Caprellid assemblages (Crustacea: Amphipoda) in shallow waters invaded by <Emphasis Type="Italic">Caulerpa racemosa</Emphasis> var. <Emphasis Type="Italic">cylindracea</Emphasis> from southeastern Spain

Growth of the invasive algae Caulerpa racemosa var. cylindracea in shallow habitats may influence the faunal assemblage composition. We studied its effects on caprellid assemblages associated with shallow-water habitats of hard and soft bottoms from the SE Iberian Peninsula (native rocky-bottom algae, C. racemosa from hard and soft bottoms, and Caulerpa prolifera, Cymodocea nodosa and Posidonia oceanica from soft bottoms). Samples were taken in two different sampling periods (September 2004 and March 2005). A total of seven caprellid species were identified, with important differences in their distribution in different habitats. Total abundance of caprellids was very high in March on native algae on hard bottoms, and on C. racemosa on both soft and hard bottoms. On both hard and soft bottoms, abundances of Caprella hirsuta recorded from C. racemosa were low. On the other hand, a higher abundance of other species, namely C. acanthifera, C. santosrosai, Phtisica marina and Pseudoprotella phasma, was recorded from C. racemosa. The results indicate that C. racemosa may have a positive influence on some caprellid species, while seasonal changes are also evident. It is concluded that introduced C. racemosa may serve as a new habitat, promoting and maintaining caprellid populations in shallow Mediterranean habitats.     

The indirect role of nutrients in enhancing the invasion of Caulerpa racemosa var cylindracea

The effects of nutrients dynamics on biological invasions in marine habitats have not been fully investigated. The present study aimed to evaluate the role of nutrient pollution in determining the successful invasion of the introduced seaweed Caulerpa racemosa var. cylindracea in a Mediterranean subtidal rocky habitat. To this end, a manipulative field experiment was carried out by supplying the water column with nutrients for a one-year period. Afterwards C. racemosa was transplanted in both nutrient-enriched and control macroalgal assemblages. Results showed that the penetration and biomass of C. racemosa in the assemblages previously treated with nutrients were higher than in control ones, indicating that communities stressed by nutrient pollution are more vulnerable to invasion. The nutrient enrichment changed the structure of natural macroalgal assemblages, mainly by encouraging the growth of turf species. No significant effects were detected for the erect and prostrate layers and for the number of species, suggesting that the susceptibility of the community to invasion may depend more on the morpho-functional identity of macroalgae rather than on the diversity of assemblages. Changes in the availability of seawater nutrients may foster the spread of C. racemosa, both by enhancing its growth and eroding the natural resistance of macroalgal assemblages. Thus, the maintenance of good water quality may play an important role in containing both C. racemosa and other introduced seaweeds.     

Effects of <Emphasis Type="Italic">Caulerpa racemosa</Emphasis> invasion on soft-bottom assemblages in the Western Mediterranean Sea

The present study aimed at evaluating the effects of Caulerpa racemosa var. cylindracea spread on Mediterranean soft-bottom assemblages. The benthic assemblages colonized by C. racemosa were compared with non invaded assemblages at multiple spatial scales. In addition, a manipulative experiment has been conducted over a one-year period in order to compare the structure of native assemblages invaded by the alga with others where the alga has been manually removed and others that were not invaded. Results of both studies showed that Mediterranean soft-bottom assemblages invaded by C. racemosa differed from non invaded ones in terms of species composition, abundance and patterns of spatial variability. Moreover, in areas cleaned out from the alga, the benthic assemblages begin to recover their structure and after one year they get more similar to the assemblages observed in non invaded areas. The present paper, taking into account different aspects of C. racemosa invasion in Mediterranean soft bottoms, highlighted that the observed increase in alpha diversity did not correspond to an increase in the overall diversity of the studied system. Infact, the loss of beta diversity in invaded sites, together with the spread of species typical of vegetated habitats, may contribute to a homogenization of the Mediterranean coastal system. Furthermore, a possible role of ecosystem engineer for C. racemosa can be hypothesized.     

