Study of the crustacean community associated to the invasive seaweed Asparagopsis armata Harvey, 1855 along the coast of the Iberian Peninsula.

Zool. baetica, 22: 33-49, 2011 Study of the crustacean community associated to the invasive seaweed Asparagopsis armata Harvey, 1855 along the coast of the Iberian Peninsula Estudio de la comunidad de crustáceos asociados al alga invasora Asparagopsis armata Harvey, 1855 del litoral de la Península Ibérica M. M. SOLER-HURTADO & J. M. GUERRA-GARCÍA Laboratorio de Biología Marina, Departamento de Fisiología y Zoología, Facultad de Biología, Universidad de Sevilla, Avenida de Reina Mercedes 6, 41012, Sevilla (Spain). Fax: 0034954233480; E-mail: mar.s.hur[email protected] Corresponding autor: JMGG (jmguer[email protected]) Recibido el 1 de octubre de 2010. Aceptado el 10 de noviembre de 2010. ISSN: 1130-4251 (2011), vol. 22, 33-49 Key words: Asparagopsis armata, invasive species, peracarids, Crustacea, Gammaridea, Caprellidea, Isopoda, Tanaidacea, Decapoda. Palabras clave: Asparagopsis armata, especie invasora, peracáridos, Crustacea, Gammaridea, Caprellidea, Isopoda, Tanaidacea, Decapoda. ABSTRACT We studied the community of crustaceans associated to the seaweed Asparagopsis armata along the coast of the Iberian Peninsula. Nineteen stations were selected along the Cantabrian, Atlantic and Mediterranean coast. In the intertidal, five physicochemical parameters (temperature, dissolved oxygen, salinity, pH and turbidity) were measured at each station; algae samples were collected (three replicates of 20x20 cm), and its coverage was estimated (five grids of 50x50 cm). Crustaceans were the dominant group (over 80% in number of specimens) followed by annelids, molluscs and echinoderms. We identified a total of 60 crustacean species (38 gammarids, seven caprellids, nine isopods, four decapods and two tanaids). The caprellids and gammarids were dominant in number. Although univariate analysis showed no significant differences regarding the number of species, abundance, diversity and evenness of Pielou among stations, the multivariate analysis showed different species composition. According to the canonical correspondence analysis, the biomass of algae, as well as the oxygen concentration, pH and salinity were the variables that best explained the distribution of species. The number of crustacean species found Zool. baetica, 22: 33-49, 2011 M. M. SOLER-HURTADO & J. M. GUERRA-GARCÍA 34 on A. armata in this study is similar to that recorded in the literature for other native algae. RESUMEN Se estudió la comunidad de crustáceos asociados al alga Asparagopsis armata en el litoral de la península Ibérica. Se seleccionaron un total de 19 estaciones situadas a lo largo de toda la costa cantábrica, atlántica y mediterránea En cada estación se midieron cinco parámetros fisicoquímicos (temperatura, oxígeno disuelto, salinidad, pH y turbidez), se recolectaron muestras del alga (tres réplicas de 20x20 cm), y se estimó su cobertura (cinco cuadrículas de 50x50 cm) en el intermareal. Los crustáceos fueron el grupo dominante (más del 80% en número de individuos), seguido de anélidos, moluscos y equinodermos. Se identificaron 60 especies de crustáceos (38 gammáridos, siete caprélidos, nueve isópodos, cuatro decápodos y dos tanaidáceos). Los gammáridos y los caprélidos fueron dominantes en número. Aunque los análisis univariantes no reflejaron diferencias significativas en el número de especies, abundancia, diversidad de Shannon y equitatividad de Pielou entre las distintas estaciones, los multivariantes mostraron diferencias en la composición de especies. Según el análisis canónico de correspondencias, la biomasa de alga, la concentración de oxígeno, el pH y la salinidad fueron las variables que mejor explicaron la distribución de las especies. El número de especies de crustáceos encontrado sobre A. armata en este estudio es similar a los registrados en la literatura para otras algas autóctonas. INTRODUCTION The morphology of the genus Asparagopsis (Bonnemaisoniales, Rhodophyta) (Bonin & Hawkes, 1987), its life cycle (Chihara, 1961, 1962), its cytology (Svedelius, 1933) and its physiology (Oza, 1977; Guiry & Dawes, 1992) have been well studied. Asparagopsis armata is endemic to the southern hemisphere and native from Australia, including Tasmania and New Zealand; it was introduced into the Atlantic and Mediterranean in the 1920s (Feldmann & Feldmann, 1942). It has spread out in short time, colonizing a wide area of the Mediterranean, displacing native species and causing a drastic change in