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Environmental Analysis & Ecology Studies

Invasive Macrophyte Species in the Mediterranean Sea: An Update

Nicola Cantasano* and Vincenzo Di Martino

Institute for Agriculture and Forestry Systems in the Mediterranean (ISAFoM) CNR, Italy

*Corresponding author:Nicola Cantasano, Institute for Agriculture and Forestry Systems in the Mediterranean (ISAFoM) CNR, Italy

Submission: August 23, 2024; Published: October 16, 2024

DOI: 10.31031/EAES.2024.12.000792

ISSN 2578-0336
Volume12 Issue 4

Abstract

This study aims to summarize the history of biological invasions by alien macrophytes in the Mediterranean Sea from 1880 to 2020 years on a decadal basis. At the same time, it has been analyzed the impacts of sea warming and the increasing trend of sea surface temperature affecting invasive processes. The high number of Not-Indigenous Species and Invasive Alien Species, widespread in the basin, needs a continuous and updated monitoring of the process. In this way, the traditional recording methods, realized by scientific surveys are, actually, improved by Citizen Science activities very useful to study and update the presence of invasive allochthonous macrophytes widespread in the Mediterranean. From the resulting data, it has been highlighted the large diffusion of thermophilic and invasive alien macrophytes, by tropical and subtropical origin, coming from Indo-Pacific regions. Finally, to manage this invasive process, it is necessary to have a close collaboration between Science, Policy, and Citizenship.

Keywords:Biological invasions; Macrophytes; Warming; Non-Indigenous species; Invasive alien species; Citizen science

Introduction

In the anthropocene era, characterized by human-driven processes [1], biological invasions are becoming one of the most important issues affecting terrestrial and aquatic ecosystems worldwide [2-5]. This phenomenon is a serious threat to the sensitive balance of marine ecosystems in the Mediterranean Sea [6]. Nevertheless, global warming, Sea Surface Temperature (hereafter, SST) and the introduction of alien species in a climate change scenario, are actually increasing but the link between these trends is still unclear and very debated in the scientific community. Indeed, in these last decades it has been observed a coupled increase of SST and bio invasions [7]. So, it has been suggested that such thermal rise could support, in time, the spread of Not-Indigenous Species (hereafter NIS) in the Mediterranean [8]. European Union has defined NIS as species able to spread outside their native biogeographic regions to new areas [9]. However, the introduction of NIS species into a new marine environment is not directly related to their success in diffusion and establishment. The outcome of an invasive process depends on the interactions between the biological characteristics of what we refer to as invasive species and the species indicated as indigenous. Really, the establishment of NIS species depends on their potential to settle, spread and colonize local biotopes [10]. At the end of the process, some NIS become stable and widespread in the Mediterranean Sea changing their status to Invasive Alien Species (hereafter IAS), as a subset of NIS. IAS are defined by IAS Regulation, issued by the European Union [11], as alien species whose spreading could threaten marine biodiversity and the right functioning of ecosystem services [12-14].

More generally, this invasive trend may cause, also, social and economic impacts [15,16]. Worldwide, the financial costs of biological invasions have been estimated to be US $1.288 trillion in the period 1970-2017 [17]. The high number of NIS and IAS species, actually widespread in the basin, makes the Mediterranean Sea a real hotspot for bio invasions [18-21]. Amongst the main abiotic factors influencing the evolution of this invasive process, temperature is certainly one of the most important driving forces affecting the success or the failure of NIS invasion because all these species thrive within their thermal niches [22,23]. Since the 1980s, the Mediterranean Sea has become warmer, according to an increasing trend twice than ocean seawaters [24,25]. However, just 10% of the whole scientific literature analyses the relationship between the progressive warming of Mediterranean Sea and the present trend of biological invasions occurring in the basin [26]. In particular, SST is one of the most important thermal variables to value the present climate conditions of the basin and to foresee the future impacts of climate changes on global and regional scales, in this way, it has been highlighted that SST, in the period 1985-2011, increased +0.25 °C decade-1 in the western sub-basin and +0.65 °C decade-1 in the eastern one [27]. This growing trend has determined, over time, the spread of Indo-Pacific species of tropical and subtropical origin, with a slow and gradual tropicalization of the basin [28,29], which is becoming more sensitive to the establishment of a termophilic biota. Indeed, many of these tropical and subtropical invaders have reached, in time, the northern sectors of the basin [30,31], causing their meridionalization [32]. To the considerations just made, it is necessary to add the human factor. In fact, what is known as Citizen Science, in the last two decades, has taken up an important factor in the identification of alien species, initially understood as NIS and which then took on the role of IAS [33-36].

