Interaction Between the Invasive Macroalga Lophocladia Lallemandii and the Bryozoan Reteporella Grimaldii at Seagrass Meadows: Density and Physiological Responses
Total Page：16
File Type：pdf, Size：1020Kb
Biol Invasions DOI 10.1007/s10530-009-9428-1 ORIGINAL PAPER Interaction between the invasive macroalga Lophocladia lallemandii and the bryozoan Reteporella grimaldii at seagrass meadows: density and physiological responses S. Deudero Æ A. Blanco Æ A. Box Æ G. Mateu-Vicens Æ M. Cabanellas-Reboredo Æ A. Sureda Received: 18 April 2008 / Accepted: 12 January 2009 Ó Springer Science+Business Media B.V. 2009 Abstract Invasive epiphyte Lophocladia lallemandii (-19.30% invaded to -2.84% at noninvaded plots), macroalga induces changes in the erect bryozoan suggesting modification of food sources. Induced shifts Reteporella grimaldii at shallow Posidonia oceanica of a filter-feeding erect bryozoan by dense algal turfs at meadows at a Mediterranean pristine location. invaded seagrasses are demonstrated, highlighting the Bryozoan densities at noninvaded seagrass plots need to further address interaction across natural (88.32 ± 3.11 colonies m-2) are higher than those at communities and alien species invaded systems before invaded plots (13.39 ± 1.09 colonies m-2)witha further cascade effects are driven. fourfold decrease in number of colonies. Activation of enzymatic pathways (catalase, superoxide dismutase, Keywords Bryozoans Á Seagrass Á glutathione peroxidase) and increase in lipid peroxida- Lophocladia lallemandii Á Invasive species Á tion malondialdehyde (MDA) [0.80 ± 0.06 nmol/mg ROS Á Stable isotopes prot at Posidonia oceanica plots to 1.08 ± 0.04 nmol/ mg prot at L. lallemandii (P \ 0.05)] is observed on Abbreviations sessile bryozoans as response to anoxia caused by ROS Oxygen species production L. lallemandii. d13C of bryozoan isotopic composition CAT Catalase differed among treatments, covering a broad range SOD Superoxide dismutase GPx Glutathione peroxidase MDA Malondialdehyde S. Deudero (&) Á A. Blanco Á A. Box Á M. Cabanellas-Reboredo Laboratorio de Biologı´a Marina, Universitat de les Illes Introduction Balears, Ctra. de Valldemossa s/n km. 7.5, 07022 Palma de Mallorca, Illes Balears, Spain e-mail: [email protected] Biological invasions, considered as the introductions of nonnative species, represent a threat to biodiversity G. Mateu-Vicens and ecosystem functioning (Bax et al. 2003; Galil Departament de Cie`ncies de la Terra, Universitat de les Illes Balears, Ctra. de Valldemossa s/n km. 7.5, 2007). Studies on the effects of invasive species on 07022 Palma de Mallorca, Illes Balears, Spain native biota report either a facilitation interaction among invaders (Parker et al. 2006) or a ‘‘biotic A. Sureda resistance’’ (sensu Elton 1958; Britton-Simmons Laboratori de Cie`ncies de l’Activitat Fı´sica, Universitat de les Illes Balears, Ctra. de Valldemossa s/n km. 7.5, 2006). Biotic interactions between native and intro- 07022 Palma de Mallorca, Illes Balears, Spain duced species are often inferred from correlational 123 S. Deudero et al. evidence (Scheibling and Anthony 2001) and exper- et al. 2001; Ben Mustapha et al. 2002). Reteporella imental testing (Scheibling and Gagnon 2006). grimaldii (Jullien in Jullien and Calvet 1903) is a Competitive exclusion by invasive species has been Cheilostomata bryozoan from the Phidoloporidae reported as a cause of the progressive regression of family morphologically described as a convoluted seagrasses (Williams 2007). Seagrasses are very compact three-dimensional colony spreading up to sensitive to environmental degradation and physical 40 mm in length and 80 mm horizontally, forming disturbances (Hemminga and Duarte 2000). anastomoses defining funnels (Hayward and Ryland The endemic Posidonia oceanica (L.) Delile is the 1996). Coevolution of faunal assemblages at seag- most widespread seagrass species in the Mediterranean rasses dates back to the Cretaceous (Ivany et al. Sea. Nowadays, more than 60 species of macrophytes 1990) including the cheilostomate bryozoan such as have been introduced in the Mediterranean Sea (Bou- R. grimaldii (Voigt 1981), which is coeval with the douresque and Verlaque 2002), inducing community first documented occurrence of the genus Posidonia shifts (Piazzi and Balata 2008a). The red algae (P. cretacea) (Boudouresque and Jeudy de Grissac Lophocladia lallemandii (Montagne) F. Schmitz is 1983). Therefore, epibionts and seagrasses have widespread throughout the tropics and subtropics and coevolved since the end of the Mesozoic, which has is considered an alien species in the Mediterranean, conduced to highly adapted biocenosis with complex being probably introduced via Suez Channel (Bou- interactions with the substrate and among the differ- douresque and Verlaque 2002). L. lallemandii grows ent organisms forming such communities. Nowadays, on a wide