Human impacts on oligotrophic marine ecosystems: case studies from Cyprus, Mediterranean Sea

Highly oligotrophic marine waters cover about a third of the Earth’s surface and have diverse communities that are affected by multiple stressors, such as ocean acidification, warming, marine litter, pollution, overfishing. The low nutrient Mediterranean Sea has high biodiversity and endemism but is heavily impacted by these human pressures and a recent major influx of invasive alien species that compete, predate and infect indigenous species. Aquaculture effluents and eutrophication alter water quality and add pressure on coastal ecosystems that are already subject to habitat loss and degradation due to coastal developments. This PhD dissertation reviews human impacts on highly oligotrophic marine ecosystems (Chapter 2). It then presents case studies that cover multiple impacts around Cyprus. A major impact to the Mediterranean Sea is immigration of Indo-Pacific species, which has accelerated in recent years due to climate change and the widening of the Suez Canal. Chapter 3 compares populations of the seagrass Halophila stipulacea both in their alien and native environments. It also presents the detection of the lionfish Pterois miles providing the first evidence that a lionfish invasion in the Mediterranean is underway. Shallow rocky reefs covered by canopy-forming brown seaweed and meadows of Posidonia oceanica are declining rapidly throughout the Mediterranean. I studied these important ecosystems across the most industrialised coastline of Cyprus. Chapter 4 characterises macroalgal communities along an impact gradient and shows that macroalgae are robust indicators to assess the ecological status of coastal waters. Communities dominated by canopy-forming Cystoseira at pristine sites, shifted to turf and filamentous opportunistic seaweed on industrialised coastlines. Chapter 5 characterises sediment chemical variables, delivers the first habitat cartography, describes structural descriptors of P. oceanica and assesses the ecological condition across Vasiliko Bay. Despite mounting pressures, ancient P. oceanica meadows in Vasiliko Bay have among the highest shoot densities across the whole Mediterranean. However, lower shoot densities and more epiphytes were noted near fish farm sites. In Chapter 6 monitoring of P. oceanica descriptors from fixed plots established at the lower limits of the meadows near fish farms shows that a management decision to relocate farms into deeper waters had prevented further declines in seagrasses. Chapter 7 presents Integrated Multi-Trophic Aquaculture (IMTA) trials carried out off southern Cyprus. The concept of IMTA is to cultivate organisms (e.g. seaweed, filter feeders, detritivores) around finfish cages, converting waste effluents into product and mitigating environmental impacts. Trials lasted three years and identified opportunities and challenges that impede IMTA adoption by fish farms in warm oligotrophic conditions. Taken as a whole, this thesis demonstrates that ecology of the eastern Mediterranean Sea is changing rapidly due to multiple anthropogenic stressors, but strategic management can help halt, and in some cases reverse, the damage done

Chapter Threats to Ultraoligotrophic Marine Ecosystems

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Genetic Data Suggest Multiple Introductions of the Lionfish (Pterois miles) into the Mediterranean Sea

Widespread reports over the last six years confirm the establishment of lionfish (Pterois miles) populations in the eastern Mediterranean. Accumulated knowledge on lionfish invasions in the western Atlantic Ocean has shown that it is a successful invader and can have negative impacts on native species, indirect ecological repercussions and economic effects on local human societies. Here we analysed genetic sequences of lionfish from Cyprus as well as data from the whole distribution of the species, targeting the mtDNA markers cytochrome c oxidase subunit 1 (COI) and the control region (CR). Our results reflect a pattern of repeated introductions into the Mediterranean from the northern Red Sea and a secondary spread of this species west to Rhodes and Sicily. Presented results agree with previously published studies highlighting the genetic similarity with individuals from the northern Red Sea. Nevertheless, some individuals from Cyprus, in addition to those coming via the Suez Canal, were genetically similar to fish from the Indian Ocean, indicating genetic homogeneity among populations of P. miles across its current distribution, possibly facilitated by the ornamental fish trade and/or transport through ballast water.</jats:p