The Mediterranean Sea holds about 1500 species of macrophytes [37], including macroalgae and marine plants, with a rate of endemism of about 20% [38,39]. In particular, alien macrophytes represent a rate between 20% and 29% of the total number of NIS species living in the Mediterranean seawaters [40- 42]. These invasive species may cause negative impacts at ecological levels inducing possible reductions of local biota [43-46]. A lot of lists, regarding NIS and IAS species have been published for the Mediterranean Sea [47-51]. Furthermore, recent studies, through an in-depth review of historical data on NIS and IAS species, have shown that their number, considerably, increased over time [52]. Indeed, Citizen Science activities have considerably contributed to the knowledge of invasive processes through active information and training channels between the academic world and ordinary citizens. This close collaboration between scientists and people has, more and more, increased the number of NIS reports, as summarised in [53]. Our investigation aims to suggest an updated list of NIS and IAS macrophytes living in the Mediterranean Sea through a specific database of these invasive and alien species, excluding cryptogenic and questionable records [53]. This list is the final result of a long set of reports conducted by scientists and citizens from 1880 to 2020 years. The research analyzes, also, the warming trend of Mediterranean seawaters in these last decades and its effect on the invasive process of NIS macrophytes widespread in the basin.

Methodology

The high number of alien macrophyta species, widespread in the Mediterranean Sea, requires a constant and updated control of invasive processes. However, the traditional methods of mapping and monitoring are long, expensive and limited in space and time.

In this critical context, Citizen Science, despite all its limitations, has become a useful tool to study the widespread distribution of NIS and IAS species in the Mediterranean seawaters. So, it has been utilized the reports supplied by the activities of fishermen, divers, tourists and citizens to collect temporal and spatial information about these invasive species, side by side with the study, distribution, abundance and spread of allochtonous macroalgae widespread in the basin. The present study aims to follow on a decadal basis, the history of this invasive process, performed by alien marine macrophytes from 1880 to 2020. In parallel, it has been valued the warming impact of Mediterranean seawaters through satellite data, on a decadal basis, issued by Copernicus Marine Monitoring Service (CMMS), for the period between 1982 and 2020 years.

To date NIS and IAS lists, it has been consulted scientific literature, updated to 2023 year, using the main databases drawn by some digital platforms such as: Google Scholar, Web of Science, Scopus and Research Gate. The bibliographic search has been realized according to the following keywords: Citizen Science, Mediterranean Sea, non-indigenous species, invasive alien species, macrophytes and macroalgae. The lists of NIS and IAS species have been realized through the informations supplied by citizen scientists and by an informative bibliographic search. All these data have been updated by scientists and validated by taxonomists according to the World Register of Marine Species (WoRMS) (Figure 1). The roles of citizen scientists and taxonomists are clearly differentiated because the first ones have the main function to point out the presence of alien species in Mediterranean coastal seawaters while the second ones perform the important role to establish their systematic position. The criteria to assess the status of NIS and IAS species and to assign their biogeographical origin have been drawn by [11]. Finally, the species with a doubtful origin or with an uncertain systematic position have been defined as “uncertain”.

Figure 1:The pattern of validation of NIS and IAS species.


Results

The resulting data are shown in two databases of alien macrophytes, including macroalgae and marine plants, widespread in the Mediterranean Sea. The first directory includes 92 NIS (Table 1), while the second one shows just 26 IAS (Table 2). This information are drawn by scientific and popular records conducted from 1880 to 2020 years and summarized in two lists including altogether 118 allochtonous macrophyta species.

Table 1:List of NIS and their first years of detection at region levels in Mediterranean basin (legends: WAO=Western Atlantic Ocean; NAO=Northeast Atlantic Ocean; IPO/RS=Indo-Pacific/Read Sea; NPO=Northwest Pacific Ocean; A=Australasia; U=Uncertain). [The taxa nomenclature is updated according to www.algaebase.org consulted on 18 June 2024].


Table 2:List of IAS and their first years of detection at regional levels in Mediterranean basin (legends: WAO=Western Atlantic Ocean; NAO=Northeast Atlantic Ocean; IPO/RS=Indo-Pacific/Read Sea; NPO=Northwest Pacific Ocean; A=Australasia; U=Uncertain). [The taxa nomenclature is updated according to www.algaebase.org consulted on 18 June 2024].


