The Invasive Species Asparagopsis Taxiformis

Ascpta rBagootapnsisc ata Mxiafolarmciitsa nona A33n.d 5a-lu1s5ian coasts Málaga, 20058

THE INVASIVE SPECIES ASPARAGOPSIS TAXIFORMIS (BONNEMAISONIALES, RHODOPHYTA) ON ANDALUSIAN COASTS (SOUTHERN SPAIN): REPRODUCTIVE STAGES, NEW RECORDS AND INVADED COMMUNITIES

María ALTAMIRANO1*, Antonio Román MUÑOZ2**, Julio DE LA ROSA3, Agustín BARRAJÓN-MÍNGUEZ4, Agustín BARRAJÓN-DOMENECH4, Carlos MORENO-ROBLEDO5 & M. Carmen ARROYO6

1 Departamento de Biología Vegetal (Botánica), Facultad de Ciencias, Campus de Teatinos s/n, Universidad de Málaga. 29071, Málaga 2Departamento de Biología Animal, Facultad de Ciencias, Campus de Teatinos s/n, Universidad de Málaga. 29071, Málaga **Present address: Fundación MIGRES, Huerta Grande, N-340, Km 96, El Pelayo, 11390 Algeciras, Cádiz 3 Departamento de Botánica, Facultad de Ciencias, Campus de Fuentenueva, Universidad de Granada, 18071, Granada 4 C/ Nuzas 14, 5ºA, 29010 Málaga 5C/ Fuente de la Manía 1, 1º Piso, 29012 Málaga 6 C/ Calañas 5, Bl. 1 4º A, 29004 Málaga *Corresponding author: [email protected]

Recibido el 24 de diciembre de 2007, aceptado para su publicación el 9 de julio de 2008 Publicado "on line" en julio de 2008

ABSTRACT. The invasive species Asparagopsis taxiformis (Bonnemaisoniales, Rhodophyta) on Andalusian coasts (Southern Spain): reproductive stages, new records and invaded communities. The present study provides new records from Andalusian coasts of the exotic invasive seaweed Asparagopsis taxiformis (Delile) Trevisan. These records demonstrate that A. taxiformis has rapidly and widely expanded its distribution range in this region, from Almería to Cádiz (Strait of Gibraltar). The latter locality may represent the western geographical limit of the species in the Mediterranean Sea. Spermatangial heads and cystocarps were observed in the collected gametophytes. Additionally, we report the first record of the tetrasporophytic stage, Falkenbergia hillebrandii (Bornet) Falkenberg from the Andalusian coast, although tetraspores were not encountered in these samples. Consequently, information on the affected communities and arguments for considering A. taxiformis as an invasive species in the Andalusian coast are provided.

Key words. Asparagopsis taxiformis, Bonnemaisoniales, distribution, Falkenbergia hillebrandii, invasive species, Mediterranean Sea, new record, reproductive stage, Rhodophyta

RESUMEN. La especie invasora Asparagopsis taxiformis (Bonnemaisoniales, Rhodophyta) en las costas andaluzas (Sur de España): fases reproductivas, nuevas citas y comunidades invadidas. El 6 M. Altamirano et al. presente trabajo aporta nuevas citas para las costas andaluzas de la especie exótica invasora de macroalga Asparagopsis taxiformis (Delile) Trevisan. Estas citas muestran que la especie ha aumentado ampliamente su área de distribución de manera rápida en esta región, desde Almería hasta Cádiz (Estrecho de Gibraltar). Esta última localidad representaría el límite occidental de la especie en el mar Mediterráneo. En las muestras recogidas de gametofitos se pudieron observar ramas espermatangiales y cistocarpos. Se aporta la primera cita del estadio tetrasporofítico, Falkenbergia hillebrandii (Bornet) Falkenberg en las costas andaluzas, aunque no se observaron tetrásporas en estas muestras. Se informa sobre las comunidades afectadas y se dan argumentos para considerar a A. taxiformis invasora en las costas andaluzas.