endemic marine communities. The successful dispersal and establishment of this alga seems to lie in the strategy it adopts to fend off herbivores, releasing caulerpina. This makes many herbivores to reject it, similarly to the defence system used by other red algae, which are indigestible to indigenous fish. Asparagopsis armata is mainly found in the low intertidal zone (Fa et al., 1997), extending to the first meters of the subtidal zone. Intertidal ecosystems represent areas where various parameters define an environment Zool. baetica, 22: 33-49, 2011 CRUSTACEAN COMMUNITY ASSOCIATED TO A. ARMATA 35 subjected to sudden changes in a small spatial and temporal scale. These factors are further modified by regular events (for example, tides) and stochastic (such as wave action). There are few studies on fauna associated to algae along the Iberian Peninsula; it is probably due to the complexity of separation and identification of samples and the great dedication that it requires. We can highlight the study of Sanchez-Moyano (1996), Sánchez-Moyano & García-Gómez (1998) and Sánchez-Moyano et al. (2000a, 2000b, 2001, 2002, 2007) on the animal communities associated to Caulerpa prolifera (Forsskål) Lamouroux and Stypocaulon scoparium (L.) Kützing., and the study of Guerra-García et al. (2009) on the diversity and biogeography of peracaridean crustacea associated to Corallina elongata in the Strait of Gibraltar. These contributions focused on the description of the epiphytic fauna are focused in order to characterize the overall diversity of the marine ecosystems and to understand patterns of distribution and abundance of organisms. Moreover, invertebrate communities associated to algae reflect the environmental characteristics of the area and they can be used as indicators of the quality of water (Guerra-García & García-Gómez, 2001). Crustaceans are one of the dominant groups of macrofauna associated to macroalgae at rocky substrates, especially in the intertidal zone (Lewis, 1987). Their abundance and diversity depend mainly on factors such as interactions with predators (Caine, 1980), wave exposure and habitat complexity (Guerra-Garcia, 2001) as well as the diversity of resources and the physiological tolerance range to the environmental physicochemical conditions in which they live. The dispersal ability of the peracarid crustacean is low compared to other crustaceans, such as decapods (Lopes et al., 1993). They have direct development (Thiel & Vásquez, 2000) and lack pelagic larval stage, which could be considered relevant for displacement over long distances along the ocean. On the other hand, the abundance and distribution of peracarid crustaceans present in rocky coastlines are also influenced by the shape and morphological complexity of the host algae (Guerra-García, 2001). Peracarid crustaceans are a food source for fish and birds in marine environments, and for fish, birds, amphibians and insects in freshwater environments. They are also widely used as a bioindicator and in toxicology studies. Marine algae are known to provide habitats for a wide range of animal species (Pereira et al., 2006). This study contributes to our understanding of the factors which determine the distribution of Asparagopsis armata in the Iberian Peninsula, and the impact that this algae might have on the macroinvertebrate fauna, especially crustaceans. The main objectives of the present study are: (1) to describe the crustacean fauna associated to A. armata and its pattern of abundance and distribution; (2) to quantify the coverage and biomass of A. armata at the Zool. baetica, 22: 33-49, 2011 M. M. SOLER-HURTADO & J. M. GUERRA-GARCÍA 36 stations selected; (3) to explore the relationships between the fauna associated to algae A. armata with physical-chemical environmental variables as water temperature, conductivity, pH, oxygen and biomass of the algae itself. MATERIALS AND METHODS The study area covered the entire coast of the Iberian Peninsula. Sampling was carried out in the summer of 2008 (from 5 July to 5 August); it was conducted in the intertidal zone and gametophyte phase of A. armata was collected at low tide. Nineteen stations were selected along the north and south coasts of Spain and Portugal (Figure 1). The alga was present Fig. 1.—Sampling stations along the Iberian Peninsula. White circles indicate stations where A. armata was not present. (1) Ogella; (2) Oyambre; (3) Cetarea; (4) Cabo Silleiro; (5) Playa Azul; (6) Labruge; (7) Castelo; (8) Bolonia; (9) Tarifa; (10) Torreguadiaro; (11) Cerro Gordo-Herradura. Fig. 1.