Montenegro – Ulcinjska Saline

In the 19^th century, the area NE of Ulcinj was an impassable marshland (about 25 km²) with brackish water, known as Zoganjsko blato. To combat malaria, drainage works were carried out, connecting it to the sea via the Port Milena canal and enclosing it from the Bojana River with embankments. The Saline was established in 1920 and was constructed from 1927 to 1934 (with the first salt harvest in 1935). This area was significant not only for salt production but also for its rich biodiversity. The protection of the “Ulcinj Saline” began in 1984 with a hunting ban, and in 1989 it gained international importance as a bird area (Important Bird Area – IBA). Its privatization in 2005 led to the cessation of production, with the last salt harvest occurring in 2013. In 2019, this area received national recognition (designated as the Nature Park “Ulcinjska Salina”) and international protection status (inscription on the Ramsar List) (EPA 2015; Iković 2020). Until 2023, Ulcinjska Saline has not been the subject of comprehensive and systematic research on bryophytes (Fig. 2A). For the protected territory, only one published record is available, referring to the presence of the moss Entosthodon hungaricus (Boros) Loeske. The species was documented along a path that separates water basins from the area protected for birds (41.92034°N 19.27329°E) (Ellis et al. 2016).

Italy – Western Sicily – Birgi Novo

The study area is located between the San Teodoro salt pans and Birgi Novo, on the western coast of Sicily, in a region rich in brackish humid environments and salt pans. In recent centuries, these environments have been reduced in surface area due to landfilling and/or drainage aimed at reducing malaria transmission, expanding cultivable land and by urbanization. This is a fate like that of many other Sicilian aquatic systems (La Mantia et al. 2022). The area presently is protected by multiple environmental protection measures. It is located within the boundaries of the Nature Reserve “Isole dello Stagnone di Marsala”, of the Special Area of Conservation “Saline di Marsala” (ITA010021), of the Special Protection Area “Stagnone di Marsala and Saline di Trapani” (ITA010028) and borders the boundary of the Important Bird Area “Stagnone di Marsala and Saline di Trapani” (IBA158). Despite contributions to vascular floristic knowledge being abundant for this part of Sicily, contributions regarding bryophyte flora are scarce. There is no previous publication of research conducted in the area where we found the Riella population.

Greece – Attica – Alykes Anavyssos and Peloponnese – Paralia Astros

Attica: Alykes Anavyssos, located in the residential area of Anavyssos in the Saronikos municipality of East Attica, is a former saline. Cultivated since 1924 by Greek refugees from Asia Minor, in 1969, following a royal decree, it was abandoned and designated for development as a public tourist complex. Over the years, various proposals have been made to exploit the area, including the construction of hotel facilities, sports centers, and more. These projects have consistently failed, partly due to disputes among the numerous private owners, as the land has remained highly fragmented. In 2014, under the new national master plan, Alykes Anavyssos was designated as a recognized wetland, granting it a certain level of environmental protection (Ergo Saronikos 2014).

Peloponnese: Eastern Arcadia, Paralia Astros, in a flooded parking place next to a small beach in the area of a former coastal wetland, not subject to any form of protection.

Figure 1. 

Distribution of Riella helicophylla and R. macrocarpa (Ellis et al. 2018; Segarra-Moragues et al. 2022; Colacino 2023; Osman et al. 2024; our data). Turkey is not included since the relevant report is “without precise collection data or locality” (Ros et al. 2007). The unmasked portion of land corresponds to the Mediterranean Biome according to Dinerstein et al. (2017). “Old observations” means that the last report is older than 50 years. Satellite images 2023 © Google.

Through independent field research carried out in Montenegro, Sicily, and Greece, new populations of Riella macrocarpa were discovered in the following locations:

Montenegro, Ulcinj municipality, Nature Park “Ulcinjska Salina”, 4 m a.s.l., temporary pools with stagnant and brackish water, and damp meadows with small inundated depressions with Characeae, 12^th, 17^th, 28^th, and 30^th April, 6^th, and 23^rd May, and 1^st June 2023, 13^th, 19^th May 2024, leg. R. Romanov, S. Dragićević, and V. Biberdžić, det. R. Romanov, S. Dragićević conf. B. Papp. Recorded locations (1–13) are situated inside protected zones within the area of the Nature Park “Ulcinjska Salina” (Fig. 2A, see Table 1 for coordinates and relevés). This finding represents a new species and new genus for the bryophyte flora of Montenegro.

