Back from presumed local extinction: the case of Sargassum hornschuchii C.Agardh (Fucales: Heterokontophyta) in the Spanish Mediterranean

2025 ● 46 ● 6 AlgologieAlgologie Cryptogamie, Algologie est indexé dans / Cryptogamie, Algologie is indexed in: – Aquatic Sciences & Fisheries Abstracts Part I. – Biological Abstracts – Chemical Abstracts – Current Contents – Marine Science Contents Tables (FAO) – Science Citation Index – Publications bibliographiques du CNRS (Pascal) Cryptogamie, Algologie est distribué en version électronique par / Cryptogamie, Algologie is distributed electronically by: – BioOne® (http://www.bioone.org/loi/crya) Cryptogamie, Algologie est une revue en flux continu publiée par les Publications scientifiques du Muséum, Paris Cryptogamie, Algologie is a fast track journal published by the Museum Science Press, Paris Les Publications scientifiques du Muséum publient aussi / The Museum Science Press also publish: Adansonia, Geodiversitas, Zoosystema, Anthropozoologica, European Journal of Taxonomy, Naturae, Comptes Rendus Palévol, Cryptogamie sous-sections Bryologie, Mycologie. Diffusion – Publications scientifiques Muséum national d’Histoire naturelle CP 41 – 57 rue Cuvier F-75231 Paris cedex 05 (France) Tél. : 33 (0)1 40 79 48 05 / Fax : 33 (0)1 40 79 38 40 [email protected] / http://sciencepress.mnhn.fr © Publications scientifiques du Muséum national d’Histoire naturelle, Paris, 2025 ISSN (électronique / electronic) : 1776-0984 Directeur De la publication / Publication director: Gilles BLOCH Président du Muséum national d’Histoire naturelle réDactrice en chef / editor-in-chief: Line le Gall Muséum national d’Histoire naturelle assistant De réDaction / assistant editor: Violette GRUNENBERGER ([email protected]) Mise en paGe / Page layout: Violette GRUNENBERGER réDacteurs associés / associate editors Ecoevolutionary dynamics of algae in a changing world Stacy KRUEGER-HADFIELD Virginia Institute of Marine Science Eastern Shore Laboratory, Wachapreague, VA 23480 (United States) Jana KULICHOVA Department of Botany, Charles University, Prague (Czech Republic) Cecilia TOTTI Dipartimento di Scienze della Vita e dell’Ambiente, Università Politecnica delle Marche, Via Brecce Bianche, 60131 Ancona (Italy) Phylogenetic systematics, species delimitation & genetics of speciation Sylvain FAUGERON UMI3614 Evolutionary Biology and Ecology of Algae, Departamento de Ecología, Facultad de Ciencias Biologicas, Pontificia Universidad Catolica de Chile, Av. Bernardo O’Higgins 340, Santiago (Chile) Marie-Laure GUILLEMIN Instituto de Ciencias Ambientales y Evolutivas, Universidad Austral de Chile, Valdivia (Chile) Diana SARNO Department of Integrative Marine Ecology, Stazione Zoologica Anton Dohrn, Villa Comunale, 80121 Napoli (Italy) Comparative evolutionary genomics of algae Nicolas BLOUIN Department of Molecular Biology, University of Wyoming, Dept. 3944, 1000 E University Ave, Laramie, WY 82071 (United States) Heroen VERBRUGGEN School of BioSciences, University of Melbourne, Victoria, 3010 (Australia) Algal physiology & photosynthesis Janet KÜBLER California State University Northridge, Department of Biology, California State University, Northridge, CA 91330-8303 (United States) Prokaryotic algae Nico SALMASO IASMA Research and Innovation Centre, Fondazione Mach-Istituto Agrario di S. Michele all’Adige, Limnology and River Ecology, Via E. Mach, 1, 38010 San Michele all’Adige, Trento (Italy) Vitor VASCONCELOS Faculdade de Ciências da Universidade do Porto and CIIMAR, Rua do Campo Alegre, s/n, 4169-007 Porto (Portugal) couverture / cover: Extrait de la Figure 5/Extract of Figure 5 81 CRYPTOGAMIE, ALGOLOGIE • 2025 • 46 (6) © Publications scientifiques du Muséum national d’Histoire naturelle, Paris. www.cryptogamie.com/algologie Back from presumed local extinction: the case of Sargassum hornschuchii C.Agardh (Fucales: Heterokontophyta) in the Spanish Mediterranean Enric BALLESTEROS† Centre d’Estudis Avançats de Blanes-CSIC, Acc. Cala Sant Francesc 14, 17300 Blanes, Girona (Spain) Sònia DE CARALT Institut d’Ecologia Aquàtica (IEA), Departament de Ciències Ambientals, Universitat de Girona, Campus Montilivi, 17003 Girona (Spain) Emma CEBRIAN Centre d’Estudis Avançats de Blanes-CSIC, Accés Cala Sant Francesc 14, 17300 Blanes, Girona (Spain) [email protected] (corresponding author) Submitted on 10 June 2024 | Accepted on 2 July 2025 | Published on 28 November 2025 Ballesteros E., de Caralt S. & Cebrian E. 2025. — Back from presumed local extinction: the case of Sargassum hornschuchii C.Agardh (Fucales: Heterokontophyta) in the Spanish Mediterranean. Cryptogamie, Algologie 46 (6): 81-88. https://doi.org/10.5252/cryptogamie-algologie2025v46a6. http://cryptogamie.com/algologie/46/6 ABSTRACT We report on a new record of Sargassum hornschuchii C.Agardh in the Spanish Mediterranean after having no reports for more than a century. Sargassum hornschuchii was found in a deep-water rocky bottom offshore Menorca together with the kelp Laminaria rodriguezii Bornet and the rockweed Ericaria zosteroides (C.Agardh) Molinari & Guiry. We make an accurate morphological description and provide pictures of the specimens collected. This new record puts into question the assignment of the IUCN “extinct” category for deep-water rare macroalgae as they can go unnoticed for a long time. This also highlights the need to protect remote deep-water spots where biodiversity can still be flourishing. RÉSUMÉ De retour après une extinction locale présumée : le cas du Sargassum hornschuchii C.Agardh (Fucales: Heterokontophyta) en Méditerranée espagnole. Nous rapportons la redécouverte de Sargassum hornschuchii C.Agardh dans la Méditerranée espagnole après plus d’un siècle d’absence de signalement. Sargassum hornschuchii a été trouvé dans un fond rocheux profond au large de Minorque avec la laminaire Laminaria rodriguezii Bornet et le cystoseire Ericaria zosteroides (C.Agardh) Molinari & Guiry. Nous faisons une description morphologique précise et fournissons des photos des spécimens collectés. Cette découverte remet en question l’attribution de la catégorie « éteinte » de l’UICN aux macroalgues rares des eaux profondes, car elles peuvent passer longtemps inaperçues. Cela souligne également la nécessité de protéger les zones profondes éloignées des côtes, où la biodiversité peut être encore florissante. KEY WORDS Macroalgae, Mediterranean, extinction, Sargassum, rediscovery. MOTS CLÉS Macroalgues, Méditerranée, extinction, Sargassum, redécouverte. 82 CRYPTOGAMIE, ALGOLOGIE • 2025 • 46 (6) Ballesteros E. et al. INTRODUCTION Marine forests in the Mediterranean Sea are not usually dominated by kelps but by species of the order Fucales (Rodríguez-Prieto et al. 2013). Two genera of the order Fucales were considered to be present in the Mediterranean until recently. However, molecular data has supported the division of the previous genus Cystoseira C.Agardh into three different genera: Cystoseira C.Agardh, Ericaria Stackhouse and Gongolaria Boehmer (Molinari-Novoa & Guiry 2020), which are the main engineering species of these forests. However, the genus Sargassum C.Agardh, with nine species known to inhabit the Mediterranean Sea (Aouissi et al. 2018; Blanfuné et al. 2022), were also reported to be relevant in the past in these forests. Nevertheless, all but two (the invasive Sargassum muticum (Yendo) Fesholt and the native Sargassum vulgare C.Agardh) have become extremely rare or even locally extinct (Thibaut et al. 2016). Three of the nine species reported are considered to be Mediterranean endemisms and, thus, they require a special attention when dealing with conservation issues: Sargassum hornschuchii C.Agardh, Sargassum ramentaceum Zarmouth & Nizamuddin, and