A DNA barcode inventory of the genus Ulva (Chlorophyta) along two Italian regions: updates and considerations

Simona Armeli Minicante; James T. Melton; Damiano Spagnuolo; Antonio Manghisi; Giuseppa Genovese; Marina Morabito; Juan Lopez-Bautista

doi:10.1515/bot-2023-0071

Article Open Access

A DNA barcode inventory of the genus Ulva (Chlorophyta) along two Italian regions: updates and considerations

Simona Armeli Minicante

Simona Armeli Minicante is research technologist at the Institute of Marine Sciences of the National Research Council (CNR-ISMAR). Referent of the ISMAR Herbarium, her research concerns studies on the biodiversity of marine macroalgae, integrating research on the biotechnological applications of seaweeds, including alien and invasive species, in the field of circular economy and sustainability.
, James T. Melton

James T. Melton III is a senior lecturer in the Biology Department at Spelman College in Atlanta, Georgia, USA. His research interests include algal diversity, phylogenetics, and genomics with a focus on the green algal genus Ulva. He is also currently teaching a CURE (course-based undergraduate research) course on bacteriophage discovery and genomics.
, Damiano Spagnuolo

Damiano Spagnuolo is currently a post-doc at the University of Messina, Italy, is engaged in pioneering research within the field of marine biotechnology. His expertise lies in the sustainable utilization of macroalgae, exploring taxonomy, genetic labelling, and the extraction of bioactive compounds. His contributions encompass not only in-depth taxonomic studies but also innovative extraction techniques for eco-friendly bioactive molecules. His work is poised to revolutionize marine bioproducts and contribute to a more sustainable future.
, Antonio Manghisi , Giuseppa Genovese , Marina Morabito

Dr Marina Morabito is full professor in Systematic Botany at the University of Messina, Italy, where she is the coordinator of the course in Marine and Terrestrial Environmental Sciences and serves in Quality Insurance and Student Orientation Committees. Her research interests regard the systematics and ecology of aquatic plants, with focuses on the Mediterranean Sea, and the valorisation of biomasses in biotechnological and economic frameworks. She serves as a forensic expert in technical-scientific consultancy for the Procura della Repubblica.
and Juan Lopez-Bautista

Juan Lopez-Bautista, a professor in the Department of Biological Sciences at The University of Alabama, USA, is interested in the biodiversity, molecular systematics, and evolution of marine and terrestrial algae. Current efforts include environmental DNA metabarcoding technologies applied to algal communities and the architecture of the green and red algal plastomes.

Published/Copyright: June 24, 2024

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From the journal Botanica Marina Volume 68 Issue 1

Abstract

The genus Ulva Linnaeus 1753 is well known for its global distribution and containing many taxonomically debated species. Their morphological plasticity and cryptic nature overrepresent and underrepresent, respectively, the biodiversity of these species. The difficulty in morphologically identifying Ulva species has led to the accumulation of many species names that are currently considered synonyms. The correct identification of these species is crucial due to their significant role in marine ecosystems and mariculture. In the last 30 years, several checklists and taxonomic contributions have been made from the Italian coast on Ulva species, almost entirely based on morphological studies and only a few papers with molecular data have been published. In this study, samples deposited at the Institute of Marine Sciences (ISMAR) and Phycological Lab (PHL) herbaria have been reviewed by sequencing the chloroplast-encoded elongation factor Tu (tufA) barcode marker. The results obtained provide an update of the DNA barcode inventory of Ulva species for the Lagoon of Venice and the Strait of Messina, two ecosystems characterized by a high algal biogeographical diversity and continuous introduction due to anthropogenic activities. Here, ten Ulva species were identified based on molecular data. Furthermore, we record the presence of Ulva chaugulei on the coast of Tunisia.

Keywords: Ulva ; Mediterranean Sea; Ulva chaugulei ; tufA; LTER-Italy

1 Introduction

The study of the genus Ulva (Chlorophyta) is always full of surprises, as Papenfuss (1960) already reported in his works. Due to phenotypic plasticity and prompt morphological adaptation to changes in the natural environment – in marine and some freshwater ecosystems – the identification of species of Ulva is particularly challenging, and many taxonomic synonyms have been generated over time.

In the last few years, extensive molecular investigations of Ulva species have been performed around the world with nuclear (ITS1-5.8S-ITS2) and chloroplast (rbcL and tufA) barcoding markers (Figure 1). This is reflected in numerous records (Chávez-Sánchez et al. 2019; Hofmann et al. 2010; Kirkendale et al. 2013; Manghisi et al. 2011; Miladi et al. 2018; Steinhagen et al. 2019; Woo and Ki 2017; Xie et al. 2020) that have led to many rearrangements and taxonomic revisions of the Ulva species (Cui et al. 2018; Hughey et al. 2019, 2021], 2022]; Krupnik et al. 2018; Rybak et al. 2014). As recorded by Guiry and Guiry (2023), only 155 of the 622 taxa described at the species and infraspecific levels are currently accepted; additionally, 105 names are currently of uncertain status.

Figure 1:

Optimized investigations of Ulva species through barcoding markers around the world.

The Italian seaweed flora includes over 800 taxa (Furnari et al. 2010). The biogeographical origin of this biodiversity is characterized by a high incidence of Atlantic (41.87 %), followed by Mediterranean (25.74 %) and cosmopolitan taxa (21.51 %), whereas a lower percentage of species have Indo-Pacific (5.06 %), Circumtropical (4.03 %) and Circumboreal (1.79 %) origins (Furnari et al. 2010). However, according to taxonomic and molecular revisions, seaweed biodiversity data are constantly being updated and revised. Unveiling the biodiversity will allow us to better understand the phenomenon of introduced or Non-Indigenous Species (NIS).

Along the Italian coasts, several checklists and taxonomic contributions have been made to the species of Ulva in the last 30 years (Cormaci et al. 2014; Cuomo et al. 1993; Flagella et al. 2010; Manghisi et al. 2011; Miladi et al. 2018; Petrocelli et al. 2019; Serio et al. 2009; Sfriso 2010a, b; Wolf et al. 2012). In 2019, 19 species of this taxon were reported (Cormaci et al. 2014; Miladi et al. 2018). However, the knowledge of both diversity and distribution was almost entirely based on morphological studies and there have only been a few published papers dealing with molecular data (Miladi et al. 2018; Wolf et al. 2012).

The need to explore the diversity of Ulva species is further due to the ecological and economic importance of these algae (Melton and Lopez-Bautista 2021), and are often well represented in the Transitional Water Ecosystems (TWE). Represented mainly by estuaries, deltas and lagoons, the TWE are intermediate in time or space between marine and nonmarine environments (Tagliapietra et al. 2009). In this study, the diversity of Ulva species was assessed in two Italian TWE, over a period of 10 years.

A molecular approach by sequencing the tufA molecular marker (plastid) was used to compile a DNA barcode inventory and to update the reported species list.

2 Materials and methods

2.1 Study area

The samples revised in this study were collected during different seasons, between 2009 and 2019, from the intertidal to shallow subtidal from the Lagoon of Venice (Veneto Region), the Lake Ganzirri and the Strait of Messina (Sicily Region) (Figure 2; Supplementary Table 1).

Figure 2:

Sampling sites from the Lagoon of Venice (A), Lake Ganzirri and the Strait of Messina (B).

The Lagoon of Venice is the largest Italian lagoon and the Mediterranean transitional environment with the highest floristic richness; however, this ecosystem is exposed to intense anthropogenic pressures, including the introduction of alien species. In order to obtain the best representation of Ulva species, 24 sampling stations falling within the four classification areas on the basis of the Macrophyte Quality Index (MaQI, Sfriso et al. 2009) were chosen (Figure 2A).

Furthermore, of these research sites, 8 belong to the Long-Term Ecological Research (LTER) network LTER-Italy (Armeli Minicante et al. 2019), an essential component of worldwide efforts to improve our knowledge of the structure of ecosystems and of their long-term response to environmental, societal and economic drivers (Mirtl et al. 2018).

The Strait of Messina and Lake Ganzirri, in Capo Peloro Lagoon are noteworthy areas in the Mediterranean Sea, with special and unique biological communities, and are included in the “Natura 2000” network and in the Sites of Community Interest, respectively. A floristic list based on literature data was performed by Serio et al. (2009) for Lake Ganzirri, whereas there are few recent studies based on molecular methods for these two environments (Bertuccio et al. 2014). The 12 sampling stations include 7 stations in Lake Ganzirri (ST01-ST07), 4 stations along the Strait of Messina coast (ST09-ST12), and one station (ST08) in the channel which connects Lake Ganzirri to the sea (Figure 2B).

2.2 Algal material processing

All samples collected from the Lagoon of Venice and from Sicilian coasts were pressed in herbarium sheets, vouchered, and deposited in the Herbarium of the Institute of Marine Sciences of Venice (ISMAR, https://www.archiviostudiadriatici.it/index.php/it/) and the Phycological Lab Herbarium (PHL) of the University of Messina, respectively. Abbreviations of herbaria follow the online Index Herbariorum (Thiers 2024).

For each voucher, two subsamples were prepared: one dried in silica gel for molecular analysis, and a second preserved in 4 % formalin in seawater for morphological studies.

2.3 DNA sequencing

For PhL vouchers, the DNA was extracted using a modified CTAB-extraction method (Miladi et al. 2018). The plastid tufA gene was PCR amplified as described in Saunders and Kucera (2010), using tufGF4 and tufAR as primers. Sequencing reactions were performed by an external company (Macrogen Europe, The Netherlands).

For ISMAR vouchers, a QIAGEN DNeasy Plant kit (QIAGEN, Valencia, CA, USA) was used to extract DNA. The tufA molecular marker was amplified by PCR according to Saunders and Kucera (2010). PCR products were run on a gel electrophoresis (1 % agarose gel) and bands were cut from the gel and cleaned with a QIAGEN MinElute Gel Extraction kit (QIAGEN, Valencia, CA, USA). Sanger sequencing of the PCR products was performed at the University of Kentucky (UK) HealthCare Genomics Centre in Lexington, Kentucky.

2.4 Molecular analyses

Fifty-three tufA sequences from the Mediterranean Sea were trimmed and assembled with Geneious v11.1.5 (Biomatters Ltd., Auckland, New Zealand; available at http://www.geneious.com/). After performing a BLASTn (Altschul et al. 1990) of the sequences, 90 tufA sequences were selected from GenBank. This included sequences from the type material of Ulva lacinulata (MW543061), Ulva ohnoi (AP018696), Ulva expansa (MH731007), Ulva fenestrata (MK456404), and Ulva rigida (MW543060). Percursaria percursa (AY454403), Umbraulva kaloakulau (KT932974), and Ulvaria obscura (HQ610406) were used as an outgroup. In total, 143 sequences were aligned with MAFFT (Katoh and Standley 2013; Katoh et al. 2002) to form an 802 bp alignment. A maximum likelihood analysis was then performed with RAxML v8 (Stamatakis 2014) using a GTR + I + G model of nucleotide evolution and 1,000 bootstrap replicates. The resulting tree was then edited with FigTree v1.4 (Rambaut 2012). Sequence divergences were calculated with MEGA7 (Kumar et al. 2016). The ‘pairwise deletion’ option was selected for the gaps and missing data treatment. Taxonomic names were assigned based on molecular species concepts from previous studies. Intraclade divergences from Melton and Lopez-Bautista (2021) were taken into consideration when assigning taxonomic names.

3 Results and discussion

The 52 tufA sequences generated from coastal Italy in this study clustered in 10 distinct clades: Ulva australis (six samples), U. californica (two samples), U. compressa (11 samples), U. flexuosa subsp. flexuosa (one sample), U. lacinulata (15 samples), U. lactuca (eight samples), U. linza/procera/prolifera (three samples), U. ohnoi (two samples), Ulva sp. 1 (one sample), and Ulva sp. 2 (three samples) (Figures 3–5; Table 1). Nine of the species in this study had an intraclade divergence of 1 % or less, which falls within intraspecific divergences from previous studies (e.g., Kirkendale et al. 2013; Melton and Lopez-Bautista 2021). The intraclade divergence of U. compressa (0–1.4 %) was the largest in this study; however, it has been previously noted that this group could potentially represent a cryptic clade instead of a single species (Melton and Lopez-Bautista 2021).

Figure 3:

A maximum likelihood (ML) phylogenetic tree of Ulva based on tufA (802 bp alignment). The “Clade 1” and “Clade 2” for two major groups of Ulva species were collapsed and shown in detail in Figures 4 and 5, respectively. The phylogenetic tree was run with a GTR + I + G model of nucleotide evolution and 1,000 bootstrap replicates.

