The puzzling occurrence of the upside-down jellyfish <i>Cassiopea</i> (Cnidaria: Scyphozoa) along the Brazilian coast: a result of several invasion events?

Stampar, Sergio N.; Gamero-Mora, Edgar; Maronna, Maximiliano M.; Fritscher, Juliano M.; Oliveira, Bruno S.P.; Sampaio, Cláudio L.S.; Morandini, André C.

doi:10.3897/zoologia.37.e50834

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Research Article • Zoologia (Curitiba) 37 • 2020 • https://doi.org/10.3897/zoologia.37.e50834 copy

The puzzling occurrence of the upside-down jellyfish Cassiopea (Cnidaria: Scyphozoa) along the Brazilian coast: a result of several invasion events?

Authorship SCIMAGO INSTITUTIONS RANKINGS

ABSTRACT

The massive occurrence of jellyfish in several areas of the world is reported annually, but most of the data come from the northern hemisphere and often refer to a restricted group of species that are not in the genus Cassiopea. This study records a massive, clonal and non-native population of Cassiopea and discusses the possible scenarios that resulted in the invasion of the Brazilian coast by these organisms. The results indicate that this jellyfish might have invaded the Brazilian coast multiple times.

KEY WORDS:
Invasive species; jellyfish bloom; medusa; non-native species

Terminal ID	Molecular species ID	Locality	GenBank accession number	Reference
CandroHaw1	C. andromeda	Hilton Lagoon, Waikiki Beach, Oahu, Hawaii, USA	AF231109.1	Holland et al. (2004Holland 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. Marine Biology 145(6): 1119-1128. https://doi.org/10.1007/s00227-004-1409-4 https://doi.org/10.1007/s00227-004-1409-... )
CxamaUSAFl1	C. andromeda	Key Largo, Florida Keys	AY319468.1	Holland et al. (2004Holland 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. Marine Biology 145(6): 1119-1128. https://doi.org/10.1007/s00227-004-1409-4 https://doi.org/10.1007/s00227-004-1409-... )
CfrondUSAFl1	C. andromeda	Key Largo, Florida Keys	AY319467.1	Holland et al. (2004Holland 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. Marine Biology 145(6): 1119-1128. https://doi.org/10.1007/s00227-004-1409-4 https://doi.org/10.1007/s00227-004-1409-... )
CxamaBerm1	C. andromeda	Walsingham Pond, Bermuda	AY319466.1	Holland et al. (2004Holland 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. Marine Biology 145(6): 1119-1128. https://doi.org/10.1007/s00227-004-1409-4 https://doi.org/10.1007/s00227-004-1409-... )
CxamaBerm2	C. andromeda	Richardson Bay, Bermuda	AY319465.1	Holland et al. (2004Holland 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. Marine Biology 145(6): 1119-1128. https://doi.org/10.1007/s00227-004-1409-4 https://doi.org/10.1007/s00227-004-1409-... )
CxamaBerm3	C. andromeda	Richardson Bay, Bermuda	AY319464.1	Holland et al. (2004Holland 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. Marine Biology 145(6): 1119-1128. https://doi.org/10.1007/s00227-004-1409-4 https://doi.org/10.1007/s00227-004-1409-... )
CxamaBerm4	C. andromeda	Walsingham Pond, Bermuda	AY319463.1	Holland et al. (2004Holland 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. Marine Biology 145(6): 1119-1128. https://doi.org/10.1007/s00227-004-1409-4 https://doi.org/10.1007/s00227-004-1409-... )
CandroEgyRSea	C. andromeda	El Ghardaqa, Egypt, Red Sea	AY319458.1	Holland et al. (2004Holland 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. Marine Biology 145(6): 1119-1128. https://doi.org/10.1007/s00227-004-1409-4 https://doi.org/10.1007/s00227-004-1409-... )
CandroHaw4	C. andromeda	Kainaone fish pond, Moloka’i, Hawaii, USA	AY319454.1	Holland et al. (2004Holland 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. Marine Biology 145(6): 1119-1128. https://doi.org/10.1007/s00227-004-1409-4 https://doi.org/10.1007/s00227-004-1409-... )
