The Portuguese Man-of-war, One of The Most Dangerous Marine Species, Has Always Entered The Mediterranean Sea: Strandings, Sightings And Museum Collections


 A search from different kinds of sources has been carried out to review the incidence of Physalia physalis, the Portuguese man-of-war, in the Mediterranean Sea; scientific and grey literature, social media, zoological museums were accessed. The records of the species were considered validated if documented with images or collected specimens. It was possible to date the putative first record of Physalia physalis in the Mediterranean Sea, thanks to a couple of colonies preserved in a historical collection, originating from the Gulf of Naples in 1914. Some massive strandings occurred in localities of the Alboran Sea, area of entrance from the Atlantic from where the species spread mainly along the Sicilian waters, in the central Mediterranean Sea. The records from the Italian maritime regions were then subdivided into three categories of risk according to the season of occurrence. These categories were created to assign a level of danger for swimmers to the sightings of Physalia physalis. The increasing sightings of such a poisonous organism in coastal waters can represent a risk to human health, and also to all those activities linked to the marine tourism sector. The involvement of citizens and touristic structures for the early detection of Physalia physalis can play a key role in preventing encounters with the species, allowing marine tourist facilities to operate within a range of reasonable security.


Introduction
The presence or even the blooms of marine jelly sh, the gelatinous animals which have a planktonic lifestyle, can have several negative impacts on ecosystems, on the economy (e.g., tourism, sheries, aquaculture) and human health (De Donno et al. 2014;Bosch-Belmar et al. 2017). About this latter aspect, it is well known that speci cally the cnidarians, commonly named jelly sh, can generate serious wounds and poisoning to humans, and in some cases the death (Burnett and Gable 1989;Burke 2002). However, since this gelatinous zooplankton is not usually targeted by sheries and not easily surveyed or collected by researches activity, data on dispersal and impact on human life are scarce or sometimes lacking (Condon et Gravili and Rossi 2021). Hence, we cannot state with absolute certainty for several species that a general increase of their abundance is occurring or will occur in a speci c region. In this regard, Citizen Science and local public networks can be of great help in collecting data on a large spatial-temporal scale in order to better understand the dynamics of jelly sh populations (Baumann and Schernewski 2012;Fleming et al. 2013).
One of the most dangerous species in the Mediterranean Sea is the Portuguese man-of-war, Physalia physalis (Linnaeus, 1758), a pleustonic colonial organism rarely observed in the Mediterranean basin, whose direct observations mainly concern stranded specimens ( Berdar Deidun et al. 2020). This species, belonging to the Cnidarian group -order Siphonophores, is part of the oating community of ocean organisms that live at the interface between water and air (Boero 2013;Munro et al. 2019). Though the whole body seems a single individual, it is a colony in which small individuals (zooids) perform different functions such as oating, feeding, defence and reproduction (Lane 1960). The structure of the colony is complex; on the whole, it can be described as composed of two portions: a portion visible oating on the ocean surface -pneumatophore -and a not visible tentacular portion expanding below the water surface -the complex of zooids (Munro et al. 2019).
Physalia physalis is easily recognized by its bluish pneumatophore, and by an air bladder developed from one of the zooids that can reach 30 cm in length (Bardi and Marques 2007;Munro et al. 2019), surmounted by a crest that acts like a sail that helps to navigate and oat on the surface of the sea (Lane 1960; Iosilevskii and Weihs 2009). The tentacles of this species, may be up to 30 m long and containing more than 750,000 stinging cells each (Munro et al. 2019), contain the "physaliatoxin" (Bardi and Marques 2007) that is the cause of its painful sting, which causes a series of symptoms, from local skin necrosis to neurological and cardiorespiratory problems that can cause death (Labadie et al. 2012). Furthermore, unlike other cnidarian species, the nematocysts of the Portuguese man-of-war seem can penetrate surgical gloves (Pierce 2006). Physalia physalis behaves like a predator, plays an important ecological role and in uences the abundance of populations of small animals, in particular juveniles of shes and larvae that it captures with tentacles (Purcell 1984). On the other hand, the Portuguese man-of-war can be preyed upon by shes, turtles, lepadomorph barnacles and glaucid nudibranchs (Wangersky and Lane 1960;Bieri 1966; Thompson and Bennett 1970;Arai 2005), and other taxa not disclosed yet (Arai 2005).
Physalia physalis is a cosmopolitan species, distributed from tropical to temperate waters roughly comprised from 51°N to 38°S (Shannon and Chapman 1983;Kirkpatrick and Pugh 1984;Haddad et al. 2002;Elston 2007;Pontin et al. 2011;Oliveira et al. 2016). The locomotion of P. physalis is affected by winds. The species is surface-dwelling thanks to the chamber lled with air and carbon monoxide which represents a sail (the pneumatophore extending above the water's surface) thus the colony moves with the prevailing wind (Mapstone 2015).
It is interesting to underline that the colonies of P. physalis, which move towards coastal areas, where they nd optimal trophic conditions, and oat along the shoreline, as a consequence of the direction and energy of prevailing winds and surface currents, originate from unknown marine georeferenced points (Graham et al. 2001). Thus, the continuously updating of records is much relevant to foresee the dispersal routes.
Up to date, the rst documented record of P. physalis for the Mediterranean Sea dates back to 1980 (Berdar and Cavallaro 1980). The species has been subsequently reported sporadically, in the western and central basins, Gathering the baseline information on this species records over time and space constitutes an important task for the elaboration of management programs aimed to alert the local human population and touristic structures. Physalia physalis represents an important species to be aware of, and for which dissemination of data about its presence should be improved.
Here we introduce a review of sightings, strandings and museum records of the species for the Mediterranean Sea, and the rst documented Mediterranean records, originating from the southern Tyrrhenian basin. Relevant biodiversity information can be extrapolated from materials and data collected in the past and preserved in the Natural History Museums, which can provide overlooked data and, in many cases, still unpublished (Tedesco et al. 2020;Lo Brutto et al. 2021). The sightings and strandings summarized herein highlight the potential role of the zoological museums and the citizens' participatory science. The data from social media and local Citizen Science projects can have a key role if well managed; the information is often uploaded on the web but not archived in the scienti c literature or summarized in any report. The case P. physalis is herein reported to ll such gap.

