Sie können Operatoren mit Ihrer Suchanfrage kombinieren, um diese noch präziser einzugrenzen. Klicken Sie auf den Suchoperator, um eine Erklärung seiner Funktionsweise anzuzeigen.
Findet Dokumente, in denen beide Begriffe in beliebiger Reihenfolge innerhalb von maximal n Worten zueinander stehen. Empfehlung: Wählen Sie zwischen 15 und 30 als maximale Wortanzahl (z.B. NEAR(hybrid, antrieb, 20)).
Findet Dokumente, in denen der Begriff in Wortvarianten vorkommt, wobei diese VOR, HINTER oder VOR und HINTER dem Suchbegriff anschließen können (z.B., leichtbau*, *leichtbau, *leichtbau*).
The Westernmost Record of the Scyphomedusa Cassiopea andromeda (Forskål, 1775) in the Mediterranean: Marine Citizen Science Contributions to Invasive Species Detection and Monitoring
Der Artikel präsentiert den ersten phylogenetisch bestätigten Nachweis der invasiven Quallenart Cassiopea andromeda in spanischen Gewässern und den westlichsten Nachweis im Mittelmeer. Er diskutiert die Rolle der marinen Bürgerwissenschaft bei der Früherkennung und Überwachung invasiver Arten und hebt die Beiträge der Plattform Observadores del Mar hervor. Der Text untersucht auch die ökologischen und sozioökonomischen Auswirkungen von Cassiopea andromeda, einschließlich seiner hohen Toleranz gegenüber thermischer Belastung und seines Potenzials, sich rasch auszubreiten. Darüber hinaus geht der Artikel auf die genetische Analyse zur Identifizierung von Arten und die Bedeutung öffentlicher DNA-Datenbanken ein. Die Schlussfolgerung betont die Bedeutung der marinen Bürgerwissenschaft für die Ausweitung der räumlich-zeitlichen Meeresforschung und für die Förderung der Alphabetisierung der Ozeane und der Bemühungen zum Schutz der Meere.
KI-Generiert
Diese Zusammenfassung des Fachinhalts wurde mit Hilfe von KI generiert.
Abstract
The Mediterranean Sea, although a biodiversity hotspot, is one of the most affected seas by non-indigenous species (NIS). This problem is worsened by rising sea temperatures due to climate change, which promotes the spread of thermophilic species. Among the NIS scyphozoan jellyfish species recorded in the Mediterranean, Cassiopea andromeda – commonly known as the “upside-down jellyfish”– is a notable example. Observadores del Mar (OdM) is the leading platform for marine citizen science in Spain and works towards ocean conservation and health. It is a well-established tool for generating knowledge in marine research and has successfully provided early warning of NIS reports in the Mediterranean, while also serving as an effective network for the monitoring of NIS and other indicators. Three reports of C. andromeda from Almeria, southern Spain, have been reported in OdM and thanks to the involvement of its community, 12 samples were collected for phylogenetic analysis and monitoring was done for 15 months in the study area. The results confirmed the first record of C. andromeda in Spanish Mediterranean waters representing the westernmost record in the basin. Monitoring also suggests the species establishment in the area. This study contributes to the knowledge of C. andromeda invasiveness and highlights the importance of marine citizen science in the detection and monitoring of NIS. It also underscores the collaboration and commitment already established between scientists and citizens, which will allow further progress in the fields of biological invasions, management, and policy.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Introduction
The Mediterranean Sea, listed as one of the main hotspots in the world, is home to more than 17,000 marine species, accounting for 7% of the world’s total species (Coll et al. 2010). However, this biodiversity is changing because of various human-mediated impacts, such as species introduction, direct or indirect (Coll et al. 2010; Stock et al. 2018). In particular, the presence of non-indigenous species (NIS), also called exotic, non-native, or alien species, has been used as a biodiversity loss indicator (Katsanevakis et al. 2014), and invasive alien species are considered one of the major threats to marine biodiversity (Roy et al. 2019; Pyšek et al. 2020).
The Mediterranean Sea is one of the most affected seas by biological invasions (Zenetos et al. 2010). Recent studies have listed over 950 alien species introduced into the Mediterranean (Zenetos et al. 2020), a fact that has been favored since the opening of the Suez Canal in 1869 (Galil 2012). The Suez Canal, indeed, is the main entry point for NIS into the Mediterranean (Katsanevakis et al. 2013; Galil et al. 2018), a phenomenon known as “Lessepsian migration”. For jellyfish, scyphozoans in particular, there are records of 18 species in the Mediterranean (reviewed in Badreddine and Bitar 2020), and at least 5 of them are Lessepsian migrants (Galil et al. 1990, 2013, 2017); Rhopilema nomadica Galil et al. 1990; Phyllorhiza punctata von Lendenfeld 1884; Cotylorhiza erythraea Stiasny 1920; Marivagia stellata Galil et al. 2017; and Cassiopea andromeda (Forskål 1775).
Anzeige
Cassiopea andromeda, native to the Red Sea and the Indo Pacific (Mariotini and Pane 2010), was the first Lessepsian jellyfish species described after the opening of the Suez Canal. It was first sighted in Cyprus in 1903 (Mass 1903), and since then, it has been reported (at least punctually or repeatedly observed) in almost the entire eastern basin (Goy et al. 1988; Spanier 1989; Çevik et al. 2006; Schembri et al. 2010; Zenetos et al. 2011; Siokou et al. 2013; Yokes et al. 2018; Servello et al. 2019; Crocetta et al. 2021) (Fig. 1). Regarding the western basin, the presence of C. andromeda has been documented on rare occasions, and the only records come from northern Tunisia (Amor et al. 2015) and Sicily (Cillari et al. 2018; Maggio et al. 2019). Later, Cassiopea sp. was reported in Mar Menor (Murcia, Spain) in 2017 (Rubio 2017); however, it was an occasional grey-literature report of a single small individual without species identification.
Fig. 1
First records of Cassiopea andromeda in the Mediterranean Sea after the Suez Canal opening. 1: Maas (1903); 2-3: Galil et al. (1990); 4: Çevik et al. (2006); 5: Schembri et al. (2010); 6: Zenetos et al. (2011); 7: Siokou et al. (2013); 8: Amor et al. (2015); 9: Yokes et al. (2018); 10: Cillari et al. (2018); 11: Crocetta et al. (2021). The map was obtained and modified from www.d-maps.com
Within the genus Cassiopea (order Rhizostomeae), which contains several species (e.g., C. mayeri, C. frondosa, C. ornata, C. xamachana, C. andromeda), C. andromeda is the only species reported in the Mediterranean Sea. Most reports in this area identify C. andromeda by morphology without confirming it through molecular barcoding (Cillari et al. 2022; Deidun et al. 2018; Çevik et al. 2006), except for that from Palermo, Sicily (Maggio et al. 2019). However, Cassiopea is considered a cryptic species, therefore identification based on physical characters such as the color or pattern of spots at the exumbrella, number of rhopalia, shape and number of mouth appendages, length of oral arms, or arrangement of canals in the umbrella, are not entirely reliable and rigorous, as they can be highly variable between individuals of the same species (Jarms and Morandini 2019). For this reason, the use of molecular tools such as 16S ribosomal RNA (16S) and mitochondrial cytochrome c oxidase subunit I (COI) gene identity is especially relevant in any study involving this genus (Muffett and Miglietta 2023; Holland et al. 2004). In addition, NIS such as C. andromeda can also be detected through environmental DNA (eDNA), a powerful and cost-effective method capable of identifying species even when they are not yet conspicuous. For instance, C. andromeda was detected via eDNA along the northern, eastern, and southern coasts of Sicily, during periods when medusae were not visually observed (Aglieri et al. 2023).
C. andromeda is commonly known as the “upside down jellyfish” because it lies on its umbrella surface to expose to the light the symbiotic dinoflagellates of the family Symbiodiniaceae (De Domenico et al. 2025) present in their oral arms to facilitate photosynthesis (Lampert et al. 2011). This species typically inhabits warm and well-illuminated shallow waters such as mangroves and seagrass beds and areas with muddy or sandy bottoms. Recent studies have presented records of C. andromeda in harbors, such as the case of Malta (Schembri et al. 2010) and Augusta and Palermo in Sicily (De Rinaldis et al. 2021; Cillari et al. 2018, 2022).