Palabras clave. Asparagopsis taxiformis, Bonnemaisoniales, distribución, especie invasora, estadio reproductivo, Falkenbergia hillebrandii, mar Mediterráneo, nueva cita, Rhodophyta

INTRODUCTION are included (Boudouresque & Verlaque 2002), with different introduction times. Biological invasions are one of the Asparagopsis armata, a temperate major threats to biodiversity, ecosystem distributed species, is considered a functions and services, both in terrestrial and Lessepsian immigrant, first reported from the marine environments (Norse 1993; Grosholz Algerian coasts in 1923 (Feldmann & 2002). In coastal habitats, macroalgae Feldmann 1942). Asparagopsis taxiformis, a constitute an important component of tropical to warm temperate species, is introduced biota, ranging from 8 to 38% of considered a pre-Lessepsian immigrant or the total number of the recorded non- native in the eastern Mediterranean indigenous species (Schaffelke et al. 2006). (Andreakis et al. 2004), since the first record According to Boudouresque & Verlaque in the Mediterranean Sea was given in Egypt (2002) there are 85 introduced seaweeds in in 1813 (Delile 1813). Both taxa exhibit a the Mediterranean Sea, compared to only 49 strong invasive behaviour, and are included species detected along the European Atlantic in the list of the “Worst invasive alien species coasts (Ribera 2003). However, these threatening biodiversity in Europe” (EEA numbers are probably higher due to the 2007) and also in the list of the 100 “Worst existence of cryptic and/or cryptogenic Invasives in the Mediterranean Sea” species (Carlton 1996). In fact, the (Streftaris & Zenetos 2006). Mediterranean Sea is considered a hot spot The first record of Asparagopsis armata of exotic marine macroalgae due to the on Andalusian coasts was in 1965 (Seoane diversity of environmental habitats, the 1965), on the Atlantic coast of Cádiz. intense maritime traffic, the connectivity Nowadays, the species can be found from with the Atlantic and the Indo-Pacific Oceans Cádiz to Almería (Conde et al. 1996), via the Strait of Gibraltar and the Suez Canal forming natural vegetation belts on exposed respectively, aquaculture activities and the coasts between 0 and -15m depth low number of large perennial algae and (Ballesteros & Pinedo 2004), representing herbivores (Ribera 2003). the first reported macroalgal invasion in In the list of introduced marine Andalusian coasts. macroalgae in the Mediterranean Sea, both The introduction of A. taxiformis is species of the genus Asparagopsis, A. armata much more recent, as it was cited for the first Harvey and A. taxiformis (Delile) Trevisan, time in Alboran Sea (Chafarinas Islands) in Asparagopsis taxiformis on Andalusian coasts 7

