Tomás Vega Fernández

The effects of an invasive seaweed on native communities vary along a gradient of land-based human impacts

The difficulty in teasing apart the effects of biological invasions from those of other anthropogenic perturbations has hampered our understanding of the mechanisms underpinning the global biodiversity crisis. The recent elaboration of global-scale maps of cumulative human impacts provides a unique opportunity to assess how the impact of invaders varies among areas exposed to different anthropogenic activities. A recent meta-analysis has shown that the effects of invasive seaweeds on native biota tend to be more negative in relatively pristine than in human-impacted environments. Here, we tested this hypothesis through the experimental removal of the invasive green seaweed, Caulerpa cylindracea, from rocky reefs across the Mediterranean Sea. More specifically, we assessed which out of land-based and sea-based cumulative impact scores was a better predictor of the direction and magnitude of the effects of this seaweed on extant and recovering native assemblages. Approximately 15 months after the start of the experiment, the removal of C. cylindracea from extant assemblages enhanced the cover of canopy-forming macroalgae at relatively pristine sites. This did not, however, result in major changes in total cover or species richness of native assemblages. Preventing C. cylindracea re-invasion of cleared plots at pristine sites promoted the recovery of canopy-forming and encrusting macroalgae and hampered that of algal turfs, ultimately resulting in increased species richness. These effects weakened progressively with increasing levels of land-based human impacts and, indeed, shifted in sign at the upper end of the gradient investigated. Thus, at sites exposed to intense disturbance from land-based human activities, the removal of C. cylindracea fostered the cover of algal turfs and decreased that of encrusting algae, with no net effect on species richness. Our results suggests that competition from C. cylindracea is an important determinant of benthic assemblage diversity in pristine environments, but less so in species-poor assemblages found at sites exposed to intense disturbance from land-based human activities, where either adverse physical factors or lack of propagules may constrain the number of potential native colonizers. Implementing measures to reduce the establishment and spread of C. cylindracea in areas little impacted by land-based human activities should be considered a priority for preserving the biodiversity of Mediterranean shallow rocky reefs.

Assessing Posidonia oceanica Seedling Substrate Preference: An Experimental Determination of Seedling Anchorage Success in Rocky vs. Sandy Substrates

In the last decades the growing awareness of the ecological importance of seagrass meadows has prompted increasing efforts to protect existing beds and restore degraded habitats. An in-depth knowledge of factors acting as major drivers of propagule settlement and recruitment is required in order to understand patterns of seagrass colonization and recovery and to inform appropriate management and conservation strategies. In this work Posidonia oceanica seedlings were reared for five months in a land-based culture facility under simulated natural hydrodynamic conditions to identify suitable substrates for seedling anchorage. Two main substrate features were investigated: firmness (i.e., sand vs. rock) and complexity (i.e., size of interstitial spaces between rocks). Seedlings were successfully grown in culture tanks, obtaining overall seedling survival of 93%. Anchorage was strongly influenced by substrate firmness and took place only on rocks, where it was as high as 89%. Anchorage occurred through adhesion by sticky root hairs. The minimum force required to dislodge plantlets attached to rocky substrates reached 23.830 N (equivalent to 2.43 kg), which would potentially allow many plantlets to overcome winter storms in the field. The ability of rocky substrates to retain seedlings increased with their complexity. The interstitial spaces between rocks provided appropriate microsites for seedling settlement, as seeds were successfully retained, and a suitable substrate for anchorage was available. In conclusion P. oceanica juveniles showed a clear-cut preference for hard substrates over the sandy one, due to the root system adhesive properties. In particular, firm and complex substrates allowed for propagule early and strong anchorage, enhancing persistence and establishment probabilities. Seedling substrate preference documented here leads to expect a more successful sexual recruitment on hard bottoms compared with soft ones. This feature could have influenced P. oceanica patterns of colonization in past and present time.