New features in the vegetative and reproductive morphology of Cystoclonium purpureum (Cystocloniaceae,Rhodophyta) from the North Atlantic Ocean

The aim of this study was to evaluate whether the success of invasive Caulerpa cylindracea (Caulerpa racemosa var. cylindracea) in Mediterranean habitats may be linked to particular nutritional requirements and/or nutrient accumulation/reallocation dynamics within the algal thallus. To this end, a manipulative field experiment was carried out transplanting C. cylindracea and supplying nutrients to subtidal rocky macroalgal assemblages. Morphological features of C. cylindracea were measured, while percentage cover and tissue nitrogen, carbon and phosphorus were determined for C. cylindracea and two co-occurring species (the introduced Laurencia chondrioides and native Flabellia petiolata) in nutrient-enriched and unenriched conditions. Growth of C. cylindracea was greater in the nutrient-enriched plots while no effect of nutrient enrichment was detected in co-occurring macroalgae. A particularly high requirement for nitrogen has been observed in C. cylindracea, but without severe N-limitation, while a general nutritional state of P-limitation was detected in both invasive and co-occurring macroalgae. The absence of inhibition in hypertrophic conditions and under high levels of ammonia together with a strong uptake and quick reallocation of nutrients within the coenocytic thallus probably represent the main advantages over the other co-occurring species which could explain part of the success of C. cylindracea in the Mediterranean Sea.     

<Emphasis Type="Italic">Caulerpa racemosa</Emphasis> var. <Emphasis Type="Italic">cylindracea</Emphasis> as a potential source of organic matter for benthic consumers: evidences from a stable isotope analysis

Caulerpa racemosa var. cylindracea has been invading various types of substrates in wide areas throughout the Mediterranean Sea. However, the effects of the distribution of this alga on zoobenthos are scanty. The aim of this study was to evaluate the effects of C. racemosa invasion on the feeding habits of some zoobenthic taxa inhabiting the upper infralittoral rocky shores. This was done by identifying the isotopic N and C ratios of several potential food sources and testing differences in isotope composition among the taxa collected from areas invaded and not-invaded areas by C. racemosa. Results suggest that C. racemosa detritus was a significant food source for the polychaete Syllis prolifera, the gammarid Corophium sextonae and the gastropods Cerithium rupestre and Pisinna glabrata. They would also suggest that stable carbon and nitrogen isotope ratios deserve further attention as a possible valuable approach to understand the overall effect of C. racemosa spread on the trophic interactions among the species.     

Impact of Caulerpa taxifolia colonization on the littoral ichthyofauna of North-Western Mediterranean sea: preliminary results

After its accidental introduction in the French waters of the Mediterranean, the green seaweed Caulerpa taxifolia is now spreading along the coast of the Alpes-Maritimes, invading various biotopes (rock, sand and Posidonia oceanica seagrass beds). During the spring and fall of 1992, we evaluated the impact of C. taxifolia on the infralittoral ichthyofauna of Cap Martin (Menton) and compared invaded and reference sites, in shallow (3–8 m) and deep (11–25 m) stations. Caulerpa taxifolia apparently does not have any effect on the composition and global species richness of the ichthyofauna. Therefore, no exclusion phenomenon has been observed and fish behavior has remained normal (feeding habits, reproduction, recruitment). However, fish density and biomass are slightly lower in the colonized sites. Negative regression was observed, in shallow sites during the spring season, between the percentage of substrate invaded by C. taxifolia and the average density of fish assemblages (slope= –0.13, r=0.26, p<0.01). Despite these observations, C. taxifolia meadows seem to be a favorable environment for the recruitment of some species of Labridae (Coris julis, Symphodus ocellatus), Sparidae (Diplodus annularis) and Serranidae (Serranus cabrilla) in the fall.The relative importance of C. taxifolia as environmental parameter and of other habitat characteristics (structural complexity, substrate slope, hydrodynamism, depth, fishing pressure) is discussed to explain these differences. The results of this first study indicate that there exists no simple relation between the presence of C. taxifolia and fish assemblages.     

