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The Mediterranean Deep-Water Kelp Laminaria Rodriguezii Is An Mar Biol (2016) 163:69 DOI 10.1007/s00227-016-2821-2 ORIGINAL PAPER The Mediterranean deep‑water kelp Laminaria rodriguezii is an endangered species in the Adriatic Sea Ante Žuljevic´1 · Akira F. Peters2 · Vedran Nikolic´1 · Boris Antolic´1 · Marija Despalatovic´1 · Ivan Cvitkovic´1 · Igor Isajlovic´1 · Hrvoje Mihanovic´1 · Slavica Matijevic´1 · Dawn M. Shewring3 · Simonepietro Canese4 · Christos Katsaros5 · Frithjof C. Küpper3 Received: 31 May 2015 / Accepted: 20 January 2016 © The Author(s) 2016. This article is published with open access at Springerlink.com Abstract Deep-water kelps are little-known large brown We propose to classify L. rodriguezii as “Endangered” in algae occurring close to the lower limit of photosynthetic the Adriatic Sea under IUCN criteria B1ab(i,iii,iv), ver 3.1. life in the sea. This study compares historical and recent Oceanographic characteristics of the habitat suggest that records of the deep-water Mediterranean kelp Laminaria besides high water transparency, presence of North Adri- rodriguezii in the Adriatic Sea. Historical records include atic Dense Water with both strong currents and stable low data from herbarium collections and trawling fishery expe- temperatures of around 14 °C are essential oceanographic ditions in the mid-twentieth century, while recent data factors for the development of L. rodriguezii in the Cen- comprise records of the last 17 years from MEDITS expe- tral Adriatic. The origin of cold water thus differs from ditions, ROV surveys of historical kelp locations, benthic that at upwelling sites permitting populations of tropical surveys and records by fishermen. Altogether, these find- deep-water kelps. The phylogenetic position of L. rod- ings demonstrate that the Adriatic population of L. rod- riguezii is so far unknown. DNA sequences from nuclear riguezii has suffered a decline of more than 85 % of its and cytoplasmic markers of two thalli from Croatia and the historical range and is now present only around the small western Mediterranean confirmed that L. rodriguezii is a offshore island of Palagruža. Bottom trawling activities are member of the Laminariaceae and most closely related to presumably responsible for the disappearance elsewhere. L. ochroleuca, L. pallida and the Brazilian deep-water kelp L. abyssalis. Responsible Editor: K. Bischof. Keywords Endangered algae · Circalittoral · cox1 · Reviewed by E. Ballesteros and undisclosed experts. Rubisco spacer · ITS · Kelp · Bottom trawling · IUCN criteria Electronic supplementary material The online version of this article (doi:10.1007/s00227-016-2821-2) contains supplementary material, which is available to authorized users. Introduction * Frithjof C. Küpper [email protected] Surface waters of the Mediterranean Sea show strong sea- 1 sonal temperature fluctuations. While winter and spring Institute of Oceanography and Fisheries, Šet. I. Meštrovića 63, 21000 Split, Croatia temperatures in the range of 12–17 °C are similar to neigh- 2 Bezhin Rosko, 40 rue des pêcheurs, 29250 Santec, Brittany, bouring areas of the North Atlantic, summer temperatures France of 20–28 °C are closer to the temperatures of tropical seas 3 Oceanlab, University of Aberdeen, Newburgh AB41 6AA, (e.g. Coll et al. 2010). Consequently, biota living in these Scotland, UK surface waters are subject to a strong, temperature-driven 4 Institute for Environmental Protection and Research ISPRA, selective pressure, excluding organisms from both cold- Via Vitaliano Brancati 48, Rome 00144, Italy temperate and tropical regions. 5 Department of Botany, Faculty of Biology, University Kelps (Laminariales) are generally considered as mac- of Athens, Panepistimiopolis, Athens 157 84, Greece roalgae with temperate and cold-water affinities (Steneck 1 3 69 Page 2 of 12 Mar Biol (2016) 163:69 et al. 2002). Their distribution in lower latitudes is limited In the Adriatic Sea, L. rodriguezii is only reported from to waters rarely exceeding 20 °C; furthermore, many spe- the Central Adriatic (mainly in Croatian, occasionally in cies require lower winter temperatures for gametogenesis international waters). First detailed knowledge of its dis- (Lüning 1980). In cases of strong stratification and high tribution in the region was obtained during the Hvar fish- water transparency, kelp communities may occur in a cold- eries biology expedition in 1948–1949 (Ercegović 1960), water layer receiving enough sunlight for photosynthesis which was conducted to gather data on commercial trawl beneath a constantly or seasonally warmer surface layer. resources after several years of suspension of fishing dur- Currently known deep-water kelps include Laminaria rod- ing the Second World War. This dataset is a baseline (zero riguezii Bornet