[Cnidaria • 2017] Multigene Phylogeny of the Scyphozoan Jellyfish Family Pelagiidae reveals that the Common U.S. Atlantic Sea Nettle Comprises Two Distinct Species (Chrysaora quinquecirrha & C. chesapeakei) ---ScRaBBlE

 Figure 3: Various morphs of Chrysaora quinquecirrha s.l. 
(A) Offshore South Carolina (OSC); (B) Sample taken from offshore Georgia; (C) Engelhard, NC (PAM); (D) White Chesapeake Bay color morph (Broome’s Island, MD—Patuxent River); (E) Red-striped Chesapeake Bay color morph (Solomons, MD—Patuxent River).

 Bayha​, Collins & Gaffney, 2017.    DOI: 10.7717/peerj.3863

Abstract

Background

Species of the scyphozoan family Pelagiidae (e.g., Pelagia noctiluca, Chrysaora quinquecirrha) are well-known for impacting fisheries, aquaculture, and tourism, especially for the painful sting they can inflict on swimmers. However, historical taxonomic uncertainty at the genus (e.g., new genus Mawia) and species levels hinders progress in studying their biology and evolutionary adaptations that make them nuisance species, as well as ability to understand and/or mitigate their ecological and economic impacts.

Methods

We collected nuclear (28S rDNA) and mitochondrial (cytochrome c oxidase I and 16S rDNA) sequence data from individuals of all four pelagiid genera, including 11 of 13 currently recognized species of Chrysaora. To examine species boundaries in the U.S. Atlantic sea nettle Chrysaora quinquecirrha, specimens were included from its entire range along the U.S. Atlantic and Gulf of Mexico coasts, with representatives also examined morphologically (macromorphology and cnidome).

Results

Phylogenetic analyses show that the genus Chrysaora is paraphyletic with respect to other pelagiid genera. In combined analyses, Mawia, sampled from the coast of Senegal, is most closely related to Sanderia malayensis, and Pelagia forms a close relationship to a clade of Pacific Chrysaora species (Chrysaora achlyos, Chrysaora colorata, Chrysaora fuscescens, and Chrysaora melanaster). Chrysaora quinquecirrha is polyphyletic, with one clade from the U.S. coastal Atlantic and another in U.S. Atlantic estuaries and Gulf of Mexico. These genetic differences are reflected in morphology, e.g., tentacle and lappet number, oral arm length, and nematocyst dimensions. Caribbean sea nettles (Jamaica and Panama) are genetically similar to the U.S. Atlantic estuaries and Gulf of Mexico clade of Chrysaora quinquecirrha.

Discussion

Our phylogenetic hypothesis for Pelagiidae contradicts current generic definitions, revealing major disagreements between DNA-based and morphology-based phylogenies. A paraphyletic Chrysaora raises systematic questions at the genus level for Pelagiidae; accepting the validity of the recently erected genus Mawia, as well as past genera, will require the creation of additional pelagiid genera. Historical review of the species-delineating genetic and morphological differences indicates that Chrysaora quinquecirrha Desor 1848 applies to the U.S. Coastal Atlantic Chrysaora species (U.S. Atlantic sea nettle), while the name C. chesapeakei Papenfuss 1936 applies to the U.S. Atlantic estuarine and Gulf of Mexico Chrysaora species (Atlantic bay nettle). We provide a detailed redescription, with designation of a neotype for Chrysaora chesapeakei, and clarify the description of Chrysaora quinquecirrha. Since Caribbean Chrysaora are genetically similar to Chrysaora chesapeakei, we provisionally term them Chrysaora c.f. chesapeakei. The presence of Mawia benovici off the coast of Western Africa provides a potential source region for jellyfish introduced into the Adriatic Sea in 2013.

Figure 3: Various morphs of Chrysaora quinquecirrha s.l.  (A) Offshore South Carolina (OSC); (B) Sample taken from offshore Georgia; (C) Engelhard, NC (PAM); (D) White Chesapeake Bay color morph (Broome’s Island, MD—Patuxent River); (E) Red-striped Chesapeake Bay color morph (Solomons, MD—Patuxent River).