—Estaciones de muestreos a lo largo de la Península Ibérica. Los círculos blancos indican las estaciones en las que A. armata no estuvo presente. (1) Ogella; (2) Oyambre; (3) Cetarea; (4) Cabo Silleiro; (5) Playa Azul; (6) Labruge; (7) Castelo; (8) Bolonia; (9) Tarifa; (10) Torreguadiaro; (11) Cerro Gordo-Herradura. Zool. baetica, 22: 33-49, 2011 CRUSTACEAN COMMUNITY ASSOCIATED TO A. ARMATA 37 in the Cantabrian and Portuguese coasts and in the Strait of Gibraltar, but it was not found in the Mediterranean stations sampled. Natural rocky shores with low anthropogenic influence were selected to prevent that the natural biogeographic patterns could be affected by the effects of pollution, tourism or other human activities. We selected sites with the same degree of exposure and orientation. Regarding to the environmental parameters, pH and salinity were measured in each station with a probe CRISON MM40, temperature and oxygen concentration with a probe OXI 45 P, and turbidity with a portable turbidimeter WTW 355 IR. Details of measures can be found in Guerra-García & Izquierdo (2010). We conducted a total of three measures and calculated the mean and standard deviation for each sampling point. At each station, A. armata was collected with a grid of 20 x 20 cm by scraping. We selected three replicates per station in order to avoid the effect of aggregation and to cover the maximum potential diversity of crustaceans. The samples (macrofauna associated and algae) were bagged and preserved in 70% ethanol. To estimate the coverage of algae at each station, we used 0,5 x 0,5 m subdivided into 25 units of 0.1 x 0.1. At each unit, we scored the presence or absence of A. armata from a total of five replicates. In the laboratory, samples were sieved through a mesh size of 0.5 mm, and all fauna of the alga was sorted and identified at the level of large groups: crustaceans (amphipods, isopods, tanaids and decapods), echinoderms (ophiuroids, echinoids, asteroids and crinoids), molluscs (gastropods, bivalves and polyplacophoran) and annelida (polychaetes and oligochaetes). Crustaceans were identified to species level. The volume of each algal sample was estimated measuring the water displaced by the algae in a test tube. After the volume had been measured we obtained the dry weight of the samples (after 24 hours at 70 º C). The total number of species, the Shannon–Weiner diversity index (Shannon & Weaver, 1963), and Pielou’s evenness index (Pielou, 1966) were calculated for each station. Any differences between seasons were tested with ANOVA checked for normality with the Kolmogorov-Smirnov test, and homogeneity of variances with the Levene test. The affinities among stations based on the peracarid species were established by cluster analysis using UPGMA (unweighted pair group method using arithmetic averages). A multivariate canonical correspondence analysis (CCA) was also conducted to explore relationships among crustacean species, cover of A. armata and environmental measures. Zool. baetica, 22: 33-49, 2011 M. M. SOLER-HURTADO & J. M. GUERRA-GARCÍA 38 RESULTS Biomass of Asparagopsis armata was similar through the stations, while higher covers of the algae were found in stations located in the Strait of Gibraltar zone (Figure 2). Details of physicochemical data of each station are detailed in Guerra-García and Izquierdo (2010). Crustaceans (identified to species level in this study) were the most abundant group of associated macrofauna compared to echinoderms, molluscs and annelids (Figure 3). Sixty crustacean species were collected (38 gammarids, 7 caprellids, 9 isopods, 4 decapods and 2 tanaid) (Table I). The most common species collected during the present study were the gammarids Hyale schmidtii (1469 ind/m2), Hyale pontica (262 ind/m2), Aora spinicornis (136 ind./m2) and Apherusa bispinosa (105 ind/m2); the caprellids Caprella penantis (4564 ind/m2) Caprella liparotensis (98 ind/m2); the isopod Dynamene magnitorata (18 ind./m2) and the tanaid Tanais dulongii (25 ind/m2). Amphipod was the dominant group in all the stations; gammarids were more abundant in the Atlantic stations, while caprellids showed high Fig. 2.—Cover (%) and biomass (g/m2) of A. armata at each sampling station. Fig. 2.—Cobertura (%) y biomasa (g/m2) de A. armata en cada estación de muestreo. Zool. baetica, 22: 33-49, 2011 CRUSTACEAN COMMUNITY ASSOCIATED TO A. ARMATA 39 Fig. 3.—Contribution of each macrofaunal group to the total abundance per station. Fig. 3.