Most of the reports regards the coastline of France (34.7%) followed by Italy (26.3%), Spain (16.8%), Israel (6.6%), Turkey (4.2%), Greece (3.2%), Tunisia (2.1%), Egypt (2.1%) and other Mediterranean regions with low percentages (Figure 2). The geographic distribution of the reports could be explained by two different factors that interacted one each other. On one hand, the nations with the highest percentages of collected NIS are those in which the study of marine biology shows an older tradition. Another reason, for the high number of records, regarding marine alien species, is certainly linked to the spread of recreational diving activities which were born in France immediately after the Second War World (WWII) and, subsequently, began to spread also in Italy and in Spain.

Figure 2:Regional percentages of NIS and IAS macrophyta species reported for Mediterranean regions.


From a careful analysis of the temporal records, it is possible to observe that the trend of this invasive process is rather unstable and strongly fluctuating decade after decade. In fact, in the first period, between 1880 and 1950, a small number of reports were recorded with only eleven alien species identified (Figure 3). This condition was probably caused by the long period of conflicts that affected the European continent, culminating in the first War World (WWI) and in the Second War World (WWII), leading to some indifference in this type of scientific research. In the following period, between 1950 and 2000, when the socio-economic conditions of European countries enjoyed a period of relative wellbeing, with a resulting increase in the tourist industry linked to underwater activities, the number of NIS reports increased strongly up to a maximum value of twenty-five NIS in the decade 1980/1990. This growing trend significantly decreased in the decades 2000-2010 and 2010-2020 with eleven and ten NIS records respectively (Figure 4 & 5). Also in this case, socio-economic reasons could have affected research activities linked to marine biology. Really, the low number of NIS recorded in these last decades is, probably, caused by the declining survey efforts, as stated by the Kumminga Montreal Global Biodiversity Framework (GBF) that calls for a 50% reduction of monitoring efforts by 2030 [54]. However, in these last years, there is a higher number of tropical and subtropical thermophilic macrophytes than temperate and cosmopolitan ones (Figure 6 & 7). In fact, from the collecting data, it is highlighted a clear drop of these last species since 2000 year [55].

Figure 3:The temporal trend of the invasive process of NIS and IAS from 1880 to 2020 years on a decadal basis.


Figure 4:Geographic distribution of school and diving centers in Mediterranean countries (from: Scuba Diving centers and diving sites, https://www.divescover.com).


Figure 5:The increasing trend of SST in Mediterranean seawaters.


Figure 6:Number of NIS and IAS macrophytes distinguished by their biogeographic origins (legends: WAO=Western Atlantic Ocean; NAO=Northeast Atlantic Ocean; IPO/RS=Indo-Pacific/ Read Sea; NPO=Northwest Pacific Ocean; A=Australasia; U=Uncertain).


Figure 7:Pie chart detailing the percentages of NIS and IAS macrophytes distiguished by their biogeographic origins (legends: WAO=Western Atlantic Ocean; NAO=Northeast Atlantic Ocean; IPO/RS=Indo-Pacific/ Read Sea; NPO=Northwest Pacific Ocean; A=Australasia; U=Uncertain).


At the same time, there was a clear drop in the industry of underwater tourism with the closure of dozens of school and diving centers previously widespread along the coastlines of Mediterranean Sea (Figure 4). The different number of invasive macrophytes from tropical and temperate NIS is becoming more evident in the last decades. Really, in Mediterranean seawaters the global media of SST rised of about 1 °C since 1980s and such increasing trend is actually ongoing (Figure 5).

So, these conditions have caused, in time, ideal thermic values for the growth and the expansion of thermophilic macrophytes by Indo-Pacific regions. In a climate change scenario, SST appears strictly connected with the increasing trend of Marine Heatwaves (MHWs), as highlighted also by scientific literature [56]. The coupled effects of these climate factors can increase the spreading of tropical and subtropical species in the Mediterranean seawaters [57]. Globally, the non-indigenous macrophytes are about the 10% of the whole Mediterranean marine flora but these data must be distinguished according to the biogeographic origins of NIS and IAS macroalgae. In this way, a greater number of tropical and subtropical thermophilic macrophytes, coming from NPO, IPO/RS and A regions, arrived at the basin, compared to cosmopolitan and temperate species native of WAO and NAO regions (Figure 6). In particular, NIS and IAS, coming from NPO, IPO/RS and A regions are prevailing with respective percentages of 38%, 23% and 13%, while the cosmopolitan and temperate species, by WAO and NAO regions, show respectively rates of 13% and 3% of the whole (Figure 7).