CandroHaw5	C. andromeda	Kainaone fish pond, Moloka’i, Hawaii, USA	AY319453.1	Holland et al. (2004Holland 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. Marine Biology 145(6): 1119-1128. https://doi.org/10.1007/s00227-004-1409-4 https://doi.org/10.1007/s00227-004-1409-... )
CandroHaw7	C. andromeda	Hilton leeward, Oahu, Hawaii, USA	AY319451.1	Holland et al. (2004Holland 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. Marine Biology 145(6): 1119-1128. https://doi.org/10.1007/s00227-004-1409-4 https://doi.org/10.1007/s00227-004-1409-... )
CandroHaw8	C. andromeda	Hilton leeward, Oahu, Hawaii, USA	AY319450.1	Holland et al. (2004Holland 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. Marine Biology 145(6): 1119-1128. https://doi.org/10.1007/s00227-004-1409-4 https://doi.org/10.1007/s00227-004-1409-... )
CandroHaw9	C. andromeda	Hilton leeward, Oahu, Hawaii, USA	AY319449.1	Holland et al. (2004Holland 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. Marine Biology 145(6): 1119-1128. https://doi.org/10.1007/s00227-004-1409-4 https://doi.org/10.1007/s00227-004-1409-... )
CandroHaw10	C. andromeda	Hilton leeward, Oahu, Hawaii, USA	AY319448.1	Holland et al. (2004Holland 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. Marine Biology 145(6): 1119-1128. https://doi.org/10.1007/s00227-004-1409-4 https://doi.org/10.1007/s00227-004-1409-... )
CandroBra1	C. andromeda	Cabo Frio, Rio de Janeiro, Brazil	KC464458.1	Morandini et al. (2017Morandini AC, Stampar SN, Maronna MM, Silveira FL (2017) All non-indigenous species were introduced recently? The case study of Cassiopea (Cnidaria: Scyphozoa) in Brazilian waters. Journal of the Marine Biological Association of the United Kingdom 97(2): 321-328. https://doi.org/10.1017/S0025315416000400 https://doi.org/10.1017/S002531541600040... )
Cassiopea_Alagoas_4	C. andromeda	Pratagy, Maceió, Alagoas, Brazil	MT806178	This study
Cassiopea_Alagoas_3	C. andromeda	Pratagy, Maceió, Alagoas, Brazil	MT806179	This study
Cassiopea_Alagoas_2	C. andromeda	Pratagy, Maceió, Alagoas, Brazil	MT806180	This study
Cassiopea_Alagoas_1	C. andromeda	Pratagy, Maceió, Alagoas, Brazil	MT806181	This study
CfrondPan1	C. frondosa	San Blas Islands, Panama	AY319470.1	Holland et al. (2004Holland 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. Marine Biology 145(6): 1119-1128. https://doi.org/10.1007/s00227-004-1409-4 https://doi.org/10.1007/s00227-004-1409-... )
CfrondPan2	C. frondosa	San Blas Islands, Panama	AY319469.1	Holland et al. (2004Holland 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. Marine Biology 145(6): 1119-1128. https://doi.org/10.1007/s00227-004-1409-4 https://doi.org/10.1007/s00227-004-1409-... )
CandroInd1	C. ornata	Kakaban, Kalimantan, Indonesia	AY319473.1	Holland et al. (2004Holland 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. Marine Biology 145(6): 1119-1128. https://doi.org/10.1007/s00227-004-1409-4 https://doi.org/10.1007/s00227-004-1409-... )
CandroInd2	C. ornata	Kakaban, Kalimantan, Indonesia	AY319472.1	Holland et al. (2004Holland 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. Marine Biology 145(6): 1119-1128. https://doi.org/10.1007/s00227-004-1409-4 https://doi.org/10.1007/s00227-004-1409-... )
CandroFiji	C. ornata	Dravuni, Fiji	AY319457.1	Holland et al. (2004Holland 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. Marine Biology 145(6): 1119-1128. https://doi.org/10.1007/s00227-004-1409-4 https://doi.org/10.1007/s00227-004-1409-... )
CandroPal1	C. ornata	Short Drop Off, Palau	AY319456.1	Holland et al. (2004Holland 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. Marine Biology 145(6): 1119-1128. https://doi.org/10.1007/s00227-004-1409-4 https://doi.org/10.1007/s00227-004-1409-... )