—Contribución de cada grupo de macrofauna a la abundancia total en cada estación. densities around the Strait of Gibraltar and stations with Mediterranean influence (Figure 4). The number of species was similar in all stations, although it was a trend of decrease from Atlantic to Mediterranean stations (Figure 4). The highest abundance was measured in station 6, due to the high density of the caprellid Caprella penantis. Shannon diversity index and Pielou evenness were lower at stations 6, 9 and 10, showing maximum values in stations 7 (Figure 5). However, according to the results of the ANOVA, regardless of the identity of the species, no significant differences in species richness, abundance, diversity and evenness among stations were found (Species richness: F=1.8, p=0.2; Abundance: F=0.4, p=0.6; Diversity (H’): F=1.4, p=0.2; Evenness (J): F=1.1, p=0.4). Regarding with the multivariate analysis, cluster showed a different crustacean composition in stations 9, 10, 11 with Mediterranean influence (Figure 6). Axis 1 of the CCA (Figure 7, Table II) explained almost 30% of the variance of the data and negatively correlated with biomass of A. armata and salinity. Atlantic stations 1-5 were mainly influenced by higher Zool. baetica, 22: 33-49, 2011 M. M. SOLER-HURTADO & J. M. GUERRA-GARCÍA 40 Table I.—Abundance of crustacean species associated to A. armata (ind/ m2) in the eleven stations studied. Tabla I.—Abundancia de las especies de crustáceas asociadas a A. armata (ind/ m2) en las once estaciones estudiadas. 1234567891011 AMPHIPODA Caprellidea Caprella acanthifera Leach, 1814 --8---91 8 -50 841 Caprella danilevskii Czerniavskii, 1868 --16 33 --41 375 --- Caprella grandimana Mayer, 1882 ---------8Caprella hirsuta Mayer, 1890 ---------358 - Caprella liparotensis Haller, 1879 -------91 -683 300 Caprella penantis Leach, 1814 125 531 8 33 866 31800 108 50 6933 9750 - Pseudoprotella phasma Montagu, 1804 ----------8 Gammaridea Ampelisca serraticuada Chevreux, 1888 -------8--- Amphilochus neapolinatus Della Valle, 1893 ---25 -16 ----- Ampithoe ferox (Chevreux, 1902) --------25 -133 Ampithoe gammaroides (Bate, 1856) -325 -------- Ampithoe neglecta Lincoln, 1976 -3-16 -41 ----- Ampithoe ramondi Audouin, 1826 -----150 8 --16 8 Aora spinicornis Lincoln, 1976 100 64 125 558 458 41 83 ---66 Apherusa bispinosa (Bate, 1857) -6 133 275 383 141 175 41 --- Apherusa chiereghinii Giordani-Soika, 1950 --------41 -- Apherusa mediterranea Chevreux, 1911 --------116 -- Apherusa ovalipes Norman & Scott, 1906 ------66 16 --- Apocorophium acutum (Chevreux, 1908) -------33 --- Dexamine spiniventris (Costa, 1853) 41 52 108 458 191 58 116 50 -88 Dexamine spinosa (Montagu, 1813) --41 -------- Echinogammarus sp. --16 -------- Elasmopus pocillimanus (Bate, 1862) -------166 33 50 33 Elasmopus rapax Costa, 1853 85--8------ Elasmopus sp. ------16 ---- Elasmopus vachoni Mateus & Mateus, 1966 ----33 316 --91 -16 Gammaropsis maculata (Johnston, 1828) -------8--16 Hyale nilssoni (Rathke, 1843) -121 16 25 0 75 ----- Hyale perieri (Lucas, 1849) --------16 -- Hyale pontica Rathke, 1837 433 769 1183 341 158 ------ Hyale schmidtii (Heller, 1866) 116 938 1266 2116 4116 3200 150 983 2066 1075 133 Hyale sp. --------8-- Zool. baetica, 22: 33-49, 2011 CRUSTACEAN COMMUNITY ASSOCIATED TO A. ARMATA 41 Jassa dentex Chevreux & Fage, 1925 16 24 --------- Jassa marmorata Holmes, 1903 -25 --8975 -- 16 8 - Jassa sp1. 25 17 --------- Jassa sp2. --25 -------- Leptocheirus guttatus (Grube, 1864) ----8--8--- Maera inaequipes (Costa, 1857) ---------- 91 Melita bulla Karaman 1978 --------8-- Microdeutopus chelifer (Bate, 1862) ---16 -25 ----- Parajassa pelagica Leach, 1814 827 ---0----- Podocerus varigeatus Leach, 1814 -9-41 58 625 -8--- Stenothoe gallensis Walker, 1904 --------- 141 41 Stenothoe monoculoides (Montagu, 1813) ---175 33 725 41 ---- Stenothoe sp. 85 --------- ISOPODA Cymodoce truncata Leach, 1814 16 11 --8------ Dynamene magnitorata Holdich, 1968 33 23 66 25 -16 8 16 -8Dynamene torellidae Holdich, 1968 ---41 --8---- Idotea pelagica Leach, 1815 -3--------- Jaeropsis brevicornis Koehler, 1855 -----8----- Paranthura costana Bate & Westwood, 1868 33 26 50 ----16 16 -- Synisoma acuminatum (Leach, 1815) -------016 -- Synisoma capito (Rathke, 1837) ------- 16 --- Synisoma lancifer (Miers, 1881) ----33 ------ TANAIDACEA Leptochelia dubia (Krøyer, 1842) ------8---- Tanais dulongii (Audouin, 1826) 100 71 -8-5888-88 DECAPODA Acanthonyx lunulatus (Risso, 1816) ---------8Hipolyte sp. -------8--- Pilumnus hirtellus Linnaeus, 1758 ----------16 Thoralus cranchii (Leach, 1817) 16 11 -50 ------- Table I.—(Continued). 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