Italy, Sicily, near Birgi Novo, 2 m a.s.l., temporary brackish wetland, 6^th and 19^th April 2023, leg./det. A. Troia, D. Salemi. Recorded location 14–16 (Fig. 2B, see Table 1 for coordinates and relevés). New species for the bryophyte flora of Sicily (Aleffi et al. 2020).

Greece. 1) Attica, Anavissos, Alykes Anavissos, former coastal saline, coordinates: 37.72939°N, 23.93848°E, two vernal pools, 30^th April 2011, 7^th May 2011, leg. Uwe Raabe, rev. A. Troia, D. Salemi, C. Schmidt (Fig. 4C); 2) Peloponnese, Paralia Astros, 37.42333°N, 22.76583°E, 18^th March 2014, flooded parking place next to a small beach, leg. Uwe Raabe, det. A. Troia, D. Salemi (Fig. 4A). New species for the bryophyte flora of Greece (Hodgetts and Lockhart 2020) (the record from Alykes Anavissou was reported as “R. helicophylla” s.l. by Zogaris (2013), but never published in scientific reports).

Riella macrocarpa is a liverwort ranging from 5–45 mm in height, standing erect with either a single stem or occasionally branching from the base and seldom branching further above. R. macrocarpa is described as having thallus wing with undulations, female involucres with an apical pore, truncated distal spines of spores with flat, dilated apices, and proximal spines with lacerate apices (Segarra-Moragues et al. 2022). On the material collected in Ulcinj Salina in Montenegro, but also in Birgi Novo, Sicily, and in Attica, and the Peloponnese in Greece, these characters are easily recognizable (Fig. 3).

Figure 2. 

A. Montenegro: Nature Park “Ulcinjska Salina” and marked locations with Riella macrocarpa (locations 1–13); B. Sicily: temporary brackish lagoon near Birgi Novo and marked locations with R. macrocarpa (locations 14–16). In green the areas where R. macrocarpa has been detected. Locations 1–16 as in Table 1. The boundaries of the Natura 2000 site are shown in red. Satellite images 2023(B), 2024(A) © Google.

Figure 3. 

Habitus of Riella macrocarpa and species traits: A. Male and female individuals in the same patches in the field; Birgi Novo, Sicily, Italy; B. habitus of female plants; Ulcinj Salina, Montenegro; C. Female plants with sporophytes; Birgi Novo, Sicily, Italy; D. Male plants with ripe and unripe antheridia; Birgi Novo, Sicily, Italy; E. A spore escaping from the female involucre. Note the opened apex of the involucre; Birgi Novo, Sicily, Italy. (Photographs: A – A. Troia; C–E – D. Salemi; B – R. Romanov).

Montenegro. In temporary ponds of the Ulcinj Salina R. macrocarpa was associated with charophytes: Chara canescens Desv. & Loisel. in Loisel. (parthenogenetic populations), C. galioides DC., Lamprothamnium papulosum (Wallr.) J.Groves, Tolypella glomerata (Desv. in Loisel.) Leonh., T. hispanica Nordst. ex Allen, and T. nidifica (O.F.Müll.) A.Braun, as well as with angiosperms Ruppia maritima L., Zannichellia palustris L. (a morphotype known as Z. repens Boenn.), Ranunculus baudotii Godr., and R. cf. trichophyllus Chaix., macroscopic mats of filamentous green algae Rhizoclonium riparium (Roth) Harvey species complex, and Rhizoclonium sp., and cyanobacterium Lyngbya aestuarii Liebman ex Gomont (Table 1). Female plants of R. macrocarpa were much more abundant than male ones. Dry beds of temporary ponds appearing after water evaporation were sparsely occupied by Salsola soda L. plants whose seedlings, submersed or emerged from the water, were found to be common during a survey of some inundated ponds. The higher water level in the pond with relevé No. 7 during 2024, in combination with the destructive impact of bottom sediments by the presence of numerous feeding Greater flamingoes, had a deleterious effect on aquatic macrophytes (Rodríguez-Pérez et al. 2007). It also resulted in less water transparency and obscured the appearance of R. macrocarpa in this water body.

