11, 14–15, 28–45].

For data analysis, the spatial distance in meters between each pair of sampling sites was calculated based on the registered geographical points. Thus, a geographic distance matrix (Table 2) was constructed for further comparison using the matrices from biological similarity of relative abundance (abundance of individuals by taxa) (Table 3) and species composition (presence and absence of taxa in points).

Table 2. Distance table in meters between sampling points where Prasiola crispa was collected in Antarctica.

Sample sites	Ardley	Copacabana	Halfmoon	Punta Plaza	Steinhouse	Voureal
Ardley	0
Copacabana	25.17	0
Halfmoon	66.76	89.14	0
Punta Plaza	31.07	10.43	97.19	0
Steinhouse	32.74	12.37	99.00	1.98	0
Voureal	33.13	7.96	96.46	10.20	10.55	0

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Table 3. List of all observed species with their acronyms and abundance in the samples from Antarctic Islands.

		Sample points
Species	Acro	Ard	Cop	Hal	Pup	Ste	Vou
Luticola amoena Van der Vijver, Kopalová, Zidarova & Levkov	A	0	0	0	0	5.57	0
Luticola austroatlantica Van de Vijver, Kopalová, S.A. Spaulding & Esposito	B	0	0	0	0	2.29	0
Luticola muticopsis (Van Heurck) D.G. Mann	C	0	0	0	0	1.97	1.35
Achnanthes sp.	D	0	0	0	2.41	0	0
Achnanthidium aff indistinctum Van de Vijver & Kopalová	E	0	1.31	0	0	10.49	0
Cyclotella meneghiniana Kützing	F	0	1.74	0	0	0	0
Cocconeis pinnata var. matsii Al-Handal, Riaux-Gobin & Wulff	G	2.44	44.12	10.59	12.65	7.22	11.97
Eunotia aff pseudopaludosa Van de Vijver, de Haan & Lange-Bertalot	H	0	0	32.71	21.68	24.92	2.51
Fragilaria cf parva Tuji & D.M. Williams	I	2.44	4.36	1.87	3.32	0.33	0
Hantzschia amphioxys f. muelleri Ts. KoBayashi	J	7.32	4.36	0	0	0	0
Pteroncola carlinii Almandoz & Ferrario	K	0	0	0	8.43	7.54	0
Mayamaea cf atomus (Kützing) Lange-Bertalot	L	0	0	4.98	0	0	0
Navicula aff perminuta Ǿstrup	M	0	2.18	0	0	0	0
Pinnularia aff microstauron (Ehrenberg) Cleve	N	0	3.06	3.43	0	0	0
Pinnularia australoschoenfelderi Zidarova, Kopalová & Van de Vijver	O	51.21	0	13.39	0	0	53.86
Pinnularia austroshetlandica (Carlson) Cleve-Euler	P	24.39	9.61	0	4.82	6.23	17.57
Pinnularia borealis Ehrenberg sensu lato	Q	12.19	0	3.12	9.94	14.75	0
Psammonthidium rostrogermainii Van de Vijver, Kopalová & Zidarova	R	0	2.18	0	0	6.56	0
Psammothidium germainii (Manguin) Sabbe	S	0	0	7.78	0	3.94	0
Psammothidium papilio (D.E. Kellogg et al.) Kopalová & Zidarova	T	0	13.1	2.18	7.23	8.19	9.85
Pseudogomphonema kamtschaticum (Grunow) L.K.Medlin	U	0	6.98	4.05	0	0	2.89
Luticola olegsakharovii Zidarova, Levkov & Van de Vijver	V	0	0	8.09	20.18	0	0
Thalassiosira gracilis var.expecta G. Fryxell & Hasle	X	0	7.86	7.78	0	0	0

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Acro = Acronyms; Ard = Ardley; Cop = Copacabana; Hal = Halfmoon; PuP = Punta Plaza; Ste = Steinhouse; Vou = Voureal.

The estimation of species richness was based on a simple arithmetic of the estimators, without consideration of standard deviations [46]. The samples sufficiency was calculated based on the percentage of values observed in relation to the estimated values. In order to compare the species richness among the sample points, individual rarefaction curves were constructed, and compared in the lowest abundance value among them (N = 41), in order to correct for differences in size and sample effort. For this purpose, the abundance data of each species were used for each sampling point. The EstimateS program (Department of Ecology & Evolutionary Biology, University of Connecticut, Storrs, USA) was used for analyses, with 100 randomisations of the data [47]. Rank-abundance diagrams were constructed to describe and compare the distribution of abundance and dominance of species at each sampling site using relative abundance data [48]. To describe these distributions numerically, the Pielou equitability index was adopted, based on the Shannon diversity index.

The diversity was partitioned into the alpha, beta and gamma components using Hill’s numbers [49,50] with the “entropart” package [51] in the R program (R Foundation for Statistical Computing, Vienna, Austria) (R Core Team 2017), with the approach of multiplicative partitioning of diversity.

Jaccard and Bray-Curtis dissimilarity coefficients were used to calculate dissimilarity between pairs of sampling points based on incidence and abundance data. An array of geographical (Euclidean) distances between points was derived from the longitude and latitude coordinates. Subsequently, the Jaccard and Bray-Curtis distance matrices were regressed with the geographic distance matrix using linear regressions [52].