Illegal trawling and induced invasive algal spread as collaborative factors in a Posidonia oceanica meadow degradation

Posidonia oceanica, a key seagrass species of the Mediterranean Sea, shows clear signs of regression throughout the Mediterranean and illegal trawling is recognized as one of the main causes. We examined the condition of a P. oceanica meadow in Alykes Bay (Zakynthos Island, western Greece), a typical Mediterranean littoral area where illegal trawling is common practice, in respect to the total area affected, and in terms of possible ecological substitution. A side scan sonar (SSS) survey of the seafloor provided an image of the condition of the meadow and biological sampling evaluated the ecological status in affected meadow areas. SSS images revealed that trawling has a serious effect on the meadow, with 11% of the vegetated area being abraded, and the affected areas were also found to be fully colonized by the invasive alga Caulerpa racemosa. Moreover, unusually high densities of the polychaete Sabella pavonina were detected in the affected areas among C. racemosa fronds. Recolonization by P. oceanica of the affected meadow areas that have been colonized by C. racemosa seems improbable considering the allelopathic interactions between the species, with the alga displaying phytotoxic properties through caulerpenyne production and deterioration of the sediment quality.     

Comparative study of the growth of the two co-occurring introduced green algae Caulerpa taxifolia and Caulerpa racemosa along the Tuscan coast (Italy,western Mediterranean)

Caulerpa taxifolia and C. racemosa are tropical green algae now found in the Mediterranean, where the former was accidentally introduced and the latter presumably also introduced; both species have spread rapidly and invaded a variety of habitats. Since 1996, the two algae have co-inhabited a region along the Tuscan coast near Livorno. The present study has been carried out to evaluate the invasive capacity of the two species. After one year, the increase in surface area was 67.5 % for C. taxifolia and 284.8 % for C. racemosa, while the increase in patch number was 11.4 % and 121.4 % respectively. The stolon growth of the two algae followed a similar trend, as is showing the same temporal variations with the maximum growth rate between August and October. At the end of the study period, the increase in stolon length and number was significantly higher in C. racemosa than in C. taxifolia. The results of the present study show a higher invasive potential in C. racemosa than in C. taxifolia, although further studies are necessary to evaluate the competition between the two algae and the effect of their simultaneous presence on the benthic community.     

Habitat heterogeneity promotes the coexistence of exotic seaweeds

Despite the progressive accumulation of exotic species in natural communities, little effort has been devoted to elucidating the mechanisms underpinning the coexistence of invaders in environmentally and biologically heterogeneous systems. The exotic seaweeds, Asparagopsis taxiformis and Caulerpa racemosa, exhibit a segregated distribution on Mediterranean rocky reefs. A. taxiformis dominates assemblages in topographically complex habitats, but is virtually absent on homogenous platforms. In contrast, C. racemosa achieves extensive cover in both types of habitat. We assessed whether differences in their distribution were generated by biotic interactions (between invaders and/or between invaders and natives) or by environmental constraints. Three models were proposed to explain seaweed distribution patterns: (1) invaders inhibit one another; (2) native assemblages, differing between complex and simple habitats, prevent the establishment/spread of one invader, but not that of the other; and (3) environmental conditions regulate the establishment/persistence of the seaweeds in different habitats. We removed the dominant invader and resident assemblages in each type of habitat. Moreover, A. taxiformis thalli were transplanted into the habitat dominated by C. racemosa to establish whether its failure to colonize the simple habitat was due to the lack of propagules or post-recruitment mortality. C. racemosa spread in the complex habitat was not influenced by the removal of resident assemblages, but it was slightly enhanced by A. taxiformis removal. Neither C. racemosa removal nor that of resident assemblages promoted A. taxiformis colonization and survival in simple habitats. Our results suggest that heterogeneity in environmental conditions can promote invader coexistence by mitigating the effects of negative biotic interactions. Therefore, the accumulation of introduced species in native communities does not necessarily imply established invaders fostering further invasion.     

