The ever-increasing arrival of alien marine organisms is evident in the whole Mediterranean Sea, but is particularly pronounced in the eastern Mediterranean, primarily due to oceanic warming.

The coasts of the Dodecanese Islands (south-eastern (SE) Aegean Sea, Figure 1) receive westward flowing Levantine water masses, and are close to the route of intense maritime traffic using the Suez Canal. The area therefore represents the gateway for dispersal of Red Sea alien species westwards into the rest of the Mediterranean. Indeed, a significant increase in aliens’ diversity along the Dodecanese coasts has been documented over the last three decades, while marine temperature data show that the area has undergone a remarkable warming.

Given this apparent connection, we attempted to link temperature alterations with new tropical species arrivals. Comparison between the regional satellite-derived sea surface temperatures (SST) with the whole northern hemisphere temperatures (NHT) dataset of the Hadley Centre since 1985, clearly revealed that the SE Aegean Sea is going through a substantial warming (Figure 2a). The significant relationship between the Dodecanese water temperature and that of the northern hemisphere illustrates that this warming signal is not a regional phenomenon, but part of the global warming and climate change trend (Figure 2b). As evident from the NHT, the temperature rise of the last 30 years, encompassing the abrupt shift in the mid-1990s, is the warmest period since 1850. Based on the SST means, the Dodecanese temperature difference between the two decades (pre-shift [1985–1997] and post shift [1998–2007]) is 0.85ºC.

Fig. 2. Long-term relationships between global and regional temperatures: (a) satellite derived sea surface temperature (SST) (1985–2007) for the south-eastern Aegean Sea (Rhodes Island) against northern hemisphere temperature (NHT); (b) NHT anomalies (1850–2007). The solid black line corresponds to the 5 year mean.

Fig. 1. Case study area: Dodecanese Islands, Eastern Mediterranean.

Fig. 3. Long-term 5 year averaged alien species against northern hemisphere temperature (NHT) anomalies (1929–2008). The solid black line represents the statistically significant shift for alien species (black dot represents alien species; grey dot represents NHT data).

To see if global warming has influenced the rate of new alien species arrival, the NHT was plotted against the local alien species data (Figure 3). The 80 years (1929–2008) period showed a significant parallel between the introduction rate of alien species in the SE Aegean Sea and increasing marine temperatures. The period 1929 to 1980 showed a stable neutral trend in both temperature and alien species arrivals. From the 1980s until present an abrupt parallel increasing trend can be observed (Figures 2b & 3).

Forty-three per cent of the 239 known alien species in Greek seas are found along the Dodecanese coasts, and nearly all (98%) are of warm/tropical origin. Eightyfour per cent of these alien species arrived via the Suez Canal (see Figure 4). The first alien species recorded in the area were the seagrass Halophila stipulacea, and the macroalga Hypnea cornuta, both found in Rhodes in 1894. Over the next 50 years nine fish species and four algae of Indo-Pacific origin were introduced with consequent alterations to native communities and local fisheries. Indeed, soon after its introduction in 1925, the marbled spinefoot, Siganus rivulatus was commercially targeted. Between 1951 and 1980 another 18 (16 tropical) species were recorded. After almost a century of gradual colonization, the introduction rate of Indo-Pacific biota assumed the character of an invasion, with the addition of 68 new species from 1981 to date (see Figure 5).

Concern about the future tropicalization of the Mediterranean is increasing. The Suez Canal, until now a barrier to many species due to its high salinity, is to be widened and deepened. Furthermore, the Canal salinity is decreasing while that of the Eastern Mediterranean is increasing. While earlier introductions were limited to euryhaline (species tolerant of fluctuations in salinity) and littoral species, the door is now open to deep-water species.

The Dodecanese Islands belong to the ‘Lessepsian Province’, the sub-tropical character of which explains the very high percentage of warm/tropical alien species in the alien biota. Scientists predict that lessepsian immigrants will expand further west if the climate warms up further. Although the Indo-Pacific biota is mostly confined to the eastern Mediterranean, recent findings show that climate warming is enabling alien species to spread to the westernmost part of the Mediterranean.

Acting together, stressors such as climate change, human impacts and alien species invasions may have unexpected and irreversible consequences for native communities and for fisheries. Owing to their very recent and rapid expansion, there is insufficient evidence to assess the real impact of aliens on native biota; however, many instances of ecosystem changes in the study area have been observed. The observed and potential impacts of four invasive species living along the Dodecanese coasts are presented below.

Fig. 4. Pathways for introduction of alien species in the study area. The percentage of aliens entering through the Suez Canal confirms the importance of the area as a crossroad for tropical species expansion.