C. andromeda jellyfish is considered an invasive species (Katsanevakis 2011), and like every invasive species, it may have an ecological impact, as it can proliferate rapidly, forming large blooms within a short time frame (Zenetos et al. 2011; Deidun et al. 2018). Additionally, it possesses certain characteristics that could facilitate its spread and establishment, particularly its high tolerance to thermal stress (Banha et al. 2020), being able to survive at 13 °C (Deidun et al. 2018) but also at 36 °C (Çevik et al. 2006). Moreover, increasing temperatures due to global change enhance growth and sexual reproduction making it a species capable of proliferating in the currently warming conditions (Mammone et al. 2023). On the other hand, it may also have a socio-economic impact affecting tourism and human health as it is considered a mid-stinging species; therefore, prevention and mitigation measures must be taken where it is present, as well as the development of species-specific stinging protocols (Ballesteros et al. 2023).
Anzeige
With the rapid expansion of NIS in the Mediterranean, the use of early detection and warning tools is essential to prevent significant ecological and/or socio-economic impacts caused by the establishment of these species in marine ecosystems. Marine citizen science, volunteers participating in marine research (Thiel et al. 2014), is expanding and gaining great value (Earp and Liconti 2020). Evidence shows that it is a robust tool for providing scientific data for biodiversity conservation (McKinley et al. 2016), improving scientific monitoring at large scales (Bonney et al. 2009; Dickinson et al. 2010), and contributing to research on biological invasions by acting as a tool for early detection of NIS (Delaney et al. 2008; Crall et al. 2010; Giovos et al. 2019; Tiralongo et al. 2020; Encarnação et al. 2021). Another recent and very useful early detection method is the environmental DNA metabarcoding (eDNA) survey, that can be used to monitor NIS in some specific areas (Aglieri et al. 2023; Ye et al. 2024).
Observadoresdel Mar (OdM; www.observadoresdelmar.es), the marine citizen science platform of reference in Spain, is focused on marine conservation, answering questions to improve the understanding of marine ecosystems and working beyond ocean health. Currently, the platform houses 15 projects addressing five relevant topics: marine biodiversity, vulnerable species, marine impacts, climate change, and exotic and invasive species. OdM has managed to establish a very committed community in its 13 years of experience made up of several actors: scientific expert teams, stakeholders, collaborating organizations, the Sentinel Observatory network, and the large community of volunteers. The Sentinel Observatory (SO) network was created in 2016, currently comprising over 20 diving centers and clubs, associations, and other entities. The objective of this SO network is to establish a more systematic data collection and monitoring by expanding even more the spatio-temporal range, therefore, acting as an early alert and becoming a functional network. The SO network goes one step further in their commitment with OdM by systematically monitoring one or more projects of the platform through increased sampling, project-specific dives or research into a particular data. They report on a recurring basis and OdM provides them with specific training and a more constant and dedicated exchange of information.
OdM’s commitment and dedication is not only to the SO network, but to the community in general, with the aim of providing with sufficient tools to ensure the correct collection and veracity of data, to analyze and obtain results and answers to the research questions. For this reason, different tools have been developed and made available, including identification guides, a large photo database accessible to participating citizens, adapted standardized protocols, online and in-person training, as well as validation by an expert scientific team, resulting in high scientific value and an excellent-quality database (Figuerola-Ferrando et al. 2023; Coppari et al. 2024).
As for jellyfish research, various initiatives have demonstrated the effectiveness of citizen science (reviewed in Marambio et al. 2021), some of which provide valuable information about the ecology, spatio-temporal distribution, and the socio-economic impact in certain coastal areas (De Donno et al. 2014; Kienberger and Prieto 2017; Marambio et al. 2021; Tirelli et al. 2021). In OdM, one of the most successful projects is “Jellyfish Alert” (Marambio et al. 2023), which has been part of the platform since its creation in 2012 and currently has a very active community. The project is focused on data collection related to the presence and absence of gelatinous zooplankton organisms, including “true jellyfish” (scyphozoans), native and non-native, hydrozoans, ctenophores and salps. Data of one or few individuals and blooms are commonly registered, and records come mainly from the Mediterranean but also from around the world. In the years that the project has been active, a database of more than 2500 observations has been created including valuable records of the species present mainly on the Spanish coast. Recently, a protocol for monitoring climate change indicator species has been included in the project to collect data more systematically and help understand the effects of rising sea temperatures on the population and reproductive cycles of some common Mediterranean jellyfish species.
This study aims to report the first phylogenetically confirmed record of the scyphomedusa C. andromeda (Forskal, 1775) in Spanish waters and the westernmost record of the species in the Mediterranean Sea, which has formed large aggregations of a self-sustained reproductive population and has remained established in the last year, even expanding its distribution in the waters of the Aguadulce Marina in Almeria, southern Spain. Furthermore, this work emphasizes the importance of marine citizen science initiatives such as OdM and the involvement of its community in reporting the presence of the species, collecting samples for further scientific analyses, and monitoring the population with a temporarily systematic approach.
Materials and Methods
Study Area
The Marina Aguadulce is located at 36° 48.51’ N and 2° 33.42’ W, in the town of Roquetas de Mar, 8 km from Almería, province of the Autonomous Community of Andalusia in Spain (Fig. 2). It is mainly a touristic port with a total area of 170,462 m2 and more than 750 moorings available. The sides of the different channels of the marina are formed by rocks, but the central part is made of silt (~15 cm deep) and has an approximate width of 5–8 m depending on the channel.
Fig. 2
a Map of Spain highlighting the coast of Almeria as the study area; b Zoom into the Marina Aguadulce study area, highlighting the sampling protocol used for individual collection. The transects (T1, T2, T3, and T4) represent the sampling paths where C. andromeda individuals were found in 2023. Orange circles indicate collection sites
Three observations (March 2021, February 2023 and December 2023) of Cassiopea individuals were registered in the Jellyfish Alert project in the OdM platform by one SO of the network. The last record, from December 2023, corresponded to an aggregation of considerable abundance (i.e. more than 10 individuals/m2; Fig. 3d), therefore the expert scientific team considered it relevant to carry out a phylogenetic analysis as it is a cryptic NIS. For this purpose, twelve Cassiopea individuals of ~5 cm umbrella diameter were hand-collected by scuba divers at various locations (Fig. 2) within the study area on February 11 and 12, 2024. Temperature and salinity were recorded in each sampling point. The rationale for collecting twelve individuals distributed along the Marina Aguadulce was to account for the possibility of more than one species coexisting, as other studies have detected for Cassiopea (Muffett and Miglietta 2023). After collection, the specimens were preserved in 96% ethanol at room temperature and analyzed three days later.
Fig. 3
a Screenshot of Cassiopea spp. observation uploaded to OdM in March 2021; b Screenshot of Cassiopea spp. observation uploaded to OdM in February 2023; c Screenshot of C andromeda observation uploaded to OdM in December 2023; d Photographs of the population and individuals registered in the Marina Aguadulce in Andalucia in December 2023. The complete observation can be accessed at https://www.observadoresdelmar.es/Observations/3/23385
When first observed in December 2023, population density was estimated in one of the seven channels (4 m wide × 50 m long) (corresponding to T4 in Fig. 2), using 1 × 1 m quadrants. The umbrella diameter of 52 specimens was measured to estimate a rough size range. Additionally, monitoring was carried out for 15 months, from December 2023 until February 2025, and consisted of observing the presence and absence of Cassiopea in each of the seven channels that comprise the marina, as well as in the entrance channel, to assess its establishment and adaptation in the study area.
DNA Sequencing
DNA was extracted from each of the twelve Cassiopea specimens from a small portion of the umbrella margin following the standard phenol‒chloroform protocol. The quantity of DNA was assessed using Nanodrop, and its quality was checked via agarose 1% gel electrophoresis. Mitochondrial cytochrome c oxidase subunit I (COI) and 16S ribosomal RNA (16S) were amplified using primers ‘LCO1490-JJ2’ (5′-CHACHACWAAYCAYAARGAYATYGG-3′) and ‘HCO2198-JJ2’ (5′-ANACTTCNGGRTGNCCAAARAATCA-3′) for COI and ‘C&B1’ (5′-TCGACTGTTTACCAAAAACATAGC-3′) and ‘C&B2’ (5′-ACGGAATGAACTCAAATCATGTAAG-3′) for 16S, as described by Gamero-Mora et al. (2022). The polymerase chain reaction (PCR) was performed under the same conditions for both COI and 16S: 5 min at 94 °C for initial denaturation, followed by 35 cycles of amplification (denaturation at 94 °C for 15 s, annealing at 53 °C for 15 s and elongation at 72 °C for 45 s) and a final extension for 5 min at 72 °C. The PCR products were validated through 1% gel electrophoresis, purified by 1:5 dilution and Sanger sequenced at Stab Vida S. A.