Sargassum trichocarpum J.Agardh (Blanfuné et al. 2022). Sargassum hornschuchii is a species apparently reported from the coastal areas of most Mediterranean regions and countries (Aouissi et al. 2018). However, Aouissi et al. (2018) did not include Egypt in its distribution, although it has been widely reported, mainly around the coastal area of Alexandria (Fakhry et al. 2013; Noaman et al. 2013a, 2013b; El-Zabalawy & ElKenany 2015; Fathy et al. 2017; Abdel-Kareem et al. 2020; Ghallab et al. 2022) but also from other sites west from the Nile Delta (Shams El-Din & El-Sherif 2012). The species seems also to be present in Libya (Alghazeer et al. 2019, 2021). Sargassum hornschuchii has also been reported from the Black Sea (Karacuha & Okudan 2017). Thus, according to past and present reports, S. hornschuchii shows a wide Mediterranean distribution, with the continental coasts of Spain being the only place where the species has never been reported (Gómez-Garreta et al. 2000). Unless S. hornschuchii has been widely reported all across the Mediterranean, being very common in the Adriatic Sea (Ercegović 1960; Špan 2005), it has always been considered rare in the Western Mediterranean. In Spain, S. hornschuchii has only been reported from the Balearic Islands (RodríguezFemenías 1889; de Buen 1916; Garcias 1919; Bellón 1921) but there are no citations and no herbarium specimens collected after 1950 (Gómez-Garreta et al. 2000). In France, S. hornschuchii was reported to be present along all the French Mediterranean coasts (Thibaut et al. 2016), although there are not recent reports of the species, even in the Albères Coast, where according to Feldmann (1937), it was rather frequent in deep water assemblages dominated by Gongolaria montagnei (J.Agardh) Kuntze (as Cystoseira spinosa Sauvageau). Thibaut et al. (2005) considered S. hornschuchii extinct from the Albères coast and Thibaut et al. (2015) considered it extinct from the French Riviera. The last recorded report from France dates back to 1988 from Galeria, Corsica (Thibaut et al. 2016). However, Verlaque et al. (2019), even if the species has not been seen for the last 35 years, consider extinction only as a hypothesis, as S. hornschuchii has always been very rare. In the Tyrrhenian Sea (Italy), S. hornshuchii has been reported to be present in Giannutri, Gorgona Islands and other Tyrrhenian islands (Piazzi & Cinelli 2002; Piazzi et al. 2009; Piazzi & Ceccherelli 2020). Sargassum hornschuchii was also reported from different spots in the Sicily Channel (Giaccone et al. 1972, 1973). In the Mediterranean western coasts of Africa, S. hornschuchii has been reported only from La Galite (Tunisia) (Feldmann 1961), Algeria (Perret-Boudouresque & Seridi 1989) and Morocco (González-García & Conde-Poyales 1994) although it has not been recently seen (Moussa et al. 2018). In short, the only twenty first century western Mediterranean records come from the Tyrrhenian islands, while the species has not been recorded in Spain, France, Tunisia, Algeria or Morocco for at least the last 30 years. Here we provide a recent record of S. hornschuchii from Menorca (Balearic Islands). Given the extreme scarcity of this species and the fact that it has not been recorded in Spanish waters for the last 100 years, we also provide a morphological description of the specimens and a short comment on the habitat where the specimens were collected. MATERIAL AND METHODS Specimens were collected onboard the fishing vessel Curniola based on Ciutadella Harbor (Menorca) on April 26th, 2022. Sampling was performed by trammel nets set in fishing grounds for lobster. Marine biologists were on board to collect macroalgae brought from the seabed by the nets. Location of the collection was given by the GPS and plotter of the fishing vessel. GPS bottom accuracy is low, due to the length of the net and the