Spatial Management of Fisheries in the Mediterranean Sea: Problematic Issues and a Few Success Stories

Fishing has been important in the Mediterranean region for many centuries and still has a central role in its economic importance and cultural heritage. A multitude of fishery-oriented marine managed areas have been implemented under a highly complex political and legislative framework to protect fishery resources and sensitive habitats from high impact uses. However, a review of the literature revealed that few data are available to support their effectiveness, except for a few studies on fishery reserves and marine reserves. In these cases, fish biomass has increased and some evidence of ecological and socioeconomic benefits has been documented. The environmental and geopolitical complexity of the Mediterranean region as well as the dominant top-down management approaches, constitute the weakest points in the spatial management of fisheries at regional level. A coordinating role of all national and supranational bodies present in the area is desirable in the near future.

The Sea Urchin Arbacia lixula: A Novel Natural Source of Astaxanthin

Several echinoderms, including sea urchins, are valuable sources of bioactive compounds but their nutraceutical potential is largely unexplored. In fact, the gonads of some sea urchin species contain antioxidants including carotenoids and polyhydroxylated naphthoquinones (PHNQ’s), such as echinochrome A. Astaxanthin is known to have particular bioactivity for the prevention of neurodegenerative diseases. This carotenoid is produced by microalgae, while several marine invertebrates can bioaccumulate or synthetize it from metabolic precursors. We determined the carotenoid content and analyzed the bioactivity potential of non-harvested Atlantic-Mediterranean sea urchin Arbacia lixula. The comparison of methanol crude extracts obtained from eggs of farmed and wild specimens revealed a higher bioactivity in farmed individuals fed with a customized fodder. HPLC-analysis revealed a high concentration of astaxanthin (27.0 μg/mg), which was the only pigment observed. This study highlights the potential of farmed A. lixula as a new source of the active stereoisomer of astaxanthin.

Food Modulation Controls Astaxanthin Accumulation in Eggs of the Sea Urchin Arbacia lixula

The carotenoid astaxanthin has strong antioxidant properties with beneficial effects for various degenerative diseases. This carotenoid is produced by some microalgae species when cultivated in particular conditions, and, interestingly, it is a predominant carotenoid in aquatic animals throughout a broad range of taxa. Recently, astaxanthin was detected in the eggs of the sea urchin Arbacia lixula in relevant concentrations when this organism was maintained in culture. These results have paved the way for deeper research into astaxanthin production by this species, particularly in regards to how astaxanthin production can be modulated by diet. Results showed that the highest content of astaxanthin in eggs was observed in sea urchins fed on a diet enriched with Spirulina platensis. This result was confirmed by the high antioxidant activity recorded in the egg extracts of these animals. Our results suggest that (i) the sea urchin A. lixula is able to synthesize astaxanthin from precursors obtained from food, and (ii) it is possible to modulate the astaxanthin accumulation in sea urchin eggs by modifying the proportions of different food ingredients provided in their diet. This study demonstrates the large potential of sea urchin cultivation for the eco-sustainable production of healthy supplements for nutraceutical applications.

Worming its way into Patagonia: an integrative approach reveals the cryptic invasion by Eulalia clavigera (Annelida: Phyllodocidae)

A phyllodocid polychaete belonging to the genus Eulalia is reported from Nuevo Gulf, Patagonia (South-western Atlantic Ocean) with abundant populations thriving in the intertidal zone. Morphological and molecular data allowed assigning this population to Eulalia clavigera (Audouin & Milne-Edwards, 1834), a species typically occurring along the north-eastern Atlantic coast. The absence of genetic structuring between north-eastern and south-western Atlantic E. clavigera strongly supports a non-native origin of the Patagonian population. Conversely, the majority of the Mediterranean Eulalia cf. clavigera analysed in this study turned out to belong to a different, probably undescribed species, suggesting that the diversity and taxonomy of green Eulalia is more complex than previously supposed. The high adaptation capabilities to stressed environments showed by E. clavigera, along with its possible high impact on native assemblages through predation, compel to carefully monitor its spread along the Patagonian coasts.