Sicily. In the external and shallower portion of a temporary brackish ponds system near Birgi Novo (Fig. 2B), R. macrocarpa grows in almost monospecific communities with some individuals of Chara galioides, Tolypella hispanica, and Ruppia drepanensis Tineo ex Guss. (Table 1), sharing the space in a mosaic pattern like with Salicornietea fruticosae communities (Fig. 4). As already reported by Segarra-Moragues et al. (2022) for other R. helicophylla s.l. populations, and as reported above for Montenegro, female individuals were much more abundant than male ones. At the end of April 2023, the parameters recorded in water were as follows: electrical conductivity 22.7 mS (~13.7 PSU), pH 9.34, and temperature of 22 °C.

Greece. In Attica R. macrocarpa occurred together with Ruppia maritima agg., Ranunculus aquatilis agg., Chara vulgaris s. l., and Chara canescens. In Paralia Astros, Peloponnese, the species occurred in monospecific stands. In all cases the water was clear.

Figure 4. 

Habitats of Riella macrocarpa: A. Flooded parking place next to a small beach, Paralia Astros, Peloponnese, Greece, Astros 18^th March 2014; B. Temporary brackish wetland, Ulcinj Salina, Montenegro, 19^th May 2024, relevé 12; C. A vernal pool at former coastal saline, Alykes Anavissou, Anavissos, Attica, Greece, 07^th May 2011; D. Temporary brackish lagoon near Birgi Novo, Sicily, Italy, 6^th April 2023. (photographs: A, C – U. Raabe, B – R. Romanov, D – D. Salemi).

At the time of publication of Rielletum helicophyllae, the variety R. helicophylla var. macrocarpa Allorge and the form R. helicophylla var. macrocarpa f. latealata Allorge, both described from Spain (Allorge 1929; Allorge and Allorge 1946) were recognized under R. helicophylla (cf. Cirujano et al. 1988). Recently, as mentioned above, these infraspecific taxa were separated and raised to the species level as R. macrocarpa (Segarra-Moragues et al. 2022). This made the name of R. helicophylla in the description of Rielletum helicophyllae a name of an aggregate taxon from a contemporary perspective. Moreover, of the 14 relevés used in the description of the Rielletum helicophyllae, only 7 of these can be georeferenced through the work of Segarra-Moragues et al. (2022). All 7 of these localities belong to sites of R. macrocarpa, including the one of the holotype. In contrast, the revision of extensive herbarium material as well as recent sampling found that R. helicophylla is an exceptionally rare species reliably known from only 4 Spanish sites, while more than 50 Spanish sites are known for R. macrocarpa (Segarra-Moragues et al. 2022). Therefore, the probability that Rielletum helicophyllae was described based on communities of R. macrocarpa is very high. The question of whether both these non-synonymous species were growing in the same community or if a community of R. helicophylla was included in the typus of Rielletum helicophyllae remains open. It may not be resolvable considering the unstable appearance of Riella at different years. We suggest a phytosociological nomenclatural decision for the association of Rielletum helicophyllae described as an aggregate taxon, i.e., a change of the name of the syntaxon of Rielletum helicophyllae with the name of Rielletum macrocarpae according to Art. 45 of ICPN (Theurillat et al. 2020). The name Riella macrocarpa was used in eight recent publications, including one taxonomic paper, two checklists, one index, and one national species novelty record (see below), allowing this change according to ICPN.