range of substrates (bare bedrocks, rocky the appearance of erect bryozoans such as R. grimal- macroalgae bottoms, Posidonia oceanica seagrass dii on rocky bottom meadows (Reverter-Gil and meadows, and over coralligenous communities; Bal- Ferna´ndez-Pulpeiro 1999) and in association with the lesteros 2006). L. lallemandii displays a particular seagrass rhizomes (Ben Mustapha et al. 2002, Heß pattern of invasion in P. oceanica meadows (Ballest- 2004) has been documented. eros et al. 2007). The alga initially settles on rhizomes Bryozoan colonies are considered good indicators and occasionally settles over old leaves, growing as an reflecting changing environmental conditions (Elia epiphyte, and finally completely overgrows the ben- et al. 2007). Since the invasive macroalgae Lophocl- thic communities. L. lallemandii invasion induces a adia lallemandii is capable of growth over all types decrease in size and weight of the seagrass shoots, leaf of substrates, including sessile invertebrates, it can chlorosis, leaf necrosis, and shoot death of P. oceanica potentially induce a shift in regimen fluxes for sessile plants (Ballesteros et al. 2007). The development of organisms such as bryozoans. Therefore, evaluation turfs, which occurs widely in western Mediterranean of bryozoan’s physiological responses to oxygen seagrass beds, seems to modify strongly the structure depletion and flux modification due to epiphytism can of macroalgal assemblages of rhizomes, mostly via the be quantified by determination of antioxidant decrease in species and functional diversity (Piazzi defenses. It is known that oxidative stress results et al. 2002). The modification of the microhabitat from the disruption of cellular homeostasis of reac- characteristics of the seagrass beds induced by the tive oxygen species (ROS) production (Halliwell and presence of L. lallemandii translated into a decrease in Gutteridge 1999). Overproduction of ROS causes cell size and weight of the canopy and also affects the damage through oxidation of membrane lipids, faunal communities associated to the seagrasses nucleic acids, and proteins (Imlay and Linn 1998; (Patzner 1998). Collen et al. 2003; Li et al. 2006). To counteract Among several species Posidonia oceanica com- these ROS damaging effects, the organisms have munities include primary producers such as developed efficient defense systems in scavenging of codiacean and red algae and several faunal taxa cellular ROS (Elias et al. 1999). These protective epibionts (bryozoans, cnidarians, foraminifers, poly- mechanisms involve a number of antioxidant chaetes, sponges, etc.) and vagile biota (echinoderms, enzymes such as catalase (CAT), superoxide dismu- crustaceans, molluscs, fish; Templado et al. 2004). tase (SOD), and glutathione peroxidase (GPx). The Seagrass-associated faunal communities encompass antioxidant defense adaptation against ROS is crucial many taxonomic groups, including few bryozoans for the survival of organism under stressful condi- species (Trautman and Borowitzka 1999; Bonhomme tions. Several reports have shown a tight association 123 Interaction of invasive Lophocladia with endemic Reteporella between antioxidant capacity and the presence of W Mediterranean; 39°340N–2°200E). Sa Dragonera alien competing species (Sureda et al. 2006, 2007). Island was declared a protected area in 1995 in con- Nevertheless, studies about the effects of L. lall- sideration of its biodiversity, natural, and pristine emandii on the antioxidant defenses of invertebrates characteristics. The sampling design was set by are lacking. choosing three sites over Posidonia oceanica mead- Another useful tool to determine the energy ows and over P. oceanica seagrass meadows sources and the functioning of the coastal food webs epiphyted by the algae Lophocladia lallemandii. at altered ecosystems is the analysis of isotopes ratios There were invaded and noninvaded seagrass mead- of carbon and nitrogen (13dC and 15dN) (Davenport ows within each of the three sites. At each site eight and Bax 2002; Smit et al. 2006; Le Loc’h F Hily and linear transects (20 m length 9 1 m wide) were laid Grall 2007). Comparison of isotopes ratios from the down by scuba diving, and at each transect ten plots bryozoan of invaded meadows and bryozoans of of 40 9 40 cm polyvinylchloride (PVC) were ran- noninvaded meadows give clues about potential shifts domly displayed in order to quantify total abundances in food sources at filtering sedentary species (Riera of Reteporella grimaldii colonies; therefore a total 2007). Most isotopic studies of bryozoan community 480 plots were quantified for bryozoan densities were related with paleoenvironmental and climate determination. The sites were separated by hundreds change (Brenchley et al. 2006), and only a few of meters and the distance among noninvaded and address partly contributions of isotopes ratios