Figure 4:

Ulva “Clade 1” from the maximum likelihood (ML) phylogenetic tree based on tufA (802 bp alignment). The phylogenetic tree was run with a GTR + I + G model of nucleotide evolution and 1,000 bootstrap replicates. Samples from this study are in bold. Sequences from the type specimen are labelled as ‘type’. Pairwise distances were calculated for each species. *Specimen of U. chaugulei (RM0287) from Tunisian coast.

Figure 5:

Ulva “Clade 2” from the maximum likelihood (ML) phylogenetic tree based on tufA (802 bp alignment). The phylogenetic tree was run with a GTR + I + G model of nucleotide evolution and 1,000 bootstrap replicates.

Table 1:

Specimens of Ulva analysed by DNA barcoding in this study; previous names have been assigned both by morphological and molecular analyses.

Herbarium code	Specimen ID	Previous name	Name resulting from this study	Collectors	Collection date	Country	Region	Exact site	tufA GenBank/BOLD accession number
PHL	CB164	Ulva sp.	Ulva sp. 2	Clara Bertuccio	24/06/2009	Italy	Sicily	Lake Ganzirri, ST01	GB# KM212027
PHL	CB164	Ulva sp.	Ulva sp. 2	Clara Bertuccio	24/06/2009	Italy	Sicily	Lake Ganzirri, ST01	BOLD# ITGRE020-11
PHL	CB284	Ulva ohnoi	Ulva ohnoi	Clara Bertuccio	13/10/2009	Italy	Sicily	Lake Ganzirri, ST01	GB# MF544113
PHL	CB284	Ulva ohnoi	Ulva ohnoi	Clara Bertuccio	13/10/2009	Italy	Sicily	Lake Ganzirri, ST01	BOLD# GRAPP015-17
PHL	CB174	Ulva sp.	Ulva sp. 2	Clara Bertuccio	24/06/2009	Italy	Sicily	Lake Ganzirri, ST02	GB# KM212021
PHL	CB174	Ulva sp.	Ulva sp. 2	Clara Bertuccio	24/06/2009	Italy	Sicily	Lake Ganzirri, ST02	BOLD# ITGRE023-11
PHL	CB175	Ulva sp.	Ulva sp. 2	Clara Bertuccio	24/06/2009	Italy	Sicily	Lake Ganzirri, ST02	GB# KM212024
PHL	CB175	Ulva sp.	Ulva sp. 2	Clara Bertuccio	24/06/2009	Italy	Sicily	Lake Ganzirri, ST02	BOLD# ITGRE021-11
PHL	CB182	Ulva lactuca	Ulva lactuca	Clara Bertuccio	24/06/2009	Italy	Sicily	Lake Ganzirri, ST03	GB# KM212025
PHL	CB182	Ulva lactuca	Ulva lactuca	Clara Bertuccio	24/06/2009	Italy	Sicily	Lake Ganzirri, ST03	BOLD# ITGRE016-11
PHL	CB141	Ulva lactuca	Ulva lactuca	Clara Bertuccio	17/06/2009	Italy	Sicily	Lake Ganzirri, ST05	GB# KM212026
PHL	CB141	Ulva lactuca	Ulva lactuca	Clara Bertuccio	17/06/2009	Italy	Sicily	Lake Ganzirri, ST05	BOLD# ITGRE018-11
PHL	CB203	Ulva lactuca	Ulva lactuca	Clara Bertuccio	14/07/2009	Italy	Sicily	Lake Ganzirri, ST05	GB# KM212022
PHL	CB203	Ulva lactuca	Ulva lactuca	Clara Bertuccio	14/07/2009	Italy	Sicily	Lake Ganzirri, ST05	BOLD# ITGRE017-11
PHL	CB305	Ulva lactuca	Ulva lactuca	Clara Bertuccio	20/11/2009	Italy	Sicily	Lake Ganzirri, ST05	GB# MF544102
PHL	CB305	Ulva lactuca	Ulva lactuca	Clara Bertuccio	20/11/2009	Italy	Sicily	Lake Ganzirri, ST05	BOLD# GRAPP013-17
PHL	SAM029	Ulva lactuca	Ulva lactuca	Simona Armeli Minicante	18/03/2010	Italy	Sicily	Lake Ganzirri, ST05	GB# KM212023
PHL	SAM029	Ulva lactuca	Ulva lactuca	Simona Armeli Minicante	18/03/2010	Italy	Sicily	Lake Ganzirri, ST05	BOLD# ITGRE003-11
PHL	CB278	Ulva ohnoi	Ulva ohnoi	Clara Bertuccio	13/10/2009	Italy	Sicily	Lake Ganzirri, ST06	GB# MF172088
PHL	CB278	Ulva ohnoi	Ulva ohnoi	Clara Bertuccio	13/10/2009	Italy	Sicily	Lake Ganzirri, ST06	BOLD# ITGRE019-11
PHL	PhL665	Ulva sp.	Ulva lacinulata	Antonio Manghisi	09/03/2016	Italy	Sicily	Torre Faro, ST08	GB# MF544105
PHL	PhL665	Ulva sp.	Ulva lacinulata	Antonio Manghisi	09/03/2016	Italy	Sicily	Torre Faro, ST08	BOLD# GRAPP007-17
PHL	PhL668	Ulva sp.	Ulva lacinulata	Antonio Manghisi	09/03/2016	Italy	Sicily	Torre Faro, ST08	GB# MF544109
PHL	PhL668	Ulva sp.	Ulva lacinulata	Antonio Manghisi	09/03/2016	Italy	Sicily	Torre Faro, ST08	BOLD# GRAPP008-17
PHL	PhL669	Ulva sp.	Ulva lacinulata	Antonio Manghisi	09/03/2016	Italy	Sicily	Torre Faro, ST08	GB# MF544104
PHL	PhL669	Ulva sp.	Ulva lacinulata	Antonio Manghisi	09/03/2016	Italy	Sicily	Torre Faro, ST08	BOLD# GRAPP009-17
PHL	PhL670	Ulva sp.	Ulva lacinulata	Antonio Manghisi	09/03/2016	Italy	Sicily	Torre Faro, ST08	GB# MF544103
PHL	PhL670	Ulva sp.	Ulva lacinulata	Antonio Manghisi	09/03/2016	Italy	Sicily	Torre Faro, ST08	BOLD# GRAPP010-17
PHL	PhL671	Ulva sp.	Ulva lacinulata	Antonio Manghisi	09/03/2016	Italy	Sicily	Torre Faro, ST08	GB# MF544112
PHL	PhL671	Ulva sp.	Ulva lacinulata	Antonio Manghisi	09/03/2016	Italy	Sicily	Torre Faro, ST08	BOLD# GRAPP011-17
PHL	PhL673	Ulva sp.	Ulva lacinulata	Antonio Manghisi	09/03/2016	Italy	Sicily	Torre Faro, ST08	GB# MF544111
PHL	PhL673	Ulva sp.	Ulva lacinulata	Antonio Manghisi	09/03/2016	Italy	Sicily	Torre Faro, ST08	BOLD# GRAPP012-17
PHL	PhL654	Ulva sp.	Ulva lacinulata	Antonio Manghisi	09/03/2016	Italy	Sicily	Torre Faro, ST09	GB# MF544108
PHL	PhL654	Ulva sp.	Ulva lacinulata	Antonio Manghisi	09/03/2016	Italy	Sicily	Torre Faro, ST09	BOLD# GRAPP004-17
PHL	PhL655	Ulva sp.	Ulva lacinulata	Antonio Manghisi	09/03/2016	Italy	Sicily	Torre Faro, ST09	GB# MF544107
PHL	PhL655	Ulva sp.	Ulva lacinulata	Antonio Manghisi	09/03/2016	Italy	Sicily	Torre Faro, ST09	BOLD# GRAPP005-17
PHL	SAM143	Umbraulva dangeardii	Umbraulva dangeardii	Simona Armeli Minicante	21/04/2010	Italy	Sicily	Torre Faro, ST09	GB# MF172091
PHL	SAM143	Umbraulva dangeardii	Umbraulva dangeardii	Simona Armeli Minicante	21/04/2010	Italy	Sicily	Torre Faro, ST09	BOLD# ITGRE007-11
PHL	SAM144	Ulva sp.	Ulva lacinulata	Simona Armeli Minicante	21/04/2010	Italy	Sicily	Torre Faro, ST09	GB# MF544133
PHL	SAM144	Ulva sp.	Ulva lacinulata	Simona Armeli Minicante	21/04/2010	Italy	Sicily	Torre Faro, ST09	BOLD# GREVE003-17
PHL	SAM202	Ulva sp.	Ulva lacinulata	Simona Armeli Minicante	10/06/2010	Italy	Sicily	Torre Faro, ST09	GB# MF172084
PHL	SAM202	Ulva sp.	Ulva lacinulata	Simona Armeli Minicante	10/06/2010	Italy	Sicily	Torre Faro, ST09	BOLD# ITGRE009-11
PHL	VF135	Ulva sp.	Ulva lacinulata	Valeria Fiore	05/02/2010	Italy	Sicily	Torre Faro, ST09	GB# MF544110
PHL	VF135	Ulva sp.	Ulva lacinulata	Valeria Fiore	05/02/2010	Italy	Sicily	Torre Faro, ST09	BOLD# GRAPP014-17
PHL	PhL662	Ulva compressa	Ulva compressa	Antonio Manghisi	09/03/2016	Italy	Sicily	Torre Faro, ST10	GB# MF544100
PHL	PhL662	Ulva compressa	Ulva compressa	Antonio Manghisi	09/03/2016	Italy	Sicily	Torre Faro, ST10	BOLD# GRAPP003-17
PHL	PhL663	Ulva sp.	Ulva lacinulata	Antonio Manghisi	09/03/2016	Italy	Sicily	Torre Faro, ST10	GB# MF544106
PHL	PhL663	Ulva sp.	Ulva lacinulata	Antonio Manghisi	09/03/2016	Italy	Sicily	Torre Faro, ST10	BOLD# GRAPP006-17
PHL	PhL658	Ulva compressa	Ulva compressa	Antonio Manghisi	09/03/2016	Italy	Sicily	Torre Faro, ST11	GB# MF544101
PHL	PhL658	Ulva compressa	Ulva compressa	Antonio Manghisi	09/03/2016	Italy	Sicily	Torre Faro, ST11	BOLD# GRAPP002-17
PHL	SAM175	Umbraulva dangeardii	Umbraulva dangeardii	Simona Armeli Minicante	09/06/2010	Italy	Sicily	Torre Faro, ST12	GB# MF172090
PHL	SAM175	Umbraulva dangeardii	Umbraulva dangeardii	Simona Armeli Minicante	09/06/2010	Italy	Sicily	Torre Faro, ST12	BOLD# ITGRE008-11
PHL	SAM283	Ulva laetevirens	Ulva lacinulata	Simona Armeli Minicante	28/06/2010	Italy	Veneto	Lagoon of Venice, Bocca di Porto di Lid o	GB# MF172085
PHL	SAM283	Ulva laetevirens	Ulva lacinulata	Simona Armeli Minicante	28/06/2010	Italy	Veneto	Lagoon of Venice, Bocca di Porto di Lid o	BOLD# ITGRE010-11
PHL	SAM047	Ulva australis	Ulva australis	Simona Armeli Minicante	22/03/2010	Italy	Veneto	Lagoon of Venice, Celestia	GB# MF172078
PHL	SAM047	Ulva australis	Ulva australis	Simona Armeli Minicante	22/03/2010	Italy	Veneto	Lagoon of Venice, Celestia	BOLD# ITGRE004-11
PHL	SAM051	Ulva linza	“Ulva linza/procera/prolifera”	Simona Armeli Minicante	22/03/2010	Italy	Veneto	Lagoon of Venice, Celestia	GB# MF172089
PHL	SAM051	Ulva linza	“Ulva linza/procera/prolifera”	Simona Armeli Minicante	22/03/2010	Italy	Veneto	Lagoon of Venice, Celestia	BOLD# ITGRE005-11
ISMAR	SAM1179	Ulva sp.	Ulva compressa	Simona Armeli Minicante	17/05/2019	Italy	Veneto	Lagoon of Venice, Isola della Certosa	GB# OR734315
ISMAR	SAM1180	Ulva sp.	Ulva australis	Simona Armeli Minicante	17/05/2019	Italy	Veneto	Lagoon of Venice, Isola della Certosa	GB# OR734321
ISMAR	SAM1182	Ulva sp.	Ulva australis	Simona Armeli Minicante	17/05/2019	Italy	Veneto	Lagoon of Venice, Isola della Certosa	GB# OR734322
PHL	SAM518	Ulva australis	Ulva australis	Simona Armeli Minicante	09/05/2011	Italy	Veneto	Lagoon of Venice, Isola della Certosa	GB# MF544131
PHL	SAM518	Ulva australis	Ulva australis	Simona Armeli Minicante	09/05/2011	Italy	Veneto	Lagoon of Venice, Isola della Certosa	BOLD# GREVE001-17
PHL	SAM522	Ulva compressa	Ulva compressa	Simona Armeli Minicante	09/05/2011	Italy	Veneto	Lagoon of Venice, Isola della Certosa	GB# MF544132
PHL	SAM522	Ulva compressa	Ulva compressa	Simona Armeli Minicante	09/05/2011	Italy	Veneto	Lagoon of Venice, Isola della Certosa	BOLD# GREVE002-17
ISMAR	SAM1162	Ulva sp.	Ulva compressa	Simona Armeli Minicante	17/05/2019	Italy	Veneto	Lagoon of Venice, Lido (canale)	GB# OR734314
ISMAR	SAM1163	Ulva sp.	Ulva compressa	Simona Armeli Minicante	17/05/2019	Italy	Veneto	Lagoon of Venice, Lido (canale)	GB# OR734317
ISMAR	SAM1164	Ulva sp.	Ulva compressa	Simona Armeli Minicante	17/05/2019	Italy	Veneto	Lagoon of Venice, Lido (canale)	GB# OR734316
ISMAR	SAM1165	Ulva sp.	Ulva flexuosa subsp. flexuosa	Simona Armeli Minicante	17/05/2019	Italy	Veneto	Lagoon of Venice, Ido (canale)	GB# OR734311
ISMAR	SAM1166	Ulva sp.	Ulva sp. 1	Simona Armeli Minicante	17/05/2019	Italy	Veneto	Lagoon of Venice, Lido (canale)	GB# OR734320
PHL	SAM357	Ulva compressa	Ulva compressa	Simona Armeli Minicante	30/06/2010	Italy	Veneto	Lagoon of Venice, Ottagono S. Pietro in Volta	GB# MF172081
PHL	SAM357	Ulva compressa	Ulva compressa	Simona Armeli Minicante	30/06/2010	Italy	Veneto	Lagoon of Venice, Ottagono S. Pietro in Volta	BOLD# ITGRE013-11
ISMAR	SAM1173	Ulva sp.	Ulva compressa	Simona Armeli Minicante	17/05/2019	Italy	Veneto	Lagoon of Venice, Pellestrina	GB# OR734319
ISMAR	SAM1176	Ulva sp.	Ulva compressa	Simona Armeli Minicante	17/05/2019	Italy	Veneto	Lagoon of Venice, Pellestrina	GB# OR734318
ISMAR	SAM1133	Ulva sp.	Ulva lactuca	Simona Armeli Minicante	18/09/2018	Italy	Veneto	Lagoon of Venice, St. 1	GB# OR734313
ISMAR	SAM1138	Ulva sp.	Ulva californica	Simona Armeli Minicante	18/09/2018	Italy	Veneto	Lagoon of Venice, St. 1	GB# OR734309
ISMAR	SAM1074	Ulva sp.	“Ulva linza/procera/prolifera”	Simona Armeli Minicante	24/05/2018	Italy	Veneto	Lagoon of Venice, St. 10	GB# OR734307
ISMAR	SAM1076	Ulva sp.	“Ulva linza/procera/prolifera”	Simona Armeli Minicante	24/05/2018	Italy	Veneto	Lagoon of Venice, St.10	GB# OR734308
ISMAR	SAM1086	Ulva sp.	Ulva australis	Simona Armeli Minicante	24/05/2018	Italy	Veneto	Lagoon of Venice, St. 14	GB# OR734323
ISMAR	SAM1142	Ulva sp.	Ulva lactuca	Simona Armeli Minicante	18/09/2018	Italy	Veneto	Lagoon of Venice, St. 2	GB# OR734312
ISMAR	SAM1143	Ulva sp.	Ulva californica	Simona Armeli Minicante	18/09/2018	Italy	Veneto	Lagoon of Venice, St. 2	GB# OR734310
PHL	SAM315	Ulva laetevirens	Ulva lacinulata	Simona Armeli Minicante	30/06/2010	Italy	Veneto	Lagoon of Venice, Porto S. Leonardo	GB# MF172086
PHL	SAM315	Ulva laetevirens	Ulva lacinulata	Simona Armeli Minicante	30/06/2010	Italy	Veneto	Lagoon of Venice, Porto S. Leonardo	BOLD# ITGRE011-11
PHL	SAM316	Ulva australis	Ulva australis	Simona Armeli Minicante	30/06/2010	Italy	Veneto	Lagoon of Venice, Porto S. Leonardo	GB# MF172079
PHL	SAM316	Ulva australis	Ulva australis	Simona Armeli Minicante	30/06/2010	Italy	Veneto	Lagoon of Venice, Porto S. Leonardo	BOLD# ITGRE012-11
PHL	SAM361	Ulva compressa	Ulva compressa	Simona Armeli Minicante	30/06/2010	Italy	Veneto	Lagoon of Venice, Porto S. Leonardo	GB# MF172080
PHL	SAM361	Ulva compressa	Ulva compressa	Simona Armeli Minicante	30/06/2010	Italy	Veneto	Lagoon of Venice, Porto S. Leonardo	BOLD# ITGRE014-11
PHL	SAM369	Ulva lactuca	Ulva lactuca	Simona Armeli Minicante	30/06/2010	Italy	Veneto	Lagoon of Venice, Porto S. Leonardo	GB# MF172082
PHL	SAM369	Ulva lactuca	Ulva lactuca	Simona Armeli Minicante	30/06/2010	Italy	Veneto	Lagoon of Venice, Porto S. Leonardo	BOLD# ITGRE015-11
PHL	RM0089	Ulva torta	Ulva torta	Ramzi Miladi	28/06/2014	Tunisia		Chaffar, Sfax	GB# MF614794
PHL	RM0089	Ulva torta	Ulva torta	Ramzi Miladi	28/06/2014	Tunisia		Chaffar, Sfax	BOLD# TUGRE013-17
PHL	RM0279	Ulva ohnoi	Ulva ohnoi	Ramzi Miladi	10/08/2015	Tunisia		Gabes	GB# MF614793
PHL	RM0279	Ulva ohnoi	Ulva ohnoi	Ramzi Miladi	10/08/2015	Tunisia		Gabes	BOLD# TUGRE012-17
PHL	RM0287	Ulva sp.	Ulva chaugulei	Ramzi Miladi	10/08/2015	Tunisia		Gabes	GB# OR773464
PHL	RM0067	Ulva compressa	Ulva compressa	Ramzi Miladi	01/06/2014	Tunisia		Kerkennah	GB# MF614783
PHL	RM0067	Ulva compressa	Ulva compressa	Ramzi Miladi	01/06/2014	Tunisia		Kerkennah	BOLD# TUGRE007-17
PHL	RM0228	Ulva compressa	Ulva compressa	Ramzi Miladi	08/04/2015	Tunisia		Korbous	GB# MF614787
PHL	RM0228	Ulva compressa	Ulva compressa	Ramzi Miladi	08/04/2015	Tunisia		Korbous	BOLD# TUGRE003-17
PHL	RM0229	Ulva compressa	Ulva compressa	Ramzi Miladi	08/04/2015	Tunisia		Korbous	GB# MF614786
PHL	RM0229	Ulva compressa	Ulva compressa	Ramzi Miladi	08/04/2015	Tunisia		Korbous	BOLD# TUGRE004-17
PHL	RM0134	Ulva laetevirens	Ulva lacinulata	Ramzi Miladi	03/08/2014	Tunisia		Monastir	GB# MF614792
PHL	RM0134	Ulva laetevirens	Ulva lacinulata	Ramzi Miladi	03/08/2014	Tunisia		Monastir	BOLD# TUGRE009-17
PHL	RM00S1	Ulva compressa	Ulva compressa	Ramzi Miladi	10/08/2015	Tunisia		Sousse	GB# MF614785
PHL	RM00S1	Ulva compressa	Ulva compressa	Ramzi Miladi	10/08/2015	Tunisia		Sousse	BOLD# TUGRE005-17
PHL	RM0270	Ulva laetevirens	Ulva lacinulata	Ramzi Miladi	12/04/2015	Tunisia		Sousse	GB# MF614790
PHL	RM0270	Ulva laetevirens	Ulva lacinulata	Ramzi Miladi	12/04/2015	Tunisia		Sousse	BOLD# TUGRE011-17
PHL	RM0296	Ulva compressa	Ulva compressa	Ramzi Miladi	26/03/2016	Tunisia		Sousse	GB# MF614784
PHL	RM0296	Ulva compressa	Ulva compressa	Ramzi Miladi	26/03/2016	Tunisia		Sousse	BOLD# TUGRE006-17
PHL	RM0190E	Ulva laetevirens	Ulva lacinulata	Ramzi Miladi	04/04/2015	Tunisia		Tabarka	GB# MF614791
PHL	RM0190E	Ulva laetevirens	Ulva lacinulata	Ramzi Miladi	04/04/2015	Tunisia		Tabarka	BOLD# TUGRE010-17
PHL	RM0190S	Ulva compressa	Ulva compressa	Ramzi Miladi	04/04/2015	Tunisia		Tabarka	GB# MF614782
PHL	RM0190S	Ulva compressa	Ulva compressa	Ramzi Miladi	04/04/2015	Tunisia		Tabarka	BOLD# TUGRE001-17
PHL	RM0203	Ulva compressa	Ulva compressa	Ramzi Miladi	04/04/2015	Tunisia		Tabarka	GB# MF614788
PHL	RM0203	Ulva compressa	Ulva compressa	Ramzi Miladi	04/04/2015	Tunisia		Tabarka	BOLD# TUGRE002-17
PHL	RM000A	Ulva flexuosa	Ulva aragoënsis	Ramzi Miladi	12/03/2014	Tunisia		Zarat	GB# MF614789
PHL	RM000A	Ulva flexuosa	Ulva aragoënsis	Ramzi Miladi	12/03/2014	Tunisia		Zarat	BOLD# TUGRE008-17