Data Analysis
The 16S and COI sequences from the 12 individuals in Almeria Harbor collected in this study were aligned using the ‘msa’ function (from the ‘msa’ package) with other Cassiopea sequences available in the GenBank database: C. andromeda, C. xamachana, C. mayeri, C. culionensis, and C. frondosa, as well as with the outgroup species Mastigias papua and Phyllorhiza punctata (Table 1). The alignments were trimmed to 546 bp for 16S and 514 bp for COI using ‘msaTrim’ (from the ‘microseq’ package). Phylogenetic analyses were conducted separately for 16S and COI using maximum likelihood as the optimality criterion for each. The optimal substitution model was selected via ModelFinder, choosing the model with the lowest Akaike information criterion (AIC) score: TIM2 + F + I + G4 for 16S and TIM2 + F + I for COI (Kalyaanamoorthy et al. 2017). Each optimal model was bootstrapped 1000 times to generate the final consensus phylogenetic tree with branch support values (Hoang et al. 2018). The phylogenetic analyses were performed via IQ-TREE multicore (ver. 2.3.2). The consensus trees were visualized in Rstudio (RStudio Team 2020) using the ‘ggtree’ package, which was previously rooted in the outgroup species M. papua with the ‘root’ function (from the ‘ape’ package).
Table 1
Sequences of the mitochondrial ribosomal gene 16S rRNA and the mitochondrial protein-encoding gene cytochrome c oxidase I (COI) were used for phylogenetic analysis
GenBank accession numbers of sequences in bold were obtained in this study
Species with ‘a’ were reported as C. frondosa in the sequence publication but fall into the C. xamachana clade, which is supported by Muffett and Miglietta (2023)
bIndicates that the sequences are not available in GenBank and were given by the authors
Results
After genetic analysis of the twelve collected specimens, the results revealed that they corresponded to the species Cassiopea andromeda, becoming the first phylogenetically confirmed record of this species in Spain and the westernmost record of the Mediterranean basin. The observation was validated in the Jellyfish Alert project of the OdM platform as a confirmed record of C. andromeda species (Fig. 3c). The other two previous observations, from March 2021 and February 2023, were validated morphologically and only at the genus level because no phylogenetic analysis was performed (Fig. 3a, b).
During the sampling in February 2024, the temperature was 14.33 ± 0.12 °C and the salinity 37.58 ± 0.08. The aggregations of C. andromeda were observed in various channels, mainly in the central silt area, covering the length and width of the channels at an approximate depth of 4–5 m. Some of them were also observed over the meadows of another invasive species, the Rugulopteryx okamurae algae, which has also colonized areas of the marina. No individuals were observed over the rocky lateral areas.
Individuals were characterized by a brownish color with whitish and blue rounded and flattened vesicles (Fig. 3d). During the monitoring carried out in December 2023, the density of the population was estimated to be 80–100 individuals/m2 and the umbrella diameter ranged from 4 to 30 cm.
The monitoring conducted over 15 months indicated that the population has survived all seasons and has even expanded its distribution, having already colonized all the marina channels by 2025 (Fig. 4). Moreover, different stages and sizes of individuals have been observed, indicating active reproduction in the study area.
Fig. 4
Representation of the population’s expansion inside the Marina Aguadulce, by indicating in green areas where individuals appeared after 1-year monitoring
Phylogenetic analyses of the 12 sequences of Cassiopea from Almeria, Spain, combined with 24 additional sequences (most of which are available in the GenBank database), confirmed that Cassiopea specimens from Almeria clearly belong to C. andromeda. Four COI sequences (from sampling points T1.1, T2.2, T3.1, and T4.1 in Fig. 2), although matching the species, exhibited several nucleotide variations that led to unexpected stop codons and failed the NCBI quality check. Therefore, we assumed these sequences had Sanger sequencing errors and excluded them from the analyses to include only high-quality sequences. All specimens were clearly grouped within the clade of C. andromeda, which also includes specimens from Egypt, Florida Keys, and Sicily. At the same time, the phylogenetic tree revealed the presence of other clades, such as C. xamachana, which was closest to C. andromeda, along with C. culionensis, C. ornata, C. mayeri, and C. frondosa. The bootstrap values for most nodes of the tree were greater than 80%, indicating that the consensus maximum likelihood tree was highly reliable (Fig. 5).
Fig. 5
Phylogenetic tree illustrating the evolutionary relationships among different Cassiopea species. Maximum likelihood consensus tree with bootstrap support for (left) the mitochondrial ribosomal gene 16S rRNA and (right) the mitochondrial protein-encoding gene cytochrome c oxidase I (COI) DNA. Names in bold indicate sequences generated in the present study. Gray squares group sequences that belong to the same clade. Scale bars indicate evolutionary distance. See Table 1 for information about all the sequences used
Sequences from Almería showed 100% nucleotide identity with the two sequences from Florida, except for one COI sequence that differed by a single nucleotide and four 16S sequences that differed by five nucleotides. However, the molecular distance, measured by the Kimura 2-parameter (K80), among the sequenced individuals remained very low (0.2 ± 0.2% for 16S and 0.0 ± 0.1% for COI). These values did not differ from those of C. andromeda from Egypt, Florida, and Sicily (16S: 0.2 ± 0.2% and COI: 0.2 ± 0.3%). The intraspecific variation in C. andromeda (16S: 0.2 ± 0.2% and COI: 0.2 ± 0.3%) was much smaller than the interspecific variation (16S: 11.2 ± 5.1% and COI: 14.3 ± 6.0%). Accordingly, all these groups presented high genetic distance from the outgroup species M. papua and P. punctata (16S: 21.0 ± 1.5% and COI: 25.1 ± 1.9%) (Supplementary Information file).
Discussion
According to Zenetos et al. (2020), almost 1000 marine NIS have been introduced into the Mediterranean. Although the number of alien species in the Mediterranean varies between regions (Zenetos et al. 2012), the majority occur in the Eastern sub-region. The Sicily Channel plays an important role in this distribution pattern since it has been traditionally considered a biogeographical barrier that prevents the spread of these species, restricting them to the eastern basin (e.g., Quignard and Tomasini 2000). Nevertheless, some species have crossed the Sicily channel and have been found in the western region. This is the case for some Lessepsian scyphomedusae species, such as our target species Cassiopea andromeda (Morandini et al. 2017; Aljbour et al. 2017; Maggio et al. 2019), and others, such as Rhopilema nomadica (Balistreri et al. 2017) and Phyllorhiza punctata (Deidun et al. 2017).
C. andromeda is one of the 18 species of jellyfish reported as NIS in the Mediterranean. Its records, although not all phylogenetically confirmed, are diverse. Until now, the species had not been confirmed in Mediterranean Spanish waters, and its westernmost record was from Italy (Maggio et al. 2019). In this work, we report the first phylogenetically confirmed record of the NIS C. andromeda in Spanish waters and the westernmost record of this species in the Mediterranean Sea. The analysis suggests that the population in this location consists solely of C. andromeda (Fig. 5), excluding any coexistence with C. xamachana, as described in other studies (Muffett and Miglietta 2023). Overall, the bootstrap values (an indicator of the confidence in the placement of a particular clade within a phylogenetic tree) were between 80% and 99%, with few values lower than 70%, in accordance with other phylogenetic studies of Cassiopea species (Muffett and Miglietta 2023; Gamero-Mora et al. 2022; Arai et al. 2017). When comparing the COI and 16S trees, the former had higher bootstrap values, except for the node between the clades C. ornata/C. culionensis and C. mayeri (63%). However, the bootstrap value of the analogous node in the 16S tree was greater (81%). Therefore, the phylogenetic results in this study are highly reliable.