Invasive macrophytes in a marine reserve (Columbretes Islands,NW Mediterranean): spread dynamics and interactions with the endemic scleractinian coral Cladocora caespitosa

The invasive algae Lophocladia lallemandii and Caulerpa racemosa are becoming an important threat to benthic assemblages in the Mediterranean Sea. Both species were first detected in Illa Grossa Bay (Columbretes Islands Marine Reserve, NW Mediterranean) in 2006, and their invasion was monitored until 2012. L. lallemandii showed a rapid outburst, spreading around the entire bay in just 2 years and showing the highest abundances between 5 and 10 m of depth (82.07 ± 3.53 % (±SE) in 2011). Caulerpa racemosa showed a slower but steady spread and remained in deeper areas during the first years; however, drastic changes in the depth distribution, with algae invading toward shallower areas, were noted beginning in 2010 and reached abundances of 57.76 ± 1.07 % (±SE) between 10 and 20 m of depth in 2011. Illa Grossa Bay hosts one of the most important populations of the endemic coral Cladocora caespitosa. This study is the first to quantitatively assess interactions between the coral and invasive algae. Although both invasive species L. lallemandii and C. racemosa had overlapping distributions with C. caespitosa, we did not find any lethal or sublethal effects of either invasive algal species. On the other hand, C. caespitosa exhibited toxic activity, which could explain the low overgrowth of living colony parts by C. racemosa.     

Macrobenthic assemblages of newly introduced <Emphasis Type="Italic">Caulerpa taxifolia</Emphasis> from the Eastern Mediterranean coast of Turkey

Caulerpa taxifolia is one of the most important and best-studied alien species in the Mediterranean Sea. The present study reveals the macrobenthic assemblages associated with C. taxifolia from the region. We found 26 species from Polychaeta, 31 species from Crustacea, 22 species from Mollusca and 5 species from Echinodermata. In conclusion, C. taxifolia in İskenderun Bay can be considered an ecosystem engineer that modifies local habitats and also enhances biodiversity.     

The importance of shore height and host identity for amphipod assemblages

The spatial distribution of organisms associated with marine intertidal macroalgae may be a direct result of their tolerance to air exposure or an indirect consequence of the distribution of their host. We compared amphipod assemblages from five intertidal macroalgae to investigate their relationship with algal identity. To test the effect of height regardless of algal characteristics, we transplanted coralline algal turfs to three different levels within the intertidal zone and compared amphipod assemblages after 1 and 14 days. Interstitial volume was positively correlated to the abundance of amphipods, suggesting that this attribute may correspond better to the potential space for their occupation when compared to algal biomass, thallus volume or the ratio between thallus and interstitial volume. Algal level determined the structure of the amphipod assemblages. Upper-level (Acanthophora spicifera and Caulerpa racemosa) and intermediate-level (coralline) algae host similar amphipod assemblages dominated by Apohyale media, but different from lower-level algae (Padina gymnospora and Sargassum cymosum), which were dominated by Hyale niger. Ten of the 15 amphipod species reported from natural communities were found in the transplanted plots. Distinct pools of amphipod species colonized coralline transplants at upper and lower levels after 1 day. However, regardless of the position on the shore, transplanted coralline turfs supported similar assemblages after 14 days, indicating that algal identity is also important for species assemblages. Our results suggest that both height on the shore and host identity combine to determine the vertical structure of amphipod assemblages in the rocky intertidal.     

Do native herbivores provide resistance to Mediterranean marine bioinvasions? A seaweed example

Generalist herbivores in marine ecosystems are poorly examined for their potential to serve as a source of biotic resistance against algal invasion. We assessed how one of the main generalist herbivores in Mediterranean rocky reefs (the sea urchin Paracentrotus lividus) affects Lophocladia lallemandii and Caulerpa racemosa, two algal invaders with strong detrimental effects on native benthic communities. In a comparison of sea urchin gut contents to algal community composition, strong preferences were exhibited, leading to no relationship between consumption and availability. Both C. racemosa and L. lallemandi were abundant in algal assemblages (>60% occurrence), but C. racemosa (20% of diet) was consumed more than L. lallemandi (3.5%). Experimental enclosures of sea urchins (12 sea urchins * m⁻²) were carried out in locations where L. lallemandii was already established and C. racemosa was rare (new invasion) or abundant (established invasion). C. racemosa was negatively affected by sea urchins only when it was rare, and no effect was detected when the alga was already abundant. Results for L. lallemandi were exactly opposite: urchins limited seasonal increases in L. lallemandi in highly-invaded areas. Because of the small amount of direct consumption of L. lallemandi, its decrease in abundance may be related to the grazing of native algae where L. lallemandii is attached. Overall, our results show that high densities of native herbivores may reduce invasive algae at low densities, due to a combination of direct and indirect effects, but it has no significant effect in highly-invaded areas.     