3.1 Ulva australis Areschoug

From the analysis of the data obtained from the Lagoon of Venice, we report U. australis Areschoug (Figure 5) as established in the area between Celestia and Certosa Island, with a good MaQI index. However, the latest samplings also report it in more inland areas of the lagoon, including Porto S. Leonardo and ST14, and with a poor MaQI index.

According to Sfriso et al. (2023), U. australis is now the most widespread NIS in the Lagoon of Venice. It is possible that the species growth is being aided by the decrease in the lagoon’s trophic conditions.

This Indo-Pacific species was introduced in the Mediterranean Sea by mollusc farming and recorded, as U. pertusa Kjellman, from the Thau Lagoon (France) (Cormaci et al. 2004), the Gulf of Naples (Flagella et al. 2010) and the Lagoon of Venice (Manghisi et al. 2011). ITS1 and rbcL data of U. pertusa from Spain suggested their synonymy with U. australis (Couceiro et al. 2011). Wolf et al. (2012) confirmed the presence of U. australis in the Lagoon of Venice by analyses based on rbcL and tufA markers.

Womersley (1984) reported U. laetevirens among synonyms of U. australis, pointing out that the sizes of cells of the lectotype of U. laetevirens were superimposable to those of U. australis. Subsequently, Phillips (1988) considered U. australis to be a synonym of U. rigida.

Furthermore, molecular investigations performed by Kraft et al. (2010) have demonstrated that U. rigida was distinct from U. australis. The recent phylogenetic analysis of rbcL gene sequences by Hughey et al. (2021), supports the taxonomic synonymy between U. laetevirens and U. australis assumed by Womersley (1984).

In the Lagoon of Venice, Sfriso (2010a), probably following Phillips (1988), listed U. australis among synonyms of U. rigida. Santarelli (1931) listed Ulva lactuca f. laciniata (Wulfen) J. Agardh from Trani (Adriatic Sea), indicating the species is synonymous with U. australis Kützing; as reported by the author, this species was collected in Adriatic Sea also by Van Den Bosch, Kützing and Hauck.

Whereas Schiffner (Schiffner and Vatova 1938) labelled samples of U. lactuca var. laciniata (Wulfen) J. Agardh, including also the “f. australis” in the “Vatova and Schiffner” collection, hosted at the Natural History Museum of Venice. Observing these herbarium samples in the “Vatova and Schiffner” collection, we do not exclude the possibility that U. australis was already present in the Lagoon of Venice in the early 1990s.