The standard coefficients of these regression models were used as measures of the decay rate when comparing similarity as a function of geographical distance between points [22]. In addition, biotic distance data were correlated with the geographic distance matrix in order to corroborate the relationship probability values based on 10,000 permutations using the Mantel test [23]. Statistical analyses were performed in the R program using the "vegan" packages [53] and "betapart" [54] packages, and visualised through dendrograms also using the "vegan" package [53] in R environment.

In order to verify which component of the beta diversity predominantly contributed to the dissimilarity between sampling points, species presence/absence dissimilarity was decomposed into substitution (turnover) and nestedness [54] components, while abundance based dissimilarity was decomposed into the components of abundance balanced variation and abundance gradients [55]. For this, Jaccard and Bray-Curtis dissimilarity coefficients were used in the "betapart" package [56] implemented in the R program. The matrices of beta diversity components based on presence / absence and abundance were also associated to the geographic distance matrix, as previously described, in order to verify which dissimilarity component was related to the spatial configuration of the sampling sites.

The protocols used for the present study can be accessed through protocols (dx.doi.org/10.17504/protocols.io.6tcheiw).

Results and discussion

The diatom flora associated with Prasiola crispa at the six sampling sites were represented by 23 species (Figs 2 and 3) distributed in 15 genera. Two species are typical of marine environments: Pseudogomphonema kamtschaticum, Cocconeis pinnata var. matsii and Pteroncola carlinii. The presence of these species in these terrestrial sites is probably related to their proximity to the sea.

Fig 2 — 1. *Achnanthes* sp, 2. *Achnanthidium aff indistinctum*, 3. *Cyclotella meneghiniana*, 4–10. *Cocconeis pinnata* var. *matsii*, 11. *Eunotia aff pseudopaludosa*, 12. *Fragilaria* cf *parva*, 13. *Hantzschia amphioxys*, 14–17. *Luticola amoena*, 18–21. *Luticola austroatlantica*, 22–25. *Luticola muticopsis*, 26. *Luticola olegsakharovii e* 27. *Mayamaea* cf *atomus*. LM scale bar = 10 μm.

Fig 3 — 28–31. *Navicula aff perminuta*, 32–34. *Pinnularia australoschoenfelderi*, 35–37. *Pinnularia austroshetlandica*, 38–41. *Pinnularia borealis*, 42–44. *Pinnularia aff microstauron*, 45–48. *Psammothidium germainii*, 49. *Psammothidium papilio*, 50. *Psammonthidium rostrogermainii*, 51–55. *Pseudogomphonema kamtschaticum*, 56–59. *Pteroncola carlinii* e 60. *Thalassiosira gracilis var*.expecta. LM scale bar = 10 μm.

Comparing the rarefied richness of the islands, in order to correct for sample size differences between sites, we observed that Steinhoose and Halfmoon had higher species richness, even when comparing the same number of individuals (total abundance = 41 in both sites) (Fig 4). Intermediate richness was observed in Copacabana and Punta Plaza, and even though Voureal had the largest number of individuals, this site had similar rarefied richness to that of Ardley, which had the lowest number of species and individuals (Fig 4).

Fig 4 — The vertical line represents the point of comparison between the islands. Confidence intervals were omitted for better visualization. Ard = Ardley; Cop = Copacabana; Hal = Half Moon; PuP = Punta Plaza; Ste = Steinhoose; Vou = Voureal.

The most abundant species were Pinnularia australoschoenfelderi (20.0%), Luticola austroatlantica (15.5%), Luticola amoena (15.3%), Pinnularia austroshetlandica (9.2%) and Psammothidium papilio (8.0%), which altogether represented 68% of the total number of individuals collected. There was a difference in the most abundant species between each sampling site (Fig 5). The dominance pattern in Steinhoose and Punta Plaza, the two areas closest to each other in this study, was similar, with high abundance of L. austroatlantica and P. borealis. These two areas also had the highest Pielou equitability values (Punta Plaza: Pielou = 0.91, Steinhoose: Pielou = 0.89). However, L. austroatlantica, was also the most abundant at the other extreme of the distance gradient in Halfmoon (Pielou = 0.86). P. australoschoenfelderi dominated in Ardley (Pielou = 0.73) and Voureal (Pielou = 0.71), while L. amoena dominated in Copacabana (Pielou = 0.76). This species was also among the three most abundant species in Halfmoon, Punta Plaza and Voureal.

Fig 5 — The abbreviations refer to the names of the species in Table 2.

The diversity partition demonstrated that true diversity based on species richness (greater weight on rare species), Shannon’s entropy (similar weight on common and rare species), and Simpson index (greater weight on dominant species) showed similar response patterns, with higher values in Steinhoose (Table 4). The alpha diversity was approximately ten species for species richness; this analysis further showed that the true beta diversity of Shannon index (¹D) was lower than the richness based on species richness (⁰D) and based on the inverse concentration of Simpson index (²D). This shows that differences between sampling sites occurred due to the contrast between the most abundant and the rarest species at each site (Table 4). The beta diversity values for all orders were close to 2, indicating that there are at least two large groups of species with high substitutions.

Table 4. Multiplicative partitioning of the diatom species diversity associated with Prasiola crispa for the sampled sites.