The phylogenetic tree, which uses either 16S or COI markers, indicates that each Cassiopea species diverged through distinct evolutionary paths, in accordance with other phylogenetic studies of Cassiopea (Gamero-Mora et al. 2022; Muffett and Miglietta 2023). These trees show that C. frondosa is distinct from the other species, indicating early divergence. Interestingly, this is the only Cassiopea species that can be unequivocally identified by morphology (it has a different number of rhopalia) (Morandini et al. 2017). Later in evolution, there was a divergence into two distinct clades: the “C. andromeda/C. xamachana” and “C. mayeri/C. ornata/C. culionensis” clades, where C. mayeri diverged from the latter. Finally, C. andromeda-C. xamachana, and C. ornata-C. culionensis diverged from their most recent common ancestors, indicating recent evolution, and suggesting potential cryptic species within these groups (Fig. 5).
Crypticity is common in Scyphozoa and can lead to species misidentification when it is detected only by morphology (Moura et al. 2022; Holland et al. 2004; Dawson 2003). In the context of invasive species, crypticity complicates their detection and management, hampering the prediction and control of their impacts (Jarić et al. 2019). In that sense, when a species has been sighted in a new location, barcoding identification — alone or combined with morphological description — is indispensable to ensure correct identification and management. There is a large difference between naming a study species and labeling it with DNA barcodes (such as 16S or COI markers), with the latter being much more precise. In addition, if the generated DNA barcodes are stored in public databases, they may be available for future phylogenetic studies. For example, our phylogenetic tree revealed that Cassiopea from Panama, which Gómez Daglio and Dawson 2017 identified as C. frondosa, corresponds to C. xamachana, which is in accordance with the findings of Muffett and Miglietta (2023). This fact, together with other examples of reidentification of Cassiopea species (Gamero-Mora et al. 2022), highlights how DNA barcoding allows species identification to be adapted in future studies, considering that taxonomy can change over time.
The introduction pathway of C. andromeda into Spanish waters is unknown. As an epibenthic scyphozoan, this jellyfish has a very limited movement capability, and most of the translocations reported in this species are more likely to be related to maritime transportation rather than natural transport by currents or by its own displacement (Holland et al. 2004; Schembri et al. 2010). We hypothesize that C. andromeda from this study, possibly the polyp stage, could have arrived by vessel transportation and probably as biofouling, since the study area is a marina and does not have ballast water loads (i.e., ambient water loaded into ballast tanks of commercial vessels). This hypothesis agrees with the case of Turkey, where the authors also suggested that polyps may have arrived in ships as biofouling (Çevik et al. 2006) while the pelagic stages in ballast water (Özgür and Öztürk 2008). In any case, independent of the arrival pathway, the current environmental conditions in the study area are certainly suitable for the species to develop and establish large populations, as has been observed in the last year after its first detection. The presence of this species in harbors and marinas has also been described in other areas, such as Malta, Sicily and Turkey (Schembri et al. 2010; Cillari et al. 2018; Çardak et al. 2011, respectively). Harbors have been described as an ideal region for NIS introduction because of high maritime traffic (Ferrario et al. 2017) and, in the case of C. andromeda and its congeneric, it has been demonstrated that human-impacted coastal habitats may enhance its ability to sustain populations and contribute to its establishment (Çevik et al. 2006; Thé et al. 2023; Stoner et al. 2011).
Following the history of invasive species in the Mediterranean, several authors have suggested that finding Lessepsian species in the western basin may be considered an indicator of the warming trend of the Mediterranean Sea (Boero et al. 2009; Daly Yahia et al. 2013). Water warming facilitates the natural spread of tropical and subtropical species, enabling them to expand their distribution range (Lasram et al. 2008; Parravicini et al. 2015). In this context, the Mediterranean Sea stands out as one of the most significant and susceptible regions to climate change (Giorgi 2006; Lionello et al. 2012), experiencing a warming rate per decade that exceeds the global average by more than threefold. These climate change conditions, and the resulting increase in sea temperature, may support the distribution and establishment of thermophilic species such as C. andromeda (Çevik et al. 2006), which is considered to enhance its physiological response to global warming (Aljbour et al. 2017, 2019; Banha et al. 2020; Mammone et al. 2023), and whose thermal tolerance could promote an increase in the population and expansion of its geographic distribution range (Aljbour et al. 2019).
C. andromeda records in the Mediterranean are from semi-enclosed eutrophic shallow waters with low hydrodynamics (Maggio et al. 2019). This is the case for the harbors mentioned above and for nature reserves (Malta, Deidun et al. 2018), marine protected areas (Tunisia, Amor et al. 2015), the cooling water drainage channel of a factory (Turkey, Çevik et al. 2006) or lagoons (Turkey, Özgür and Öztürk 2008). These shallow areas, although quite stressful (e.g., high temperatures/irradiation and potential extreme salinity changes), have been demonstrated to be suitable for their establishment, probably because of the high tolerance of this jellyfish to environmental variation (Morandini et al. 2017; Mammone et al. 2021). In previous works, it has been described at different temperatures ranging from 14.1–17.6 °C in Palermo (Maggio et al. 2019), 13.36–14.49 °C in Malta (Deidun et al. 2018), and 29–36 °C in Turkey (Çevik et al. 2006; Özgür and Öztürk 2008). In this study, C. andromeda was first detected in winter (December‒February) when the water temperature was ~14.2 °C and has been monitored and observed throughout the year following the yearly temperature range. The high abundances (80‒100 individuals/m2) recorded in the present study, are much higher compared with other studies where the maximum abundances described were 30‒40 individuals/m2 (Niggl and Wild 2010), especially considering that it is very likely that the density is underestimated since according to the information reported by the SO during the monitoring reporting, the jellyfish were one on top of the other forming layers that did not allow counting all the individuals in each quadrant.
Marine citizen science, as a growing opportunity for marine research (Sandahl and Tøttrup 2020; Earp and Liconti 2020; Changeux et al. 2020; García-Soto et al. 2021), has been reported in previous studies as a highly valuable tool for increasing knowledge about jellyfish distribution (Johansen et al. 2021; Marambio et al. 2021; Tirelli et al. 2021; Edelist et al. 2022; Dobson et al. 2023; Terenzini et al. 2023). Additionally, it provides essential data for establishing and/or improving preventive programs to mitigate jellyfish impacts in some coastal areas. In recent years, another growing area of citizen science is the reporting of NIS, therefore considered a useful tool for expanding the scale of data collection, for early detection and for monitoring exotic and invasive species (Delaney et al. 2008; Crall et al. 2010; Mannino and Balistreri 2018; Giovos et al. 2019; Tiralongo et al. 2020; Pocock et al. 2024). All this represents a clear benefit in expanding exotic and invasive species knowledge, and in their monitoring, management, and related policy development (Groom et al. 2019; Pyšek et al. 2020; Price-Jones et al. 2022).
Detecting NIS as early as possible, along with monitoring and research, is essential for determining the ecological and socio-economic impacts that their presence and establishment could have on invaded areas (Giovos et al. 2019; Pocock et al. 2024). In these instances, marine citizen science requires significant involvement from volunteers, as participation goes beyond mere observation reporting. Therefore, it is essential that platforms and initiatives have a track record and are well established, with strong community engagement. In this sense, OdM has a large and highly engaged community of volunteers from different sectors and a robust network of Sentinel Observatories (SO). Aquatours Almeria, the diving center that reported the presence of C. andromeda, has been part of this SO network since the beginning. In fact, 75% of the SO network consists of diving centers or clubs, which represents a good opportunity for marine citizen science, as divers are considered one of the most committed user groups, according to previous studies (Martin et al. 2016; Lucrezi et al. 2018). Moreover, OdM has demonstrated its consistency in effectively contributing to the early detection of NIS, expanding knowledge and contributing to decision-making related to marine conservation (Azzurro et al. 2013, 2020; Castejón-Silvo et al. 2023; Figuerola-Ferrando et al. 2023).
The OdM platform, through its specific project Jellyfish Alert, provides the necessary identification clues and expert support to recognize jellyfish species easily under good conditions. However, in some cases phylogenetic analysis is required for a correct identification, especially for cryptic species such as Cassiopea individuals. When further analysis is needed, the close collaboration with the OdM’s SO enables the collection of samples as they immediately receive a protocol from the scientific team with instructions for sample collection, ultimately allowing for species confirmation. Furthermore, as a SO of the platform’s network, they regularly conduct structured monitoring at the same location during their year-round dives. This has allowed them to track the species for more than 12 months since its detection, and they have been able to observe and report on its reproduction and expansion in the colonized area. This will allow us to get valuable information to assess the impact of the species over time (Pocock et al. 2024). Moreover, with this confirmed record, the message can be expanded to the public and encourage attention to this species. It will also contribute to understanding the importance and impact of invasive species on marine ecosystems and contribute to adaptive management strategies within a citizen science approach (Giovos et al. 2019; Pocock et al. 2024).