3.2 Ulva californica Wille

We report the presence of Ulva californica Wille (Figure 4) in the most internal sites of the Lagoon of Venice, ST01 and ST02. This species was first reported in 2012 in the historic centre of Venice by Wolf et al. (2012).

U. californica was first described in 1899 from La Jolla, California (Collins et al. 1899). Opinions about the original range of the species are very different (Wei et al. 2022), from a distribution limited to North America (Scagel 1989; Wolf et al. 2012) or wider, including European temperate coasts (Loughnane et al. 2008). New and numerous reports of this species have been made in different biogeographical areas through molecular data, including Japan (Kawai et al. 2007), New Zealand (Heesch et al. 2009), Italy (Wolf et al. 2012) and Australia (Kirkendale et al. 2013).

3.3 Ulva compressa Linnaeus

The species was collected in the marine sites of Torre Faro (ST10 and ST11); in the Lagoon of Venice, Ulva compressa Linnaeus (Figure 5) was collected in Ottagono S. Pietro in Volta, Pellestrina, Lido and Porto S. Leonardo. Due to the high intraclade divergence, it is possible that this group represents a species complex (Melton and Lopez-Bautista 2021).

U. compressa is a very common marine green macroalga, distributed on the coasts of Asia, Europe, and America (Guiry and Guiry 2023), with a high intraspecific morphological plasticity, from the narrow, blade-like morphotype, to the foliose free-floating thallus (Liu and Melton 2021). The species could grow rapidly in eutrophic environments, accumulating massive biomass and causing notorious green tides (Blomster et al. 2002).

3.4 Ulva flexuosa subsp. flexuosa Wulfen

The only sample of Ulva flexuosa subsp. flexuosa Wulfen (SAM1165; Figure 4) was collected at the Lido station (sufficient MaQI Index) in the spring of 2019.

According to Cormaci et al. (2014), U. flexuosa colonizes several habitats, both sheltered and exposed; however, it is more common in brackish lagoon environments and in canals with poor water exchange (Cormaci et al. 2014).

In the Lagoon of Venice, Pignatti (1962), reported U. flexuosa (as Enteromorpha flexuosa) as a species characteristic of the photophilous community of Fucetum virsoidis, established on the north-eastern Adriatic rocky coasts in the presence of large tidal ranges, low average temperatures, low salinity, and eutrophic waters (Pignatti 1962).

Three subspecies of U. flexuosa were reported for the Lagoon of Venice by Sfriso et al. (2009): U. flexuosa Wulfen subsp. biflagellata (Bliding) Sfriso et Curiel, U. flexuosa Wulfen subsp. paradoxa (C. Agardh) M. J. Wynne and U. flexuosa Wulfen subsp. pilifera (Kützing) M. J. Wynne.

3.5 Ulva lacinulata (Kützing) Wittrock

The presence of U. lacinulata (Kützing) Wittrock (Figure 4) is confirmed in the marine sites ST09 and ST10 of Torre Faro and in the channel connecting Lake Ganzirri to the sea (ST08). The presence of U. lacinulata from the Lagoon of Venice is reported in Porto S. Leonardo and Bocca di Porto di Lido. These samples had been previously identified as U. laetevirens by Armeli Minicante (2013), being genetically conspecific with U. laetevirens from Australia (type area, Port Phillip, South Australia) (Kirkendale et al. 2013).

According to Hughey et al. (2021), U. lacinulata is the correct name to apply to the globally [excluding European] distributed species that was previously but incorrectly known as U. rigida. In Europe, both the genuine U. rigida and U. lacinulata occurs; however, according to the distribution based on DNA sequences reported by Hughey et al. (2021), at present, U. rigida appears to be restricted to the European north-eastern Atlantic Ocean, whereas U. lacinulata – variously reported either as U. rigida or U. laetevirens – is distributed further in the Mediterranean Sea.

In the Lagoon of Venice, U. lacinulata was already reported as U. lactuca f. lacinulata by Schiffner and Vatova (1938) and Pignatti (1962). Sfriso (1987) and later (Sfriso 2010b; Sfriso and Curiel 2007), referring to Bliding (1968), listed U. lactuca f. lacinulata as a synonyms of U. rigida.

Furthermore, the comparison of the sequences from Tunisia published by Miladi et al. (2018) showed that U. lacinulata was previously labelled as U. laetevirens in Monastir, Sousse and Tabarka sites (Figure 4) for the same reason stated above (Kirkendale et al. 2013).

3.6 Ulva lactuca Linnaeus

Samples of U. lactuca Linnaeus (Figure 4) were collected in stations ST1, ST2, and Porto San Leonardo, all three falling within the inner part of the Lagoon of Venice, a poor-quality area according to the MaQI index. In Lake Ganzirri, the species was collected in ST05.

According to Hughey et al. (2019), the holotype of U. lactuca is the species previously called U. fasciata in the subtropical area and U. lobata in the eastern Pacific Ocean. The current distribution of U. lactuca confirmed by DNA sequences is in the eastern (Australia) and northern (India) Indian Ocean, central (Hawai’i, USA) and temperate southeast (Chile, Peru), southwest (Australia), and northwest (South Korea, Japan) Pacific Ocean, warm temperate eastern (Azores) and western Atlantic Ocean (including the Gulf of Mexico and Atlantic Florida, USA) and the eastern (Egypt, Israel) and western (Italy) Mediterranean Sea (Hughey et al. 2019). The presence of this species in the two sites in Italy, in Capo Peloro Lagoon and the Lagoon of Venice (Miladi et al. 2018), might be due to recent introductions as both sites have anthropogenic impacts, also according to Hughey et al. (2019). However, their introduction date might be older. The first record of U. lactuca in the Lagoon of Venice dates to 1987 as U. fasciata (Sfriso 1987); in 1938, Schiffner reported as “U. fasciata Delile […] has also been collected in the Adriatic at Makarska (Dalmatia); is rare and is often confused with U. lactuca” (Schiffner and Vatova 1938).

3.7 “Ulva linza/procera/prolifera”

Samples of “U. linza/procera/prolifera” (Figure 4) were collected in spring at the ST10 in 2018 and at Celestia station in 2010 (Table 1), with a poor and good MaQI Index, respectively. The latter specimen had previously been identified by Armeli Minicante (2013) as U. linza (Supplementary Table 2).

ITS sequence data obtained by Brodie et al. (2007) showed Ulva procera (Ahlner) Hayden, Blomster, Maggs, Silva, Stanhope et Waaland as conspecific with typical Ulva linza Linnaeus. Furthermore, Kang et al. (2014) note that several authors regard U. procera as a separate species from U. linza (Heesch et al. 2009; Kirkendale et al. 2013; Saunders and Kucera 2010).

The lectotype of U. prolifera O. F. Müller is a drawing in Müller (Müller 1778), the epitype was designated and sequences for the ITS-2 and 5S rDNA spacer regions generated. The ITS-2 sequence of this specimen was not made publicly available but was reported to be identical to a previously published sequence with GenBank accession number AJ012276 (Kuba et al. 2022).

To date, there are two major opinions (Cui et al. 2018) on the classification of U. prolifera based on molecular markers. One point of view is that the true U. prolifera is included in the linza–procera–prolifera (LPP) complex clade (consisting of U. linza Linnaeus, U. procera (Ahlner) Hayden, Blomster, Maggs, Silva, Stanhope et Waaland, and U. prolifera), and the other is that U. prolifera forms a separate clade that includes specimens from Scotland and Ireland, while the entire LPP complex clade is U. linza.

Using ITS and 5S rRNA gene spacer region as barcode markers on Ulva LPP complex, U. procera was recently reduced into synonymy under U. prolifera by Cui et al. (2018).

Based on this synonymy, Kuba et al. (2022) identified U. procera specimens from San Juan Islands (USA) on the basis of ITS-2 sequences, that were 1–2 base pairs different (0.47–0.93 %) from that of the U. prolifera epitype. However, the San Juan Islands specimens molecularly identified as U. prolifera, were not branched tubes, the characteristic morphology of the species, but distromatic blades that became tubular where they were basally narrow near the point of attachment. This latter morphology has been identified as U. linza in the Northeast Pacific (Kuba et al. 2022). In the light of these observations, the authors suggest that the concept of U. prolifera needs to be expanded to include blade-form thalli.

The LPP-clade has been a troublesome group, and morphology does not appear to be helpful because this clade is known to have wide-ranging morphologies from linza-like to prolifera-like. Additionally, only tufA sequence data was obtained for our samples since this has shown to be an excellent barcoding marker for green algae, and therefore, we were not able to compare this sequence data with the 5S rRNA and ITS sequence data from the epitype. For these reasons, we choose to call the clade “U. linza/procera/prolifera” as the designation for the samples from the Lagoon of Venice identified in this study. Multi-gene or genomic analysis should be considered in the future.

3.8 Ulva ohnoi Hiraoka et Shimada

Samples of U. ohnoi Hiraoka et Shimada (Figure 4) were found in human-impacted sites (ST01 and ST06) of Lake Ganzirri, and its introduction was probably attributable either to maritime traffic, particularly relevant in the Strait of Messina, or to mollusc trading, similarly to what was proved for Agardhiella subulata (C. Agardh) Kraft et M. J. Wynne in the same site (Manghisi et al. 2010). In the Mediterranean, the first detection of U. ohnoi had been by Mineur et al. (2007) in the algal fouling biomass on ships arriving at the commercial harbour at Sète (Mediterranean coast of France); similarly, a few years later, Flagella et al. (2010) recorded the species in ballast water from ships, coming from Singapore, in the harbour of Naples (Italy).

However, colonization by this species had not been detected in the area (Flagella et al. 2010). U. ohnoi is commonly regarded as a NIS, having a disjointed distribution and being recorded in highly disturbed sites. However, its presence in the Mediterranean Sea, as well as in other sites, might be underestimated and its actual distribution, as well as its native range, might be far different from what presently known (Miladi et al. 2018).

3.9 Ulva sp. 1 and Ulva sp. 2

Of the 52 tufA sequences generated, two have remained unresolved at the species level.

The sample SAM1166, collected in the Lido station in the Lagoon of Venice, falls into the Ulva sp. 1 clade (Figure 4) with a sample from Tasmania (Australia), reported as Ulva sp.10GWS (GenBank Accession number JN029338, Kirkendale et al. 2013).

Additionally, three samples from Lake Ganzirri (CB174, CB175 and CB164) fall into the Ulva sp. 2 clade (Figure 4) with a sample from Aransas Pass, Texas, USA (GenBank Accession number MT859901, Melton and Lopez-Bautista 2021). Clarifying the taxonomic identity of these spp. requires further work.

3.10 Ulva chaugulei M. G. Kavale et M. A. Kazi

Ulva chaugulei M. G. Kavale et M. A. Kazi (Figure 4) was reported for first time in Pacific Ocean (type locality: Vayangani Maharashtra, India) by Kazi et al. 2016. To date, the distribution of U. chaugulei is reported by molecular data in Brazil (Carneiro et al. 2023) and Persian Gulf (Pirian et al. 2016). In Mediterranean Sea, the first record of U. chaugulei was reported by Krupnik et al. (2018) through molecular analyses of herbarium samples collected in 2015/2016 from the Israel coasts. In this study, we record the presence of a sample of U. chaugulei (RM0287) also on the Tunisia coast (Gabes) and previously reported as Ulva sp. by molecular analyses.

4 Discussion

Ulva species play a considerable role in marine ecosystems, providing significant advantages and additional services (Cotas et al. 2023; Israel and Shpigel 2023). Edible Ulva species hold considerable nutritional value (Peñalver et al. 2020; Xu et al. 2023) and are extensively used in aquaculture to feed and enhance the growth of marine organisms (Abdel-Warith et al. 2016). Ulva species contain bioactive compounds with potential pharmaceutical applications (Guo et al. 2022; Yang et al. 2021) or as a source of plant growth regulators (Spagnuolo et al. 2022).

Given all these properties and benefits, these green algae have been identified as the most suitable candidate and model organism for a novel kind of European mariculture and included in the COST Action CA20106 (SeaWheat, https://seawheat.ussl.info/), with the aim to improve knowledge in the biology of the most promising Ulva spp., capitalize on their economic potential, and explore commercial applications in the human food, animal feed, pharmaceutical industries, and ecosystem service.

In addition to the numerous positive aspects highlighted, it is essential to acknowledge that Ulva, like many other prolific macroalgae, can have unintended consequences in certain environments. Notably, in eutrophic conditions, Ulva species have been known to undergo rapid and extensive growth, often resulting in the formation of large-scale accumulations, commonly referred to as “green tides” (Blomster et al. 2002; Kang et al. 2014; Xie et al. 2020). These events can have detrimental effects on local ecosystems, impacting water quality, marine biodiversity, and aquaculture operations. In this context, the correct identification of Ulva species and a comprehensive review of past efforts, especially if based only on morphological investigations, is becoming increasingly crucial.