Discussion

Mediterranean Sea has become, in time, very sensitive to biological invasions, leading to a gradual change of its marine biota. This growing trend leads to the introduction of many alien algal species coming from Indian, Pacific and Atlantic oceans through two marine corridors, as are the Strait of Gibiltrar and the Suez Canal. There are two driving forces supporting the process of bio invasions. Firstly, the increasing commercial trade by maritime traffic into the basin has caused the introduction of many macrophyta species through ballast waters and biofouling [58,59]. Secondly, the opening of Suez Canal in 1880, the reduction of salinity levels in bitter lakes since 1960s and the late doubling of this corridor in 2015, have established a steady sea-level waterway for thermophilic species including animals, plants, fungi, bacteria, etc., by Indo-Pacific origin, into the Mediterranean Sea [60]. To the databases presented here, most of NIS and IAS macrophytes belong to the systematic division of Rhodophyta with respective percentages of 68.0% and 53.8%, while lower rates are represented by Ochrophyta (23.1% and 16.3%) and Chlorophyta (23.1% and 15.5%) of the whole marine invasive flora (Figure 8).

Figure 8:Bar chart representing NIS and IAS percentages within macroalgal divisions.


Generally speaking, the increasing introduction of NIS and IAS is leading to the tropicalization of the basin [61]. Indeed, the Mediterranean regions more affected by invasive processes are French and Italian coastlines (Figure 2), as confirmed by the presence of two important hotspots for the introduction of alien macrophytes. The main area prone to invasive processes is the Thau Lagoon (France) where 58 macroalgal NIS, as the 63% of the whole number of alien marine flora, are well established [62]. The second zone, sensitive to bio invasions, is the Venice Lagoon, where 14 macroalgal NIS, as the 15% of the whole, are reported by scientific literature [63-65]. So, Mediterranean is actually exposed to a gradual and steady warming of its seawaters at a rate 2/3 times faster than ocean ones [66]. This warming trend, inserted in a climate change scenario, supports the introduction and the establishment of thermophilic tropical and subtropical alien macrophytes coming from Indo-Pacific regions [67].

In this way, NIS and IAS macroalgae are characterized by thermal ranges higher than those of indigenous species, showing a greater capacity to adapt quickly to the increasing temperatures of the basin [68,69]. Therefore, NIS are able to maintain their populations alive within a wider thermal niche. So, the higher number of alien tropical and subtropical macroalgal species could be related to their better resistance towards the lowest temperatures of the basin, enabling them to widespread in the Mediterranean Sea. On the contrary, the lower introduction rates of temperate and cosmopolitan alien species, reported in these last decades, could be ascribed to the highest summer values of Mediterranean SST (Figure 5). Indeed, MHWs could have caused a lower rate in the spreading of invasive temperate macrophytes and, in some serious cases, large-scale mortality events [70-72]. From the resulting data, it is possible to assert that most of NIS and IAS macrophytes, spreading in Mediterranean seawaters, come from the warmer waters of Pacific and Indian oceans with respective percentages of 38% and 23% of the whole invasive macroalgal division (Figure 6 & 7).

After all, the success of thermophilic macrophytes is supported, also, by their greater capacity in the interactions with other indigenous macroalgal species. In fact, Indo-Pacific NIS, accustomed to a great species richness and to high levels of interspecific competition in their native environments [73,74], might have great advantages invading Mediterranean temperate seawaters for the lower or absent mutual contest. In a climate change scenario, the native biodiversity levels could suffer a clear drop caused by the negative effects of marine global warming, so affecting the right functioning of ecosystem services. These data confirm that Mediterranean marine flora is gradually changing its composition from temperate and cosmopolitan species, by Atlantic origin, to tropical and subtropical ones, coming from the warmer waters of Indo-Pacific oceans.

Finally, a lot of reports, supporting decision-making processes, come from Citizen Science [75]. Also in this study, the information collected by citizen scientists on some NIS and IAS macrophytes, by special importance, has supplemented the scientific monitoring according to other surveys conducted worldwide [76,77]. In this way, Citizen Science has become an important tool not only to counterbalance the limited financial means available to researchers, but also to generate greater public awareness towards possible solutions and political actions.

Conclusion

This study highlights the successful invasive process and the widespread diffusion of thermophilic NIS macrophytes by tropical and subtropical origins, from the southeastern areas of Mediterranean towards the northwestern ones. The increasing trend in the introduction of NIS macrophytes, the warming of Mediterranean seawaters and the rise of commercial trade by maritime transport make the basin a real hotspot for biological invasions. Indeed, the environmental impacts of NIS and IAS on coastal ecosystems could be more marked in the present context of climate change [78]. So, cold water macrophytes could be replaced by warm water ones while the impacts of MHWs on vegetal communities could lead to the disappearance of canopy-forming species and to the prevalence of turf ones. An effective management of invasive processes requires a prompt report of NIS and IAS and their continuous monitoring in time and in space involving tourists, fishermen, divers and citizens in data collection.