Class Rielletea helicophyllae Cirujano, Velayos et García-Mur. in Rivas-Martínez et al. 1999: 367

Holotypus (Rivas-Martínez et al. 1999: 367): Rielletalia helicophyllae Cirujano, Velayos et García-Mur. in Rivas-Martínez et al. 1999: 367

Order Rielletalia helicophyllae Cirujano, Velayos et García-Mur. in Rivas-Martínez et al. 1999: 367

Holotypus (Rivas-Martínez et al. 1999: 367): Riellion helicophyllae Cirujano, Velayos et García-Mur. in Rivas-Martínez et al. 1999: 366

Alliance Riellion helicophyllae Cirujano, Velayos et García-Mur. in Rivas-Martínez et al. 1999: 366

Holotypus (Rivas-Martínez et al. 1999: 367): Rielletum helicophyllae Cirujano, Velayos et García-Mur. 1993: 204

Association Rielletum macrocarpae Cirujano, Velayos et García-Mur. 1993 mut. Romanov et al. nom. mut. nov.

Original form of the name (Cirujano et al. 1993: 205): Rielletum helicophyllae Cirujano, Velayos et García-Mur. 1993

Name-giving taxon of the original syntaxon name: Riella helicophylla (Bory & Mont.) Mont. 1852: 12

Name-giving taxon of the mutated syntaxon name: Riella macrocarpa (P.Allorge) Puche, Segarra-Moragues, Sabovlj., M.Infante et Heras 2022: 520

Authoritative taxonomic sources that use the name Riella macrocarpa: Gil-López et al. (2022), Segarra-Moragues et al. (2022), Colacino (2023), Kashta et al. (2023), Söderström et al. (2023), Kutschera (2024), Osman et al. (2024), Ros et al. (2024).

Holotypus: relevé 4 in table 2 at p. 208 by Cirujano et al. (1993).

Type locality: Spain, Zaragoza: Sástago, salina del Rebollón (Cirujano et al. 1993: 208).

Appearance and habitat: Open to nearly fully closed submerged carpets of attached ephemeral liverwort Riella macrocarpa (>25% cover), with other taxa found in low numbers. They can be found in brackish water varying from very shallow to 15 cm deep in ombrotrophic temporary Mediterranean ponds.

Diagnostic taxon (% constancy): Riella macrocarpa (100%).

Distribution: Spain (Cirujano et al. 1993), Sicily, Montenegro, Greece, and probably elsewhere in countries of the Mediterranean basin where R. macrocarpa is reported.

Habitat references: EUNIS (EEA 2024), Littoral sediments dominated by aquatic angiosperms, code A2.6; NATURA 2000, Coastal lagoons, 1150*.

Syntaxonomic note: The current syntaxonomic treatments usually include this association in the alliance Ruppion maritimae Br.-Bl. ex Westhoff in Bennema et al. 1943, order Ruppietalia J. Tx. ex Den Hartog et Segal 1964, class Ruppietea maritimae J. Tx. ex Den Hartog et Segal 1964 (e.g. Chytrý et al. 2024).

Based on the current understanding of the range (Fig. 1), population status and ecological requirements of R. macrocarpa and R. helicophylla, and also considering that these species have often been found in sympatric populations, Segarra-Moragues et al. (2022) assessed both species as Endangered (EN) under IUCN criteria, specifically B2b(ii,iii,v)c(ii,iv). This categorization is not currently implemented by the IUCN due to nomenclatural incongruences with liverwort species list. However, considering the known distribution of the R. helicophylla populations (Fig. 1), and the vulnerability of their habitats to climate change (Estrela-Segrelles et al. 2021), the authors recognize further investigation could lead to including this species under the category of Critically Endangered (CR).

Many records of R. helicophylla s.l. around the Mediterranean, especially in African countries (Fig. 6), are older than 50 years (up to 180 years old). This fact, the lack of field investigations (especially of “unattractive” habitats such as disturbed areas, parking sites, etc.), the ephemeral and irregular life cycle of the species, and the changes in the landscape in the last decades, all need to be considered in the assessment of the conservation status of both species.

With the aim of contributing to a deeper understanding of the species’ conservation status and supporting national assessment processes, the authors present the following considerations regarding the studied territories:

Montenegro. After the initial discovery of R. macrocarpa in the Ulcinj area in February 2023, intensive searches for similar habitats were conducted in Montenegro in 2023 and 2024, focusing on the coastal region and the Montenegrin coastline. Despite expectations and detailed investigations, especially in areas of the Tivat saline, Buljarica, and Velika plaža, R. macrocarpa was not found even in the vicinities of the “Ulcinj Salina”. Therefore, based on the knowledge of the Montenegrin coast and the habitat of R. macrocarpa, the probability of its presence at other locations in Montenegro, i.e. outside of the “Ulcinj Salina” is believed to be low.