1999 (Altamirano 1999). Later the species samples were pressed and prepared for was found in Andalusian coast, in Punta de herbarium sheets to be included in the la Mona (Granada) (Báez et al. 2001), Cala Herbarium of the University of Málaga Rijana (Granada) and Punta de la Polacra, (MGC). Herbarium acronyms follow P.N. Cabo de Gata (Almería) (Ballesteros & Holmgren et al. (1990). Pinedo 2004), but in none of these cases the species was considered invasive. Whether the species can complete its diplohaplontic RESULTS heteromorphic life-cycle or not in Andalusian coasts, is still unclear, as only Gametophytes of A. taxiformis (fig. 1) non-reproductive gametophytes have been were found between 0 and -17m depth on found, and the tetrasporophytic stage, rocky substratum in eleven new locations in Falkenbergia hillebrandi (Bornet) Andalusia from March to December (fig. 2, Falkenberg, has never been reported before. tab. 1). Four new locations are given for The present work provides new records Almería, three for Granada, three for Málaga of gametophytes of A. taxiformis in and one for Cádiz yet, no populations were Andalusian coasts, and the first record of the encountered in Huelva. Spermatangial tetrasporophyte, “Falkenbergia-stage”, in branches were observed in one specimen this region. Habitat and reproductive from Málaga (fig. 3) in July, and cystocarps information is also provided, and arguments were observed in specimens from Almería for considering this species as invasive on (fig. 4) in September. In several locations, Andalusian coasts are exposed. such as Paraje Natural de los Acantilados de Maro-Cerro Gordo (Málaga-Granada), gametophytes of A. taxiformis formed MATERIAL AND METHODS conspicuous monospecific stands. In these sites, the species appeared to act as a Samples of gametophytes and keystone species. In other sampling sites, tetrasporophytes of Asparagopsis taxiformis such as Marina del Este (Granada), the were collected between 2005 and 2007 at the species was observed inhabiting on the infralitoral zone of different locations in community of Cystoseira tamariscifolia Cádiz, Málaga, Granada and Almería (Hudson) Papenfuss. In Parque Natural Cabo provinces (Andalusia, Southern Spain), by de Gata (Almería) gametophytes were snorkeling and SCUBA diving. Several observed growing on rhizomes of the locations in Huelva province were also seagrass Posidonia oceanica L. Often A. visited. Samples were preserved in 4% of taxifomis occurred in sympatry with A. formaline in seawater. Recognition of the armata. In these cases the former was found “Falkenbergia-stage” was achieved deeper in the infralittoral zone, although both according to Ní Chualáin et al. (2004), species overlap for a few meters at considering the length and width of one of approximately -6m depth. the three pericentral cells at cells 30, 40 and In October 2007, when gametophytes of 50 from the apex of one branch of twenty A. taxiformis were observed, but no A. specimens. Microscopic samples were armata, Falkenbergia filaments were studied using a microscope Nikon Eclipse collected in Marina del Este (Granada) (fig. E800; photographs were obtained with a 5). Cell length of pericentral cells at cells digital camera Nikon DXM 1200. Identified 30, 40 and 50 from the apex (58,3±9,5mm, 8 M. Altamirano et al.

Figure 1. Gametophytes of Asparagopsis taxiformis. a) Habitat and b) basal stolons and rhizoids (MGC-Phyc 3844).Gametofitos de Asparagopsis taxiformis. a) Hábito y b) estolones basales y rizoides (MGC-Phyc 3844). Asparagopsis taxiformis on Andalusian coasts 9

,-1

-5/-9m

-6/-16m

tamariscifolia

armata

-0,5m -0,5m

armata

Observations

Cystoseira tamariscifolia

bellow

Below

Cystoseira

Coordinates

273382X3991249Y 429754X4066838Y

435502X4065352Y

589055X4079400Y

430941X4066030Y

575921X4065571Y

463645X4062064Y 583817X4072892Y

425108X4068002Y

430254X4066456Y

512704X4061737Y

heads

oductive

Cystocarps

Repr

Spermatangial

3915

3844

3832

3841

3914

3834

3851

3852

3843

3840

3930

3855

3835

MGC

Phase

tetrasporophyte

1-2005

Collection

28-1

01-03-2006

28-05-2006

07-10-2007

27-08-2006

29-08-2006

30-04-2006

08-04-2006

09-07-2006

21-09-2006

12-12-2007

onym

CÑ

Acr

Natural

N. Cabo de Gata

la Blanca,

Paraje

Calahonda

Gata

N. Cabo de Gata

gantín, P

ejas

Maro,

site

Cabo

N. del Estrecho

Cala del Ber Acantilado de la P Cala Rajá, P Guardias

Acantilado Marina del Este Marina del Este Marina del Este Peñón del Fraile, Paraje Natural de Maro-Cerro Gordo

Playa del Cañuelo, Paraje Natural de Maro Cerro-Gordo Cantarriján

Cala de Maro-Cerro Gordo

Punta del Parque Eólico, P

Sample

Almería

Granada

Málaga

Cádiz

MGC: Málaga University Herbarium record; G: gametophyte;

T 10 M. Altamirano et al.

a FRANCE

SPAIN PORTUGAL Andalusia Mediterranean Sea

Atlantic Ocean Alborán Alborán Island 100 km Strait of Gibraltar Sea AFRICA Chafarinas Islands