in the Mediterranean (Feldmann 1934), L. state) dataset of trawling bottom species till 400 m depth abyssalis A. B. Joly et E. C. Oliveira in Brazil (Joly and (Vrgocˇ et al. 2004). The expedition also collected data on Oliveira 1967), L. philippinensis J. E. Petrov & M. V. bycatch including benthic seaweeds. L. rodriguezii was Suchovejeva in the Philippines (Petrov et al. 1973) and found in the areas of Jabuka Pit (henceforth referred to as Eisenia galapagensis W. R. Taylor in the Galapagos Islands “Jabuka”), Biševo Island (“Biševo”) and Palagruža Island (Graham et al. 2007). (“Palagruža”). Between 1956 and 1961, further fisheries In contrast to their well-studied relatives in shallow expeditions also recorded data on deep-water algae (Gamu- waters, deep-water kelp taxa remain poorly known in lin–Brida 1965). During fisheries expeditions in the follow- key aspects of their biology (Bartsch et al. 2008). Lami- ing three decades, data on L. rodriguezii were not collected. naria abyssalis is the best studied deep-water kelp species Since 1996, annual fishery surveys (Mediterranean (Yoneshigue-Valentin 1990; Braga and Yoneshigue-Valen- International Bottom Trawl Suveys, MEDITS) using trawl tin 1996; Rodrigues et al. 2000, 2002; Yoneshigue-Valentin nets have been conducted, covering transects similar to et al. 2003; Romanos et al. 2011; Marins et al. 2012). In the Hvar expedition (Bertrand et al. 2002). This allowed a contrast, only the original description (Petrov et al. 1973) comparison of historical fisheries data with new records. exists for L. philippinensis. Within the framework of the project “Brown algal biodi- Laminaria rodriguezii is an endemic deep-water Medi- versity and ecology in the Eastern Mediterranean Sea”, we terranean macroalga consisting of a branched holdfast, have recently conducted deep-water transects in the areas a stipe and an undivided blade of up to 150 30 cm in of the Adriatic Sea where L. rodriguezii was recorded in the × size (Beck 1896; Hamel 1931–1939). It is able to produce 1950s and 1960s, using a ship-deployed remotely-operated adventive blades vegetatively on stolons (Huvé 1955), vehicle (ROV). The results of these transects, together with which is a rare feature in the Laminariales and shared in the the biological surveys performed from the mid-1990s, com- genus Laminaria only with L. sinclairii (Harvey) Farlow, bined with information provided by professional fishermen, Anderson & Eaton from the northeast Pacific (Demes and give an overview of the recent populations of L. rodriguezii Graham 2011). Originally described by Bornet (1888), it is in the Adriatic Sea and allow to evaluate its distribution and scattered in the Western Mediterranean and Adriatic Sea. conservation status. The main populations occur around the Balearic Islands Little is known about the biology of L. rodriguezii, and (Joher et al. 2012) and on seamounts in the Tyrrhenian Sea in particular, there is no physiological knowledge about this (Giaccone 1967; Bo et al. 2011). The species occurs in species, which is without doubt because of the difficulty to areas of very specific biotic and abiotic parameters, which collect live material. Also, the phylogenetic position of L. are still only partly understood. It was mainly reported rodriguezii has not been clarified so far, with no sequence from depths >70 m, seldom found between 50 and 70 m, data having been reported. Using two thalli from the Adri- and exceptionally less deep on seamounts or in upwelling atic and the western Mediterranean, as well as samples of systems (30 m at Galite Island area in Tunisia; Balles- putative relatives, we have generated sequences of nuclear teros 2006). The maximum depth, 260 m, was recorded in and cytoplasmic markers, which suggest a close relation- the Adriatic Sea (Ercegović 1960). L. rodriguezii occurs ship with other Atlantic members of Laminaria. on loose-lying deep-water coralligenous beds (Balles- teros 2006) and may cover sea mounts, slopes and rocky ledges of offshore islands with prevailing highly transpar- Methods ent waters (Feldmann 1934; Giaccone 1969; Fredj 1972; Barcelo 1985; Bo et al. 2011). The upper limit possibly Historical and spatial distribution of Laminaria depends on temperature, while the lower limit is presum- rodriguezii ably determined by light availability (Joher et al. 2012). Since L. rodriguezii also lives in bottom trawling areas, Data on the historical and current distribution of L. rodri- there is concern on its conservation status (UNEP/IUCN/ guezii in the Adriatic were obtained from published and GISPosidonie 1990). unpublished records. Unpublished data included specimens 1 3 Mar Biol (2016) 163:69 Page 3 of 12 69 of L. rodriguezii housed in the main European and all Croa- Kimura-2-parameter distances, maximum parsimony
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