	Islands						Components of diversity
	Ard	Half	Cop	PuPl	Stei	Vou	A	β	γ
⁰D	6	12	12	9	13	7	10	2.3	23
¹D	3.73	8.45	6.68	7.31	9.75	3.95	6.38	1.92	12.26
²D	2.91	6.17	4.22	6.32	7.92	2.88	4.44	2.01	8.92

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Ard = Ardley; Half = Halfmoon; Cop = Copacabana; Pupl = Punta Plaza; Stei = Steinhouse; Vou = Voureal; true beta diversity of Shannon (¹D); species richness (⁰D); concentration of Simpson (²D).

Total dissimilarity based on the presence / absence and abundance of species between the islands was 80.7% and 80.5%, respectively. Similarly, analyses of parity-by-pair dissimilarity, both presence / absence and abundance based, showed similar patterns of response, but no formation of distinct groups (Fig 6). The high similarity between the nearest sites, Steinhoose and Punta Plaza, with the most distant site, Halfmoon, for presence / absence as well as for number of individuals, should be emphasized. Copacabana had the highest average dissimilarity with the other sampling sites based on species composition (Fig 6A), while Ardley had the greatest dissimilarity based on abundance of individuals (Fig 6B).

The decomposition of beta diversity based on the presence / absence of species showed that the species substitution component was the most important relative to dissimilarity among the sampling sites (73.1%). The relative importance of the nesting component was only 7.6%, corroborating the beta diversity values slightly higher than two shown by the partitioning analysis of diversity in the alpha, beta and gamma components. These results were strongly influenced by the observed species richness in each sampling site, as well as the high number of exclusive species (26.1% of the total species). In addition, only 26.1% of the species occurred in more than 50% of the sites.

Community similarity between sampling sites was not related to the geographical distance between them, based on incidence (t = -0.509, p = 0.619) and abundance (t = -1.041, p = 0.3167) (Fig 7A and 7D). Species substitution components (t = 0.610, p = 0.553) and nesting (t = -0.403, p = 0.693) of incidence-based beta diversity were also not related to geographical distance (Fig 7B and 7C). Similarly, beta diversity components based on the abundance from balanced variation of abundance (t = 0.180, p = 0.860) and abundance gradients (t = 0.654, p = 0.525) were not related to the geographical distance between sampling sites (Fig 7E and 7F). The Mantel tests, based on 10.000 permutations, corroborated the probability values for this lack of relationship between the similarity matrix and dissimilarity components with the between-sites geographical distance. The lack of a positive or negative similarity relationship with geographical distance occurred due to the high similarity in composition and abundance among the most distant sampling points. In other words, even very close or very distant sites have high similarity in diatom composition and abundance, which resulted in the absence of a linear relationship pattern withdistance. It is possible, however, that if the distances between samples were greater, a clearer relationship might have been observed. According to [57], when studying phytoplankton, at small scales in general there is no effect of the distance, and environmental conditions are more significant. The composition of macroscopic organisms in a habitat seems to be more affected by geographical distances than microorganisms, which is mainly shaped by local conditions [58]. On the other hand, [59], in diatom communities of microbial mats of Antarctic ponds within a similar distance range as our study, found considerable spatial variation that could not be explained by local physical and chemical variables. They concluded that the history of dispersal and colonization of diatoms played an important role in their community structures.

Prasiola crispa is found in drainage lines in Antarctica and because it is ornithocoprophilous, presents considerable biomass mainly around penguin colonies [60], which makes nutrient availability for both the green algae and the surrounding diatom community higher, when compared to e.g. epilithic habitats. The lack of differentiation between the communities with geographic distance could also be attributed to the lower climatic variation in Antarctica compared to tropical and subtropical regions. In a previous study on three marine red macroalgae in Newfoundland Bay, Antarctica [61], the biophysical-chemical characteristics of each sampling site affected the diatom communities more markedly than the different species of host macroalgae or even depth of sampling. Moreover, the diversity of the epiphytic community of diatoms associated with red macroalgae collected near the sea ice of Cape Evans, Antarctica, showed that species diversity decreased as the depth below the sea ice increased, whereby the dominant taxa had also changed in relation to depth [62, 63].

Our study showed that even with marked distance between sampling points, there was high similarity in the composition and abundance of the diatom communities, which resulted in the absence of a linear relationship pattern with distance. However, it was possible to demonstrate that regarding dominant species, the closest sampling sites were more similar. Thus, the inexpressive differentiation of the communities showed that P. crispa as a substrate seems to be an important factor for the selection of the existing epiphytic community.

There have been an increasing number of studies reporting changes in the community of Antarctic organisms due to global warming. Some penguin communities are experiencing population declines as a result of rising temperatures [64] and moss communities are increasing on King George Island, colonizing fields in uncovered areas due to shrinking glaciers [65]. Decreases in microbial diversity patterns has also been reported in regions of Patagonian and other Antarctic lakes, mainly found to decrease in diatom diversity [66,67], as well with evidence for the decline of phytoplankton [68] and bacterioplankton [69]. Such aspects lead us to reflect on how much the diatom communities as well as the substrate of the present study, P. cripa can be affected since it grows in humid places with high nutrient input. If we eleminate these factors, we would also affect the existence of this macroalgae species and, consequently, that of the associated aerophytic diatom community. Although we have not observed any exclusive communities present in this substrate we believe that by affecting the stability of P. crispa in terrestrial wetlands we would also affect the dispersal of associated diatoms.