All this, however, could lead to a wrong perception, evaluating the presence of exotic species marked as NIS. Therefore, it is suggested that, in studies concerning the spread of exotic species, it is necessary to carefully value the relative SST components, the migratory routes of NIS and IAS and the contribution of Citizen Science. Only in this case, it is possible to avoid false beliefs relating the invasiveness of species which, despite being NIS, do not have the typical characteristics of IAS. Anyhow, in these last years the interest of the whole scientific community towards this complementary tool is, remarkably, increased [79-81] not only to point out the presence of NIS and IAS macrophytes, but also to increase a public awareness about this important topic. In conclusion, it is necessary to counteract the negative effects of bio invasions through a sound coastal governance and coordinate actions at international level so to prevent NIS introductions and to manage IAS establishment, reducing their impacts at ecological and economic levels.

References

  1. Lewis SL, Maslin MA (2015) Defining the anthropocene. Nature 519(7542): 171-180.
  2. Primack R (1995) A primer of conservation biology. Sinaeur Associates Inc Publishers, Sunderland, Massachusetts, USA, p. 292.
  3. Rilov G, Crooks JA (2009) Biological invasions in marine ecosystems: Ecological, management and geographic perspectives. Springer, Berlin, Germany, p. 641.
  4. Ehrenfeld JG (2010) Ecosystem consequences of biological invasions. Annual Review of Ecology, Evolution, and Systematics. Annual Reviews 41(1): 59-80.
  5. Vilà M, Rohr RP, Espinar JL, Hulme PE, Pergl J, et al. (2015) Explaining the variation in impacts of non‐native plants on local‐scale species richness: The role of phylogenetic relatedness. Global Ecology and Biogeography 2(2): 139-146.
  6. Díaz SU, Pascual M, Stenseke B, Martín-López RT, Watson Z, et al. (2019) Assessing nature’s contributions to people. Science 359(6373): 270-272.
  7. Guastella R, Marchini A, Caruso A, Evans J, Cobianchi M, et al. (2021) Reconstructing bioinvasion dynamics through micropaleontologic analysis highlights the role of temperature change as a driver of Alien Foraminifera Front Mar Sci 8: 675807.
  8. Giangrande A, Pierri C, Del Pasqua M, Gravili C, Gambi MC, et al. (2020) The mediterranean in check: Biological invasions in a changing sea. Mar Ecol 41(2): e12583.
  9. Gian-Reto W, Roques A, Hulme PE, Martin T, Sykes T, et al. (2009) Alien species in a warmer world: Risks and opportunities. Trends in Ecology & Evolution 24(12): 686-693.
  10. Early R, Bradley B, Dukes J, Lawler JL, Olden JD, et al. (2016) Global threats from invasive alien species in the twenty-first century and national response capacities. Nature Communications 7: 12485.
  11. European Union (2014) Regulation (EU) No 1143/2014 of the European parliament and of the council of 22 October 2014 on the prevention and management of the introduction and spread of invasive alien species. Off J Eur Union L 317: 35-55.
  12. Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, et al. (2001) The population biology of invasive species. Annual Review of Ecology and Systematics 32(1): 305-332.
  13. Wallentinus I, Nyberg C (2007) Introduced marine organisms as habitat modifiers. Marine Pollution Bulletin 55(7-9): 323-332.
  14. Essl F, Bacher S, Genovesi P, Hulme PE, Jeschke J, et al. (2018) Which taxa are alien? criteria, applications, and uncertainties. BioScience 68(7): 496-509.
  15. Katsanevakis S, Wallentinus I, Zenetos A, Leppäkoski E, Çinar ME, et al. (2014) Impacts of invasive alien marine species on ecosystem services and biodiversity: A pan-European review. Aquatic Invasions 9(4): 391-423.
  16. Vergés A, Steinberg PD, Hay ME, Alistair GB, Poore AH, et al. (2014) The tropicalization of temperate marine ecosystems: Climate-mediated changes in herbivory and community phase shifts. Proc R Soc B 281(1789): 20140846.
  17. Diagne C, Leroy B, Vaissière AC, Gozlan RE, Roiz DA, et al. (2021) High and rising economic costs of biological invasions worldwide. Nature 592: 571-576.
