# Alien crab species as potential carriers of pathogens impacting the health and conservation status of marine megafauna

Giovanni Di Guardo

► To cite this version:

Giovanni Di Guardo. Alien crab species as potential carriers of pathogens impacting the health and conservation status of marine megafauna. BioInvasions Records, 2023, 12, pp.8. hal-04194280

HAL Id: hal-04194280

https://hal.science/hal-04194280v1

Submitted on 2 Sep 2023

HAL is a multi-disciplinary open access
archive for the deposit and dissemination of sci-
entific research documents, whether they are pub-
lished or not. The documents may come from
teaching and research institutions in France or
abroad, or from public or private research centers.

L'archive ouverte pluridisciplinaire HAL, est
destinée au dépôt et à la diffusion de documents
scientifiques de niveau recherche, publiés ou non,
émanant des établissements d'enseignement et de
recherche français ou étrangers, des laboratoires
publics ou privés.

<figure><img src="image_1.png" /></figure>

Distributed under a Creative Commons CC BY 4.0 - Attribution - International License
# LETTER TO THE EDITOR

1

2

3

4

5

6

7

8

Alien crab species as potential carriers of pathogens impacting the health and conservation status of marine megafauna

Giovanni Di Guardo, DVM, Dipl. ECVP,

Retired Professor of General Pathology and Veterinary Pathophysiology at the Veterinary Medical Faculty of the University of Teramo, Località Piano d'Accio, 64100 Teramo, Italy

Current address: Viale Pasteur, 77

00144 - EUR - Rome, Italy

(E-mail address: gdiguardo@unite.it)

14

15

16

17

18

19

**Key words:** Alien species, crabs, *Portunus segnis*, *Callinectes sapidus*, *Portunus trituberculatus*, sharks, Wenzhou shark flavivirus, Adriatic Sea, Mediterranean Sea.

22

23

24

25
26

27

28

29

30

31

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). Indeed, the last 8 years (2015-2022) have been the hottest ones ever experienced by Mother Earth throughout the last 140 years (Di Guardo 2023a).

32

33

34

35

36

37

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).

38

39

40

41

42

43

44

45

46

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
47

48

49

50

51

52

53

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).

54

55

56

57

58

59

60

61

62

63

64

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).

65

66

67

68

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
69

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).

70

71

72

73

74

75

76

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).

77

78

79

80

81

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.

82

83

84

85

86

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

87

88

89

90
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.

102

103

104

105

106

107

108

109

110
References

Bradai MN, Saidi B, Enajjar S (2012), Elasmobranchs of the Mediterranean and Black Sea: Status, ecology and biology. Bibliographic analysis. Studies and Reviews. General Fisheries Commission for the Mediterranean, Food and Agriculture Organization of the United Nations, Rome, Italy, pp. 103

Cantile C, Di Guardo G, Eleni C, Arispici M (2000), Clinical and neuropathological features of West Nile virus equine encephalomyelitis in Italy. *Equine Veterinary Journal* 32: 31-35, doi:10.2746/042516400777612080

Carpenter KE, Niem VH, Norsk utviklingshjelp, South Pacific Forum Fisheries Agency, Food and Agriculture Organization of the United Nations (1998), The living marine resources of the Western Central Pacific, Volume 1, Food and Agriculture Organization of the United Nations, Rome, Italy

Cerri J, Chiesa S, Bolognini L, Mancinelli G, Grati F, Dragičević B, Dulčić J, Azzurro E (2020), Using online questionnaires to assess marine bio-invasions: A demonstration with recreational fishers and the Atlantic blue crab *Callinectes sapidus* (Rathbun, 1986) along three Mediterranean countries. *Marine Pollution Bulletin* 156: 111209, https://doi.org/10.1016/j.marpolbul.2020.111209

Constant O, Maarifi G, Barthelemy J, Martin MF, Tinto B, Savini G, Van de Perre P, Nisole S, Simonin Y, Salinas S (2023), Differential effects of Usutu and West Nile viruses on
neuroinflammation, immune cell recruitment and blood-brain barrier integrity. *Emerging Microbes and Infections* 12: 2156815, doi:10.1080/22221751.2022.2156815

Del Piero F, Stremme DW, Habecker PL, Cantile C (2006), West Nile flavivirus polioencephalomyelitis in a harbor seal (*Phoca vitulina*). *Veterinary Pathology* 43: 58-61, doi: 10.1354/vp.43-1-58

Di Guardo G (2023a), Land-to-sea pathogen transfer. *Veterinary Record* 192: 216-217, doi:10.1002/vetr.2814

Di Guardo G (2023b), Sci. Adv.: Global warming, extreme weather events, and scientific research (Letter to the Editor/e.Letter). *Science Advances*, https://www.science.org/doi/10.1126/sciadv.adf8119#elettersSection

Grati F, Froglia C, Souissi JB, Bolognini L, Azzurro E (2023), The blue swimming crab *Portunus segnis* (Forskål, 1775) reaches the Adriatic Sea: A distant and disjointed occurrence. *BioInvasions Records* 12, https://doi.org/10.3391/bir.2023.12.4.15

Habarugira G, Suen WW, Hobson-Peters J, Hall RA, Bielefeldt-Ohmann H (2020), West Nile virus: An update on pathobiology, epidemiology, diagnostics, control and "One Health" implications. *Pathogens*. 9: 589, doi:10.3390/pathogens9070589
156 Longdon B, Murray GG, Palmer WJ, Day JP, Parker DJ, Welch JJ, Obbard DJ, Jiggins FM (2015), 157 The evolution, diversity, and host associations of rhabdoviruses. *Virus Evolution* 1: vev014, doi: 158 10.1093/ve/vev014

159 Parry R, Asgari S (2019), Discovery of novel crustacean and cephalopod flaviviruses: Insights into 160 the evolution and circulation of flaviviruses between marine invertebrate and vertebrate hosts. 161 *Journal of Virology* 93: e00432-19, doi: 10.1128/JVI.00432-19

162
163 Shi M, Lin XD, Chen X, Tian JH, Chen LJ, Li K, Wang W, Eden JS, Shen JJ, Liu L, Holmes EC, 164 Zhang YZ (2018), The evolutionary history of vertebrate RNA viruses. *Nature* 556: 197-202, doi: 165 10.1038/s41586-018-0012-7

166
167 St Leger J, Wu G, Anderson M, Dalton L, Nilson E, Wang D (2011), West Nile virus infection in 168 killer whale, Texas, USA, 2007. *Emerging Infectious Diseases* 17: 1531-1533, doi: 169 10.3201/eid1708.101979

170
171 Zenetos A, Galanidi M (2020), Mediterranean non indigenous species at the start of the 2020s: Recent 172 changes. *Marine Biodiversity Records* 13: 10, https://doi.org/10.1186/s41200-020-00191-4