Acknowledgments

We acknowledge the Coordination of Improvement of Higher-Level Personnel (CAPES), for the scholarship granted to the first author. The authors would also like to thank the brazilian Ministry of the Environment and the Inter-Ministerial Secretary for Sea Resources (SECIRM) for the autorizations granted for field collection activities under the Brazilian Antarctic Program. We would like to thank the researchers at Luxembourg Institute of Science and Technology, Luc Ector and Carlos Wetzel, for helping to species identification.

Data Availability

All relevant data are within the manuscript and its Supporting Information files. The protocols used in the presented work are submitted to protocols.io platform.

Funding Statement

This work are funded by the National Council for Research and Development (CNPq; process no. 574018/2008) and the Research Foundation of the State of Rio de Janeiro (FAPERJ; process E-26/170.023/2008). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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PLoS One. doi: 10.1371/journal.pone.0226691.r001

Decision Letter 0

Jinzhuang Xue

Transfer Alert

This paper was transferred from another journal. As a result, its full editorial history (including decision letters, peer reviews and author responses) may not be present.

1 Aug 2019

PONE-D-19-16073

Distribution of diatom communities associated with terrestrial green macroalgae in the South Shetland Islands, Maritime Antarctica

PLOS ONE

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Reviewer #1: Distribution of diatom communities associated with terrestrial green macroalgae in the South Shetland Islands, Maritime Antarctica

Juliana Ferreira da Silva et al.

This study reports diatom diversity in communities associated with the alga Prasiola crispa in terrestrial habitats in the South Shetland Islands, maritime Antarctic, as well as attempting to examine whether diversity of specific communities was related in any way to separation distance from other locations examined. In reality most locations were on King George Island, while Ardley Island is only separated from that by a tidally inundated isthmus. As such, it is an original study, contributing to the knowledge of this group in Antarctica.

Language is generally clear, though some minor syntax and spelling editing is required throughout; I note that this journal does not offer copy editing, so this will have to be done carefully during revision. Is the citation format in the text correct for the journal? It is unusual to list both numbered references and fully named author lists together.

Abstract – the description of the role of distance (‘isolation by distance’) in structuring (or not) diatom community composition could be reworded a bit to make it clearer: at present the sentence structure seems to suggest initially that distance is being considered from each of the six sampling sites individually (for instance along a transect from a central sampling location at each), and rather it later becomes clear that the intention is to look at distance as a factor between the six sampling locations.

Introduction – the opening para should make it clear from the outset that the focus is on diatoms; at present the opening sentences appear to make statements applying to the Antarctic flora more generally – if this is the case then they need expanding into a separate general opening para, before subsequently focussing in on diatoms specifically. However, I think the intention is to focus on diatoms from the outset.

Terminology in the para describing the influence of distance – it should be ‘community similarity’ rather than ‘species similarity’.

Within the methods section there is no reference given to how the diatoms obtained were identified? I appreciate the long list of recent species descriptions early in the Introduction, but something specific should be said in this section. Other than these comments, the approaches and analyses used are appropriate.

Taxonomic authorities – I believe that journal format only requires these to be listed once, so there are many instances where repeat listings can be deleted. If acceptable to the journal, I would suggest placing all authorities within Table 2 and deleting them from the text, which will also help make the text more readable.

Diversity indices – I am not familiar with what 0D, 1D, 2D annotation means?

Overall, while the study found differences in various indices between sites, community similarity was high across the entire study area, emphasised by the highest similarity being found between the most distant sites, and there was no overall relationship between separation distance and diversity. I wonder if this might reflect the overall physical scale of the study area, where most of the sampling sites were actually quite close to each other – in other words does this indicate the scale of the study was not large enough to identify such effects, and that ‘isolation’ was not a significant factor at this scale? Perhaps a larger geographical sampling scale would lead to identification of such a relationship, as predicted by the study’s overall hypothesis?

Figures – the labels on the diatom photo figs are blurred in my pdf?

Table 1 – I think I would suggest presenting this data in km rather than m

Peter Convey

British Antarctic Survey

19 July 2019

Reviewer #2: Review for PLOS one of manuscript PONE-D-19-16073 by da Silva et al.

In this manuscript the authors analyze a set of epiphytic diatom samples collected from the terrestrial macroalgae Prasiola crispa from six sites located in the South Shetland Islands, Maritime Antarctica. They observed rather species-poor and homogeneous diatom communities. In addition to reporting the species list, they used various statistical methods on their abundance data to demonstrate that the geographical distance is not the factor driving the distribution of the diatoms identified in their samples.

In my opinion this is a valuable diatom dataset collected from an interesting habitat in a very remote region. The authors provide high-quality illustrations of the diatom taxa they could observed (obtained with both light and scanning electron microscopes). Their conclusions are supported by the statistical analyses carried out. I think this study is of interest for researchers interested in the distribution of these microorganisms in such extreme habitat. I think this manuscript requires some corrections and improvements before it can be published in PLoS One. Please see below my main suggestions, followed by a list of specific comments.

General comments:

Diatom identification: In the method section of the manuscript, the authors only referenced Round et al. (1990) as the source for the identification of the diatoms they observed in their samples. This is not suitable as this book by Round et al. only deals with taxonomy at the generic level and some of the genera the authors identified where not even described at the time it was published (e.g. Psammothidium, Mayamaea). It would be much better to list all the papers and flora used for identification. In addition, I found particularly surprising that you did not make use of the flora published by Zidarova et al. (2016) specifically dealing with Maritime Antarctica, including the South Shetlands Islands. In particular, the species the authors identified as Luticola aff beyensis and Luticola muticopsis morphotype 1 may be Luticola amoena and Luticola austroatlantica, respectively, as illustrated in the book by Zidarova et al. (2016). Cocconeis aff costata may also correspond to Cocconeis pinnata var. matsii as described by Al-Handal et al. (2010) from King George Island.