 Note that medusae from (A) to (B) have five tentacles per octant, while (C)–(E) have three tentacles per octant. Medusae in (A, C) were included in this study’s phylogenetic analyses. (A: OSC1; C: PAM1). (A, B) represent individuals finally designated as Chrysaora quinquecirrha; (C–E) represent individuals finally designated as Chrysaora chesapeakei. Photo Credits: (A) Shannon Howard; (B) Greg McFall-NOAA; (E) Robert Condon.

Systematics

Chrysaora quinquecirrha Desor, 1848

Figs. 3A, 3B, 4–9; Figs. S1 and S2.

  

Diagnosis: Living medusae up to 40 cm (observed 59.0–176.0 mm) (Figs. 3A and 3B); tentacles typically 40 or more; 5.28 ± 0.45 (95% CI) tentacles/octant on average (Table 3; Fig. 8A); lappets rounded typically 48 or more; 6.26 ± 0.46 lappets/octant on average; rhopalar lappets slightly larger than tentacular lappets; can be differentiated from Chrysaora chesapeakei based on (1) smaller size of holotrichous Aisorhiza nematocysts: average: 20.25 [±0.38] × 11.27 [±0.37] μm (Table 3; Fig. 8C); (2) larger tentacle number (more than five per octant); and (3) typically shorter maximum oral arm length (average: 1.24 ± 0.27 time bell diameter).

Type locality: Nantucket Bay, Nantucket Island, Massachusetts, East Coast of USA.

Habitat: Medusae are found in open coastal waters on the U.S. Atlantic coast.

Distribution: Western North Atlantic, east coast of the USA south of Cape Cod in coastal Atlantic waters at least as far south as Georgia/Northern Florida.

Biological data: Although the name Chrysaora quinquecirrha applies to the U.S. coastal Atlantic species, almost no ecological studies have been done on the coastal species, apart from (Kraeuter & Setzler, 1975), which found the largest Chrysaora quinquecirrha individual was found in a coastal area about 90 km offshore in full seawater (salinity >30).

Notes: Since this species retains the scientific name Chrysaora quinquecirrha, we advocate it retaining the common name “U.S. Atlantic sea nettle”, since it is also a coastal and open ocean species.

Chrysaora chesapeakei Papenfuss, 1936

Figs. 3C–3E and 4–9; Figs. S1 and S2

Diagnosis: Living medusae up to 20 cm (observed 17.0–175.0 mm; average: 63.0 mm); tentacles typically number 24 or 3 per octant (average 3.07 ± 0.07); primary tentacle central and secondary tentacles lateral (2-1-2); rarely, additional tentacles arise lateral to secondary tentacles (3-2-1-2-3) and are typically undeveloped; marginal lappets rounded and typically 32 or 4 per octant (average 4.08 ± 0.06); rhopalar lappets are typically about the same size as tentacular lappets; can be differentiated from Chrysaora quinquecirrha based on (1) larger size of holotrichous A-isorhiza nematocysts: 26.21 [±0.50] × 19.74 [±0.55] μm; (2) smaller tentacle number (∼3 tentacles per octant); and (3) larger maximum oral arm length (average: 3.00 ± 0.39 times bell diameter).

Type locality: Gloucester Point (VA), Chesapeake Bay, east coast of USA.

Habitat: Medusae are found in estuarine waters on the U.S. Atlantic coast and estuarine and nearshore waters of the Gulf of Mexico.

Distribution: Western North Atlantic, east coast of the USA south of New England to the Gulf of Mexico, restricted to estuarine waters on the Atlantic coast, known to exist outside of estuaries in the Gulf of Mexico.

Keith M. Bayha​, Allen G. Collins and Patrick M. Gaffney. 2017. Multigene Phylogeny of the Scyphozoan Jellyfish Family Pelagiidae reveals that the Common U.S. Atlantic Sea Nettle Comprises Two Distinct Species (Chrysaora quinquecirrha and C. chesapeakei).  PeerJ. 5:e3863.   DOI: 10.7717/peerj.3863

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