Figure 2. a) Location of the study area, Andalusia, in the Iberian Peninsula. b) Distribution of Asparagopsis taxiformis in Andalusia. Black dots show new records with acronym meanings given in Table 1; previous records are shown with white dots with acronyms in italics (PM: Punta de la Mona, Granada, CJ: Cala Rijana, Granada, PP: Punta de la Polacra, Almería). HU: Huelva, SE: Sevilla, CO: Córdoba, JA: Jaén, AL: Almería, GR: Granada, MA: Málaga, CA: Cádiz. a) Localización del área de estudio, Andalucía, en la Península Ibérica. b) Distribución de Asparagopsis taxiformis en Andalucía. Los puntos negros muestran las citas nuevas con los acrónimos de las localidades, cuyos significados se dan en la Tabla 1; las citas anteriores se muestran con puntos blancos y los acrónimos de sus localidades en cursiva (PM: Punta de la Mona, Granada, CJ: Cala Rijana, Granada, PP: Punta de la Polacra, Almería). HU: Huelva, SE: Sevilla, CO: Córdoba, JA: Jaén, AL: Almería, GR: Granada, MA: Málaga, CA: Cádiz.

66,9±8,5mm, 70,3±9,5mm, respectively) (Aplysiidae, Mollusca) were observed (fig. 6) was in the range given by Ní Chualáin feeding on gametophytes of A. taxiformis in et al. (2004) for the A. taxiformis Caribbean Paraje Natural de los Acantilados de Maro- clade, but longer than values provided by Cerro Gordo. these authors for A. armata. Cell width of these cells (20,0±2,7mm, 23,3±3,8mm, 23,0±1,9mm, respectively) (fig. 6) was DISCUSSION intermediate in size between A. armata and A. taxiformis clades reported by Ní Chualáin The present work provides the first et al. (2004). Given these results, we assign records of the exotic invasive seaweed tetrasporophytes found in Granada to Asparagopsis taxiformis from the provinces Falkenbergia hillebrandii on the basis of cell of Málaga and Cádiz, the latter representing biometry differences obtained by Ní the up to date western geographical limit of Chualáin et al. (2004) for cultured isolates. the species in the Mediterranean Sea. We also No tetrasporangia were observed in these report the first record of the tetrasporophyte samples. Tetrasporophytes grew between 0 of this species for Andalusian coasts, as cell and -1,5m depth in sheltered waters, epiphyte size of the filaments were in the ranges of on Halopteris filicina (Grateloup) Kützing, those given by Ní Chualáin et al. (2004) for Corallina officinalis L. and Jania rubens (L.) A. taxiformis tetrasporophytes in culture, Lamouroux. although, it should be necessary to clarify if Sea hares, Aplysia fasciata Poiret differences between both Asparagopsis Asparagopsis taxiformis on Andalusian coasts 11

Figure 3. Spermatangial branches of Asparagopsis taxiformis (MGC-Phyc 3835). Ramas espermatangiales de Asparagopsis taxiformis (MGC-Phyc 3835). species tetrasporophytes obtained in culture sexual reproduction also occurs, as proved remains in wild specimens. The absence of by the presence of gametangia in some of Asparagopsis from the Huelva province the recorded samples. Yet, we cannot state might be related to the sandy conditions of the fulfilling of the complete life-cycle the coastline, where suitable rocky substrata because, although tetrasporophytes were for the establishment of Asparagopsis found, no tetrasporangia could be observed. populations are very scarce. The origin of the Andalusian Recently, A. taxiformis has rapidly populations of A. taxiformis is unknown. A expanded its distribution range along the recent study on the phylogeography of the Andalusian coast. Granada has been reported species has revealed that two genetically as the geographical limit of the species in divergent lineages coexist in the the western Mediterranean until 2004 Mediterranean Sea, which are considered (Ballesteros & Pinedo 2004). One year later biologically distinct but morphologically Asparagopsis was found at the Strait of cryptic species (lineages 2 and 3, Andreakis Gibraltar, approximately 210km to the west. et al. 2007). Following these authors, lineage Prolific vegetative reproduction may explain 2 is distributed in the south of Portugal, the fast dispersal rates of the species, which central Mediterranean coasts and Indo- also exhibits an attaching system consisting Pacific waters; lineage 3 is found in the in basal stolons and rhizoids (Figure 1) Atlantic Ocean and the eastern (Womersley 1996), able to facilitate the Mediterranean coast of Lebanon. Several establishment of the propagules. However, hypotheses have been proposed to explain 12 M. Altamirano et al.