Spelling of diatom names: I’ve found numerous mistakes throughout the text of the manuscript, the legend of the figures and in the tables. Please pay attention to that and correct them.

Rarefaction analysis: Taxonomic richness assessed through rarefaction in fact consists in an interpolation to lower (and common to all sample) count size and it results in a loss of information (Giesecke et al. 2014). Moreover, samples standardized by size can have different degrees of completeness, depending on the species-abundance distributions of the assemblages that are compared. A better way is to compare samples of equal completeness, not equal size (Chao and Jost 2012). This can be done by using the species accumulation curve to extrapolate the total species richness of the less complete samples (Béguinot 2015). Several parameters can be used to estimate the completeness of the sampling such as the percentages of species represented by one individual (=singleton) and the sample intensity, i.e. abundance divided by richness (Lopez et al. 2012).

Comparison of the results: the main result is that spatial distance does not appear to drive differentiation in diatom communities in this study. Maybe this result is due to the fact that the distance covered in the study is relatively small (less than 100 km). Could you compare your result with similar studies dealing with the effect of spatial distance on diatom community composition?

Conclusion: I think the manuscript would really gain if you could broaden a little the scope of your conclusions with a few sentences. For example, could you discuss about any wider implications regarding the potential effect of further climate warming on the resilience of this community. I read that the penguin populations were threatened as their conditions for nesting are changing (change in local weather with unprecedented rain, prematurely snow melt creating puddles of water on the ground, etc…). How would this affect Prasiola and its associated diatom flora?

Specific comments:

Page 1: In the title, I would use: Distribution of aerophilous diatom communities … to make it clear what kind of samples were investigated.

Page 1: in the address of the authors, correct spelling of Antarctic (only one “t”)

Page 2, in abstract: rephrase such as: …such as the type of substrate…

Page 2: correct spelling of Luticola muticopsis (not multicopsis)

Page 2: add dots after initials such as: D.E. Kellogg et al.

Page 2:… in our samples, …

Page 2: …and abundance of their diatom community…

Page 2: keywords: replace “Diatom” by “aerophilous diatoms”, delete “Taxonomy” as this paper does not deal with taxonomy

Page 3: rewrite the sentence such as: The larger the distance between sites, the larger are the environmental variations and, therefore, the difference in species composition tends to be also larger. The following sentence, starting by “Spatial distance is a factor that influences…” is unclear, please re-write it.

Page 4: quantitative analyses: give the number of valves counted to obtain the relative abundance data

Page 4: the statement starting with “sample sufficiency…” is unclear

Page 4: regarding rarefaction, please see above in general comments

Page 5: separate thousands using a comma such as: 10,000

Page 5: use lower case for “also”

Page 5: …(Oksanen et al. 2016) in R.

Page 5: correct spelling of Pseudogomphonema and carlinii

Page 5: Cocconeis pinnata var. matsii is also a marine species (if it’s the correct identification?)

Page 6: correct spelling for muticopsis (several times)

Page 6: just give the authorities once, when a species is first mentioned. There is no need to repeat them every time thereafter.

Page 7: separate thousands using a comma such as: 10,000

Page 9: delete “1.” before “Hamsher”

Page 9: just use Fottea for title of the journal, delete “Czech Phycological Society – Praha, Czech Republic, 2007, currens.”

Page 9: in the reference by Kochman-Kedziora et al.: just use Fottea for title of the journal, delete “Czech Phycological Society – Praha, Czech Republic, 2007, currens.”

Page 10: delete “3.” before “Kopalova”

Page 11: use capital L for journal title: Limnetica

Page 11: delete “2.” before “Van de Vijver”

Fig. 1: add an insert showing the whole of Antarctica to help the reader immediately visualize the location of this region. Some locations on the map and the legend are in Portuguese (e.g Rei George instead of King George; Sistema de Coordenadas, etc…). Please change all to English. Also correct spelling of British. Also give explanation about the units used on sides of the figure.

Figs 2 and 3: indicate to what distance the scale bar corresponds (is it 5 microns?), either directly on the figures or in the legend. In the legend: add “LM photographs”; correct spelling of diatom names, use English instead of Portuguese for morphotype

Fig. 4: add “SEM photographs”, correct spelling of diatom names.

Table 1: I would give the distances in kilometers instead of meters. If you insist in using meters, at least delete the decimals…

Table 2: There are many mistakes in the diatom names:

Muticopsis instead of multicopsis

Cyclotella instead of Ciclotella

Fragilaria instead of Fragillaria

Hantzschia instead of Hantzchia

Carlinii instead of carlini

Pseudogomphonema instead of Pseudoghophonema

Olegsakharovii instead of olegsakharoni

References used in this review:

Al-Handal, A., Riaux-Gobin, C., Wiulff, A. (2010). Cocconeis pottercovei sp. nov. and Cocconeis pinnata var. matsii var. nov., two new marine diatom taxa from King George Island, Antarctica. Diatom Research 15 (1): 1-11.