  18. Boudouresque C, Verlaque M (2005) Nature conservation, marine protected areas, sustainable development and the flow of invasive species to the Mediterranean Sea. Sci Rep Port-Cross Natl Park Fr 21: 29-54.
  19. Galil B, Boero F, Fraschetti S, Piraino S, Campbell M, et al. (2015) The enlargement of the Suez Canal and introduction of non-indigenous species to the Mediterranean Sea. Limnology and Oceanography Bulletin 24: 43-45.
  20. Bellard C, Cassey P, Blackburn TM (2016) Alien species as a driver of recent extinctions. Biol Lett 12(2): 20150623.
  21. Gallardo B, Clavero M, Sánchez MI, Vilà M (2016) Global ecological impacts of invasive species in aquatic ecosystems. Glob Change Biol 22(1): 151-163.
  22. Zenetos A, Gofas S, Verlaque M, Çinar M, García Raso J, et al. (2010) Alien species in the Mediterranean Sea by 2010. A contribution to the application of European Union’s Marine Strategy Framework Directive (MSFD) Part I Spatial distribution. Mediterranean Marine Science 11: 381-493.
  23. Zenetos A, Ovalis P, Giakoumi S, Kontadakis C, Lefkaditou E, et al. (2020) Saronikos Gulf: A hotspot area for alien species in the Mediterranean Sea. BioInvasions Records 9(4): 873-889.
  24. Brown JH, Gillooly JF, Allen AD, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85(7): 1771-1789.
  25. Angilletta MJ (2009) Thermal adaptation: A theoretical and empirical synthesis. Oxford University Press, Oxford, England, 2009, p. 302.
  26. Salat J, Pascual J (2002) The oceanographic and meteoro-logical station at l’Estartit (NW Mediterranean). In: Briand F (Ed.), Tracking Long-Term Hydrological Change in the Mediterranean Sea, CIESM Workshop Ser 16, Monaco.
  27. Wesselmann M, Apostolaki ET, Anton A (2024) Species range shifts, biological invasions and ocean warming. Marine Ecology Progress Series 728: 81-83.
  28. Bianchi CN (2007) Biodiversity issues for the forthcoming tropical Mediterranean Sea. Hydrobiologia 580(1): 7-21.
  29. Vargas-Yáñez M, Moya F, Tel E, Garcia-Martinez M, Guerber E, et al. (2009) Warming and salting in the western Mediterranean during the second half of the 20th century: Inconsistencies, unknowns and the effect of data processing. Scientia Marina 73(1): 7-28.
  30. Ben Rais Lasram F, Tomasini JA, Guilhaumon F, Romdhane MS, Do Chi T, et al. (2008) Ecological correlates of dispersal success in Lessepsian fishes. Marine Ecology Progress Series 363: 273-286.
  31. Raitsos D, Beaugrand G, Georgopoulos D, Zenetos A, Pancucci-Papadopoulou AM, et al. (2010) Global climate change amplifies the entry of tropical species into the eastern Mediterranean Sea. Limnology and Oceanography 55(4): 1478-1484.
  32. Bianchi CN, Morri C, Chiantore M, Montefalcone M, Parravicini V, et al. (2012) Mediterranean Sea biodiversity between the legacy from the past and a future of change. In: Stambler N (Ed.), Life in the Mediterranean Sea: A look at habitat changes. Nova Science Publishers, New York, USA, pp. 1-55.
  33. Chandler M, See L, Copas K, Bonde AM, López BC, et al. (2017) Contribution of citizen science towards international biodiversity monitoring. Biol Conserv 213: 280-294.
  34. Roy H, Groom Q, Adriaens T, Agnello G, Antic M, et al. (2018) Increasing understanding of alien species through citizen science (Alien-CSI). Res Ideas Outcomes 4: e31412.
  35. Encarnação J, Teodósio MA, Morais P (2021) Citizen science and biological invasions: A review. Front Environ Sci 8: 602980.
  36. Marchante E, López-Núñez FA, Duarte LN, Marchante H (2024) The role of citizen science in biodiversity monitoring: When invasive species and insects meet. Biological Invasions and Global Insect Decline, Academic Press, Cambridge, MA, USA, pp. 291-314.
  37. Boudouresque C (2004) Marine biodiversity in the mediterranean: Status of species, populations and communities. Sci Rep Port-Cros Natl Park Fr 20: 97-146.
  38. Giaccone G (1974) Typologies of mediterranean phytobenthic communities. Memoirs of Marine Biology and Oceanography 4: 149-168.
  39. Coll M, Piroddi C, Steenbeek J, Kaschner K, Ben Rais Lasram F, et al. (2010) The biodiversity of the Mediterranean Sea: Estimates, patterns, and threats. Plos One 5(8): e11842.
  40. Schaffelke B, Smith J, Hewitt C (2006) Introduced macroalgae-a growing concern. Journal of Applied Phycology 18(3): 529-541.