Conclusions
The detection of NIS is highly relevant to the ecology of ecosystems and the conservation of the marine environment. The case of C. andromeda is of particular interest because it can be easily transported as biofouling and/or ballast water, and when it arrives in a new area, it can easily adapt to different environmental conditions, being highly thermotolerant. These characteristics, together with rising sea temperatures due to climate change, make almost any point in the Mediterranean a suitable place for this species, which, in addition, can spread rapidly, affecting local populations. This study contributes to the knowledge of the NIS C. andromeda in the Mediterranean, presenting the first phylogenetically confirmed record in Spanish waters and the westernmost record in the basin, as well as the contribution to public DNA databases. On the other hand, marine citizen science has proven useful and, if well implemented, is a powerful tool that allows the expansion of spatial-temporal marine research, improves ecological understanding, and contributes to ocean literacy-enhancing knowledge. In the case of NIS, it has an important value as a detection tool that has been used in various taxonomic groups, including jellyfish. For instance, the present study demonstrates the relevance of the marine citizen science platform OdM, as it plays a fundamental role in the detection, sampling and monitoring of this species through its engaged community. The potential of marine citizen science in reporting the presence of certain species and acting as a warning tool is unquestionable, as the advantage of having a large and engaged community makes it a highly cost-effective tool. This collaboration between scientists and citizens is translated into advances in marine research, management and even policy. With more than 12 years of experience, OdM has demonstrated the commitment of its community, the importance of providing training and standardized protocols, and the quality of the data. Furthermore, it implements all the recommendations for the establishment and successful development of a marine citizen science platform, and its contributions thus far confirm its success.
The authors would like to thank all the citizen scientists involved in Observadores del Mar, as well as all the Sentinel Observatories of the platform, specially to Aquatours Almeria Aventuras Submarinas and all their staff for their implication and proactive attitude toward the sampling, monitoring and the research. We also thank Jose Maria Perez Freije from the University of Oviedo for his support on the genetic analysis. Finally, authors would like to thank the reviewers for their constructive and insightful comments, which helped improve the quality and clarity of the manuscript.
Author Contributions
Study Conceptualization and Investigation were performed by Macarena Marambio, Maria Pascual-Torner and Uxue Tilves. Data collection and Formal Analysis were performed by Macarena Marambio, Maria Pascual-Torner and Alejandra Perez. Writing of the original draft was performed by Macarena Marambio, Maria Pascual-Torner, Uxue Tilves. Review and editing of the manuscript were performed by Macarena Marambio, Maria Pascual-Torner, Uxue Tilves, Josep Maria Gili, Alejandra Perez and Ainara Ballesteros. Supervision of the study was performed by Macarena Marambio, Maria Pascual-Torner and Josep Maria Gili. All authors read and approved the final manuscript.
Compliance with Ethical Standards
Conflict of Interest
The authors declare no competing interests.
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
The Westernmost Record of the Scyphomedusa Cassiopea andromeda (Forskål, 1775) in the Mediterranean: Marine Citizen Science Contributions to Invasive Species Detection and Monitoring
Aglieri G, Quattrocchi F, Mariani S, Baillie C, Spatafora D, Di Franco A, Turco G, Tolone M, Di Gerlando R, Milazzo M (2023) Fish eDNA detections in ports mirror fishing fleet activities and highlight the spread of non-indigenous species in the Mediterranean Sea. Mar Pollut Bull 189:114792. https://doi.org/10.1016/j.marpolbul.2023.114792.CrossRef
Aljbour SM, Zimmer M, Kunzman A (2017) Cellular respiration, oxygen consumption, and trade-offs of the jellyfish Cassiopea sp. in response to temperature change. J Sea Res 128:92–97. https://doi.org/10.1016/j.seares.2017.08.006.CrossRef
Aljbour SM, Zimmer M, Al-Horani FA, Kunzman A (2019) Metabolic and oxidative stress responses of the jellyfish Cassiopea sp. to changes in seawater temperature. J Sea Res 145:1–7. https://doi.org/10.1016/j.marpolbul.2018.03.044.CrossRef
Amor KOB, Rifi Μ, Ghanem R, Draeif I, Zaouali J, Souissi JB (2015) Update of alien fauna and new records from Tunisian marine waters. Mediterr Mar Sci 17(1):124–143. https://doi.org/10.12681/mms.1371.CrossRef
Anthony CJ, Heagy MK, Bentlage B (2022) Phenotypic plasticity in Cassiopea ornata (Cnidaria: Scyphozoa: Rhizostomeae) suggests environmentally driven morphology. Zoomorphology 141:115–131. https://doi.org/10.1007/s00435-022-00558-4.
Arai Y, Gotoh RO, Yokoyama J et al. (2017) Phylogenetic relationships and morphological variations of upside-down jellyfishes, Cassiopea spp. inhabiting Palau Islands. Biogeography 19:133–141. https://doi.org/10.11358/biogeo.19.133.CrossRef
Azzurro E, Bariche M, Cerri J, Garrabou J (2020) The long reach of the Suez Canal: Lagocephalus sceleratus (Gmelin, 1789) an unwanted Indo-Pacific pest at the Atlantic gates. BioInvasions Records 9(2):204–208. https://doi.org/10.3391/bir.2020.9.2.05.
Azzurro E, Broglio E, Maynou F, Bariche M (2013) Citizen science detects the undetected: the case of Abudefduf saxatilis from the Mediterranean Sea. Manage Biol Invas 4(2):167−170. https://doi.org/10.3391/mbi.2013.4.2.10.
Badreddine A, Bitar G (2020) Cotylorhiza erythraea Stiasny, 1920 (Scyphozoa: Rhizostomeae: Cepheidae): a new lessepsian jellyfish in the Lebanese waters, the eastern Mediterranean Sea. J Black Sea Mediterr Environ 26(3):321–328.
Balistreri P, Spiga A, Deidun A, Gueroun SKM, Daly Yahia MN (2017) Further spread of the venomous jellyfish Rhopilema nomadica Galil, Spannier & Ferguson, 1990 (Rhizostomeae, Rhizostomatidae) in the western Mediterranean. Bioinvasions Rec 6:19–24. https://doi.org/10.3391/bir.2017.6.1.04.CrossRef
Ballesteros A, Marambio M, Trullas C, Jourdan E, Tena-Medialdea J, Gili J-M (2023) Effect of rinse solutions on Rhizostoma pulmo (Cnidaria: Scyphozoa) Stings and the ineffective role of vinegar in Scyphozoan jellyfish species. Int J Environ Res Public Health 20:2344. https://doi.org/10.3390/ijerph20032344.CrossRef
Banha TN, Mies M, Güth AZ, Pomory CM, Sumida PYG (2020) Juvenile Cassiopea andromeda medusae are resistant to multiple thermal stress events. Mar Biol 167:173. https://doi.org/10.1007/s00227-020-03792-w.CrossRef
Boero F, Putti M, Trainito E, Prontera E, Piraino S, Shiganova T (2009) First records of Mnemiopsis leidyi (Ctenophora) from the Ligurian, Thyrrhenian and Ionian Seas (Western Mediterranean) and first record of Phyllorhiza punctata (Cnidaria) from the Western Mediterranean. Aquat Invasions 4(4):675–680. https://doi.org/10.3391/ai.2009.4.4.13.CrossRef
Bonney R, Cooper CB, Dickinson J, Kelling S, Phillips T, Rosenberg KV, Shirk J (2009) Citizen science: A developing tool for expanding science knowledge and scientific literacy. BioScience 59:977–984. https://doi.org/10.1525/bio.2009.59.11.9.CrossRef
Çardak M, Özgür Özbek E, Kebapçıoğlu T (2011) The new location record of Cassiopea andromeda (Forsskål, 1775) from the Gulf of Antalya, Levantine coast of Turkey, Eastern Mediterranean. In: Turan C, Öztürk B (Eds) 2011. First National Workshop on Jellyfish and Other Gelatinous Species in Turkish Marine Waters. TUDAV, Istanbul, TURKEY, 35, pp. 50–52.