Béguinot J. (2015). Extrapolation of the species accumulation curve for incomplete species samplings: a new nonparametric approach to estimate the degree of sample completeness and decide when to stop sampling. Annual Research & Review in Biology 8: 1-9.

Chao A. & Jost L. (2012). Coverage-based rarefaction and extrapolation: standardizing samples by completeness rather than size. Ecology 93: 2533-2547.

Giesecke, T., Ammann, B., Brande A. (2014). Palynological richness en evenness: insights from the taxa accumulation curve. Vegetation History & Archaeobotany 23: 217-228.

Lopez L.C.S., de Aguiar Fracasso M.P., Oliveira Mesquita D., Torre Palma A.R. & Riul P. (2012). The relationship between percentage of singletons and sampling effort: a new approach to reduce the bias of richness estimates. Ecological Indicators 14: 164-169.

Zidarova, R., Kopalová, K., Van de Vijver, B. (2016). Diatoms from the Antarctic Region : Maritime Antarctica. Iconographia Diatomologica vol. 24. Koeltz Botanical Books, Schmitten-Oberreifenberg, Germany.

**********

6. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

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Reviewer #1: Yes: Peter Convey

Reviewer #2: No

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PLoS One. 2019 Dec 30;14(12):e0226691. doi: 10.1371/journal.pone.0226691.r002

Author response to Decision Letter 0

10 Sep 2019

POINT-BY-POINIT RESPONSE TO REVIEWERS

REVIEWER'S COMMENTS:

Reviewer #1:

Response to reviewer: The authors followed the guidelines for manuscript formatting for submission to Plos One Magazine. However, there were some formatting errors that have now been corrected in this review.

Response to reviewer: Its been corrected, we rewritten the description. The modification is found in the marked copy of manuscript.

Response to reviewer: Ok, the modification is found in the marked copy of manuscript.

Terminology in the para describing the influence of distance – it should be ‘community similarity’ rather than ‘species similarity’.

Response to reviewer: We change this, the modification is found in the marked copy of manuscript.

Response to reviewer: Ok, we add the references used in detail, the modification is found in the marked copy of manuscript.

Response to reviewer: Ok, we change this, the modification is found in the marked copy of manuscript.

Diversity indices – I am not familiar with what 0D, 1D, 2D annotation means?

Response to reviewer: The explanation is at the bottom of page 8 in the following excerpt: “The alpha diversity was approximately 10 species for species richness and this analysis further showed that the true beta diversity of Shannon (1D) was lower than the richness based on species richness (0D) and based on the inverse concentration of Simpson (2D). This shows that differences between sampling sites occurred due to the contrast between the most abundant and the rarest species of each site (Table 4).”

Response to reviewer: Ok, we added this discussion, the modification is found in the marked copy of manuscript.

Figures – the labels on the diatom photo figs are blurred in my pdf?

Response to reviewer: We do not understand this point. Our figures and the pdf generate in the submission process are in highest quality permited to the jounal guidelines.

Table 1 – I think I would suggest presenting this data in km rather than m

Response to reviewer: Ok, we change this, the modification is found in the marked copy of manuscript.

Reviewer #2:

Response to reviewer: Ok, we correted this, the modification is found in the marked copy of manuscript.

Spelling of diatom names: I’ve found numerous mistakes throughout the text of the manuscript, the legend of the figures and in the tables. Please pay attention to that and correct them.

Response to reviewer: Ok, we correted this, the modification is found in the marked copy of manuscript.

Response to reviewer: The authors understand the suggestion, but evaluate that would not modify the results to a significant extent. Regarding the suggestion to use species represented by only one individual in a given sample to access completeness, it cannot be applied to our data, because such species are eliminated from data.

Response to reviewer: Ok, we added this discussion, the modification is found in the marked copy of manuscript.

Specific comments:

Page 1: In the title, I would use: Distribution of aerophilous diatom communities … to make it clear what kind of samples were investigated.

Page 1: in the address of the authors, correct spelling of Antarctic (only one “t”)

Page 2, in abstract: rephrase such as: …such as the type of substrate…

Page 2: correct spelling of Luticola muticopsis (not multicopsis)

Page 2: add dots after initials such as: D.E. Kellogg et al.

Page 2:… in our samples, …

Page 2: …and abundance of their diatom community…

Page 2: keywords: replace “Diatom” by “aerophilous diatoms”, delete “Taxonomy” as this paper does not deal with taxonomy

Page 4: quantitative analyses: give the number of valves counted to obtain the relative abundance data

Page 4: the statement starting with “sample sufficiency…” is unclear

Page 4: regarding rarefaction, please see above in general comments

Page 5: separate thousands using a comma such as: 10,000

Page 5: use lower case for “also”

Page 5: …(Oksanen et al. 2016) in R.

Page 5: correct spelling of Pseudogomphonema and carlinii

Page 5: Cocconeis pinnata var. matsii is also a marine species (if it’s the correct identification?)

Page 6: correct spelling for muticopsis (several times)

Page 6: just give the authorities once, when a species is first mentioned. There is no need to repeat them every time thereafter.

Page 7: separate thousands using a comma such as: 10,000

Page 9: delete “1.” before “Hamsher”

Page 9: just use Fottea for title of the journal, delete “Czech Phycological Society – Praha, Czech Republic, 2007, currens.”