To date, 23 species of Ulva are currently reported in the Mediterranean Sea, of which molecular data are available for 12 taxa, whereas 18 species are reported for the Italian coasts, but molecular data are still lacking or under investigation for half of these (Table 2). Based on molecular analyses conducted by Hughey et al. (2021), we excluded U. rigida C. Agardh from the Mediterranean list. This species has only been confirmed by DNA sequences from Ireland, Portugal and the Atlantic coasts of Spain, and U. pseudorotundata Cormaci, G. Furnari et Alongi, for which the holotype from Italy was identical to U. lactuca (Hughey et al. 2021). Furthermore, as already discussed above, we currently consider “U. linza/procera/prolifera” as a single form, until further investigations are made.

Table 2:

Species of Ulva reported for the Mediterranean Sea and along Italian coasts (marked in bold).

Species	Morphotype	Type locality	Molecular data
Species	Morphotype	Type locality	Type specimens sequenced	Sequences from the Mediterranean	References	Sequences from Italy	References
Ulva aragoënsis (Bliding) Maggs	Tube-forming	Syntype localities: various, in Atlantic France and Mediterranean Sea	✗	✓	Krupnik et al. (2018); this study	✗	–
Ulva australis Areschoug	Blade-forming	“In caulibus Cauliniae antarcticae parasitica, ad oram Novae Hollandiae australem in sinu Port Adelaide.” Areschoug (1854)	✓	✓	–	✓	Manghisi et al. (2011); Wolf et al. (2012); Miladi et al. (2018); this study
Ulva californica Wille	Blade-forming	La Jolla, California Collins et al. (1899)	✗	✓	Bartolo et al. (2022)	✓	Wolf et al. (2012); this study
Ulva chaugulei M. G. Kavale et M. A. Kazi	Blade-forming	Vayangani, Maharashtra, India Kazi et al. (2016)	✓	✓	Krupnik et al. (2018); this study	✗	–
Ulva clathrata (Roth) C. Agardh	Tube-forming	Fehmarn, SW Baltic Berger et al. (2003)	✗	✗	–	✗	–
Ulva compressa Linnaeus	Tube-forming	“Habitat in Europae mari & tectis maritimis” [probably Bognor, Sussex, England] Hayden et al. (2003)	✗	✓	Miladi et al. (2018); Bartolo et al. (2022)	✓	Wolf et al. (2012); Miladi et al. (2018); this study
Ulva curvata (Kützing) De Toni	Tube-forming		✗	✗	–	✗	–
Ulva flexuosa Wulfen	Tube-forming	Duino (near Trieste), Adriatic Sea [marine localtion] Womersley (1984)	✗	✓	Miladi et al. (2018)	✓	–
Ulva flexuosa subsp. flexuosa Wulfen	Tube- or blade-forming		✗	✓	This study	✓	This study
Ulva intestinalis Linnaeus	Tube-forming	Woolwich, London, England Hayden et al. (2003)	✗	✗	–	✗	–
Ulva kylinii (Bliding) H. S. Hayden, Blomster, Maggs, P. C. Silva, Stanhope et Waaland	Tube-forming	Kristineberg, Sweden Silva et al. (1996)	✗	✗	–	✗	–
Ulva lacinulata (Kützing) Wittrock	Blade-forming	–	✓	✓	Miladi et al. (2018)	✓	This study
Ulva lactuca Linnaeus	Blade-forming	“In Oceano” [Atlantic Ocean] Linnaeus (1753)	✓	✓	Miladi et al. (2018)	✓	This study
Ulva linzoides Alongi, Cormaci et G. Furnari	Tube-forming	–	✗	✗	–	✗	–
Ulva ohnoi M. Hiraoka et S. Shimada	Blade-forming	Tosa Bay, Tosa, Kochi Prefecture Hiraoka et al. (2004)	✓	✓	Miladi et al. (2018)	✓	Miladi et al. (2018); this study
Ulva paradoxa C. Agardh	Tube-forming	Bangor, Wales Berger et al. (2003)	✗	✗	–	✗	–
Ulva pilifera (Kützing) Škaloud et Leliaert	Tube-forming	Tennstedt, Thüringen, Germany (Silva et al. 1996)	✗	✗	–	✗	–
Ulva polyclada Kraft	Tube-forming	Sylphs Hole, Lord Howe Island, Australia Kraft (2007)	✗	✗	–	✗	–
“ *Ulva linza/procera/prolifera* ”	Tube-forming	U. linza: “In Oceano” Linnaeus (1753) U. procera: Syntype localities: various in SwedenSilva et al. (1996) U. prolifera: “U. p. tubulosa simplex teres, adultior compressiuscula. In fossa ad Nebbelund Lalandiae” [Lolland, Denmark]	✓	✗	–	✓	This study
Ulva pseudolinza (Koeman et Hoek) H. S. Hayden, Blomster, Maggs, P. C. Silva, Stanhope et Waaland	Tube-forming	Den Helder, Netherlands Koeman and Hoek (1982)	✗	✗	–	✗	–
Ulva ralfsii (Harvey) Le Jolis	Tube-forming	Lectotype locality: Bangor, North Wales Silva et al. (1996)	✗	✗	–	✗	–
Ulva torta (Mertens) Trevisan	Tube-forming	Norderney, East Frisian Islands, Germany Silva et al. (1996)	✗	✓	Miladi et al. (2018); Bartolo et al. (2022)	✗	–
Ulva tepida Y. Masakiyo et S. Shimada	Blade-forming	Enoshima Island, Fujisawa, Kanagawa Prefecture, Japan Masakiyo and Shimada (2014)	✓	✓	Krupnik et al. (2018)	✗	–

For this first time in this study, we added molecular data for U. lactuca, “U. linza/procera/prolifera” and U. flexuosa subsp. flexuosa from the Lagoon of Venice; molecular data were also obtained for U. lacinulata, previously sequenced and labelled as U. rigida by Wolf et al. (2012). The specimens identified as “U. linza/procera/prolifera” exhibit blade forms that became tubular near the basal attachment. This morphology was also observed by Kuba et al. (2022) in specimens from the San Juan Islands (USA). Lastly, one unidentified species designated as Ulva sp. 1., was resolved in a clade with samples from Australia.

In the last 85 years, the list of data reported for the different species of Ulva has changed considerably in the Lagoon of Venice (Supplementary Table 2). The most exhaustive work, in terms of geographical coverage, has been conducted by Schiffner and Vatova (1938). However, the number of species reported in this study was over-estimated, as often happens for the work at the time based on morphological characters. Over time, updates and reports of new species have been obtained by morphological observations and/or bibliographic revisions; conversely, this high diversity is not supported in the last molecular studies (see Supplementary Table 2 and the references therein). Furthermore, the contemporary published works focus on localized areas of the Lagoon of Venice, and massive studies based on large sampling areas and long-term series (including the preservation of herbarium specimens) have reduced over time.

Regarding the sampling sites in Sicily, molecular data for U. lactuca and U. ohnoi were obtained from the brackish basin of Lake Ganzirri, whereas data for U. lacinulata and U. compressa came from the marine sampling sites in the Strait of Messina. Specimens of an unidentified species, referred to as Ulva sp. 2., formed a clade with the sequences of a specimen from the Gulf of Mexico (Texas, USA).

Of the 23 Ulva species recorded in the Mediterranean Sea, five taxa – U. ohnoi Hiraoka et Shimada, U. australis Areschoug, U. chaugulei M. G. Kavale et M. A. Kazi, Ulva tepida Y. Masakiyo et S. Shimada and U. californica Wille – are non-indigenous and cryptogenic introductions, with a point-like distribution thus far in the Mediterranean Sea (Supplementary Figure 1); however, their distribution needs to be studied further. With the exception of U. tepida and U. chaugulei, reported for the southeastern Mediterranean Sea (Bartolo et al. 2022; Krupnik et al. 2018), all the other alien species are present in Italy, in the investigated area of Lake Ganzirri (U. ohnoi) and the Lagoon of Venice (U. australis and U. californica).

According to van der Loos et al. (2023), U. californica and U. ohnoi are NIS native to the Northeast Pacific Ocean; whereas the origin of U. australis would be identified in the Northeast Asia (Hanyuda et al. 2016). Among the NIS, these authors also report U. chaugulei as a cryptogenic taxon, native to the Indo Pacific Ocean/Red Sea.

In this study, molecular analyses showed the presence of a U. chaugulei voucher among the Ulva samples hosted in the PHL Herbarium (Table 1; Figure 4; Supplementary Figure 2). The species was collected in Tunisia (Gabes), in a highly impacted area, close to commercial and fishing harbours, chemical and oil industries, and tourist pathways, in the same site where the Japanese bloom-forming U. ohnoi was recorded (Miladi et al. 2018).

The first record of U. chaugulei in the Mediterranean Sea was reported by Krupnik et al. (2018) based on molecular analyses of herbarium samples collected in 2015/2016 from the Israel coasts. Despite the recent report of this species, the authors suggest that this species could have been previously misidentified as U. linza (Einav and Israel 2008; Krupnik et al. 2018). Being easily confused with other tube-forming Ulva species and due to the paucity of molecular data in the Mediterranean Sea, it is currently difficult to speculate on the native or non-indigenous nature of this species.

The difficulty of identifying Ulva species makes determining between indigenous, pseudo-indigenous (see Carlton 2009) and non-indigenous species even more complicated. In this context, different aspects are needed in the approach to the study of the biodiversity of Ulva.

Traceability: An accurate biodiversity assessment is essential for monitoring biological introductions, and also critical for providing a baseline to detect evidence for short- and long-term trends in biodiversity and human-induced environmental changes.

Temporal surveys allow to obtain data on vegetation and ecosystem structure, as well as will allow to uncover the trends in non-indigenous species introduction rates. According to van der Loos et al. (2023), diversifying the type of survey – from punctual to comprehensive surveys, including morphological-based and DNA-based assessments – is a need for early detection and to monitor trends over time in new species introductions.

Furthermore, the molecular identifications allow us to trace and update the nomenclatural changes over time, helping to “solve” the twisted cases of the Ulva species.

Accuracy and caution: To compare sequences from field-collected specimens with those in GenBank, accuracy and caution are required; in fact, the name applied to a GenBank accession does not always come from a comparison with the sequences from type material.

The importance of herbarium specimens: Extensive molecular investigations of Ulva have been performed around the world, revealing major taxonomic revisions also thanks to historical herbarium specimens and the type material. In this context, preserved specimens of institutional herbaria, and their associated metadata, are a fundamental tool for monitoring environmental variations and taxonomic changes. Furthermore, as reported by van der Loos et al. (2023), the herbaria play an important role in documenting spatio-temporal patterns of non-indigenous seaweeds.

Corresponding author: Simona Armeli Minicante, Consiglio Nazionale delle Ricerche, Istituto di Scienze Marine (CNR-ISMAR), Tesa 104 Arsenale, Castello 2737/F, 30122 Venezia, Italy, E-mail: simona.armeliminicante@cnr.it

Simona Armeli Minicante and James T. Melton III have contributed equally to this work and share first authorship.

About the authors

Simona Armeli Minicante

Simona Armeli Minicante is research technologist at the Institute of Marine Sciences of the National Research Council (CNR-ISMAR). Referent of the ISMAR Herbarium, her research concerns studies on the biodiversity of marine macroalgae, integrating research on the biotechnological applications of seaweeds, including alien and invasive species, in the field of circular economy and sustainability.

James T. Melton III

James T. Melton III is a senior lecturer in the Biology Department at Spelman College in Atlanta, Georgia, USA. His research interests include algal diversity, phylogenetics, and genomics with a focus on the green algal genus Ulva. He is also currently teaching a CURE (course-based undergraduate research) course on bacteriophage discovery and genomics.

Damiano Spagnuolo

Damiano Spagnuolo is currently a post-doc at the University of Messina, Italy, is engaged in pioneering research within the field of marine biotechnology. His expertise lies in the sustainable utilization of macroalgae, exploring taxonomy, genetic labelling, and the extraction of bioactive compounds. His contributions encompass not only in-depth taxonomic studies but also innovative extraction techniques for eco-friendly bioactive molecules. His work is poised to revolutionize marine bioproducts and contribute to a more sustainable future.

Marina Morabito

Dr Marina Morabito is full professor in Systematic Botany at the University of Messina, Italy, where she is the coordinator of the course in Marine and Terrestrial Environmental Sciences and serves in Quality Insurance and Student Orientation Committees. Her research interests regard the systematics and ecology of aquatic plants, with focuses on the Mediterranean Sea, and the valorisation of biomasses in biotechnological and economic frameworks. She serves as a forensic expert in technical-scientific consultancy for the Procura della Repubblica.

