Invasion History

First Non-native North American Tidal Record: 2017
First Non-native West Coast Tidal Record:
First Non-native East/Gulf Coast Tidal Record: 2017

General Invasion History:

The nudibranch Doris pseudoargus (Sea Lemon) is native to rocky coasts of the Northeast Atlantic from the north coast of the Mediterranean to the north coast of Norway. Maps suggests that its distribution is more continuous in northern waters, northern France to Norway, but spottier in the Bay of Biscay, the Iberian Peninsula, and the Mediterranean, suggesting a bias for cooler waters (WoRMS editorial Board; GBIF 2020). The first documented invasion of this nudibranch was detected in 2017 off Cape Ann, Massachusetts, by a diver. There is another undated photograph of this nudibranch from Yarmouth Nova Scotia. The current known range of D. pseudoargus on the East Coast is from Scussett beach, at the Cape Cod Canal to Yarmouth Nova Scotia, spanning the Gulf of Maine (Harris et al. 2022). This nudibranch is only known to feed on sponges, of two species, Halichondria panicea (Crumb-of Bread Sponge) and Isodictya palmata (Common Palmate Sponge or Mermaid's Glove), both of which are found in East Coast waters (Harris et al. 2022; WoRMS Editorial Board 2022).

North American Invasion History:

Invasion History on the East Coast:

In 2017–2018, scientists studying marine invasions (Larry Harris, Jim Carlton, Greg Ruiz), received emails from scuba divers, reporting a large, oval, and sometimes yellow nudibranch resembling a lemon (Paul Fofonoff, personal observations). The first documented invasion of this nudibranch was detected in 2017 off Cape Ann, Massachusetts, by a diver. There is another undated photograph of this nudibranch from Yarmouth Nova Scotia. These records, together with a morphological description, and genetic analysis of the specimens, identify it as Doris pseudoargus (Rapp 1827) (Harris et al. 2022).  The current known range of D. pseudoargus on the East Coast is from Scussett beach, at the mouth of Cape Cod Canal to Yarmouth Nova Scotia, spanning the Gulf of Maine (Harris et al. 2022). Genetic analysis suggests an origin in northern Europe. The adult animal feeds on sponges, which often occur in ship hull fouling, but the larvae are planktonic, and could be transported in ballast water. This nudibranch is only known to feed on sponges, of two species, Halichondria panicea  (Crumb-of Bread Sponge) and Isodictya palmata (Common Palmate Sponge or Mermaid's Glove), both of which are found in the Gulf of Maine. (Harris et al. 2022; WoRMS Editorial Board 2022).


Description

The nudibranch Doris pseudoargus commonly called 'Sea Lemon' for its oval shape, rough texture, typically yellowish color, and size, up to 120 mm. The mantle, which is covered with tubercles of various sizes, obscures the large, yellowish foot. There are two vestigial oral rhinophores, which are short and conical, and formed of up to 30 thin laminae. There are up to nine three-branched (tripinnate) pinnate gills, paler than the body, arranged in a circle around the anal papilla. Juveniles are often a uniform creamy yellow, but as they grow they can acquire blotches of pink, red, brown, white, and purple.  Adults can reach 120 mm long and are among the larger North Atlantic nudibranchs (Hayward and Ryland 1990; Rudman 20136; Ballesteros et al. 2022; British Conchological Society 2022).


Taxonomy

Taxonomic Tree

Kingdom:   Animalia
Phylum:   Mollusca
Class:   Gastropoda
Subclass:   Opisthobranchia
Order:   Nudibranchia
Family:   Dorididae
Genus:   Doris
Species:   pseudoargus

Synonyms

Archidoris pseudoargus (Rapp, 1827)
Archidoris tuberculata (Müller, 1778)
Doris areolata (Stuwitz, 1836)
Doris brittanica (G. Johnston, 1836)
Doris leuckarti (Delle Chiaje, 1841)
Doris mera (Alder and Hancock, 1844)
Doris flavipes (Leuckart, 1828)
Doris schembrii (Vérany, 1846)

Potentially Misidentified Species

Ecology

General:

The nudibranch Doris pseudoargus inhabits rocky shores from the intertidal to depths of 15–25 m. In northern Europe, this species is common in the intertidal, but in the Mediterranean, it is limited to subtidal waters, suggesting a preference for cooler temperatures (Ballasteros et al. 2022). Its range does not penetrate far into the Baltic, indicating a preference for marine salinities. Its food organisms, the sponges Halichondria panicea (Crumb-of Bread Sponge) and Isodictya palmata (Common Palmate Sponge or Mermaid's Glove), are marine in their distribution (Gosner 1978; MarLin 2022).