Page 9: in the reference by Kochman-Kedziora et al.: just use Fottea for title of the journal, delete “Czech Phycological Society – Praha, Czech Republic, 2007, currens.”

Page 10: delete “3.” before “Kopalova”

Page 11: use capital L for journal title: Limnetica

Page 11: delete “2.” before “Van de Vijver”

Response to reviewer: Ok, we corrected the specific comments above.

Response to reviewer: Ok, we correted this, the modification is found in the marked copy of manuscript.

Fig. 4: add “SEM photographs”, correct spelling of diatom names.

Response to reviewer: Ok, we correted this, the modification is found in the marked copy of manuscript.

Table 1: I would give the distances in kilometers instead of meters. If you insist in using meters, at least delete the decimals…

Response to reviewer: Ok, we correted this, the modification is found in the marked copy of manuscript.

Table 2: There are many mistakes in the diatom names:

Muticopsis instead of multicopsis

Cyclotella instead of Ciclotella

Fragilaria instead of Fragillaria

Hantzschia instead of Hantzchia

Carlinii instead of carlini

Pseudogomphonema instead of Pseudoghophonema

Olegsakharovii instead of olegsakharoni

Response to reviewer: Ok, we correted this, the modification is found in the marked copy of manuscript.

Attachment

Submitted filename: POINT-BY-POINIT RESPONSE TO REVIEWERS.docx

Click here for additional data file.^{(24.3KB, docx)}

PLoS One. doi: 10.1371/journal.pone.0226691.r003

Decision Letter 1

Jinzhuang Xue

4 Oct 2019

PONE-D-19-16073R1

Distribution of aerophilous diatom communities associated with terrestrial green macroalgae in the South Shetland Islands, Maritime Antarctica

PLOS ONE

Dear Dr. Victoria,

We would appreciate receiving your revised manuscript by Nov 18 2019 11:59PM. When you are ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter.

Please include the following items when submitting your revised manuscript:

A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). This letter should be uploaded as separate file and labeled 'Response to Reviewers'.
A marked-up copy of your manuscript that highlights changes made to the original version. This file should be uploaded as separate file and labeled 'Revised Manuscript with Track Changes'.
An unmarked version of your revised paper without tracked changes. This file should be uploaded as separate file and labeled 'Manuscript'.

We look forward to receiving your revised manuscript.

Kind regards,

Jinzhuang Xue

Academic Editor

PLOS ONE

Additional Editor Comments (if provided):

The reviewer provided two issues, which have been raised during the first round of reviewing but not been well dealt with during the revision. I agree with the comments of the reviewer. 1. Please consider more about the roles of rare species in the estimation of species richness. There are many methods in ecology to deal with rare species, rather than simply deleting them from the original data. 2. Please consider the comments about distance. 3. Please carefully check the text to kill the typos, some of which have been marked in the attached file from the reviewer.

[Note: HTML markup is below. Please do not edit.]

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #2: (No Response)

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

Reviewer #2: Partly

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #2: No

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

Reviewer #2: (No Response)

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

Reviewer #2: Yes

**********

6. Review Comments to the Author

Reviewer #2: Review of manuscript PONE-D-19-16073R1 by Da Silva et al.

With this revised version the authors have improved their manuscript substantially.

There are however two issues with the reply the authors gave to my comments:

1. “Regarding the suggestion to use species represented by only one individual in a given sample to access completeness, it cannot be applied to our data, because such species are eliminated from data.“ I really don't understand this reply. Species richness (i.e. the number of species present in the sample) is more or less the basis of this study, so why would you "eliminate" the rare species from the data? Please explain? In any case there was no mention of this “elimination” in the method section of the paper.

2. I also asked the authors to consider in their discussion that the relatively small distance (less than 100 km) covered in this study may in part explains the lack of relationship between spatial distance and the diatom communities similarity. Note that the other reviewer made the same remark. The authors did not answer this question directly and I could not found any mention of it in the revised version of the manuscript.

In addition, there are still a few typos in the manuscript. Please see the PDF with my comments as “sticky notes”.

Overall, I think this study can be published after minor revision.

**********

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #2: No

Attachment

Submitted filename: PONE-D-19-16073_R1_reviewer_with notes.pdf

Click here for additional data file.^{(3MB, pdf)}

PLoS One. 2019 Dec 30;14(12):e0226691. doi: 10.1371/journal.pone.0226691.r004

Author response to Decision Letter 1

2 Dec 2019

Dear Editor and Reviewers,

We would like to inform you that image 4 of the manuscript "Distribution of aerophilous diatom communities associated with terrestrial green macroalgae in the South Shetland Islands, Maritime Antarctica", with manuscript number PONE-D-19-16073R1 submitted to the journal Plos One, has not been authorized for disclosure or publication. We have therefore removed it from the updated version of the article. Nevertheless we would like to emphasize that the lack of this image does not change the context of the paper, nor does it, in any way, impair the results described, as the species previously shown in image 4 are also represented in Figures 2 and 3 as follows:

1. Cocconeis pinnata var. matsii – Cited in Figure 2 (4-10)

2. Luticola amoena - Cited in Figure 2 (14-17)

3. Luticola multicopsis - Cited in Figure 2 (22-25)

4. Navicula aff perminuta - Cited in Figure 3 (28-31)

5. Pinnularia austroshetlandica - Cited in Figure 3 (32-34)

6. Psammothidium germainii - Cited in Figure 3 (45-48)

7. Pseudogomphonema kamtschaticum - Cited in Figure 3 (51-55)

8. Pteroncola carlinii - Cited in Figure 3 (56-59)

In response to questions:

Editor Comments:

“1. Please consider more about the roles of rare species in the estimation of species richness. There are many methods in ecology to deal with rare species, rather than simply deleting them from the original data.”