Fig. 5. Temporal trend of introduction of alien species in the study area (F, fish; PB, phytobenthos; ZB, zoobenthos; ZP, zooplankton; PP, phytoplankton; other, cyanobacteria). The unprecedented increase since 1980 is particularly evident in zoobenthos (46%) and fish (32%)

The blue cornetfish, Fistularia commersonii (Figure 7) is considered one of the most successful invasive fish species in the Mediterranean Sea. Within just a few years of its arrival its range expanded not only along the Levantine coasts and up to the Aegean Sea, but also westward, reaching the eastern coast of the Iberian Peninsula within a few years. Since its first appearance in the SE Aegean Sea in 2001, it has become established on sandymuddy bottoms and Posidonia oceanica meadows around Rhodes. Regularly present in Dodecanese fisheries as by-catch, the commercially useless blue cornetfish may have serious economic and ecological impacts, since it feeds mainly on several commercially important small native fish.

Fig. 7. Fistularia commersonii dwelling along the coasts of Rhodes. Image: HCMR archives.

Fig.8. Dredging in the shallow waters surrounding Rhodes revealed a huge population of Strombus (Conomurex) persicus. Image: HCMR archives

Fig. 9. Caulerpa racemosa var. cylindracea in Posidonia oceanica meadow. Image: HCMR archives

Within a few years of its introduction, the gastropod Strombus (Conomurex) persicus (Figure 8) became one of the most important components of the epibenthic fauna of the Dodecanese. It is currently locally marketed, and could potentially become a commercially exploited species throughout the Mediterranean Sea Since its first observation in 1993, the green seaweed Caulerpa racemosa var. cylindracea (Figure 9) has expanded extremely rapidly along all Greek coasts. It is considered a marine pest as it is able to overgrow other macroalgal species. Along the south-east coast of Rhodes Island, it makes up 30% of the total macroalgal coverage. The speed of spread is alarming, as C. racemosa is responsible for changes in the structure and function of native ecosystems in the Mediterranean.

Perhaps the most formidable invader is Lagocephalus sceleratus (Figure 10), better known as the pufferfish, or fugu. The pufferfish has spread rapidly, occupying all Aegean coastal waters between 15 and 16.25 °C, and even advancing into the region limited by the 14°C isotherm. Its feeding strategy, anti-predator adaptations (inflation of the body and toxicity) and the probable absence of competitors and predators in the invaded coastal habitats are the main factors contributing to the success and abundance of the pufferfish in the area. Nor is control by commercial exploitation an option; owing to the high content of tetrodotoxin (TTX) in its tissues, it has been declared not marketable by the Greek authorities.

Fig. 10. Lagocephalus sceleratus: juveniles in the Aquarium of the Hydrobiological Station of Rhodes. Image: HCMR archives.

The public health danger and an anticipated rearrangement of the food chain are exacerbated by the already evident negative socioeconomic impacts of pufferfish: a large number of fishing hauls have to be discarded, with consequent loss of working hours, fuel, etc., and native, commercially valuable stocks of invertebrates (mainly cuttlefish and octopus) are being depleted through intense predation, resulting in higher market prices.

The increase in alien species numbers in the SE Aegean parallels the substantial warming that began at the beginning of the 1980s and accelerated towards the end of the 1990s. Further sea warming may provide tropical invasive species with a distinct advantage over native Mediterranean biota and, if the present hydrographic characteristics of the south Aegean persist, significant changes in the composition and structure of the local biota are inevitable.

The gradual tropicalization of the Mediterranean is already apparent. The accelerating rate of introduction and spread of alien species leads us to believe that the tropical alien species so apparent in the eastern basin will gradually colonize the rest of the Mediterranean.

Maria Antonietta PancucciPapadopoulou (apan@hcmr. gr) is a Senior Researcher at the Hellenic Centre for Marine Research, Institute of Oceanography. Dionysios E. Raitsos and Maria Corsini-Foka are at the same institution.

FURTHER READING

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Pancucci-Papadopoulou M.A., Raitsos D.E. and Corsini-Foka M. (2012) Biological invasions and climatic warming: implications for south-eastern Aegean ecosystem functioning. Journal of the Marine Biological Association of the United Kingdom 92, 777–789. DOI:10.1017/S0025315411000981.

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Raitsos D.E., Beaugrand G., Georgopoulos D., Zenetos A., PancucciPapadopoulou M.A., Theocharis A. and Papathanassiou E. (2010) Global climate change amplifies the entry of tropical species into the Mediterranean Sea. Limnology and Oceanography 55, 1478–1484. DOI: 10.4319/lo.2010.55.4.1478.

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Zenetos A., Katsanevakis S., Poursanidis D., Crocetta F., Damalas D., Apostolopoulos G., Gravili C., VardalaTheodorou E. and M. Malaquias (2011) Marine alien species in Greek seas: additions and amendments by 2010. Mediterranean Marine Science 12/1, 95–120.

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Maria Antonietta PancucciPapadopoulou

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