A lionfish (Pterois miles) invasion has begun in the Mediterranean Sea

Until now, few sightings of the alien lionfish Pterois miles have been reported in the Mediterranean and it was questionable whether the species could invade this region like it has in the western Atlantic. Here, we present evidence from divers and fishermen that lionfish have recently increased in abundance and within a year colonised almost the entire south eastern coast of Cyprus, likely due to sea surface warming. At least 23 different fish are reported of which 6 were removed. Groups of lionfish exhibiting mating behaviour have been noted for the first time in the Mediterranean. Managers need this information and should alert stakeholders to the potential ecological and socio-economic impacts that may arise from a lionfish invasion. Actions could involve incentives to engage divers and fishermen in lionfish removal programmes, as these have worked well at shallow depths in the Caribbean. Given that the Suez Canal has recently been widened and deepened, measures will need to be put in place to help prevent further invasion

Invasive lionfish in the Mediterranean: Low public awareness yet high stakeholder concerns

A lionfish invasion in the Western Atlantic has been one of the most ecologically harmful fish invasions to date. Experience there has shown that its management is most effective when the public and stakeholders are involved. The lionfish (Pterois miles) has recently invaded the Mediterranean, spreading at an alarming rate. To understand lionfish knowledge and perceptions, questionnaire surveys were conducted with a representative cross section of the adult general public (via telephone) and stakeholders (via organised meetings) in Cyprus. Results from 300 public surveys revealed limited awareness about the lionfish but strong support for its local management. Men and older respondents showed stronger support compared to women and younger respondents, respectively. Results from 108 stakeholder revealed high level of awareness and almost unanimous support for management measures. The majority had not experienced any effects from the recent lionfish invasion, but some reported negative impacts such as limited access to dive sites, ecosystem damage and fishing gear destruction. Few stakeholders perceived benefits of this invasive species, e.g. to dive tourism or as a food source. Almost all stakeholders expressed a willingness to get involved in lionfish management, but only around half would consider personal consumption, or sports incentives as good incentives for their participation. Encouragement from scientists through coordination , training and support was suggested as an essential part of effective management strategy. The results of this study can inform an efficient adaptive management process across the Mediterranean region and assist future engagement of citizen scientists in lionfish control and mitigation

Low Pufferfish and Lionfish Predation in Their Native and Invaded Ranges Suggests Human Control Mechanisms May Be Necessary to Control Their Mediterranean Abundances

The silver-cheeked toadfish (Lagocephalus sceleratus, from the pufferfish family Tetraodontidae) and the Pacific red lionfish (Pterois miles, family Scorpaenidae) have recently invaded the Mediterranean Sea. Lagocephalus sceleratus has spread throughout this entire sea with the highest concentrations in the eastern basin, while more recently, Pterois miles has spread from the Eastern to the Central Mediterranean Sea. Their effects on local biodiversity and fisheries are cause for management concern. Here, a comprehensive review of predators of these two species from their native Indo-Pacific and invaded Mediterranean and Western Atlantic ranges is presented. Predators of Tetraodontidae in general were reviewed for their native Indo-Pacific and Western Atlantic ranges, as no records were found specifically for L. sceleratus in its native range. Tetraodontidae predators in their native ranges included mantis shrimp (Stomatopoda), lizardfish (Synodus spp.), tiger shark (Galeocerdo cuvier), lemon shark (Negaprion brevirostris), sea snakes (Enhydrina spp.), catfish (Arius spp.), cobia (Rachycentron canadum), skipjack tuna (Katsuwonus pelamis), and common octopus (Octopus vulgaris). The only reported predator of adult L. sceleratus in the Mediterranean was loggerhead turtle (Caretta caretta), whereas juvenile L. sceleratus were preyed by common dolphinfish (Coryphaena hippurus) and garfish (Belone belone). Conspecific cannibalism of L. sceleratus juveniles was also confirmed in the Mediterranean. Pufferfish predators in the Western Atlantic included common octopus, frogfish (Antennaridae), and several marine birds. Predators of all lionfish species in their native Indo-Pacific range included humpback scorpionfish (Scorpaenopsis spp.), bobbit worms (Eunice aphroditois), moray eels (Muraenidae), and bluespotted cornetfish (Fistularia commersonii). Lionfish predators in the Mediterranean included dusky grouper (Epinephelus marginatus), white grouper (Epinephelus aeneus), common octopus, and L. sceleratus, whereas in the Western Atlantic included the spotted moray (Gymnothorax moringa), multiple grouper species (tiger Mycteroperca tigris, Nassau Epinephelus striatus, black Mycteroperca bonaci, red Epinephelus morio, and gag Mycteroperca microleps; Epinephelidae), northern red snapper (Lutjanus campechanus), greater amberjack (Seriola dumerilli), and nurse shark (Ginglymostoma cirratum). The sparse data found on natural predation for these species suggest that population control via predation may be limited. Their population control may require proactive, targeted human removals, as is currently practiced with lionfish in the Western Atlantic.</jats:p