Methods
A survey on the presence of Physalia physalis in the Mediterranean Sea was carried out. Information from scienti c and grey literature, from the web and social media, was extrapolated and analyzed.
As the Italian maritime sectors reported the most frequent records, a further search of historical museum specimens in Italy was integrated to nd out old data never published. In particular, information was acquired from the "Darwin Dohrn" Museum of the Anton Dohrn Zoological Station of Naples and the Museum of Zoology "P. Doderlein" of the University of Palermo (MZPA), Italy.
For each kind of source, only information documented with images or collected specimens was selected to consider the data validated. The records were assigned to the main Mediterranean sectors based on the sampling locality; from west to east: Alboran Sea, Western Mediterranean, North-Western Mediterranean, Central Tyrrhenian Sea, Southern Tyrrhenian Sea, Channel of Sicily, Strait of Messina.
The records from the Italian maritime regions were subdivided into three "categories of risk" according to the season of occurrence. The records of P. physalis detected in February-March were included in the low-risk category; the records occurred in April-May in the medium-risk one; the records happened in June-August in the high-risk category. These categories were created to designate a level of danger for swimmers in a particular area, thus it was assumed that the sightings of P. physalis in the summer period (June-August) could be considered the most dangerous (high-risk), according to the higher number of swimmers than the remaining months of the year; while medium and low-risk were associated to a lower frequency of human activities accordingly. The Italian records belonging to the three categories of risk were counted and grouped according to the biogeographical sectors proposed by Bianchi (2004). A nal map showed such clustering.

Results
More than 550 colonies of Physalia physalis were detected within the Mediterranean Sea, in a timescale comprised between 1914 and 2021 (April). Three colonies were found in museum collections, 530 colonies were counted from scienti c literature, and information about 14 colonies was extrapolated from the web. Most of the colonies were reported stranded. The highest incidence was recorded in the Alboran Sea, across a limited area, from the Strait of Gibraltar and the Almeria-Oran Front (Tintore et al 1988); while the central Mediterranean area was the one where P. physalis mainly spread (Table 1). None information was provided from the Eastern Mediterranean, Adriatic Sea and Aegean and Levantine basin.
All data are shown in Table 1; the records are listed according to a chronological order, and each locality is associated to a marine sector indicated by a point in the map of the Fig. 1 (see the ID numbers). The marine sectors where P. physalis was been scored are the following: Maroccan waters -Alboran Sea (corresponding to the ID number 1 on the map of  Table 1 and Fig. 1). Table 1 Records of Physalia physalis in the Mediterranean Sea, pointed out in the map of Fig. 1. The records are listed following a chronological order; year and month, when noticed, are speci ed. The locality and the marine sectors are indicated, the last according to the biogeographical division of the Mediterranean Sea and Italian waters. The oldest documented colonies in the Mediterranean Sea were collected in the Gulf of Naples in 1914. Two colonies are stored at the "Darwin Dohrn" Museum of the Anton Dohrn Zoological Station in Naples (Voucher code: HYD001) (Fig. 2). Further, by consulting the archive of the Museum of Zoology "Pietro Doderlein" of the University of Palermo, it was also possible to date a colony of P. physalis, collected along the North-Western coast of Sicily Island (southern Italy), in a period antecedent to 1980, presumably around 1960 (Silvano Riggio pers. comm.). The colony was found stored in a glass jar and is in a good state of conservation (Voucher code MZPA-IM-545).