Castejón-Silvo I, Terrados J, Morales-Nin B (2023) Citizen science in the study of marine biodiversity: the case of iconic and cryptic syngnathids. Thalassas Int J Mar Sci 39:679–686. https://doi.org/10.1007/s41208-023-00590-1.CrossRef
Çevik C, Erkol IL, Toklu B (2006) A new record of an alien jellyfish from the Levantine coast of Turkey – Cassiopea andromeda (Forsskål, 1775) [Cnidaria: Scyphozoa: Rhizostomea]. Aquat Invasions 1(3):196–197. https://doi.org/10.3391/ai.2006.1.3.18.CrossRef
Changeux T, Blazy C, Ruitton S (2020) The use of citizen science for marine biodiversity surveys: from species identification to ecologically relevant observations. Hydrobiologia 847:27–43. https://doi.org/10.1007/s10750-019-04070-7.CrossRef
Cillari T, Andaloro F, Castriota L (2018) First documented record of Cassiopea andromeda (Cnidaria: Scyphozoa) in Italian waters. Cah Biol Mar 59:193–195.
Cillari T, Allegra A, Bero D, Bosch-Belmar M, Falautano M, Maggio T, Milisenda G, Persia P, Rampazzo F, Sinopoli M, Castriota L (2022) Snapshot of the distribution and biology of alien jellyfish Cassiopea andromeda (Forsskål, 1775) in a Mediterranean touristic harbour. Biology 11:319. https://doi.org/10.3390/biology11020319.CrossRef
Coll M, Piroddi C, Steenbeek J, Kaschner K, Ben Rais Lasram F, Aguzzi J et al. (2010) The biodiversity of the Mediterranean Sea: estimates, patterns, and threats. PLoS ONE 5(8):e11842. https://doi.org/10.1371/journal.pone.0011842.CrossRef
Coppari M, Roveta C, Di Camillo C, Garrabou J, Lucrezi S, Pulido T, Cerrano C (2024) The pillar of the sea: strategies to achieve successful marine citizen science programs in the Mediterranean area. BMC Ecol Evol 24:100. https://doi.org/10.1186/s12862-024-02289-0.CrossRef
Crall AW, Newman GJ, Jarnevich CS, Stohlgren TJ, Waller DM, Graham J (2010) Improving and integrating data on invasive species collected by citizen scientists. Biol Invasions 12:3419–3428. https://doi.org/10.1007/s10530-010-9740-9.CrossRef
Crocetta F, Al Mabruk SA, Azzurro E, Bakiu R, Bariche M, Batjakas IE et al. (2021) New alien Mediterranean biodiversity records. Mediterr Mar Sci 22::724–746. https://doi.org/10.12681/mms.26668.CrossRef
Daly Yahia MN, Daly Yahia OK, Gueroun SKM, Aussi M, Deidun A, Fuentes V, Piraino S (2013) The invasive tropical scyphozoan Rhopilema nomadica Galil, 1990 reaches the Tunisian coast of the Mediterranean Sea. Bioinvasions Rec 2(4):319–323. https://doi.org/10.3391/bir.2013.2.4.10.CrossRef
Deidun A, Gauci A, Sciberras A, Piraino S (2018) Back with a bang – an unexpected massive bloom of Cassiopea andromeda (Forsskal, 1775) in the Maltese Islands, nine years after its first appearance. Bioinvasions Rec 7(4):399–404. https://doi.org/10.3391/bir.2018.7.4.07.CrossRef
Deidun A, Sciberras J, Sciberras A, Gauci A, Balistreri P, Salvatore A, Piraino S (2017) The first record of the white-spotted Australian jellyfish Phyllorhiza punctata von Lendenfeld, 1884 from Maltese waters (western Mediterranean) and from the Ionian coast of Italy. Bioinvasions Rec 6(2):119–124. https://doi.org/10.3391/bir.2017.6.2.05.CrossRef
Delaney DG, Sperling CD, Adams CS, Leung B (2008) Marine invasive species: validation of citizen science and implications for national monitoring networks. Biol Invasions 10:117–128. https://doi.org/10.1007/s10530-007-9114-0.CrossRef
Dobson JY, Fonfría ES, Palacios R, Blasco E, Bordehore C (2023) Citizen science effectively monitors biogeographical and phenological patterns of jellyfish. Ocean Coast Manag 242:106668. https://doi.org/10.1016/j.ocecoaman.2023.106668.CrossRef
De Domenico S, Toso A, De Rinaldis G, Mammone M, Fumarola LM, Piraino S, Leone A (2025) Wild or reared? Cassiopea andromeda Jellyfish as a Potential Biofactory. Mar Drugs 23:19. https://doi.org/10.3390/md23010019.CrossRef
De Donno A, Idolo A, Bagordo F, Grassi T, Leomanni A, Serio F, Guido M, Mariarita C, Zampardi S, Boero F, Piraino S (2014) Impact of stinging jellyfish proliferations along South Italian coasts: human health hazards, treatment and social costs. Int J Environ Res Public Health 11:2488–2503. https://doi.org/10.3390/ijerph110302488.CrossRef
Earp HS, Liconti A (2020) Science for the future: the use of citizen science in marine research and conservation. In: Jungblutu S, Liebich V, Bode-Dalby M (eds) YOUMARES 9 – The Oceans: Our Research, Our Future. Springer, pp 1–19. https://doi.org/10.1007/978-3-030-20389-4
Edelist D, Knutsen Ø, Ellingsen I, Majaneva S, Aberle N, Dror H, Dror A (2022) Tracking jellyfish swarm origins using a combined oceanographic-genetic-citizen science approach. Front Mar Sci 9:869619. https://doi.org/10.3389/fmars.2022.869619.CrossRef
Ferrario J, Caronni S, Occhipinti-Ambrogi A, Marchini A (2017) Role of commercial harbours and recreational marinas in the spread of non-indigenous fouling species. Biofouling 33:651–660. https://doi.org/10.1080/08927014.2017.1351958.CrossRef
Figuerola-Ferrando L, Linares C, Zentner Y, López-Sendino P, Garrabou J (2023) Marine citizen science and the conservation of Mediterranean corals: the relevance of training, expert validation, and robust sampling protocols. Environ Manag. https://doi.org/10.1007/s00267-023-01913-x
Forskål P (1775) Descriptiones animalium avium, amphibiorum, piscium, insectorum, vermium; quae in intinere orientali observavit Petrus Forskål. Hauniae 1–164.
Galil B, Spanier E, Ferguson W (1990) The Scyphomedusae of the Israeli Mediterranean coast, including two Lessepsian migrants to the Mediterranean. Zoologische Mededlingen 64(7):95–105.
Galil BS, Kumar BA, Riyas AJ (2013) Marivagia stellata Galil and Gershwin, 2010 (Scyphozoa: Rhizostomeae: Cepheidae), found off the coast of Kerala, India. BioInvasions Rec 2(4):229–235. https://doi.org/10.3391/bir.2013.2.4.09.CrossRef
Galil BS, Marchini A, Occhipinti – Ambrogi A (2018) East is east and West is west? Management of marine bioinvasions in the Mediterranean Sea. Estuar Coast Shelf Sci 201:7–16. https://doi.org/10.1016/j.ecss.2015.12.021.CrossRef
Galil BS, Gershwin LA, Zorea M, Rahav A, Rothman SBS, Fine M, Lubinevsky H, Douek J, Paz G, Rinkevich B (2017) Cotylorhiza erythraea Stiasny, 1920 (Scyphozoa: Rhizostomeae: Cepheidae), yet another erythraean jellyfish from the Mediterranean coast of Israel. Mar Biodiv 47:229–235. https://doi.org/10.1007/s12526-016-0449-6.CrossRef
Gamero-Mora E, Collins AG, Boco SR et al. (2022) Revealing hidden diversity among upside-down jellyfishes (Cnidaria: Scyphozoa: Rhizostomeae: Cassiopea): distinct evidence allows the change of status of a neglected variety and the description of a new species. Invertebr Syst 36:63–89. https://doi.org/10.1071/IS21002.CrossRef
García-Soto C, Seys JJ, Zielinski O, Busch JA, Luna SI, Baez JC, Domegan C, Dubsky K, Kotynska-Zielinska I, Loubat P, Malfatti F, Mannaerts G, McHugh P, Monestiez P, van der Meeren GI, Gorsky G (2021) Marine citizen science: current state in Europe and new technological developments. Front Mar Sci 8:621472. https://doi.org/10.3389/fmars.2021.621472.CrossRef
Giovos I, Kleitou P, Poursanidis D 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. https://doi.org/10.1007/s10530-019-02083-w.CrossRef
Gómez Daglio L, Dawson MN (2017) Species richness of jellyfishes (Scyphozoa:Discomedusae) in the Tropical Eastern Pacific: missed taxa, molecules, and morphology match in a biodiversity hotspot. Invertebr Syst 31:635–663. https://doi.org/10.1071/IS16055.CrossRef
Goy J, Lakkis S, Zeidane R (1988) Les Méduses de la Méditerranee orientale. Rapports et Procès-Verbaux des Réunions Conseil Internationale pour l’Exploration de la Mer 31:29.