Is Europe ready for integrated multi-trophic aquaculture? A survey on the perspectives of European farmers and scientists with IMTA experience

Integrated Multi-Trophic Aquaculture (IMTA) refers to the integrated farming of several species from different trophic levels in close proximity. In IMTA, one species is intended to complement another. The concept has long been in use in Asia and contributes significantly to the sustainability of aquaculture as it can potentially drive ecological efficiency, environmentally acceptability, product-diversity, profitability and benefit society. Although the concept has received increasing academic attention during the last two decades, it has not yet become a commercial reality in European mariculture. The reasons for this were explored, by interviewing farmers and scientists with previous experience on IMTA. The interviewing approach can be effective in identifying important omissions from the available literature and also possible exaggerations of positive results. For the purposes of this study, a qualitative survey was undertaken using a structured questionnaire with open-ended questions. As a result, the opinions of 34 farmers and scientists with substantial experience of IMTA from 12 European countries have been obtained. A broad spectrum of IMTA impediments has been identified. These have been separated into nine major categories; namely Biological, Conflicts, Environmental, Interest, Legislation, Market, Operational, R&D, and Vandalism. The importance of each category was found to vary among different locations and regions of Europe indicating the need for site-specific targeted approaches. Nevertheless, factors from several categories were raised in all countries/IMTA configurations which highlights that for IMTA to be further developed and adopted, the involvement of stakeholders and personnel from several disciplines is necessary (i.e. biologists, economists, engineers, farm managers, modellers, regulators, stakeholders and statisticians). This work identifies many of the challenges that European IMTA is likely to encounter, and proposes areas that are likely to benefit from focused research and development.PostprintPeer reviewe

Unpublished Mediterranean records of marine alien and cryptogenic species

Good datasets of geo-referenced records of alien species are a prerequisite for assessing the spatio-temporal dynamics of biological invasions, their invasive potential, and the magnitude of their impacts. However, with the exception of first records on a country level or wider regions, observations of species presence tend to remain unpublished, buried in scattered repositories or in the personal databases of experts. Through an initiative to collect, harmonize and make such unpublished data for marine alien and cryptogenic species in the Mediterranean Sea available, a large dataset comprising 5376 records was created. It includes records of 239 alien or cryptogenic taxa (192 Animalia, 24 Plantae, 23 Chromista) from 19 countries surrounding the Mediterranean Sea. In terms of records, the most reported Phyla in descending order were Chordata, Mollusca, Chlorophyta, Arthropoda, and Rhodophyta. The most recorded species was Caulerpa cylindracea, followed by Siganus luridus, Magallana sp. (cf. gigas or angulata) and Pterois miles. The dataset includes records from 1972 to 2020, with the highest number of records observed in 2018. Among the records of the dataset, Dictyota acutiloba is a first record for the Mediterranean Sea. Nine first country records are also included: the alga Caulerpa taxifolia var. distichophylla, the cube boxfish Ostracion cubicus, and the cleaner shrimp Urocaridella pulchella from Israel; the sponge Paraleucilla magna from Libya and Slovenia; the lumpfish Cyclopterus lumpus from Cyprus; the bryozoan Celleporaria vermiformis and the polychaetes Prionospio depauperata and Notomastus aberans from Malta

Chapter Threats to Ultraoligotrophic Marine Ecosystems

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