Recent records
The recent records herein assumed are the ones reported from 1980 to nowadays; 1980 is the year of the presumptive rst Mediterranean record, as highlighted by Berdar and Cavallaro (1980), however not con rmed by the museum collections above showed. The specimens preserved in the zoological collections did not further corroborate a record which was presumptively thought rst on the North-Western coast of Sicily. The colony By creating a map of the P. physalis records documented in the last century, and superimposing it with the trajectories of the surface currents that drive the colonies (Poulain et al. 2012), it has been shown a general pattern of occurrence of the Portuguese man-of-war within the Mediterranean Sea (Fig. 1).

Records of Physalia physalis in the Italian maritime regions
The records of Physalia physalis were grouped in four Italian biogeographical sectors: Sardinian waters, Channel of Sicily, Tyrrhenian Sea, Strait of Messina. The clustering was arranged to identify those marine areas most affected by P. physalis sightings and strandings. Furthermore, the validated records of P. physalis were subdivided into three categories of risk (Fig. 4) according to the season of occurrence and the level of danger for swimmers.
The Sardinian waters recorded eight colonies, two belonging to the low-risk category, three to medium-risk and three to high-risk class (Fig .4). The Channel of Sicily showed the largest number of colonies sighted and stranded, 31 colonies of which ten were at low-risk, seventeen at medium-risk and four at high-risk. In the Tyrrhenian marine sector ve colonies occurred, of which the only one at low-risk, two at medium-risk and two at high-risk. In this marine sector, the colonies of the Naples and Palermo museums were excluded because without data of the month. The Strait of Messina registered six colonies, of which ve at low-risk and one at medium-risk.

