Alien crab species as potential carriers of pathogens impacting marine megafauna's health and conservation

Climate change, with special emphasis on global warming, is believed to be a key driver of the accelerated rate of alien species expansion into the Mediterranean Sea basin and, more in general, into all marine and oceanic ecosystems (Zenetos and Galanidi 2020). 
Published in Microbiology
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As a matter of fact, the last 8 years (2015-2022) have been the hottest ones ever experienced by Mother Earth throughout the last 140 years (Di Guardo 2023a).

In order to provide a numerical representation of the magnitude of such an alarming phenomenon, 70 new species were added from 2017 to 2019 to the list of those inhabiting the Mediterranean Sea (Zenetos and Galanidi 2020), including the blue swimming crabs Callinectes sapidus, of common occurrence in the central Adriatic Sea (Cerri et al. 2020), along with Portunus segnis, which has just been reported in the same geographical area (Grati et al. 2023).

The colonization of marine and oceanic ecosystems different from those where a given species, either vertebrate or invertebrate, is endemically and “traditionally” found has several implications, among which the subsequently arising alterations of sea food webs and food chains are of special concern, together with an increased risk of introduction of “new” infectious agents potentially carried by alien species into the marine and ocean environments hosting them. Furthermore, since extreme weather events like the exceedingly frequent floods represent the “alter ego” of global warming  within the climate change scenario characterizing the present “Anthropocene Epoch”, adequate attention should be also paid to the land-to-sea transfer of a large number of oro-faecally transmitted viral, bacterial, fungal and protozoan pathogens impacting the health and conservation status of marine vertebrate organisms, with special emphasis on inshore or coastal species. This is the case, among others, of Toxoplasma gondii, a zoonotic and protozoan agent of global concern to free-living cetaceans, whose health and conservation status appear to be increasingly threatened by human activities as well as by several anthropogenic and non-anthropogenic factors, often acting synergistically with each other (Di Guardo 2023b).

Noteworthy, three new Flavivirus genus members - RNA viruses classified into the Flaviviridae family - have been recently discovered in crustaceans (Gammarus chevreuxi flavivirus, Gammarus pulex flavivirus and Crangon crangon flavivirus), with Wenzhou shark flavivirus (WSFV) variants having been additionally documented in several gazami crab (Portunus trituberculatus) populations. These findings strongly support the assumption that WSFV moves horizontally between sharks and gazami crabs in ocean ecosystems (Parry and Asgari 2019). P. trituberculatus, the most fished crab worldwide and an intensely investigated crustacean model, is widely distributed in Indian and West Pacific oceans, with an ubiquitous presence of it in southeast/east Asian countries as well as in northern and eastern Australian coastal waters (Carpenter et al. 1998).

While the ability of flaviviruses to infect a range of vertebrate species has been either gained or lost throughout time (Shi et al. 2018), the aforementioned study has provided clear-cut evidence of an intriguing vertebrate-invertebrate host association in flaviviral evolution, although it was not possible to establish whether WSFV jumped from sharks to P. trituberculatus or viceversa (Parry and Asgari 2019). In this respect, it has previously been shown that other RNA viral agents like rhabdoviruses have occasionally moved between distantly related species, subsequently spreading into closely related hosts (Longdon et al. 2015). While it is still unknown if any pathological changes are caused by WSFV in susceptible host species, it should be also emphasized that viral genomes and/or antigens are abundantly present within all body tissues from infected sharks (Shi et al. 2018).

Several shark species are known to populate the Adriatic and, more in general, the Mediterranean Sea, with the health and conservation status of a number of them being increasingly threatened by both anthropogenic and non-anthropogenic factors, which largely justifies their inclusion into the "Red List" of the "International Union for the Conservation of Nature" (IUCN) (Bradai et al. 2012).

Based upon the documented occurrence in the central Adriatic Sea of C. sapidus (Cerri et al. 2020) and P. segnis (Grati et al. 2023), both of which are closely related to P. trituberculatus, it would be interesting to investigate whether WSFV or other "cousin" flaviviruses circulate also between these two alien crab species as well as between them and one or more shark species and populations residing in the same geographic areas.

In this respect, it should be additionally underscored that West Nile virus (WNV), a relevant zoonotic, arthropod-borne flaviviral pathogen infecting humans and a huge number of mammalian, avian, reptilian and amphibian species (Habarugira et al. 2020), has been deemed able to infect aquatic mammals, with WNV-infected common seals (Phoca vitulina) and killer whales (Orcinus orca) developing a fatal polioencephalomyelitis (Del Piero et al. 2006) and a non-suppurative encephalitis (St. Leger et al. 2011), respectively, in a similar fashion to WNV-infected horses (Cantile et al. 2000) and human.patients (Constant et al. 2023).

As a concluding remark, while the circulation of flaviviruses between marine and oceanic vertebrates and invertebrates, along with their potential susceptibility to flaviviral infections, undoubtedly represent challenging and intriguing issues warranting ad hoc and in-depth research efforts in the next future, I also believe that a "One Health"-based approach should be the necessary prerequisite to adequately investigate such complex host-pathogen interaction and coevolutionary dynamics, provided that human, animal and environmental health are tightly and mutually linked to each other.

 

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