  41. Molnar JL, Gamboa RL, Revenga C, Spalding MD (2008) Assessing the global threat of invasive species to marine biodiversity. Frontiers in Ecology and the Environment 6(9): 485-492.
  42. Katsanevakis S, Gatto F, Zenetos A, Cardoso C (2013) How many marine aliens in Europe? Management of Biological Invasions 4(1): 37-42.
  43. Hammann M, Bucholz B, Karez R, Weingerger F (2013) Direct and indirect effects of Gracilaria vermiculophylla on native Fucus vescicolosus. Aquatic invasions 8(2): 121-132.
  44. Maggi E, Benedetti-Cecchi L, Castelli A, Chatzinikolaou E, Crowe TP, et al. (2015) Ecological impacts of invading seaweeds: a meta-analysis of their effects at different trophic levels. Diversity Distribution 21(1): 1-12.
  45. Bulleri F, Benedetti-Cecchi L, Jaklin A, Ivesa L (2016) Linking disturbance and resistance to invasion via changes in biodiversity: a conceptual model and an experimental test on rocky reefs. Ecology and Evolution 6(7): 2010-2021.
  46. Anton A, Geraldi NR, Lovelock CE, et al. (2019) Global ecological impacts of marine exotic species. Nat Ecol Evol 3(5): 787-800.
  47. Zenetos A, Cinar M, Pancucci-Papadopoulou M, Harmelin J, Furnari G, et al. (2005) Annotated list of marine alien species in the mediterranean with records of the worst invasive species. Mediterranean Marine Science 6(2): 63-118.
  48. Zenetos A, Meric E, Verlaque M, Galli P, Boudouresque C, et al. (2008) Additions to the annotated list of marine alien biota in the mediterranean with special emphasis on Foraminifera and parasites. Mediterranean Marine Science 9(1): 119-166.
  49. Galil BS (2008) Alien species in the Mediterranean Sea-which, when, where, why? Hydrobiologia 606(1): 105-116.
  50. Galil BS (2009) Taking stock: Inventory of alien species in the Mediterranean sea. Biol Invasions 11: 359-372.
  51. Zenetos Α, Gofas S, Morri C, Rosso A, Violanti D, et al. (2012) Alien species in the Mediterranean sea by 2012. A contribution to the application of European Union’s Marine Strategy Framework Directive (MSFD) Part 2. Introduction trends and pathways. Mediterranean Marine Science 13(2): 328-352.
  52. Galil BS, Douek J, Mienis HK, Rinkevich B (2016) Comments on “The Mediterranean sea as a gateway for invasion of the red sea: The case of the Indo-West Pacific head-shield slug Chelidonura fulvipunctata Baba, 1938” by Manuel António E Malaquias, Andrea Zamora-Silva, Dyana Vitale, Andrea Spinelli, Sergio De Matteo, Salvatore Giacobbe, Deneb Ortigosa and Juan L Cervera. Aquatic Invasions 11(4): 351-354.
  53. Zenetos A, Delongueville C, Scaillet R (2024) An overlooked group of citizen scientists in Non-Indigenous Species (NIS) information: Shell collectors and their contribution to molluscan NIS Xenodiversity. Diversity 16: 299.
  54. McGeoch MA, Buba Y, Arlé E, Belmaker J, Clarke DA, et al. (2023) Invasion trends: An interpretable measure of change is needed to support policy targets. Conservation Letters 16(6): e12981.
  55. Bosch S (2017) Marine species distributions: From data to predective models. Doctoral dissertation, Ghent University, Ghent, Belgium, pp. 232.
  56. Karez CS, Willemes MJ, Carvalho RT, Salgado LT (2024) Sea surface temperature and marine heatwaves impacts on marine macroalgae. Examines Mar Biol Oceanogr 6(5): 1-5.
  57. Hulme M (2009) Why we disagree about climate change Cap Seven: The Communication of Risk. Cambridge University Press, Cambridge, England, pp. 211-247.
  58. Hewitt JE, Anderson MJ, Hickey CW, Kelly S, Trush SF (2009) Enhancing the ecological significance and sediment contamination guidelines through integration with community analysis. Environmental Science & Technology 43(6): 2118-2123.
  59. Seebens H, Essl F, Dawson W, Fuentes N, Moser D, et al. (2015) Global trade will accelerate plant invasions in emerging economies under climate change. Glob Change Biol 21(11): 4128-4140.
  60. Galil BS, Marchini A, Occhipinti-Ambrogi A, Ojaveer H (2017) The enlargement of the Suez Canal-Erythraean introductions and management challenges. Management of Biological Invasions 8: 141-152.