Juan Lopez-Bautista

Juan Lopez-Bautista, a professor in the Department of Biological Sciences at The University of Alabama, USA, is interested in the biodiversity, molecular systematics, and evolution of marine and terrestrial algae. Current efforts include environmental DNA metabarcoding technologies applied to algal communities and the architecture of the green and red algal plastomes.

Acknowledgments

We thank The National Recovery and Resilience Plan of Italian Ministry of University and Research funded by EU – Next Generation EU Mission 4 “Education and Research” – Component 2: “From research to business” – Investment 3.1: “Fund for the realisation of an integrated system of research and innovation infrastructures” – Project IR0000032 – ITINERIS – Italian Integrated Environmental Research Infrastructures System – CUP B53C22002150006.

Research ethics: This article does not contain any studies involving animals and meets the ethical guidelines.
Author contributions: All authors contributed to the revised version and read and approved the final version of the manuscript.
Competing interests: The authors state no conflict of interest.
Research funding: This research was funded by FFABR2019-UniMe (Italian Ministry of University and Research). Partial funds for this project were provided by The University of Alabama from RGC/ORED. Open-access publication was founded by “DTA.AD002.976 Sustainable and efficient management of natural resources, ecosystems and biodiversity” project of CNR-ISMAR.
Data availability: Photos of the herbarium specimens presented here are available from the corresponding author. All sequences generated here are available from GenBank and BOLDSystems with accession numbers reported in Table 1.

References

Abdel-Warith, A.-W.A., Younis, E.-S.M.I., and Al-Asgah, N.A. (2016). Potential use of green macroalgae Ulva lactuca as a feed supplement in diets on growth performance, feed utilization and body composition of the African catfish, Clarias gariepinus. Saudi J. Biol. Sci. 23: 404–409, https://doi.org/10.1016/j.sjbs.2015.11.010.Search in Google Scholar PubMed PubMed Central

Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. (1990). Basic local alignment search tool. J. Mol. Biol. 215: 403–410, https://doi.org/10.1006/jmbi.1990.9999.Search in Google Scholar

Areschoug, J.E. (1854). Phyceae novae et minus cognitae in maribus extraeuropaeis collectae. Nova Acta Regiae Societatis Scientiarum Upsaliensis 1: 329–372.10.5962/bhl.title.68745Search in Google Scholar

Armeli Minicante, S. (2013). Identificazione tramite DNA barcoding di macroalghe della Laguna di Venezia e loro potenziale impiego in ambito biotecnologico, Ph.D. thesis. University Ca’ Foscari of Venice.Search in Google Scholar

Armeli Minicante, S., Piredda, R., Quero, G.M., Finotto, S., Bernardi Aubry, F., Bastianini, M., Pugnetti, A., and Zingone, A. (2019). Habitat heterogeneity and connectivity: effects on the planktonic protist community structure at two adjacent coastal sites (the Lagoon and the Gulf of Venice, Northern Adriatic Sea, Italy) revealed by metabarcoding. Front. Microbiol. 10: 1–16, https://doi.org/10.3389/fmicb.2019.02736.Search in Google Scholar PubMed PubMed Central

Bartolo, A.G., Zammit, G., and Küpper, F.C. (2022). Ulva L. biodiversity in the central Mediterranean Sea: cryptic species and new records. Cryptogam. Algol. 43: 215–225, https://doi.org/10.5252/cryptogamie-algologie2022v43a14.Search in Google Scholar

Bast, F., John, A.A., and Bhushan, S. (2014). Strong endemism of bloom-forming tubular Ulva in Indian west coast, with description of Ulva paschima sp. nov. (Ulvales, Chlorophyta). PLoS One 9: e109295, https://doi.org/10.1371/journal.pone.0109295.Search in Google Scholar PubMed PubMed Central

Berger, R., Henriksson, E., Kautsky, L., and Malm, T. (2003). Effects of filamentous algae and deposited matter on the survival of Fucus vesiculosus L. germlings in the Baltic Sea. Aquat. Ecol. 37: 1–11.Search in Google Scholar

Bertuccio, C., Genovese, G., Manghisi, A., Cruaud, C., Couloux, A., Le Gall, L., and Morabito, M. (2014). Changes in the benthic algal flora of Lake Ganzirri, north-eastern Sicily (Italy). Nat. Rerum 3: 79–91.Search in Google Scholar

Bliding, C. (1968). A critical survey of European taxa Ulvales II. Ulva, Ulvaria, Monostroma, Kornmannia. Bot. Not. 121: 535–629.Search in Google Scholar

Blomster, J., Maggs, C.A., and Stanhope, M.J. (1998). Molecular and morphological analysis of Enteromorpha intestinalis and E. compressa (Chlorophyta) in the British Isles. J. Phycol. 34: 319–340, https://doi.org/10.1046/j.1529-8817.1998.340319.x.Search in Google Scholar

Blomster, J., Back, S., Fewer, D.P., Kiirikki, M., Lehvo, A., Maggs, C.A., and Stanhope, M.J. (2002). Novel morphology in Enteromorpha (Ulvophyceae) forming green tides. Am. J. Bot. 89: 1756–1763, https://doi.org/10.3732/ajb.89.11.1756.Search in Google Scholar PubMed

Brodie, J., Maggs, C., and John, D. (2007). Green seaweeds of Britain and Ireland, 1st ed. British Phycological Society, London.Search in Google Scholar

Carlton, J.T. (2009). Deep invasion ecology and the assembly of communities in historical time. In: Rilov, G. and Crooks, J.A. (Eds.). Biological invasions in marine ecosystems. Springer, Berlin, pp. 13–56.10.1007/978-3-540-79236-9_2Search in Google Scholar

Carneiro, V.A.R., Martins, N.T., Albuquerque da Silva, S.L., de Barros-Barreto, M.B., Pereira, S.B., and Cassano, V. (2023). Revealing the diversity of the genus Ulva (Ulvales, Chlorophyta) in southeastern Brazil, with a description of Ulva kanagawae sp. nov. Phycologia 1-14: 13–56.Search in Google Scholar

Chávez-Sánchez, T., Piñón-Gimate, A., Melton III, J.T., López-Bautista, J.M., and Casas-Valdez, M. (2019). First report, along with nomenclature adjustments, of Ulva ohnoi, U. tepida and U. torta (Ulvaceae, Ulvales, Chlorophyta) from northwestern Mexico. Bot. Mar. 62: 113–123, https://doi.org/10.1515/bot-2018-0007.Search in Google Scholar

Coat, G., Dion, P., Noailles, M.C., De Reviers, B., Fontaine, J.M., Berger-Perrot, Y., and Loiseaux-De Goër, S. (1998). Ulva armoricana (Ulvales, Chlorophyta) from the coasts of Brittany (France). II. Nuclear rDNA ITS sequence analysis. Eur. J. Phycol. 33: 81–86, https://doi.org/10.1017/s0967026297001455.Search in Google Scholar

Collins, F.S., Holden, I., and Setchell, W.A. (1899). Phycotheca Boreali-Americana: a collection of dried specimens of the algae of North America. Collins, Massachusetts.Search in Google Scholar

Cormaci, M., Furnari, G., Giaccone, G., and Serio, D. (2004). Alien macrophytes in the l Mediterranean Sea: a review. Recent Res. Dev. Environ. Biol. 1.Search in Google Scholar

Cormaci, M., Furnari, G., and Alongi, G. (2014). Flora marina bentonica del Mediterraneo: Chlorophyta. Boll. Accad. Gioenia Sci. Nat. Catania. 47: FP11–FP436.Search in Google Scholar

Cotas, J., Gomes, L., Pacheco, D., and Pereira, L. (2023). Ecosystem services provided by seaweeds. Hydrobiol 2: 75–96, https://doi.org/10.3390/hydrobiology2010006.Search in Google Scholar

Couceiro, L., Cremades, J., and Barreiro, R. (2011). Evidence for multiple introductions of the Pacific green alga Ulva australis Areschoug (Ulvales, Chlorophyta) to the Iberian Peninsula. Bot. Mar. 54: 391–402, https://doi.org/10.1515/bot.2011.044.Search in Google Scholar

Cui, J., Monotilla, A.P., Zhu, W., Takano, Y., Shimada, S., Ichihara, K., Matsui, T., He, P., and Hiraoka, M. (2018). Taxonomic reassessment of Ulva prolifera (Ulvophyceae, Chlorophyta) based on specimens from the type locality and Yellow Sea green tides. Phycologia 57: 692–704, https://doi.org/10.2216/17-139.1.Search in Google Scholar

Cuomo, V., Merrill, J., Palomba, I., and Perretti, A. (1993). Systematic collection of Ulva and mariculture of Porphyra: biotechnology against eutrophication in the Venice lagoon. Int. J. Environ. Stud. 43: 141–149, https://doi.org/10.1080/00207239308710821.Search in Google Scholar

Dartois, M., Pante, E., Viricel, A., Becquet, V., and Sauriau, P.G. (2021). Molecular genetic diversity of seaweeds morphologically related to Ulva rigida at three sites along the French Atlantic coast. PeerJ 9: e11966, https://doi.org/10.7717/peerj.11966.Search in Google Scholar PubMed PubMed Central

Duan, W., Guo, L., Sun, D., Zhu, S., Chen, X., Zhu, W., Xu, T., and Chen, C. (2012). Morphological and molecular characterization of free-floating and attached green macroalgae Ulva spp. in the Yellow Sea of China. J. Appl. Phycol. 24: 97–108, https://doi.org/10.1007/s10811-011-9654-7.Search in Google Scholar

Einav, R. and Israel, A. (2008). Checklist of seaweeds from the Israeli Mediterranean: Taxonomical and ecological approaches. Isr. J. Plant Sci. 56: 127–191, https://doi.org/10.1560/ijps.57.1-2.127.Search in Google Scholar

Flagella, M.M., Andreakis, N., Hiraoka, M., Verlaque, M., and Buia, M.C. (2010). Identification of cryptic Ulva species (Chlorophyta, Ulvales) transported by ballast water. J. Biol. Res. 13: 47.Search in Google Scholar

Fort, A., McHale, M., Cascella, K., Potin, P., Usadel, B., Guiry, M.D., and Sulpice, R. (2021). Foliose Ulva species show considerable inter-specific genetic diversity, low intra-specific genetic variation, and the rare occurrence of inter-specific hybrids in the wild. J. Phycol. 57: 219–233, https://doi.org/10.1111/jpy.13079.Search in Google Scholar PubMed PubMed Central

Furnari, G., Giaccone, G., Cormaci, M., Alongi, G., Catra, M., Nisi, A., and Serio, D. (2010). Macrophytobenthos. Biol. Mar. Mediterr. 17: 801–828.Search in Google Scholar

Guidone, M., Thornber, C., Wysor, B., and O’Kelly, C.J. (2013). Molecular and morphological diversity of Narrangansett Bay (RI, USA) Ulva (Ulvales, Chlorophyta) populations. J. Phycol. 49: 979–995, https://doi.org/10.1111/jpy.12108.Search in Google Scholar PubMed

Guiry, M.D. and Guiry, G.M. (2023). AlgaeBase. World-Wide Electronic Publication. National University of Ireland, Galway, Ireland, Available at: <http://www.algaebase.org> (Accessed 1 August 2023).Search in Google Scholar

Guo, J., Qi, M., Chen, H., Zhou, C., Ruan, R., Yan, X., and Cheng, P. (2022). Macroalgae-derived multifunctional bioactive substances: the potential applications for food and pharmaceuticals. Foods 11: 3455, https://doi.org/10.3390/foods11213455.Search in Google Scholar PubMed PubMed Central

Hanyuda, T., Heesch, S., Nelson, W., Sutherland, J., Arai, S., Boo, S.M., and Kawai, H. (2016). Genetic diversity and biogeography of native and introduced populations of Ulva pertusa (Ulvales, Chlorophyta). Phycol. Res. 64: 102–109, https://doi.org/10.1111/pre.12123.Search in Google Scholar

Hayden, H.S. and Waaland, J.R. (2002). Phylogenetic systematics of the Ulvaceae (Ulvales, Ulvophyceae) using chloroplast and nuclear DNA sequences. J. Phycol. 38: 1200–1212, https://doi.org/10.1046/j.1529-8817.2002.01167.x.Search in Google Scholar

Hayden, H.S. and Waaland, J.R. (2004). A molecular systematic study of Ulva (Ulvaceae, Ulvales) from the northeast Pacific. Phycologia 43: 364–382, https://doi.org/10.2216/i0031-8884-43-4-364.1.Search in Google Scholar