lineage 2 in Faro (Southern Portugal) (Andreakis et al. 2007) suggests that Andalusian populations of A. taxiformis may represent an invasion of the latter lineage into the Atlantic Ocean, probably due to anthropogenic mediated vectors such as ballast water (Flagella et al. 2007), hull’s fouling or entangled propagules in fishing nets or ropes (Sant et al. 1996; Schaffelke & Deane 2005). Furthermore, global warming may have favoured the dispersal of the species in transforming new western habitats physiologically suitable for its survival. However, owing to the special characteristics of Alboran Sea water bodies due to the proximity of the Strait of Gibraltar and the importance of this relatively narrow channel in the introduction of non-indigenous species in the Mediterranean, the hypothesis of an invasion of the Atlantic lineage 3 to our study area cannot be rejected. A recent study on “Falkenbergia-phase” Figure 4. Female gametophyte of Asparagopsis specimens of both species of Asparagopsis taxiformis presenting globular cystocarps (MGC- demonstrated that thermal ranges for Phyc 3855) (arrow shows cystocarps). Gametofito femenino de Asparagopsis taxiformis con tetrasporangial formation differ among cistocarpos globulares (MGC-Phyc 3855) (la isolates collected from different regions of flecha muestra los cistocarpos). the world (Ní Chualáin et al. 2004). Our tetrasporophytes were not reproductive at 20 the existence of these two A. taxiformis ºC (water temperature at the collecting time), lineages in the Mediterranean Sea, related to which may fit our samples to the thermal immigration and invasions at different time limits of Caribbean, Japanese or Italian scales. A recent invasion through the Suez Falkenbergia isolates (Ní Chualáin et al. Canal has been suggested for both of them, 2004). This observation increases the debate although a more ancient immigration is on the affiliation and origins of Andalusian argued for lineage 3, linked to the reopening populations of A. taxiformis. of the Strait of Gibraltar 5 million years ago Independently of its origin, it remains (Andreakis et al. 2007). The new populations the fact that A. taxiformis was not an of A. taxiformis revealed by this work were Andalusian marine macroalgal resident until not included in the aforementioned studies. recently, yet it has widen its distribution Therefore, the affiliation of our specimens range westerly for more than two hundred to any of the two lineages occurring in the kilometres within few years. In our study Mediterranean Sea or the possibility of an area, the species colonizes protected habitats hybrid origin for the Andalusian A. such as Posidonia oceanica meadows taxiformis remain unclear. However, the (European Union 1992), and forms presence of the Indo-Pacific Mediterranean conspicuously established and self-sustained Asparagopsis taxiformis on Andalusian coasts 13

Figure 5. Tetrasporophyte of Asparagopsis taxiformis, Falkenbergia hillebrandii (MGC-Phyc 3915). Arrow shows pericentral cell at cell number 30 from the apex. Tetrasporofito de Asparagopsis taxiformis, Falkenbergia hillebrandii (MGC-Phyc 3915). La flecha muestra la célula pericentral número 30 desde el ápice. stands in protected zones threatening the spots. Nevertheless, A. taxiformis can be integrity of native Mediterranean marine found at very shallow waters (-0,5m) in other communities. Herein, in accordance to the localities where A. armata is absent. The IUCN Guidelines (The World Conservation dynamics of this competition process Union 2000), we state that A. taxiformis remains unknown. The only presence of A. exhibits an invasive behaviour in Andalusian taxiformis in places where A. armata was coasts. Consequently, in situ studies to present before (de la Rosa & Altamirano, confirm the ecological role and assess the pers. obs.) indicates that there might be impact of the species on the native several distinct stages in the invasive communities are essential as this kind of dynamics of A. taxiformis, when competing records on this invasive species remain with A. armata, in which physiological unknown in the Mediterranean Sea. adaptations, coupling of seasonal growth and In Andalusian coasts Asparagopsis reproductive cycles of both species may play taxiformis is invading localities previously an important role. In these cases, in which invaded by A. armata. The former colonizes A. taxiformis clearly competes with another the same vertical profile and, with the latter, species, the study of the factors determining it shares substratum for a few meters, for the susceptibility of the local communities which both species seem to compete. In these to the invasion attempt, may provide cases A. armata seems to be more competent valuable information on the general at shallower waters than A. taxiformis, as the knowledge of the evolution of the invasion latter remains under A. armata belts at deeper processes in temporal and spatial scales. 14 M. Altamirano et al.