drift of the boat while recovering the gear. Sargassum hornschuchii samples were collected and taken to the laboratory where they were observed and identified. The descriptions were compared with previous descriptions of the species made by other authors (Hamel 1931-1939; Cormaci et al. 2012; Aouissi et al. 2018; Blanfuné et al. 2022). Pictures were taken with an Olympus TG6 camera in the laboratory. Two vouchers specimens were mounted on herbarium sheets. RESULTS The locality of collection is a fishing ground known as “Fora de Sa Barra” (40°00’03.0”N, 3°39’23.5”E), placed over rocky substrate and at a depth around 65 meters. Specimens of a species of Sargassum were brought to the surface with other erect macroalgae, mainly Laminaria rodriguezii Bornet and Ericaria zosteroides (C.Agardh) Molinari & Guiry. Description Thallus erect, 20-40 cm high (Fig. 1); holdfast discoid; stipes cylindrical, warty, 1-4 cm high, up to 4 mm diameter, one to three stipes arising from a single holdfast (Fig. 1); primary 83 Sargassum hornschuchii C.Agardh in Spain CRYPTOGAMIE, ALGOLOGIE • 2025 • 46 (6) branches 20-36 cm long, flattened, with serrated wings at the base, cylindrical at the apex (Figs 1, 2); basal blades 7-10 × 1.01.6 cm, upper blades smaller, all lanceolate, wavy, serrated, sessile, with marked central nerve (Fig. 3); air bladders almost spherical 4-5 cm × 5-6 mm, smooth, petiolated 1-3 mm, not mucronated; receptacles pedicellated, situated in ramified branches, 2-4 mm long (Figs 3, 4); receptacles irregularly polyhedral in section, slightly warty, apiculate, up to 10 mm long and 2.0-2.5 mm wide, usually single but sometimes divided (Fig. 5); oogonia spherical (320 to 350 µm) or slightly oval (240-310 × 340-400 µm) (Fig. 6). All these features are consistent with S. hornschuchii. Vouchers have been deposited at the Herbarium of the University of Girona (HGI-A 22238 and HGI-A 22239). DISCUSSION The morphological features of the specimens collected fit into the description of S. hornschuchii. Main characteristics are the flattened and irregularly winged primary branches near the base, the pedicellated receptacles situated in ramified branches, and the big and distinct, apiculate receptacles that are polyhedral in section. In our opinion the flat receptacles usually attributed to S. hornschuchii (Hamel 1931-1939; Cormaci et al. 2012; Aouissi et al. 2018; Blanfuné et al. 2022) should come from descriptions based on pressed herbarium material and are probably incorrect. Amongst the Mediterranean species that can be confused with, none of them has winged primary branches. Moreover, reproductive specimens fall fiG. 1. — Specimen of Sargassum hornschucchii C.Agardh collected in Menorca. Notice the serrated wings at the base of the primary branches. Scale bar: 4 cm. 84 CRYPTOGAMIE, ALGOLOGIE • 2025 • 46 (6) Ballesteros E. et al. apart since in S. vulgare receptacles are much smaller and in Sargassum acinarium (Linnaeus) Setchell and S. trichocarpum receptacles are very thin (up to 1 mm wide) and cylindrical (Aouissi et al. 2018; Blanfuné et al. 2022). Sargassum hornschuchii is usually reported as a deep-water species at least in the Western Mediterranean and in the Adriatic. It is mostly reported between 15-30 m in the Albères coast (Feldmann 1937), 30 to 60 m depth in most French territories including Corsica (Thibaut et al. 2016), 30 to 64 m in Italy (Giaccone 1967, 1972) and 10 to 60 meters in the Adriatic Sea (Špan 2005), with very rare collections from the northern Adriatic at 5 m (Munda et al. 2006). Reports from Tunis (La Galite) come from 25-50 m depth (Feldmann 1961). In Menorca it has been reported by Rodríguez-Femenías (1889) between 110 and 150 m depth and in the Adriatic Sea down to 250 m depth (Ercegović 1960), although these ancient records whether belong to drift specimens or depths were measured inaccurately. Excluding