Groom Q, Strubbe D, Adriaens T, Davis AJS, Desmet P, Oldoni D, Reyserhove L, Roy HE, Vanderhoeven S (2019) Empowering citizens to inform decision-making as a way forward to support invasive alien species policy. Citiz Sci Theory Pr 4(1):33. https://doi.org/10.5334/cstp.238.CrossRef
Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS (2018) UFBoot2: improving the ultrafast bootstrap approximation. Mol Biol Evol 35:518–522. https://doi.org/10.1093/molbev/msx281.CrossRef
Holland BS, Dawson MN, Crow GL, Hofmann DK (2004) Global phylogeography of Cassiopea (Scyphozoa: Rhizostomeae): molecular evidence for cryptic species and multiple invasions of the Hawaiian Islands. Mar Biol 145:1119–1128. https://doi.org/10.1007/s00227-004-1409-4.CrossRef
Jarić I, Heger T, Castro Monzon F et al. (2019) Crypticity in biological invasions. Trends Ecol Evol 34:291–302.CrossRef
Jarms G, Morandini AC (2019) World Atlas of Jellyfish: Abhandlungen des Naturwissenschaftlichen Vereins in Hamburg, Special Volume (English Edition)
Johansen E, Aberle N, Østensen MA, Majaneva S (2021) Assessing the value of citizen science approach for ctenophore identification. Front Mar Sci 8:772851. https://doi.org/10.3389/fmars.2021.772851.CrossRef
Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14:587–589. https://doi.org/10.1038/nmeth.4285.CrossRef
Katsanevakis S (2011) Rapid assessment of the marine alien megabiota in the shallow coastal waters of the Greek islands, Paros and Antiparos, Aegean Sea. Aquat Invasions 6(1):133–137. https://doi.org/10.3391/ai.2011.6.S1.030.CrossRef
Katsanevakis S, Coll M, Piroddi C, Steenbeek J, Ben Rais Lasram F, Zenetos A, Cardoso AC (2014) Invading the Mediterranean Sea: biodiversity patterns shaped by human activities. Front Mar Sci 1:32. https://doi.org/10.3389/fmars.2014.00032.CrossRef
Kienberger K, Prieto L (2017) The jellyfish Rhizostoma luteum (Quoy & Gaimard, 1827): not such a rare species after all. Mar Biodiv. https://doi.org/10.1007/s12526-017-0637-z
Lampert KP, Bürger P, Striewski S, Tollrian R (2011) Lack of association between color morphs of the Jellyfish Cassiopea andromeda and zooxanthella clade. Mar Ecol 33:364–369. https://doi.org/10.1111/j.1439-0485.2011.00488.x.CrossRef
Lasram FBR, Tomasini JA, Guilhaumon F, Romdhane MS, Do Chi T, Mouillot D (2008) Ecological correlates of dispersal success of Lessepsian fishes. Mar Ecol Prog Ser 363:273–286. https://doi.org/10.3354/meps07474.CrossRef
Lionello P, Abrantes F, Congedi L et al. (2012) Introduction: Mediterranean Climate—Background Information. In: Lionello P (ed) The Climate of the Mediterranean Region, Elsevier, Pages xxxv-xc. https://doi.org/10.1016/B978-0-12-416042-2.00012-4.
Lucrezi S, Milanese M, Palma M, Serrano C (2018) Stirring the strategic direction of scuba diving marine Citizen Science: a survey of active and potential participants. PLoS ONE 13(8):e0202484. https://doi.org/10.1371/journal.pone.0202484.CrossRef
Maas O (1903) Die Scyphomedusen der Siboga-Expedition; Siboga-Expeditie, Buchhandlung und Druckerei Vormals, Vol 11. EJ Brill, Leiden, The Netherlands, pp. 1–9
Maggio T, Allegra A, Bosch-Belmar M, Cillari T, Cuttitta A, Falautano M, Milisenda G, Nicosia A, Perzia P, Sinopoli M, Castriota L (2019) Molecular identity of the non-indigenous Cassiopea sp. from Palermo Harbour (central Mediterranean Sea). J Mar Biol Assoc UK 1–9. https://doi.org/10.1017/S0025315419000924.
Mammone M, Ferrier-Pagés C, Lavorano S, Rizzo L, Piraino S, Rossi S (2021) High photosynthetic plasticity may reinforce invasiveness of upside-down zooxanthellate jellyfish in Mediterranean coastal waters. PLoS ONE 16(3):e0248814. https://doi.org/10.1371/journal.pone.0248814.CrossRef
Mammone M, Bosch-Belmar M, Milisenda G, Castriota L, Sinopoli M, Allegra A, Falautano M, Maggio T, Rossi S, Piraino S (2023) Reproductive cycle and gonadal output of the Lessepsian jellyfish Cassiopea andromeda in NW Sicily (Central Mediterranean Sea). PLoS ONE 18(2):e0281787. https://doi.org/10.1371/journal.pone.0281787.CrossRef
Mannino AM, Balistreri P (2018) Citizen science: a successful tool for monitoring invasive alien species (IAS) in Marine Protected Areas. The case study of the Egadi Islands MPA (Tyrrhenian Sea, Italy). Biodiversity. https://doi.org/10.1080/14888386.2018.1468280.
Marambio M, Canepa A, López L, Gauci AA, Gueroun SKM, Zampardi S, Boero F, Kéfi-Daly Yahia O, Daly Yahia MN, Piraino S, Deidun A (2021) Unfolding jellyfish bloom dynamics along the Mediterranean basin by transnational citizen science initiatives. Diversity 13:274. https://doi.org/10.3390/d13060274.CrossRef
Marambio M, Ballesteros A, Vilanova M, Gili JM, Garrabou J (2023) Jellyfish Alert in Observadores del Mar: A citizen science initiative to expand jellyfish knowledge. In: Dawson M, Kumar AB (eds) Book of Abstracts 7th International Jellyfish Blooms Symposium. JBS, Thiruvananthapuram, India
Martin VY, Christidis L, Pecl GT (2016) Public interest in marine citizen science: is there potential for growth?. BioSci 66:683–692. https://doi.org/10.1093/biosci/biw070.CrossRef
McKinley D, Miller-Rushing AJ, Ballard HL et al. (2016) Citizen science can improve conservation science, natural resource management, and environmental protection. Biol Conser 208:15–28. https://doi.org/10.1016/j.biocon.2016.05.015.CrossRef
Morandini AC, Stampar SN, Maronna MM, Da Silveira FL (2017) All non-indigenous species were introduced recently? The case study of Cassiopea (Cnidaria: Scyphozoa) in Brazilian waters. J Mar Biol Assoc UK 97(2):321–328. https://doi.org/10.1017/S0025315416000400.CrossRef
Moura CJ, Ropa N, Magalhães BI, Gonçalves JM (2022) Insight into the cryptic diversity and phylogeography of the peculiar fried egg jellyfish Phacellophora (Cnidaria, Scyphozoa, Ulmaridae). PeerJ 10, https://doi.org/10.7717/peerj.13125.