Biological Invasions in Conservation Planning: A Global Systematic Review

Biological invasions threaten biodiversity in terrestrial, freshwater and marine ecosystems, requiring substantial conservation and management efforts. To examine how the conservation planning literature addresses biological invasions and if planning in the marine environment could benefit from experiences in the freshwater and terrestrial systems, we conducted a global systematic review. Out of 1149 scientific articles mentioning both ‘conservation planning’ and ‘alien’ or any of its alternative terms, 70 articles met our selection criteria. Most of the studies were related to the terrestrial environment, while only 10% focused on the marine one. The main conservation targets were species (mostly vertebrates) rather than habitats or ecosystems. Apart from being mentioned, alien species were considered of concern for conservation in only 46% of the cases, while mitigation measures were proposed in only 13% of the cases. The vast majority of the studies (73%) ignored alien species in conservation planning even if their negative impacts were recognized. In 20% of the studies, highly invaded areas were avoided in the planning, while in 6% of the cases such areas were prioritized for conservation. In the latter case, two opposing approaches led to the selection of invaded areas: either alien and native biodiversity were treated equally in setting conservation targets, i.e. alien species were also considered as ecological features requiring protection, or more commonly invaded sites were prioritized for the implementation of management actions to control or eradicate invasive alien species. When the ‘avoid’ approach was followed, in most of the cases highly impacted areas were either excluded or invasive alien species were included in the estimation of a cost function to be minimized. Most of the studies that followed a ‘protect’ or ‘avoid’ approach dealt with terrestrial or freshwater features but in most cases the followed approach could be transferred to the marine environment. Gaps and needs for further research are discussed and we propose an 11-step framework to account for biological invasions into the systematic conservation planning design.

Substrate preference and settlement behaviour of the megalopa of the invasive crab Percnon gibbesi (Decapoda, Percnidae) in the Mediterranean Sea

The transition from a planktonic to a benthic life is a critical phase in which sub-adults are particularly exposed to the risk of predation and dispersion into unsuitable habitats, and plays a crucial role in the distribution, structure and dynamics of marine populations. Settlement involves the selection of an adequate substrate that provides shelter and food during early life stages. Percnon gibbesi is an alien brachyuran crab that has invaded the Mediterranean, where it is preferentially associated to boulders covered with shallow algal turf. The mechanisms of substrate selection leading to the settlement of megalopae are still unknown in P. gibbesi, yet their knowledge may shed light on its high invasiveness. We examined the substrate preference and settlement behaviour of 36 megalopae of P. gibbesi using three natural substrates in an experimental mesocosm: gravel, cobbles and flat stones. Video recordings of 30-min trials were used to assess the substrate preference, measure the time to selection and observe the behaviour of the megalopae. Strong preference was given to hard and stable substrates i.e., cobbles and flat stones with interstices where to hide, which are also the most suitable as they provide shelter and food. Direct selection was the dominant behaviour followed by exploration and lastly by hesitation. The megalopae selected quickly the most suitable substrate to settle, likely enhancing their chances of survival. Our findings suggest that rapid settlement on a suitable substrate contributes to the success of the biological invasion of P. gibbesi along the Mediterranean coasts.

Kleptopredation: a mechanism to facilitate planktivory in a benthic mollusc

Predation occurs when an organism completely or partially consumes its prey. Partial consumption is typical of herbivores but is also common in some marine microbenthic carnivores that feed on colonial organisms. Associations between nudibranch molluscs and colonial hydroids have long been assumed to be simple predator–prey relationships. Here we show that while the aeolid nudibranch Cratena peregrina does prey directly on the hydranths of Eudendrium racemosum, it is stimulated to feed when hydranths have captured and are handling prey, thus ingesting recently captured plankton along with the hydroid polyp such that plankton form at least half of the nudibranch diet. The nudibranch is thus largely planktivorous, facilitated by use of the hydroid for prey capture. At the scale of the colony this combines predation with kleptoparasitism, a type of competition that involves the theft of already-procured items to form a feeding mode that does not fit into existing classifications, which we term kleptopredation. This strategy of subsidized predation helps explain how obligate-feeding nudibranchs obtain sufficient energy for reproduction from an ephemeral food source.