The role of disturbance in promoting the spread of the invasive seaweed Caulerpa racemosa in seagrass meadows

Human disturbances, such as anchoring and dredging, can cause physical removal of seagrass rhizomes and shoots, leading to the fragmentation of meadows. The introduced green alga, Caulerpa racemosa, is widely spread in the North-West Mediterranean and, although it can establish in both degraded and pristine environments, its ability to become a dominant component of macroalgal assemblages seems greater in the former. The aim of this study was to estimate whether the spread of C. racemosa depends on the intensity of disturbance to the canopy structure of Posidonia oceanica. A field experiment was started in July 2010 when habitat complexity of a P. oceanica meadow was manipulated to simulate mechanical disturbances of different intensity: rhizome damage (High disturbance intensity = H), leaf removal (Low disturbance intensity = L), and undisturbed (Control = C). Disturbance was applied within plots of different size (40 × 40 cm and 80 × 80 cm), both inside and at the edge of the P. oceanica meadow, according to an orthogonal multifactorial design. In November 2011 (16 months after the start of the experiment), no C. racemosa was found inside the seagrass meadow, while, at the edge, the cover of the seaweed was dependent on disturbance intensity, being greater where the rhizomes had been damaged (H) than in leaf removal (L) or undisturbed (C) plots. The results of this study indicate that physical disturbance at the margin of seagrass meadows can promote the spread of C. racemosa.     

Diet and physiological responses of Spondyliosoma cantharus (Linnaeus, 1758) to the Caulerpa racemosa var. cylindracea invasion

Marine invasions are a worldwide problem that involves changes in communities and the acclimation of organisms to them. The invasive Chlorophyte Caulerpa racemosa var. cylindracea is widespread in the Mediterranean and colonises large areas from 0 to 70 m in depth. The omnivorous fish Spondyliosoma cantharus presents a high frequency of occurrence of C. racemosa in the stomach contents at invaded areas (76.3%) while no presence of C. racemosa was detected in control areas. The isotopic composition of muscle differed significantly between invaded and non-invaded sites for δ¹³C (− 16.67‰ ± 0.09 and − 17.67‰ ± 0.08, respectively), δ¹⁵N (10.22‰ ± 0.22 and 9.32‰ ± 0.18, respectively) and the C:N ratio (2.01 ± 0.0002 and 1.96 ± 0.009, respectively). Despite the high frequency of occurrence of C. racemosa in the stomach contents of S. cantharus and its important contribution to the δ¹³C source (20.7% ± 16.2), the contribution of C. racemosa to the δ¹⁵N in S. cantharus food sources was very low (6.6% ± 5.8). Other invertebrate prey such as decapods and polychaetes were more important contributors to the δ¹⁵N source at both invaded and non-invaded sites. Activation of enzymatic pathways (catalase, superoxide dismutase, glutathione-s-tranferase, 7-ethoxy resorufin O-de-ethylase) but not a significant increase in lipid peroxidation MDA (0.49 ± 0.01 nmol/mg prot at non-invaded and 0.53 ± 0.01 nmol/mg prot at invaded sites) was observed in S. cantharus individuals living in C. racemosa-invaded sites compared with control specimens. The low δ¹⁵N contribution values of C. racemosa by S. cantharus together with the toxicity demonstrated by the activation of the antioxidant defences and the important contribution of invertebrate prey to the δ¹⁵N could mean that the ingestion of C. racemosa by S. cantharus might be unintentional during the predation of invertebrate preys living underneath the entanglement of the C. racemosa fronds and stolons mats.     