these non-reliable depths, our collection at 65 m is, thus, at the lowest reported depth range for the species. The clear waters surrounding the Balearic Islands (Ballesteros & Zabala 1993) are probably responsible for it. Another issue is that most reports from the Levantine Sea come from very shallow water (Shams El-Din & El-Sherif 2012; Fakhry et al. 2013; Noaman et al. 2013a, 2013b; El-Zabalawy & El-Kenany 2015; Fathy et al. 2017; Abdel-Kareem et al. 2020; Ghallab et al. 2022), which casts some doubt about their correct identification. The collection of S. hornschuchii in Menorca was accompanied by L. rodriguezii and E. zosteroides. The same three species were also found growing together in Banco Appolo (Ustica, Tyrrhenian Sea) between 42 and 64 m depth (Giaccone 1967) and in La Galite (Feldmann 1961). According to Giaccone & Bruni (1973), S. hornschuchii characterizes erect macroalgal assemblages from the lower infralittoral and upper circalittoral zones subjected to a high unidirectional water movement and light intensity ranging from 20 to 0.01% of the surface light. These include assemblages dominated either by G. montagnei (as Cystoseira spinosa), by E. zosteroides (as Cystoseira zosteroides), by L. rodriguezii and, only in the Alboran Sea and the straits of Messina, by Gongolaria usneoides (Linnaeus) Molinari-Novoa & Guiry (as C. usneoides), Laminaria ochroleuca Bachelot Pylaie and Saccorhiza polyschides (Lightfoot) Batters. Feldmann (1937) reported S. hornschuchii from the assemblage dominated by E. zosteroides and G. montagnei at the Albères coast, the same kind of assemblage where it appears in some islands of the Tyrrhenian Sea (Piazzi et al. 2009; Piazzi & Ceccherelli 2020). fiG. 2. — Detail of holdfast and stipes. Scale bar: 2 cm. 85 Sargassum hornschuchii C.Agardh in Spain CRYPTOGAMIE, ALGOLOGIE • 2025 • 46 (6) Sargassum hornschuchii may be restricted to rocky bottoms since it has never been reported from Balearic Islands’ coastal detritic assemblages, where L. rodriguezii, E. zosteroides and G. montagnei are usually common (Joher et al. 2012, 2015, 2016, 2023). Sargassum hornschuchii has suffered an important regression in the western Mediterranean (Gómez-Garreta et al. 2000; Thibaut et al. 2005, 2015, 2016; Ould-Ahmed et al. 2013; Moussa et al. 2018) and it seems to be also disappearing in areas of the Ionian (Cecere et al. 1996) and the Adriatic seas (Sidari & Bressan 1992; Cormaci & Furnari 1999; Munda 1993, 2000; Cecere et al. 2001; Curiel et al. 2009; Falace et al. 2010; Perkol-Finkel & Airoldi 2010). There are no experimentally tested factors accounting for this decrease although increased turbidity, hyper-sedimentation, trawling, anchoring and uprooting by fishing nets have been blamed by Thibaut et al. (2015) and Verlaque et al. (2019). In fact, our samples come from trammel net fishing, pointing to fishing gear as a real cause of harm. Because of the current rate of decrease, S. hornschuchii is considered as “Endangered” at the Mediterranean level according to the IUCN classification (Verlaque et al. 2019). It was also included in the first internationally recognized and accepted list provided under the umbrella of the Barcelona Convention in 1996 in the Annex to the protocol concerning Specially Protected Areas and Biological Diversity in the Mediterranean that was lately updated in 2009 (Verlaque et al. 2019). This list has been roughly transcribed into some national legislations (e.g. France: Decree no. 2002-1454, December 2002 amended by Decree no. 2014-1195 of 16 October 2014; Spain: Law 42/2007 amended by Order AAA/75/2012) or has been used as a base to produce more accurate local checklists (e.g. Catalonia: Decree 172/2008 of 26 August 2023). Considering everything stated regarding S. hornschuchii’s rarity and decrease, this new record from Menorca acquires great