CandroPal2	C. ornata	Short Drop Off, Palau	AY319455.1	Holland et al. (2004Holland 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. Marine Biology 145(6): 1119-1128. https://doi.org/10.1007/s00227-004-1409-4 https://doi.org/10.1007/s00227-004-1409-... )
CxamaPan1	C. xamachana	Bocas del Toro, Panama	JN700936.1	Holland et al. (2004Holland 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. Marine Biology 145(6): 1119-1128. https://doi.org/10.1007/s00227-004-1409-4 https://doi.org/10.1007/s00227-004-1409-... )
CxamaBra1	C. xamachana	São Sebastião, São Paulo, Brazil	MN539722.1	This study
CxamaBra2	C. xamachana	Imbé, Rio Grande do Sul, Brazil	MN602311.1	Gamero-Mora et al. (2019Gamero-Mora E, Halbauer R, Bartsch V, Stampar SN, Morandini AC (2019) Regenerative capacity of the upside-down jellyfish Cassiopea xamachana. Zoological Studies 58: e37. https://doi.org/10.6620/ZS.2019.58-37 https://doi.org/10.6620/ZS.2019.58-37... )
CandroAus	Cassiopea sp. 1	Port Douglas, Queensland, Australia	AY319471.1	Holland et al. (2004Holland 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. Marine Biology 145(6): 1119-1128. https://doi.org/10.1007/s00227-004-1409-4 https://doi.org/10.1007/s00227-004-1409-... )
CandroPNG1	Cassiopea sp. 2	Observation Point, Papua New Guinea	AY319459.2	Holland et al. (2004Holland 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. Marine Biology 145(6): 1119-1128. https://doi.org/10.1007/s00227-004-1409-4 https://doi.org/10.1007/s00227-004-1409-... )
CandroPNG4	Cassiopea sp. 2	Observation Point, Papua New Guinea	AY319460.1	Holland et al. (2004Holland 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. Marine Biology 145(6): 1119-1128. https://doi.org/10.1007/s00227-004-1409-4 https://doi.org/10.1007/s00227-004-1409-... )
CandroPNG2	Cassiopea sp. 3	Emona, Papua New Guinea	AY319461.1	Holland et al. (2004Holland 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. Marine Biology 145(6): 1119-1128. https://doi.org/10.1007/s00227-004-1409-4 https://doi.org/10.1007/s00227-004-1409-... )
CandroHaw6	Cassiopea sp. 3	Wedding Chapel, windward O’ahu, Hawaii, USA	AY331594.1	Holland et al. (2004Holland 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. Marine Biology 145(6): 1119-1128. https://doi.org/10.1007/s00227-004-1409-4 https://doi.org/10.1007/s00227-004-1409-... )
CandroHaw11	Cassiopea sp. 3	Mid Pacific Golf Course pond, windward O’ahu, Hawaii, USA	AY331593.1	Holland et al. (2004Holland 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. Marine Biology 145(6): 1119-1128. https://doi.org/10.1007/s00227-004-1409-4 https://doi.org/10.1007/s00227-004-1409-... )
CandroJap1	Cassiopea sp. 5	Unknown	AB563740.1	Ojimi and Hidaka (2010Ojimi MC, Hidaka M (2010) Comparison of telomere length among different life cycle stages of the jellyfish Cassiopea andromeda. Marine Biology 157: 2279-2287. https://doi.org/10.1007/s00227-010-1495-4 https://doi.org/10.1007/s00227-010-1495-... )
CandroJap2	Cassiopea sp. 5	Unknown	AB563739.1	Ojimi and Hidaka (2010Ojimi MC, Hidaka M (2010) Comparison of telomere length among different life cycle stages of the jellyfish Cassiopea andromeda. Marine Biology 157: 2279-2287. https://doi.org/10.1007/s00227-010-1495-4 https://doi.org/10.1007/s00227-010-1495-... )
Catostylus_mosaicus	Catostylus mosaicus	Lake Illawara, New South Wales, Australia	AY319476.1	Holland et al. (2004Holland 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. Marine Biology 145(6): 1119-1128. https://doi.org/10.1007/s00227-004-1409-4 https://doi.org/10.1007/s00227-004-1409-... )

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[1] Corresponding author: Sergio N. Stampar (sergio.stampar@unesp.br)