Discussion
Physalia physalis is among the most dangerous species of cnidarians that threaten public health. This is because the sting of this species is very painful and the venom present in nematocysts can cause health complications for people attacked. In some documented cases, these incidents have had fatal outcomes (Burke 2002;Labadie et al. 2012). Physalia physalis can be harmful also in an indirect way, as prey of neustonic nudibranchs; some planktonic molluscs ingest the cnidarian and undischarged nematocysts as a defensive strategy (Thompson and Bennett 1969). The nematocysts maintain toxicity in the predators (Thompson and Bennett 1969;Ottuso 2009). The same harmfulness has been detected in the stranded P. physalis individuals on a beach, even after several days of dehydration (Tiballs 2006).
The World Health Organization (WHO) included P. physalis in the dangerous aquatic organisms for human health within the "Guidelines for safe recreational water environments" and suggested avoiding bathing in waters where Portuguese man-of-war is concentrated (WHO 2003). The assessment of the risk of contact with the Portuguese man-of-war within the Mediterranean Sea to develop policies for controlling and managing the well-being in water recreation needs a wide spatial and temporal scale of data. Further, the launch of a series of activities, through scienti c dissemination campaigns, can allow the local authorities in charge to plan effective actions regarding the protection of public health and tourism activities not as isolated measurements for managing risks Under this operational framework, it was possible to track the putative rst record of P. physalis in the Mediterranean Sea. The oldest documented capture of P. physalis occurred in the Gulf of Naples in 1914. Furthermore, it was possible to date a colony of P. physalis, presumably beached, on the North-Western coast of Sicily in a period antecedent to 1980 (Silvano Riggio pers. comm.), even older than the record by Berdar and Cavallaro (1980) in the Strait of Messina.
The role of museums was fundamental for reconstructing the past distribution of P. physalis. A new scenario on its presence in the Mediterranean Sea has been depicted, up to now suspected by the scienti c community (Boero 2013). Physalia physalis has always entered the Mediterranean Sea.
The occurrence of P. physalis in the Mediterranean had been considered rare till the last decades, due to the lack of documented records in the literature (Castriota et al. 2017). Only in recent years, an increase of P. physalis sightings in the central Mediterranean Sea was reported. The reasons are attributable to the advancement of technological innovations (smartphones), which make sightings validated with photographs or videos, in the past not allowed, as the case of the Maltese shermen who were not able to provide evidence of sightings (Calleja 2009). behave like a physical barrier, as suggested by Prieto et al. (2015). The Atlantic water in the Alboran Sea describes two anticyclonic (clockwise rotating) gyres that dominate the surface ow pattern: a quasi-permanent anticyclonic gyre in the west (Western Alboran Gyre, WAG) and a more variable circuit in the east (Eastern Alboran Gyre, EAG) ( Fig. 1) (Millot 1999). In such a situation, the vein owing from Spain to Algeria, named 'the Almeria-Oran jet' (Millot 1999), stops a large number of colonies, preventing their eastward dispersal, except some colonies that nd a favourable oceanographic route and move towards the Western and Central Mediterranean.
As the circulation features of the Alboran sector is largely controlled by meteorological conditions (Macías et al. 2008), some concerns regard climate change which could alter the role of natural barrier in the future, allowing a greater entry of P. physalis from the Atlantic Ocean. Under such a hypothetical scenario of an increasing number of colonies of P. physalis, we should limit human activities eventually exposed to risks in the central Mediterranean.
The pattern described in the map of Fig. 1 gives an idea of how the Portuguese man-of-war circulates in the Mediterranean. The records follow the surface currents and cover a limited geographical range may be due to biological constraints, as it is probable that Physalia physalis completes its life cycle in the Mediterranean Sea.
The tracking of this species in the Mediterranean Sea should not be overlooked, as the species threaten human health. For this reason, we selected some areas of risk by grouping the records of P. physalis in the most concerned four Italian maritime sectors: Sardinian waters; Channel of Sicily; Tyrrhenian Sea; Strait of Messina. The marine sectors most involved by P. physalis passage were identi ed and associated with levels of danger for swimmers according to the seasons of occurrence of the colonies (Fig. 4). The highest number of colonies were recorded in the Channel of Sicily, probably also thanks to the active monitoring that has taken place in recent years. The area showed records belonging to the three categories of risk, low-medium-and high-risk category; it means that the species occurs from February to August. The Strait of Messina seems to be the area less involved by the passage of the Portuguese man-of-war.
The recent expansion of Citizen Science projects and the use of social media for the detection of "strangelooking species" or charismatic species may have certainly contributed to increasing the number of observations in nature, including P. physalis. As a consequence, the presence of the species seems to have suddenly increased only in recent years.
In this regard, we have observed, especially in the last decade, how Citizen Science is experiencing an upsurge of interest and was demonstrated to be particularly effective for data collection and maritime monitoring (Devictor The results suggest that a national multidisciplinary summer surveillance program in the central Mediterranean Sea coast is required to provide alerts to the public, to better identify patients at risk for developing severe clinical symptoms, and hopefully to improve the quality of health care. Local authorities should set up a monitoring and alert system, with the participation of territorial organizations, and the contribution of the scienti c community, as proposed in other seas (Labadie et al. 2012). In this regard, engaging tourists as citizen scientists can be a useful and low-cost method for the monitoring of this and other dangerous species in general on a large spatialtemporal scale (Schaffer and Tham 2019). Continuous monitoring could bene cial for marine tourist facilities.
In general, the importance of obtaining time-series data to monitor biodiversity changes in the Mediterranean Sea is herein demonstrated and acquire relevant role respect the more frequent extreme events and temperature anomalies.
Declarations Figure 1 Map of Physalia physalis records in the Mediterranean Sea (1914 -2021). The black points with the ID number indicate the area where P. physalis was found. The localities reported in Table 1 are associated with the ID number of such areas according to a neighbouring criterion. The arrows indicate the model of the main surface currents present in the Mediterranean Sea, according to Millot (1999) and Poulain et al. (2012).

Figure 2
The two colonies of Physalia physalis collected in the Gulf of Naples (Italy) in 1914, preserved at the "Darwin Dohrn" Museum of Naples (photo by Akira Kihara, Science Center, Hosei University, Tokyo; ©2007 Zoological Collection Database @Stazione Zoologica "Anton Dohrn").

Figure 3
The colony of Physalia physalis recorded in the north-western coast of Sicily, southern Tyrrhenian basin (2021), photo by Rosario Badalamenti.