  61. Bianchi CN, Morri C (2003) Global sea warming and “tropicalization” of the Mediterranean Sea: Biogeographic and ecological aspects. Biogeographia-The Journal of Integrative Biogeography 24: 319-327.
  62. Verlaque M (2001) Checklist of the macroalgae of Thau lagoon (Hérault, France), a hotspot of marine species introduction in Europe. Oceanologica Acta 24(1): 29-49.
  63. Sfriso A (1987) Flora and vertical distribution of macroalgae in the lagoon of Venice: A comparison with previous studies. Giornale Botanico Italiano 121(1-2): 69-85.
  64. Rismondo A, S Volpe, D Curiel, A Solazzi (1993) Report of Undaria pinnatifida (Harvey) Suringar in Chioggia (Venetian Lagoon). Works Soc Ven Sc Nat 18: 328-330.
  65. Curiel D, Marzocchi M, Bellemo G (1996) First report of fertile Antithamnion pectinatum (Ceramiales, Rhodophyceae) in the North Adriatic Sea (lagoon of Venice, Italy). Bot Mar 39: 19-22.
  66. Schroeder K, Chiggiato J, Bryden H, M Borghini, S Ben Ismail (2016) Abrupt climate shift in the Western Mediterranean Sea. Sci Rep 6: 23009.
  67. Pisano A, Marullo S, Artale V, Falcini F, Yang C, et al. (2020) New evidence of Mediterranean climate change and variability from sea surface temperature observations. Remote Sens 12: 132.
  68. Cecere E, Alabiso G, Carlucci R, Petrocelli A, Verlaque M (2016) Fate of two invasive or potentially invasive alien seaweeds in a central Mediterranean transitional marine system: Failure and success. Botanica Marina 59(6): 451-462.
  69. Wesselmann M, Hendriks IE, Johnson M, Jordà G, Mineur F, et al. (2024) Increasing spread rates of tropical non-native macrophytes in the Mediterranean Sea. Global Change Biology 30(4): e17249.
  70. Alexander MA, Scott JD, Friedland KD, Katherine E Mills, Janet A Nye, et al. (2018) Projected Sea surface temperatures over the 21st century: Changes in the mean, variability and extremes for large marine ecosystem regions of Northern Oceans. Elem Sci Anth 6: 9.
  71. Titelboim D, Almogi-Labin A, Herut B, Michal K, Sarit A, et al. (2019) Thermal tolerance and range expansion of invasive foraminifera under climate changes. Sci Rep 9(1): 4198.
  72. Asakura A (2020) Crustaceans in changing climate: Global warming and invasion of tropical land hermit crabs (Crustacea: Decapoda: Anomura: Coenobitidae) into temperate area in Japan. Zoology 1215: 125893.
  73. Wernberg T, Bennett S, Babcock R, De Bettignies T, Cure K, et al. (2016) Climate-driven regime shift of a temperate marine ecosystem. Science 353(6295): 169-172.
  74. Zanolla M, Carmona R, De La Rosa J, Altamirano M (2018) Structure and temporal dynamics of a seaweed assemblage dominated by the invasive lineage 2 of Asparagopsis taxiformis (Bonnemaisoniaceae, Rhodophyta) in the Alboran Sea. Mediterranean Marine Science 19(1): 147-155.
  75. Pocock M, Roy H, August T, Kuria A, Munyekenye F (2018) Developing the global potential of citizen science: Assessing opportunities that benefit people, society and the environment in East Africa. Journal of Applied Ecology 56(2): 274-281.
  76. Giovos I, Kleitou P, Poursanidis D, Ioannis Batjakas, Giacomo Bernardi, et al. (2019) Citizen-science for monitoring marine invasions and stimulating public engagement: A case project from the eastern Mediterranean. Biol Invasions 21: 3707-3721.
  77. Lehtiniemi M, Outinen O, Puntila-Dodd R (2020) Citizen science provides added value in the monitoring for coastal non-indigenous species. Journal of Environmental Management 267: 110608.
  78. Katsanevakis S, Olenin S, Puntila R, Rilov G, Staehr P, et al. (2023) Marine invasive alien species in Europe: 9 years after the IAS Regulation. Frontiers in Marine Science 10: 1271775.
  79. Galil BS, Danovaro R, Rothman SBS, R Gevili, M Goren (2018) Invasive biota in the deep-sea Mediterranean: An emerging issue in marine conservation and management. Biological Invasions 21: 281-288.
  80. Bennett NJ, Blythe J, White CS, Campero C (2021) Blue growth and blue justice: Ten risks and solutions for the ocean economy. Marine Policy 125: 104387.
  81. Tiralongo F, Hall-Spencer JM, Giovos I, Kleitou P (2022) Editorial: Biological invasions in the Mediterranean Sea. Front Mar Sci 9: 1016168.

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