As a newly discovered species with limited distribution, there is currently insufficient data to assess the status of R. macrocarpa in Montenegro according to IUCN criteria. However, this year’s research indicates that the species is potentially present in all pools with brackish water or in the sediments of periodically flooded pools whitin the Ulcinjska Salina. This data on the species distribution, coupled with the endangerment of its habitat, suggests that R. macrocarpa may face significant threats.

Sicily/Italy. During 2023, following the discovery of R. macrocarpa near Birgi Novo, field investigations were conducted in similar environments throughout Sicily in an effort to locate new populations. Although these surveys did not yield any new findings, based on the ecology of the species and observation of environments resembling the site where the new Riella population was discovered, we cannot rule out the presence of further populations in Sicily. The absence of rain during the winter 2023/24 resulted in the absence of water in all the environments suitable for hosting R. macrocarpa, severely limiting the potential for discoveries in 2024.

The only other currently known population of R. macrocarpa in Italy (i.e. the Sardinian population) is still listed as R. helicophylla in the recent Italian National Red-List (Puglisi et al. 2023) where it is assessed as CR B2ab(ii,iii,iv).

Greece. After the initial finding of R. macrocarpa in Attica in 2011, several field campaigns were conducted in the following years to identify new populations. In 2014, a population was found in Paralia Astros (Peloponnese), along with several other populations of Riella species that are not included in this work because they are not yet identified. Considering the vast geographic range of Greece, the abundance of suitable habitats for Riella there and the confirmed presence of several populations, we believe there is insufficient information to properly assess the conservation status of the species.

Figure 5. 

Close-up appearance of Rielletum macrocarpae: A. R. macrocarpa and a male specimen of Tolypella hispanica, 6^th April 2023, Birgi Novo, Sicily, Italy; B. Plants in very shallow water, 17^th April 2023, Ulcinj Salina, Montenegro; C. Submersed plants, hook-shaped lines of antheridia, sporophytes with light green unripe spores and dark ripe spores are visible, 6^th May 2023, Ulcinj Salina, Montenegro (photographs: A – A. Troia, B, C – R. Romanov).

Figure 6. 

Distribution in space and time of the records of Riella helicophylla s.l. (Ellis et al. 2018; Segarra-Moragues et al. 2022; Colacino 2023; GBIF 2024; Osman et al. 2024; our data).

Riella helicophylla is listed in the Annex II of the European Union Habitats Directive 92/43/EEC, highlighting its significant conservation value and the need for coordinated efforts across EU Member States to ensure its protection. As we have seen, recent studies (Segarra-Moragues et al. 2022) have demonstrated that under the name R. helicophylla there are two different species: R. helicophylla, and R. macrocarpa. To align with current taxonomic knowledge and improve the accuracy of future biodiversity reporting to the European Union, countries such as Portugal, Spain, France, Italy, and Cyprus should adopt the taxonomic split of R. helicophylla. Such an update is crucial to comply with the “one-to-many” taxonomic split criteria outlined in the “Introduction to the updated Article 17 checklists for species and habitats” (European Commission 2017).

In Europe, the populations of Riella helicophylla s.l. benefit (at least in principle) from various forms of protection. Not only is the species itself protected by its inclusion in Annex II of the Habitats Directive, but the habitats where it occurs are also considered priorities by the same directive. Furthermore, these populations often fall within areas subject to additional protection measures, such as national parks, nature reserves, and Ramsar sites.

Similarly, North-African populations are protected at both species and habitat levels. All known south-Mediterranean populations of Riella helicophylla s.l., with the exception of those further south of Morocco, are located within Ramsar sites. At the species level R. helicophylla is included in Annex I of the Bern Convention on the Conservation of European Wildlife and Natural Habitats which has been ratified by both Tunisia (1996) and Morocco (2001). The only country that currently does not provide species protection is Algeria.