relevance. This collection is the only one in the last 35 years from the westernmost part of the Western Mediterranean sea and the first one after more than a century in Spain. We agree with Verlaque et al. (2019) that it is almost impossible to give the IUCN “Extinct” category to deep-water algal species such as S. hornschuchii, since they are naturally scarce and it is extremely difficult to look for new populations. In fact, unequivocally detecting the extinction of a species is not an easy task (Diamond 1987; Akçakaya et al. 2017; Lee et al. 2017) and specialists debate about the criteria to be considered (Butchart et al. 2006; Roberts et al. 2023). Uncertainty increases if extinction is local, since recolonisation coming from individuals from other distant populations is possible and random in space and time. But we do not expect that recolonisation could be the case for S. hornschuchii in Menorca fiG. 3. — Upper portion of the thalli with receptacles. Scale bar: 2 cm. 86 CRYPTOGAMIE, ALGOLOGIE • 2025 • 46 (6) Ballesteros E. et al. as we are very confident that it has never disappeared from the location we collected it. Remote, non-accessible areas are a good place to search for potentially extinct species as local anthropogenic impacts (i.e., fishing and associated impacts of fishing gear) are presumed to be lower and species persistence to be higher. Thus, protection to fishing of these areas is highly recommended. In fact, the area we collected S. hornschuchii is inside a Site of Community Importance (SCI) within the Natura 2000 network since 2014, and it was designated as a trawl-fishing protected zone in 2016 (Farriols et al. 2022). Moreover, all the area affecting the rocky bottoms known as “Fora de Sa Barra” has been proposed as a no-take area (Ballesteros 2022), which would greatly increase the chances of survival of the remaining specimens of S. hornschuchii as well as many more endangered species that are known to thrive in the area (Barberá et al. 2012; Joher et al. 2012, 2015; Farriols et al. 2022). CONCLUSION In conclusion, this recent unexpected finding of S. hornschuchii in Spanish waters, after more than one century of not being reported, is good news for Spanish marine biodiversity. It also tells us the lack of knowledge about the hidden diversity that still exists below the normal depths surveyed by SCUBA and the necessity of investing resources to fill this gap if we really care about conservation. Finally, it highlights the emergency of creating marine protected areas in places other than recreational diving spots where biodiversity can still be flourishing. Acknowledgements This contribution is dedicated to Joan and Xesc Canals from Ciutadella, Menorca, skippers of the fishing vessel Curniola, for their endless help and friendship. This is a contribution of the projects FoRestA Grant/Award no. PID2020-112985GBI00 from the Spanish Ministry of Science and Innovation and FoRescue-n° PCI2022-135070-2 and PCI2022-135052-2 funded by Biodiversa+ (European Biodiversity Partnership).We also thank the referees and the editor-in-chief for their valuable work. This work is dedicated to the memory of Dr. Enric Ballesteros, whose contributions to the study of Mediterranean macroalgae have left a lasting mark on the field. It was an honor to collaborate with him on what became our final joint contribution – the rediscovery of Sargassum hornschuchii in the Spanish Mediterranean. Although Enric is no longer with us, his influence continues to guide our work, and we like to think that this will not be our last contribution together. REFERENCES A bDel -K Areem m. s., m ohy e l D in s. m. & i brAhim e. s. m. 2020. — Optimization of growth conditions and biochemical composition of Microchloropsis Salina, Cultures with three macroalgal aqueous extracts. 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