Hayden, H.S., Blomster, J., Maggs, C.A., Silva, P.C., Stanhope, M.J., and Waaland, R. (2003). Linnaeus was right all along: Ulva and Enteromorpha are not distinct genera. Eur. J. Phycol. 38: 277–294, https://doi.org/10.1080/1364253031000136321.Search in Google Scholar

Heesch, S., Broom, J.E., Neill, K.F., Farr, T.J., Dalen, J.L., and Nelson, W.A. (2009). Ulva, Umbraulva and Gemina: genetic survey of New Zealand taxa reveals diversity and introduced species. Eur. J. Phycol. 44: 143–154, https://doi.org/10.1080/09670260802422477.Search in Google Scholar

Hiraoka, M., Shimada, S., Uenosono, M., and Masuda, M. (2004). A new green-tide-forming alga, Ulva ohnoi Hiraoka et Shimada sp. nov. (Ulvales, Ulvophyceae) from Japan. Phycol. Res. 52: 17–29, https://doi.org/10.1111/j.1440-1835.2004.tb00311.x.Search in Google Scholar

Hofmann, L.C., Nettleton, J.C., Neefus, C.D., and Mathieson, A.C. (2010). Cryptic diversity of Ulva (Ulvales, Chlorophyta) in the Great Bay estuarine system (Atlantic USA): introduced and indigenous distromatic species. Eur. J. Phycol. 45: 230–239, https://doi.org/10.1080/09670261003746201.Search in Google Scholar

Horimoto, R., Masakiyo, Y., and Ichihara, K. (2011). Enteromorpha-like Ulva (Ulvophyceae, Chlorophyta) growing in the Todoroki River, Ishigaki Island, Japan, with special reference to Ulva meridionalis Horimoto et Shimada, sp. nov. Bull. Mus. Natl. Hist. Nat., Sect. B: Adansonia (Bot., Phytochim.) 37: 155–167.Search in Google Scholar

Horta, P., Batista, M.B., Cunha, R.L., and Castilho, R. (2018). Sea lettuce systematics: lumping or splitting? bioRxiv, 413450.10.1101/413450Search in Google Scholar

Hughey, J.R., Maggs, C.A., Mineur, F., Jarvis, C., Miller, K.A., Shabaka, S.H., and Gabrielson, P.W. (2019). Genetic analysis of the Linnaean Ulva lactuca (Ulvales, Chlorophyta) holotype and related type specimens reveals name misapplications, unexpected origins, and new synonymies. J. Phycol. 55: 503–508, https://doi.org/10.1111/jpy.12860.Search in Google Scholar PubMed

Hughey, J.R., Gabrielson, P.W., Maggs, C.A., Mineur, F., and Miller, K.A. (2021). Taxonomic revisions based on genetic analysis of type specimens of Ulva conglobata, U. laetevirens, U. pertusa and U. spathulata (Ulvales, Chlorophyta). Phycol. Res. 69: 148–153, https://doi.org/10.1111/pre.12450.Search in Google Scholar

Hughey, J.R., Gabrielson, P.W., Maggs, C.A., and Mineur, F. (2022). Genomic analysis of the lectotype specimens of European Ulva rigida and Ulva lacinulata (Ulvaceae, Chlorophyta) reveals the ongoing misapplication of names. Eur. J. Phycol. 57: 143–153, https://doi.org/10.1080/09670262.2021.1914862.Search in Google Scholar

Israel, Á. and Shpigel, M. (2023). Photosynthetic CO2 uptake by Ulva (Chlorophyta) as a potential contribution to global warming containment. J. Appl. Phycol. 35: 1987–1994, https://doi.org/10.1007/s10811-023-02929-w.Search in Google Scholar

Kang, E.J., Kim, J.-H., Kim, K., Choi, H.-G., and Kim, K.Y. (2014). Re-evaluation of green tide-forming species in the Yellow Sea. Algae 29: 267–277, https://doi.org/10.4490/algae.2014.29.4.267.Search in Google Scholar

Kang, J.H., Jang, J.E., Kim, J.H., Byeon, S.Y., Kim, S., Choi, S.K., Kang, Y.H., Park, S.R., and Lee, H.J. (2019). Species composition, diversity, and distribution of the genus Ulva along the coast of Jeju Island, Korea based on molecular phylogenetic analysis. PLoS One 14: e0219958, https://doi.org/10.1371/journal.pone.0219958.Search in Google Scholar PubMed PubMed Central

Katoh, K. and Standley, D.M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30: 772–780, https://doi.org/10.1093/molbev/mst010.Search in Google Scholar PubMed PubMed Central

Katoh, K., Misawa, K., Kuma, K., and Miyata, T. (2002). MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30: 3059–3066, https://doi.org/10.1093/nar/gkf436.Search in Google Scholar PubMed PubMed Central

Kawai, H., Shimada, S., Hanyuda, T., Suzuki, T., and Gamagori City Office, G.C.O. (2007). Species diversity and seasonal changes of dominant Ulva species (Ulvales, Ulvophyceae) in Mikawa Bay, Japan, deduced from ITS2 rDNA region sequences. Algae 22: 221–228, https://doi.org/10.4490/algae.2007.22.3.221.Search in Google Scholar

Kazi, M.A., Kavale, M.G., and Singh, V.V. (2016). Morphological and molecular characterization of Ulva chaugulii sp. Nov., U. lactuca and U. ohnoi (Ulvophyceae, Chlorophyta) from India. Phycologia 55: 45–54, https://doi.org/10.2216/15-11.1.Search in Google Scholar

Kirkendale, L., Saunders, G.W., and Winberg, P. (2013). A molecular survey of Ulva (Chlorophyta) in temperate Australia reveals enhanced levels of cosmopolitanism. J. Phycol. 49: 69–81, https://doi.org/10.1111/jpy.12016.Search in Google Scholar PubMed

Koeman, R.P.T. and Hoek, C. (1982). Taxonomy of Enteromorpha Link, 1820,(Chlorophyceae) in the Netherlands. II. The section Proliferae. Cryptogamie: algologie 3: 37–70.10.5962/p.309049Search in Google Scholar

Kraft, G.T. (2007). Algae of Australia: Marine Benthic Algae of Lord Howe Island and the Southern Great Barrier Reef, 1: Green Algae. ABRS/CSIRO Publishing, Canberra Melbourne, pp. 1–347.Search in Google Scholar

Kraft, L.G., Kraft, G.T., and Waller, R.F. (2010). Investigations into Southern Australian Ulva (Ulvophyceae, Chlorophyta) taxonomy and molecular phylogeny Indicate both cosmopolitanism and endemic cryptic Species. J. Phycol. 46: 1257–1277, https://doi.org/10.1111/j.1529-8817.2010.00909.x.Search in Google Scholar

Krupnik, N., Paz, G.U.Y., Douek, J., Lewinsohn, E., Israel, A., Carmel, N., Mineur, F., and Maggs, C.A. (2018). Native, invasive and cryptogenic Ulva species from the Israeli Mediterranean Sea: risk and potential. Mediterr. Mar. Sci. 19: 132–146, https://doi.org/10.12681/mms.2104.Search in Google Scholar

Kuba, G.M., Carpio-Aguilar, B., Eklund, J., and Freshwater, D.W. (2022). A demonstration of DNA Barcoding-based identification of blade-form Ulva (Ulvophyceae, Chlorophyta) species from three site in the San Juan islands, Washington, USA. Diversity 14: 899, https://doi.org/10.3390/d14110899.Search in Google Scholar

Kumar, S., Stecher, G., and Tamura, K. (2016). MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33: 1870–1874, https://doi.org/10.1093/molbev/msw054.Search in Google Scholar PubMed PubMed Central

Lawton, R.J., Mata, L., de Nys, R., and Paul, N.A. (2013). Algal bioremediation of waste waters from land-based aquaculture using Ulva: selecting target species and strains. PLoS One 8: e77344, https://doi.org/10.1371/journal.pone.0077344.Search in Google Scholar PubMed PubMed Central

Leliaert, F., Zhang, X., Ye, N., Malta, E.J., Engelen, A.H., Mineur, F., Verbruggen, H., and De Clerck, O. (2009). Research note: identity of the Qingdao algal bloom. Phycol. Res. 57: 147–151, https://doi.org/10.1111/j.1440-1835.2009.00532.x.Search in Google Scholar

Linnaeus, C. (1753). Species plantarum, exhibentes plantas rite cognitas ad genera relatas cum differentiis specificis, nominibus trivialibus, synonymis selectis, locis natalibus, secundum systema sexuale digestas, 2. Impensis Laurentii Salvii, Stockholm, p. 1163.10.5962/bhl.title.59734Search in Google Scholar

Liu, F. and Melton, J.T.III (2021). Chloroplast genomes of the green-tide forming alga Ulva compressa: comparative chloroplast genomics in the genus Ulva (Ulvophyceae, Chlorophyta). Front. Mar. Sci. 8: 668542, https://doi.org/10.3389/fmars.2021.668542.Search in Google Scholar

Loughnane, C.J., McIvor, L.M., Rindi, F., Stengel, D.B., and Guiry, M.D. (2008). Morphology, rbcL phylogeny and distribution of distromatic Ulva (Ulvophyceae, Chlorophyta) in Ireland and southern Britain. Phycologia 47: 416–429, https://doi.org/10.2216/ph07-61.1.Search in Google Scholar

Malta, E.J., Draisma, S., and Kamermans, P. (1999). Free-floating Ulva in the southwest Netherlands: species or morphotypes? A morphological, molecular and ecological comparison. Eur. J. Phycol. 34: 443–454, https://doi.org/10.1017/s0967026299002474.Search in Google Scholar

Manghisi, A., Morabito, M., Bertuccio, C., Le Gall, L., Couloux, A., Cruaud, C., and Genovese, G. (2010). Is routine DNA barcoding an efficient tool to reveal introductions of alien macroalgae? A case study of Agardhiella subulata (Solieriaceae, Rhodophyta) in Cape Peloro lagoon (Sicily, Italy). Cryptogam. Algol. 31: 423.Search in Google Scholar

Manghisi, A., Bertuccio, C., Minicante, S.A., Fiore, V., Le, L., Genovese, G., and Morabito, M. (2011). Identifying alien macroalgae through DNA barcoding: the case of Hypnea cornuta (Cystocloniaceae, Rhodophyta). Trans. Wat. Bull. 5: 42–49.Search in Google Scholar

Mares, J., Leskinen, E., Sitkowska, M., Skácelová, O., and Blomster, J. (2011). True identity of the European freshwater Ulva (Chlorophyta, Ulvophyceae) revealed by a combined molecular and morphological approach. J. Phycol. 47: 1177–1192, https://doi.org/10.1111/j.1529-8817.2011.01048.x.Search in Google Scholar PubMed

Masakiyo, Y. and Shimada, S. (2014). Species diversity of the genus Ulva (Ulvophyceae, Chlorophyta) in Japanese waters, with special reference to Ulva tepida Masakiyo et S. Shimada sp. nov. Bull. Mus. Natl. Hist. Nat., Sect. B: Adansonia (Bot., Phytochim.) 40: 1–13.Search in Google Scholar

Melton III, J., Collado-Vides, L., and Lopez-Bautista, J. (2016). Molecular identification and nutrient analysis of the green tide species Ulva ohnoi M. Hiraoka et S. Shimada, 2004 (Ulvophyceae, Chlorophyta), a new report and likely nonnative species in the Gulf of Mexico and Atlantic Florida, USA. Aquat. Invasions 11: 225–237, https://doi.org/10.3391/ai.2016.11.3.01.Search in Google Scholar

Melton III, J.T. and Lopez-Bautista, J.M. (2021). Diversity of the green macroalgal genus Ulva (Ulvophyceae, Chlorophyta) from the east and gulf coast of the United States based on molecular data. J. Phycol. 57: 551–568, https://doi.org/10.1111/jpy.13120.Search in Google Scholar PubMed

Miladi, R., Manghisi, A., Armeli Minicante, S., Genovese, G., Abdelkafi, S., and Morabito, M. (2018). A DNA barcoding survey of Ulva (Chlorophyta) in Tunisia and Italy reveals the presence of the overlooked slien U. ohnoi. Cryptogam. Algol. 39: 85–107, https://doi.org/10.7872/crya/v39.iss1.2018.85.Search in Google Scholar

Mineur, F., Johnson, M.P., Maggs, C.A., and Stegenga, H. (2007). Hull fouling on commercial ships as a vector of macroalgal introduction. Mar. Biol. 151: 1299–1307, https://doi.org/10.1007/s00227-006-0567-y.Search in Google Scholar