90 ACKNOWLEDGEMENTS. The authors are 80 grateful to Parque Natural del Estrecho, Parque Natural del Cabo de Gata and Paraje Natural de 70 los Acantilados de Maro-Cerro Gordo offices for 60 their support, allowing the access to the sampling 50 sites. This work has been carried out in the m m framework of the projects “Estudio de la Flora

µ 40 µ µ µ µ Ficológica Andaluza” (Consejería de Medio 30 Ambiente de la Junta de Andalucía) and 20 “Modelación de la biodiversidad en Andalucía en 10 un escenario de cambio en el uso del suelo y clima” (P05-RNM-00935) (Consejería de 0 Innovación, Ciencia y Empresa, Junta de 30 40 50 Andalucía). Special thanks to Estibaliz Berecibar Cell number (Faro University, Portugal) for information on A. taxiformis in Portugal, and to the two anonymous reviewers for their useful suggestions. Figure 6. Cell length (shaded bars) and width (white bars) of tetrasporophytes of Asparagopsis taxiformis (Falkenbergia hillebrandii) colleted in REFERENCES Granada, at cell numbers 30, 40 and 50 from the apex. Data are shown as mean value±1SD. Longitud (barras sombreadas) y anchura (barras ALTAMIRANO, M. -1999- Nuevas citas para la blancas) de las células número 30, 40 y 50 desde flora marina del archipiélago de las Islas el ápice de tetrasporofitos de Asparagopsis Chafarinas. Acta Bot. Malacitana 24: 185- taxiformis (Falkenbergia hillebrandii) recogidos 187. en Granada. Los datos se muestran como ANDREAKIS, N., G. PROCACCINI & W.H.C.F. media 1SD. ± KOOISTRA -2004- Asparagopsis taxiformis and Asparagopsis armata (Bonnemaisoniales, Although we have no data on the effects Rhodophyta): genetic and morhological that this invasion is causing on marine identification of Mediterranean populations. Eur. J. Phycol. 39: 273-283. communities of Southern Spain, we have ANDREAKIS, N., G. PROCACCINI, C. observed that the species has a predator, the MAGGS & W.H.C.F. KOOISTRA -2007- sea hare Aplysia fasciata, which has been Phylogeography of the invasive seaweed actively recorded feeding on individuals of Asparagopsis (Bonnemaisoniales, A. taxiformis. Whether this herbivorous is Rhodophyta) reveals cryptic diversity. Mol. able to naturally control the invasion is not Ecol. 16: 2285-2299. entirely clear. Effective biocontrol of BÁEZ, J.C., F. CONDE & A. FLORES-MOYA - macroalgal invasions by herbivores has been 2001- Notas corológicas del macrofitobentos reported before. For example, a local de Andalucía (España). V. Acta Bot. Malacitana 26: 193-196. population of the invasive green algae BALLESTEROS, E. & S. PINEDO -2004- Los Codium fragile ssp. tomentosoides (Van bosques de algas pardas y rojas, in: A.A. Goor) Silva, was diminished in Scotland by Luque et J. Templado (Coords.). Praderas y natural populations of the herbivorous sea bosques marinos de Andalucía, pp. 199-222. slug Placida dentritica Alder and Hancock, Consejería de Medio Ambiente, Junta de which are themselves controlled by water Andalucía, Sevilla, 336 pp. motion (Trowbridge 2002; Harris & Jones BOUDOURESQUE, C.F. & M. VERLAQUE - 2005). However, effective biocontrol may be 2002- Biological pollution in the possible only at the first stages of the Mediterranean Sea: invasive versus introduced macrophytes. Mar. Pol. Bull. 44: invasion process. 32-38. Asparagopsis taxiformis on Andalusian coasts 15

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