Regarding the suggestion to use species represented by only one individual in a given sample to access completeness, we argue that in such cases we might be examining the result of a contaminant. Species represented by only one valve in each sample were excluded from the analyses due to the difficulty of a correct species determination and to avoid potential contaminants. We have added this fact to the manuscript methodology along with references.

“2. Please consider the comments about distance.”

We added a discussion about it in the manuscript.

“3. Please carefully check the text to kill the typos, some of which have been marked in the attached file from the reviewer.”

The text were revised.

Attachment

Submitted filename: Response to Reviewers.docx

Click here for additional data file.^{(17.6KB, docx)}

PLoS One. doi: 10.1371/journal.pone.0226691.r005

Decision Letter 2

Jinzhuang Xue

5 Dec 2019

Distribution of aerophilous diatom communities associated with terrestrial green macroalgae in the South Shetland Islands, Maritime Antarctica

PONE-D-19-16073R2

Dear Dr. Victoria,

We are pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it complies with all outstanding technical requirements.

Within one week, you will receive an e-mail containing information on the amendments required prior to publication. When all required modifications have been addressed, you will receive a formal acceptance letter and your manuscript will proceed to our production department and be scheduled for publication.

Shortly after the formal acceptance letter is sent, an invoice for payment will follow. To ensure an efficient production and billing process, please log into Editorial Manager at https://www.editorialmanager.com/pone/, click the "Update My Information" link at the top of the page, and update your user information. If you have any billing related questions, please contact our Author Billing department directly at authorbilling@plos.org.

If your institution or institutions have a press office, please notify them about your upcoming paper to enable them to help maximize its impact. If they will be preparing press materials for this manuscript, you must inform our press team as soon as possible and no later than 48 hours after receiving the formal acceptance. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org.

With kind regards,

Jinzhuang Xue

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Reviewers' comments:

PLoS One. doi: 10.1371/journal.pone.0226691.r006

Acceptance letter

Jinzhuang Xue

18 Dec 2019

PONE-D-19-16073R2

Distribution of aerophilous diatom communities associated with terrestrial green macroalgae in the South Shetland Islands, Maritime Antarctica

Dear Dr. Victoria:

I am pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

If your institution or institutions have a press office, please notify them about your upcoming paper at this point, to enable them to help maximize its impact. If they will be preparing press materials for this manuscript, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org.

For any other questions or concerns, please email plosone@plos.org.

Thank you for submitting your work to PLOS ONE.

With kind regards,

PLOS ONE Editorial Office Staff

on behalf of

Dr. Jinzhuang Xue

Academic Editor

PLOS ONE

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Attachment

Submitted filename: POINT-BY-POINIT RESPONSE TO REVIEWERS.docx

Click here for additional data file.^{(24.3KB, docx)}

Attachment

Submitted filename: PONE-D-19-16073_R1_reviewer_with notes.pdf

Click here for additional data file.^{(3MB, pdf)}

Attachment

Submitted filename: Response to Reviewers.docx

Click here for additional data file.^{(17.6KB, docx)}

Data Availability Statement

All relevant data are within the manuscript and its Supporting Information files. The protocols used in the presented work are submitted to protocols.io platform.

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PERMALINK

Distribution of aerophilous diatom communities associated with terrestrial green macroalgae in the South Shetland Islands, Maritime Antarctica

Juliana Ferreira da Silva

Maria Angélica Oliveira Linton

Raylane Ribeiro da Anunciação

Eduardo Pereira da Silva

Rodrigo Paidano Alves

Adriano Luis Schünemann

Filipe de Carvalho Victoria

Margéli Pereira de Albuquerque

Antônio Batista Pereira

Roles

Abstract

Introduction

Material and methods

Fig 1. Map of the location of sampling points where Prasiola crispa was collected in Antarctica.

Table 1. Sample site coordinates.

Table 2. Distance table in meters between sampling points where Prasiola crispa was collected in Antarctica.

Table 3. List of all observed species with their acronyms and abundance in the samples from Antarctic Islands.

Results and discussion

Fig 2. Taxa of diatoms in LM.

Fig 3. Taxa of diatoms in LM.

Fig 4. Rarefaction curves of the diatom species associated with Prasiola crispa for the sampled sites.

Fig 5. Plots of abundance (proportional [pi]) of the diatom species associated with Prasiola crispa for the sampled sites.

Table 4. Multiplicative partitioning of the diatom species diversity associated with Prasiola crispa for the sampled sites.

Fig 6. Average dissimilarity between sampling points of the diatom species associated with Prasiola crispa for the sampled sites based on the presence / absence of species (A) and abundance (B).

Acknowledgments

Data Availability

Funding Statement

References

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Jinzhuang Xue

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Author response to Decision Letter 0

Decision Letter 1

Jinzhuang Xue

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Author response to Decision Letter 1

Decision Letter 2

Jinzhuang Xue

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Acceptance letter

Jinzhuang Xue

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Associated Data

Supplementary Materials

Data Availability Statement

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