Food:

Sponges (Halichorndria pacicea; Isodictya palmata)

Consumers:

Fishes, crabs, shrimps

Competitors:

a starfish, Henricia sanguinolenta (Blood Star)

Trophic Status:

Carnivore

Habitats

General HabitatRockyNone
General HabitatBedrockNone
Salinity RangePolyhaline18-30 PSU
Salinity RangeEuhaline30-40 PSU
Tidal RangeSubtidalNone
Tidal RangeLow IntertidalNone
Vertical HabitatEpibenthicNone

Life History

The nudibranch Doris pseudoargus is a simultaneous hermaphrodite, producing both eggs and sperm, and exchanging both in copulation with another individual. In Britain (Isle of Man, Wales, England), juveniles appear in the intertidal in late summer, and widespread spawning starts in February through May. Eggs are laid in a conspicuous spiral ribbon which are abundant in May through June. Adults apparently died after spawning, and so have a semelparous life-cycle (Miller 1962l Thompson 1966). The eggs take 24–26 days to develop, at temperatures  of 7.7º to 12.3º C (Thompson 1966).  Larvae, reared on cultured flagellates (Pavlova lutherae; Rhodomonas sp.) .tooka mean of 37 days to metamorphose, stimulated by the presence of sponge tissue (Todd and Havenhand 1985).


Tolerances and Life History Parameters

General Impacts


Regional Distribution Map

Bioregion Region Name Year Invasion Status Population Status
NEA-II None 0 Native Established
NEA-III None 0 Native Established
NEA-V None 0 Native Established
AR-V None 0 Native Established
B-I None 0 Native Established
B-II None 0 Native Established
MED-II None 0 Native Established
MED-VII None 0 Native Established
NA-ET2 Bay of Fundy to Cape Cod 2017 Non-native Established
N170 Massachusetts Bay 2017 Non-native Established
N180 Cape Cod Bay 2019 Non-native Established
N125 _CDA_N125 (Piscataqua-Salmon Falls) 2021 Non-native Established
N135 _CDA_N135 (Piscataqua-Salmon Falls) 2019 Non-native Established
N165 _CDA_N165 (Charles) 2019 Non-native Established
B-I None 0 Native Established
MED-VI None 0 Native Established
NA-ET3 Cape Cod to Cape Hatteras 2017 Non-native Established

Occurrence Map

OCC_ID Author Year Date Locality Status Latitude Longitude

References

Ballesteros, E.; Madrenas, E.; Ponts, M. 2022 Doris pseudoargus in OPK Opissthobranquis. https://opistobranquis.info/en/guia/nudibranchia/doridina/doridoidei/doridoidea/doris-pseudoargus/



GBIF (Global Biodiversity Information Facility) 2017-2023 GBIF (Global Biodiversity Information Facility). https://www.gbif.org/



Harris, Larry G.; Shure, Alex; Kuzirian, Alan; Gosliner, Terrence M.; Donodoo, Samantha A. (2023) A European nudibranch new to the Gulf of Maine: Doris pseudoargus Rapp, 1827, Biological Invasions 25(2): 339-350
https://doi.org/10.1007/s10530-022-02917-0

Hayward, P.J.; Ryland, J. S. (1990) The Marine Fauna of the British Isles and North-West Europe, 1 Clarendon Press, Oxford. Pp. <missing location>

Miller, M. C. (1962) Annual Cycles of Some Manx Nudibranchs, with a Discussion of the Problem of Migration, Journal of Animal Ecology 31(3): 545-569

Picton, B.E. & Morrow, C.C. 2016 Marine Life Encyclopedia- Archidoris pseudoargus (Rapp, 1827). http://www.habitas.org.uk/marinelife/species.asp?item=W14030



Rudman, W. B. 1997-2016 Sea Slug Forum. http://www.seaslugforum.net/



The Conchological Society of Great Britain and Ireland 2022 The Conchological Society of Great Britain and Ireland- Doris pseudoargus. https://conchsoc.org/spAccount/Doris-pseudoargus-Rapp%2C-1827



Thompson, T. E. (1966) Studies on the reproduction of Archidoris pseudoargus r(Rapp) (Gastropoda Opisthobranchia), Philosophical Transactions of the Royal Society of London B 250(769): 343-374

Todd, Christopher; Havenhand, Jonanthan (19885) Preliminary observations on the embryonic and larval development of three dorid nudibranchs, Journal of Molluscan Studies 51(i): 97-99

WoRMS Editorial Board (2021). 2021 World Register of Marine Species. https://www.marinespecies.org/