Muffett K, Miglietta MP (2023) Demystifying Cassiopea species identity in the Florida keys: Cassiopea xamachana and Cassiopea andromeda coexist in shallow waters. PLoS One 18(3):e0283441. https://doi.org/10.1371/journal.pone.0283441.CrossRef
Niggl W, Wild C (2010) Spatial distribution of the upside-down jellyfish Cassiopea sp. within fringing coral reef environments of the Northern Red SEa: implications for its life cycle. Helgol Mar Res 64:281–287. https://doi.org/10.1007/s10152-009-0181-8.CrossRef
Özgür E, Öztürk B (2008) A population of the alien jellyfish, Cassiopea andromeda (Forsskål, 1775) (Cnidaria: Scyphozoa: Rhizostomea) in the Ölüdeniz Lagoon, Turkey. Aquat Invasions 3(4):423–428. https://doi.org/10.3391/ai.2008.3.4.8.CrossRef
Parravicini V, Mangialajo L, Mousseau L, Peirano A, Morri C, Montefalcone M, Francour P, Kulbicki M, Bianchi CN (2015) Climate change and warm-water species at the north-western boundary of the Mediterranean Sea. Mar Ecol 36:897–909. https://doi.org/10.1111/maec.12277.CrossRef
Pocock MJO, Adriaens T, Bertolino S, Eschen R, Essl F, Hulme PE, Jeschke JM, Roy HE, Teixeira H, de Groot M (2024) Citizen science is a vital partnership for invasive alien species management and research. iScience 27:108623. https://doi.org/10.1016/j.isci.2023.108623.CrossRef
Price-Jones V, Brown PMJ, Adriaens T, Tricarico E, Farrow RA, Cardoso AC, Gervasini E, Groom Q, Reyserhove L, Schade S, Tsinaraki C, Marchante E (2022) Eyes on the aliens: citizen science contributes to research, policy and management of biological invasions in Europe. NeoBiota 78:1–24. https://doi.org/10.3897/neobiota.78.81476.CrossRef
Quignard JP, Tomasini JA (2000) Mediterranean fish biodiversity. Biol Mar Medit 7(3):1–66.
De Rinaldis G, Leone A, De Domenico S, Bosch-Belmar M, Slizyte R, Milisenda G, Santucci A, Albano C, Piraino S (2021) Biochemical characterization of Cassiopea andromeda (Forsskål, 1775), another Red Sea Jellyfish in the Western Mediterranean Sea. Mar Drugs 19:498. https://doi.org/10.3390/md19090498.CrossRef
Rosales-Catalán L, Estrada-González MC, Rivera-Pérez C, Sánchez MAR, Gamero-Mora E, Morandini AC, Mendoza-Becerril MA (2021) Genetic and morphological evidence of the presence of Phyllorhiza punctata in the southwestern Gulf of California (NE Pacific Ocean). Aquat Invasions 16:637–652. https://doi.org/10.3391/AI.2021.16.4.04.
Roy HE, Bacher S, Essl F et al. (2019) Developing a list of invasive alien species likely to threaten biodiversity and ecosystems in the European Union. Glob Change Biol 25:1032–1048. https://doi.org/10.1111/gcb.14527.CrossRef
RStudio Team (2020) RStudio: Integrated Development for R. RStudio, PBC, Boston, MA URL http://www.rstudio.com/.
Schembri PJ, Deidun A, Vella PJ (2010) First record of Cassiopea andromeda (Scyphozoa: Rhizostomeae: Cassiopeidae) from the central Mediterranean Sea. Mar Biodivers Rec 3: 2. https://doi.org/10.1017/S1755267209990625.CrossRef
Servello G, Andaloro F, Azzurro E, Castriota L, Catra M, Chiarore A, Crocetta F, D’alessandro M, Denitto F, Froglia C, Gravili C et al. (2019) Marine alien species in Italy: a contribution to the implementation of descriptor D2 of the marine strategy framework directive. Mediterr Mar Sci 20:1–48. https://doi.org/10.12681/mms.18711.CrossRef
Siokou I, Ateş AS, Ayas D, Ben Souissi J, Chatterjee T, Dimiza M, Durgham H, Dogrammatzi K, Erguden D, Gerakaris V, Grego M et al. (2013) New Mediterranean biodiversity records (June 2013). Mediterr Mar Sci 14:238–249. https://doi.org/10.12681/mms.450.CrossRef
Spanier E (1989) Swarming of jellyfishes along the Mediterranean coast of Israel. Isr J Zool 36:55–56.
Stock A, Crowder LB, Halpern BS, Micheli F (2018) Uncertainty analysis and robust areas of high and low modeled human impact on the global oceans. Conserv Biol 32(6):1368–1379. https://doi.org/10.1111/cobi.13141.CrossRef
Stoner EW, Layman CA, Yeager LA, Hassett HM (2011) Effects of anthropogenic disturbance on the abundance and size of epibenthic jellyfish Cassiopea spp. Mar Pollut Bull 62:1109–1114. https://doi.org/10.1016/j.marpolbul.2011.03.023.CrossRef
Swift HF, Gómez Daglio L, Dawson MN (2016) Three routes to crypsis: Stasis, convergence, and parallelism in the Mastigias species complex (Scyphozoa, Rhizostomeae). Mol Phylogenet and Evol 99:103–115. https://doi.org/10.1016/j.ympev.2016.02.013.
Thé J, Mammone M, Piraino S, Pennetta A, De Benedetto GE, Garcia TM, de Oliveira Soares M, Rossi S (2023) Understanding Cassiopea andromeda (Scyphozoa) invasiveness in different habitats: a multiple biomarker comparison. Water 15:2599. https://doi.org/10.3390/w15142599.CrossRef
Thiel M, Penna-Díaz MA, Luna-Jorquera G, Salas S, Sellanes J, Stotz W (2014) Citizen Scientist and Marine Research: Volunteer participants, their contributions, and projection for the future. Oceanogr Mar Biol Ann Rev 52:257–314.
Tiralongo F, Crocetta F, Riginella E, Lillo AO, Tondo E, Macali A, Mancini E, Russo F, Coco S, Paolillo G, Azzurro E (2020) Snapshot of rare, exotic and overlooked fish species in the Italian seas: a citizen science survey. J Sea Res 164:101930. https://doi.org/10.1016/j.seares.2020.101930.CrossRef
Tirelli V, Goruppi A, Riccamboni R, Tempesta M (2021) Citizens’ eyes on Mnemiopsis: how to multiply sightings with a click!. Diversity 13:224. https://doi.org/10.3390/d13060224.CrossRef
Ye L, Peng S, Ma Y, Zhang W, Wang L, Sun X, Zhang C, Yeasmin M, Zhao J, Dong Z (2024) Biodiversity and distribution patterns of blooming jellyfish in the Bohai Sea revealed by eDNA metabarcoding. BMC Ecol Evo 24:37. https://doi.org/10.1186/s12862-024-02224-3.CrossRef
Yokes MB, Andreou V, Bakiu R, Bonanomi S, Camps J, Christidis G, Crocetta F, Giovos I, Gori A, Juretic T et al(2018) NewMediterranean Biodiversity Records (November 2018) Mediterr Mar Sci 19(3):673–689. https://doi.org/10.12681/mms.19386CrossRef
Zenetos A, Gofas S, Verlaque M et al (2010) Alien species in the Mediterranean Sea by 2010. A contribution to the application of the European Union’s Marine Strategy Framework Directive (MSFD). Part I. Spatial distribution Medit Mar Sci 11(2):381–493. https://doi.org/10.12681/mms.87CrossRef
Zenetos A, Gofas S, Morri C, Rosso A, Violanti D, García Raso JE et al(2012) Alien species in the Mediterranean Sea by 2012. Acontribution to the application of the European Union’s Marine Strategy Framework Directive (MSFD). Part II. Introduction trendsand pathways Mediterr Mar Sci 13:328–352. https://doi.org/10.12681/mms.327CrossRef
Zenetos A, Ovalis P, Giakoumi S, Kontadakis C, Lefkaditou E, Mpazios G, Simboura N, Tsiamis K (2020) Saronikos Gulf: a hotspot area for alien species in the Mediterranean Sea. BioInvasions Rec 9(4):873–889. https://doi.org/10.3391/bir.2020.9.4.21.CrossRef
Zenetos A, Katsanevakis S, Poursanidis D, Crocetta F, Damalas D, Apostolopoulos G, Gravili C, Vardala-Theodorou E, Malaquias M (2011) Marine alien species in Greek Seas: additions and amendments by 2010. Mediterr Mar Sci 12(1):95–120.CrossRef