Long-term changes in amphipod population dynamics in a temperate estuary following ecosystem restoration

The Mondego estuary (Portugal) has suffered severe ecological stress over the last two decades, as manifested in the replacement of seagrasses by opportunistic macroalgae, degradation of water quality and increased turbidity. A restoration plan was implemented in 1998, which aimed to reverse the eutrophication effects, and especially to restore the original natural seagrass (Zostera noltii) community. This article explores the long-term changes in Ampithoe valida and Melita palmata (Amphipoda) populations in response to eutrophication (with consequent seagrass loss and macroalgal proliferation) and to the subsequent restoration plan (with progressive seagrass recovery and macroalgal biomass decline). Until the early 1990s, high densities of A. valida and M. palmata were recorded in the Mondego estuary, especially during the occurrence of the macroalgal bloom and during all the periods in which green macroalgae were available. After the implementation of the restoration plan, species abundance, biomass and production levels decreased considerably due to the progressive decline of green macroalgae. This implied the virtual disappearance of the amphipod population, mainly A. valida. Distinct behaviours displayed by the two species could be related to different food strategies and habitat preferences. Ampithoe valida showed feeding preferences for ephemeral softer, filamentous or bladed algae (e.g. Ulva sp.) due to its high caloric content, using the Z. noltii bed only as a habitat for protection against predators or shelter from wave action. On the other hand, M. palmata did not suffer a strong decline in its population density, biomass and production, which may indicate that this species is probably not a primary consumer of green macroalgae and may readily shift to alternative ecological niches. Handling editor: P. Viaroli     

Effects of <Emphasis Type="Italic">Caulerpa racemosa</Emphasis> var. <Emphasis Type="Italic">cylindracea</Emphasis> on prey availability: an experimental approach to predation of amphipods by <Emphasis Type="Italic">Thalassoma pavo</Emphasis> (Labridae)

Alien plant species, such as Caulerpa racemosa var. cylindracea, that invade Mediterranean marine vegetated habitats can affect habitat structure. In turn, changes in habitat structure may affect the associated invertebrate assemblages, either through changes in habitat selection or as a result of altered predation efficiency. In order to test for effects of changes in habitat structure resulting from colonization by C. racemosa on prey availability for predators, the importance of amphipods as a trophic resource in natural vegetated habitat was first assessed, and later experiments were undertaken to assess the effects of the alien alga on predation by Thalassoma pavo of two dominant amphipods: Elasmopus brasiliensis (Gammaridea) and Caprella dilatata (Caprellidea). Laboratory experiments were conducted in separate aquaria with five vegetation habitat types: Halopteris scoparia, Jania rubens, C. racemosa without detritus, C. racemosa with detritus, Cymodocea nodosa, together with controls. The vegetation was first defaunated, and then 30 amphipods were introduced to each aquarium and exposed to a single Thalassoma pavo individual for 1 h, after which the fish’s gut contents were examined. Consumption (per fish per hour) of caprellids (11.7 ± 1.4) was higher overall than that of gammarids (8.7 ± 1.5) and likely reflects different microhabitat use by amphipods, which affects susceptibility to predators. Consumption of amphipods also varied by habitat type. The highest predation rate was found in the C. nodosa habitat (12.7 ± 2.19) and the lowest in the C. racemosa habitats with detritus (4.1 ± 1.78) and without detritus (5.2 ± 0.55), which did not differ. The pattern of predation across habitats, however, was similar for both caprellid and gammarid amphipods, indicating a more general effect of habitat on amphipod predation. Our findings showed that invasive species such as C. racemosa can decrease feeding by predators such as T. pavo. Changes in predator–prey interactions could have consequences for food web support in the Mediterranean.     

Feeding strategy of the sacoglossan opisthobranch <Emphasis Type="Italic">Oxynoe olivacea</Emphasis> on the tropical green alga <Emphasis Type="Italic">Caulerpa taxifolia</Emphasis>

The feeding behaviour of the shelled sacoglossan Oxynoe olivacea was investigated to better understand the role and importance of this species in influencing encroachments of the alien alga Caulerpa taxifolia in the Mediterranean sea. We tested whether this slug preferred, as preliminary field observations suggested, an aggregative feeding behaviour and which part of the algal thallus, phylloid vs rhizoid, it preferred. Results showed that O. olivacea fed in groups and actively selected phylloid. This outcome poses important questions regarding the possibility that this species, fragmenting the alga thallus, could enhance dispersion and regeneration of C. taxifolia.