Protocooperation among small polyps allows the coral Astroides calycularis to prey on large jellyfish

The coral Astroides calycularis (Scleractinia: Dendrophylliidae) is endemic to the Mediterranean Sea (Terr on-Sigler et al. 2016), where it can be reef forming (Musco et al. 2017: Fig. 1). In shallow water, it may cover up to 90% of rocky substrate from the surface down to 15 m depth where it is found in caves and on vertical walls. Astroides calycularis colonies frequently occur in dense aggregations (Goffredo et al. 2011), possibly favored by limited dispersion ability of both sexual (Goffredo et al. 2010) and asexual propagules (Serrano et al. 2017). High water movement promotes massive colony shapes with closely connected polyps usually forming continuous orange surfaces, leaving little space for the settlement of other benthic organisms (Casado-Amezua et al. 2013). Astroides calycularis is “polystomatous,” forming small colonies composed of polyps connected to each other as a single organism bearing several mouths. Colony morphology is also strongly controlled by food availability (Goffredo et al. 2011). Polyps are typically 4–5 mm in length but larger polyps can grow up to 8 mm long. Like other azooxanthellate corals, A. calycularis is an obligate suspension feeder (Cebrian and Ballesteros 2004) and it is assumed to feed primarily on zooplankton transported by water movement, although the identity of its most preferred prey is unknown. The venomous mauve stinger Pelagia noctiluca is a holoplanktonic jellyfish with a phosphorescent bell 3–12 cm wide. It is typical of warm water but currents may transport smacks of jellyfish into temperate and cold seas. Thus, it can be found from the tropics to the north Pacific and Atlantic, including the Mediterranean Sea. Pelagia noctiluca is usually pelagic and performs diel vertical migrations, albeit occasionally reaching the coast in large quantities. In the western Mediterranean, it forms persistent populations where it can be a nuisance to bathing people during periodic blooms in the warm season, raising increasing concerns as these blooms become more frequent (Canepa et al. 2014). Pelagia noctiluca is known to be preyed upon by fishes and turtles and parasitized by crustaceans. So far only one published picture of P. noctiluca seized by a polyp of a polystomatous coral is known (Aguilar 2007:30). Observations of predation of the mauve stinger, P. noctiluca, by the orange coral, A. calycularis, were made in 2010, 2014, and 2017 during three field survey campaigns carried out in different localities of the Mediterranean Sea (Appendix S2). Capture and ingestion of 20 observed jellyfish involved several polyps belonging to different colonies (Fig. 1a, Appendix S1: Fig. S1A–D, Video S1). The feeding behavior begins when a P. noctiluca jellyfish becomes trapped under an overhang with abundant A. calycularis. The pulsating swimming of the jellyfish moves the bell repeatedly against the overhang ceiling. Here A. calycularis polyps first adhere to the bell after which several polyps rapidly engulf the oral arms of the jellyfish, a process lasting between 1 and 5 minutes. Single polyps are able to ingest the oral arm tips preventing the jellyfish from escaping, while other polyps collaborate in ingesting pieces of jellyfish arms and umbrella (Fig. 1b, Appendix S1: Fig. S1D). Some jellyfish escape these attacks or become released as many were observed lying dead on the seafloor, with a hole on the top of the bell possibly caused by the predators. A similar behavior is shown when jellies are pushed by waves or currents onto colonies living on vertical walls along the shore (Appendix S1: Fig. S1A–D). Present data and available information do not allow us to quantify the predation pressure exerted by A. calycularis on the mauve stinger. It seems unlikely that predation by the