Mirtl, M., Borer, E.T., Djukic, I., Forsius, M., Haubold, H., Hugo, W., Jourdan, J., Lindenmayer, D., McDowell, W.H., Muraoka, H., et al.. (2018). Genesis, goals and achievements of Long-Term Ecological Research at the global scale: a critical review of ILTER and future directions. Sci. Total Environ. 626: 1439–1462, https://doi.org/10.1016/j.scitotenv.2017.12.001.Search in Google Scholar PubMed

Müller, O.F. (1778). Florae Danicae, fasc. 13, Vol. 5. Havniae, Copenhagen, Denmark, pp. 8.Search in Google Scholar

O’Kelly, C.J., Kurihara, A., Shipley, T.C., and Sherwood, A.R. (2010). Molecular assessment of Ulva spp. (Ulvophyceae, Chlorophyta) in the Hawaiian islands. J. Phycol. 46: 728–735, https://doi.org/10.1111/j.1529-8817.2010.00860.x.Search in Google Scholar

Papenfuss, G.F. (1960). On the genera of the Ulvales and the status of the order. J. Linn. Soc. Lond. Bot. 56: 303–318, https://doi.org/10.1111/j.1095-8339.1960.tb02507.x.Search in Google Scholar

Peñalver, R., Lorenzo, J.M., Ros, G., Amarowicz, R., Pateiro, M., and Nieto, G. (2020). Seaweeds as a functional ingredient for a healthy diet. Mar. Drugs 18: 301, https://doi.org/10.3390/md18060301.Search in Google Scholar PubMed PubMed Central

Petrocelli, A., Cecere, E., and Rubino, F. (2019). Successions of phytobenthos species in a Mediterranean transitional water system: the importance of long term observations. Nat. Conserv. 34: 217–246, https://doi.org/10.3897/natureconservation.34.30055.Search in Google Scholar

Phillips, J.A. (1988). Field, anatomical and development studies on southern Australian species of Ulva (Ulvaceae, Chlorophyta). Aust. Syst. Bot. 1: 411–456, https://doi.org/10.1071/sb9880411.Search in Google Scholar

Pignatti, S. (1962). Associazioni di alghe marine sulla costa veneziana, Vol. 32. Presso la Sede dell’Istituto veneto.Search in Google Scholar

Pirian, K., Piri, K., Sohrabipour, J., Tamadoni Jahromi, S., and Blomster, J. (2016). Molecular and morphological characterisation of Ulva chaugulii, U. paschima and U. ohnoi (Ulvophyceae) from the Persian Gulf, Iran. Bot. Mar. 59: 147–158, https://doi.org/10.1515/bot-2016-0009.Search in Google Scholar

Rambaut, A. (2012). FigTree v1. 4, Available at: <http://tree.bio.ed.ac.uk/software/figtree/>.Search in Google Scholar

Rybak, A., Czerwoniec, A., Gąbka, M., and Messyasz, B. (2014). Ulva flexuosa (Ulvaceae, Chlorophyta) inhabiting inland aquatic ecosystems: molecular, morphological and ecological discrimination of subspecies. Eur. J. Phycol. 49: 471–485, https://doi.org/10.1080/09670262.2014.976662.Search in Google Scholar

Santarelli, E. (1931). Contribuzione alla flora algologica del mare Adriatico. Plant Biosyst. 38: 315–321, https://doi.org/10.1080/11263503109431468.Search in Google Scholar

Saunders, G.W. and Kucera, H. (2010). An evaluation of rbcL, tufA, UPA, LSU and ITS as DNA barcode markers for the marine green macroalgae. Cryptogam. Algol. 31: 487–528.Search in Google Scholar

Scagel, R.F. (1989). A synopsis of the benthic marine algae of British Columbia, southeast Alaska, Washington and Oregon. Department of Botany, University of British Columbia, Vancouver.Search in Google Scholar

Schiffner, V. and Vatova, A. (1938). Le alghe della Laguna: Chlorophyceae, Phaeophyceae, Rhodophyceae, Myxophyceae. In: La Laguna di Venezia, 3. Carlo Ferrari, Venezia, pp. 159–250.Search in Google Scholar

Serio, D., Cormaci, M., Furnari, G., Cecere, E., Petrocelli, A., Izzo, G., and Sfriso, A. (2009). The lakes Faro and Ganzirri. In: Flora and vegetation of the Italian transitional water systems. CORILA. Stampa “Multigraf” Spinea, Venezia, pp. 229–238.Search in Google Scholar

Sfriso, A. (1987). Flora and vertical distribution of macroalgae in the lagoon of Venice: a comparison with previous studies. Giorn. Bot. Ital. 121: 69–85, https://doi.org/10.1080/11263508709431647.Search in Google Scholar

Sfriso, A. (2010a). Coexistence of Ulva rigida and Ulva laetevirens (Ulvales, Chlorophyta) in Venice lagoon and other Italian transitional and marine environments. Bot. Mar. 53: 9–18, https://doi.org/10.1515/bot.2010.009.Search in Google Scholar

Sfriso, A. (2010b). Chlorophyta multicellulari e fanerogame acquatiche. Ambienti di transizione italiani e litorali adiacenti. I Quaderni di ARPA. ARPA Emilia-Romagna, Bologna, Odoya srl, pp. 320.Search in Google Scholar

Sfriso, A. and Curiel, D. (2007). Check-list of seaweeds recorded in the last 20 years in Venice lagoon, and a comparison with the previous records. Bot. Mar. 50: 22–58, https://doi.org/10.1515/bot.2007.004.Search in Google Scholar

Sfriso, A., Facca, C., and Ghetti, P.F. (2009). Validation of the Macrophyte Quality Index (MaQI) set up to assess the ecological status of Italian marine transitional environments. Hydrobiologia 617: 117–141, https://doi.org/10.1007/s10750-008-9540-8.Search in Google Scholar

Sfriso, A., Wolf, M.A., Buosi, A., Sciuto, K., and Sfriso, A.A. (2023). Alien macroalgal rearrangement in the soft substrata of the Venice Lagoon (Italy): impacts, threats, time and future trends. Sustainability 15: 8256, https://doi.org/10.3390/su15108256.Search in Google Scholar

Shimada, S., Hiraoka, M., Nabata, S., Lima, M., and Masuda, M. (2003). Molecular phylogenetic analyses of the Japanese Ulva and Enteromorpha (Ulvales, Ulvophyceae), with special reference to the free-floating Ulva. Phycol. Res. 51: 99–108, https://doi.org/10.1046/j.1440-1835.2003.00296.x.Search in Google Scholar

Silva, P.C., Basson, P.W., and Moe, R.L. (1996). Catalogue of the benthic marine algae of the Indian Ocean, 79. University of California Publications in Botany, Berkeley, pp. 1–1259.Search in Google Scholar

Spagnuolo, D., Russo, V., Manghisi, A., Di Martino, A., Morabito, M., Genovese, G., and Trifilò, P. (2022). Screening on the presence of plant growth regulators in high biomass forming seaweeds from the Ionian Sea (Mediterranean Sea). Sustainability 14: 3914, https://doi.org/10.3390/su14073914.Search in Google Scholar

Spalding, H.L., Conklin, K.Y., Smith, C.M., O’Kelly, C.J., and Sherwood, A.R. (2016). New Ulvaceae (Ulvophyceae, Chlorophyta) from mesophotic ecosystems across the Hawaiian archipelago. J. Phycol. 52: 40–53, https://doi.org/10.1111/jpy.12375.Search in Google Scholar PubMed

Stamatakis, A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312–1313, https://doi.org/10.1093/bioinformatics/btu033.Search in Google Scholar PubMed PubMed Central

Steinhagen, S., Karez, R., and Weinberger, F. (2019). Cryptic, alien and lost species: molecular diversity of Ulva sensu lato along the German coasts of the North and Baltic Seas. Eur. J. Phycol. 54: 466–483, https://doi.org/10.1080/09670262.2019.1597925.Search in Google Scholar

Tagliapietra, D., Sigovini, M., and Volpi Ghirardini, A. (2009). A review of terms and definitions to categorise estuaries, lagoons and associated environments. Mar. Freshw. Res. 60: 497–509, https://doi.org/10.1071/mf08088.Search in Google Scholar

Thiers, B. (2024). Index herbariorum: a global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium, Available at: <https://sweetgum.nybg.org/science/ih/>.Search in Google Scholar

Tan, I.H., Blomster, J., Hansen, G., Leskinen, E., Maggs, C.A., Mann, D.G., Sluiman, H.J., and Stanhope, M.J. (1999). Molecular phylogenetic evidence for a reversible morphogenetic switch controlling the gross morphology of two common genera of green seaweeds, Ulva and Enteromorpha. Mol. Biol. Evol. 16: 1011–1018, https://doi.org/10.1093/oxfordjournals.molbev.a026190.Search in Google Scholar PubMed

van der Loos, L.M., Bafort, Q., Bosch, S., Ballesteros, E., Bárbara, I., Bercibar, E., Blanfuné, A., Bogaert, K., Bouckenooghe, S., Boudouresque, C.-F., et al.. (2023). Non-indigenous seaweeds in the Northeast Atlantic Ocean, the Mediterranean Sea and Macaronesia: a critical synthesis of diversity, spatial and temporal patterns. Eur. J. Phycol. 59: 127–156, https://doi.org/10.1080/09670262.2023.2256828.Search in Google Scholar

Wang, J., Jiang, P., Cui, Y., Li, N., Wang, M., Lin, H., He, P., and Qin, S. (2010). Molecular analysis of green-tide-forming macroalgae in the Yellow Sea. Aquat. Bot. 93: 25–31, https://doi.org/10.1016/j.aquabot.2010.03.001.Search in Google Scholar

Wei, X., Liu, W., Lin, X., Liu, Q., and Jiang, P. (2022). First record of Ulva californica in the mainland of China: a single alien parthenogenetic population in discontinuous distribution. J. Ocean. Limnol. 40: 2343–2353, https://doi.org/10.1007/s00343-022-1392-y.Search in Google Scholar

Wolf, M.A., Sciuto, K., Andreoli, C., and Moro, I. (2012). Ulva (Chlorophyta, Ulvales) biodiversity in the North Adriatic Sea (Mediterranean, Italy): cryptic species and new introductions. J. Phycol. 48: 1510–1521, https://doi.org/10.1111/jpy.12005.Search in Google Scholar PubMed

Womersley, H.B.S. (1984). Handbooks to the flora of South Australia. Adelaide, Woolman, D.J.Search in Google Scholar

Woo, A.J. and Ki, N.W. (2017). First record of Ulva torta (Ulvales, Chlorophyta) in Korea. Korean J. Environ. Biol. 35: 329–334, https://doi.org/10.11626/kjeb.2017.35.3.329.Search in Google Scholar

Woolcott, G.W. and King, R.J. (1999). Ulva and Enteromorpha (Ulvales, Ulvophyceae, Chlorophyta) in eastern Australia: comparison of morphological features and analyses of nuclear rDNA sequence data. Aust. Syst. Bot. 12: 709–725, https://doi.org/10.1071/sb97034.Search in Google Scholar

Xie, W.F., Wu, C.H., Zhao, J., Lin, X.Y., and Jiang, P. (2020). New records of Ulva spp. (Ulvophyceae, Chlorophyta) in China, with special reference to an unusual morphology of U. meridionalis forming green tides. Eur. J. Phycol. 55: 412–425, https://doi.org/10.1080/09670262.2020.1740946.Search in Google Scholar

Xu, J., Liao, W., Liu, Y., Guo, Y., Jiang, S., and Zhao, C. (2023). An overview on the nutritional and bioactive components of green seaweeds. Food Prod. Process. Nutr. 5: 18, https://doi.org/10.1186/s43014-023-00132-5.Search in Google Scholar

Yang, Q., Jiang, Y., Fu, S., Shen, Z., Zong, W., Xia, Z., Zhan, Z., and Jiang, X. (2021). Protective effects of Ulva lactuca polysaccharide extract on oxidative stress and kidney injury induced by D-Galactose in mice. Mar. Drugs 19: 539, https://doi.org/10.3390/md19100539.Search in Google Scholar PubMed PubMed Central

Supplementary Material

This article contains supplementary material (https://doi.org/10.1515/bot-2023-0071).

Received: 2023-08-30

Accepted: 2024-05-08

Published Online: 2024-06-24

Published in Print: 2025-02-25

This work is licensed under the Creative Commons Attribution 4.0 International License.

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https://doi.org/10.1515/bot-2023-0071

Keywords for this article

Ulva; Mediterranean Sea; Ulva chaugulei; tufA; LTER-Italy

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