Aeolidia papillosa (Linnaeus, 1761)

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Synonyms: Limax papillosus Linnaeus, 1761; Eolis papillosa (Linnaeus, 1761).

Current taxonomy: World Register of Marine Species www.marinespecies.org/aphia.php?p=taxdetails&id=138709

Vernacular names: Common grey sea slug; Shag-rug aeolis; Plumed sea slug (English); Môrwlithen lwyd (Welsh); Stor trådsnegl (Danish); Vlokkige zeenaaktslak; Grote vlokslak (Dutch); Eolidien à papilles (French); Breitwartige Fadenschnecke (German).

GLOSSARY BELOW

Preface
In 2016, Kienberger et al. segregated with molecular sequencing what had previously been generally accepted in Europe as A. papillosa into Aeolidia papillosa sensu stricto (Linnaeus, 1761) and Aeolidia filomenae Kienberger et al., 2016. Descriptions published before 2016 combine features of the two species and often, such as in Alder & Hancock (1845-1855) 31 Aeolidia papillosa and Thompson & Brown (1984), illustrated the descriptions with images of probable A. filomenae. This account draws on the description in Kienberger et al. (2016).

Description
The large, broad and relatively low body sometimes grows to a maximum length of 120 mm. The ground colour of the notum varies from light white–beige, through mustard brownish, to reddish brown or dark brown with, often dense, darker flecks spread over it 01 Aeolidia papillosa & 02 Aeolidia papillosa .
Kienberger et al. (2016) state, “A white Y–shaped or triangular mark extending from the oral tentacles to the pericardial area between the rhinophores may be present.” (See appendix below for discussion of this). Dorsal surfaces are usually concealed by dense cerata apart from the head and a bare zone extending back from the rhinophores 01 Aeolidia papillosa & 03 Aeolidia papillosa .
The cleioproctic anus is located between the ninth and tenth row of the right side.
( 04 Aeolidia papillosa & 01 Aeolidia papillosa & Kienberger et al. 2016). The genital aperture is situated on the right side between the sixth and eighth anterior rows of cerata, which usually conceal it.
The numerous, crowded cerata are arranged in up to 25 close, difficult to discern, rows of eight to twelve cerata each, on each side of the body. They decrease in size towards the posterior of the body, and the anterior cerata positioned by the rhinophores are small 05 Aeolidia papillosa . The cerata are often elongate and thin, with a uniform diameter for most of their length 06 Aeolidia papillosa . Their dimensions can be altered but they are never flattened. They are translucent but usually covered with dark pigment marks and, sometimes, some white marks 05 Aeolidia papillosa . Where the pigment is less intense, usually at the basal half of the posterior, the digestive gland may be visible 07 Aeolidia papillosa , and the dull whitish cnidosac is visible when not obscured by white apical pigment 08 Aeolidia papillosa . The general colour of individuals depends largely on the colour of the ceratal pigment, which is usually darker than the notum 03 Aeolidia papillosa but the peripheral cerata are sometimes pale 09 Aeolidia papillosa .
The smooth, conical rhinophores are similar in colour to or a little darker than the body. The truncated tip usually has a small, terminal, translucent, pale spot 10 Aeolidia papillosa & 11 Aeolidia papillosa . The internal eye at the base of each rhinophore is rarely visible through the body, but may be discerned on some pale American specimens 12 Aeolidia papillosa .
The head has translucent, whitish, oral tentacles with variable amounts of dark and/or white freckling 09 Aeolidia papillosa & 10 Aeolidia papillosa but the white does not form a well defined line. They are longer than the rhinophores and placed apart on the anterior edge of the head at a distance, when it is spread, equal to about three times the thickness of a tentacle base (IFS, pers. obs. 10 Aeolidia papillosa ).
The broad foot has small triangular propodial tentacles at the anterior 10 Aeolidia papillosa .

Key identification features

Features vary and may sometimes overlap with similar species. Identifications should be made on the basis of more than a single feature. American specimens differ in some respects.
Aeolidia papillosa
Features as in Kienberger et al. (2016). [IFS pers. obs. in square brackets.]
1) Maximum length 120 mm.
2) Body colour extremely variable: from light white-beige, through mustard brownish, to reddish brown or dark brown.
3) “A white Y–shaped or triangular mark extending from the oral tentacles to the pericardial area between the rhinophores may be present”. [Pale marks on the head are frequent on A. papillosa in America 13 Aeolidia papillosa , where A. filomenae is absent, but seem to be rare in Europe. See appendix below.]
4) Elongate thin cerata, not flattened, usually with uniform diameter for most of length 06 Aeolidia papillosa . In difficult to count crowded rows.
5) Cerata darker than body.
6) [Dull whitish cnidosac visible if not obscured by white apical pigment 08 Aeolidia papillosa .]
7) Rhinophores dark, [usually with a small, terminal, translucent, pale spot on the truncated tip 10 Aeolidia papillosa & 11 Aeolidia papillosa ].
8) Internal eyes at base of rhinophores, visible rarely if ever in Europe. [Sometimes visible in America 12 Aeolidia papillosa ].
9) [Distance between oral tentacles at base about three times thickness of tentacle base, 10 Aeolidia papillosa ].

Similar species
Aeolidia filomenae Kienberger, Carmona, Pola, Padula, Gosliner & Cervera, 2016.
Features as in Kienberger et al. (2016). [IFS pers. obs. in square brackets.]
1) Longest specimen described in Kienberger et al. (2016) was 45 mm; maximum possible length not stated; at least 70 mm 16 Aeolidia papillosa.
2) Body white 14 Aeolidia papillosa, light beige, pink 16 Aeolidia papillosa or greenish with white or brown flecks [which may concentrate into dense brown on the head, rhinophores and pericardial area 18 Aeolidia papillosa].
3) White ‘Y’ mark on oral tentacles and head, with stem passing back between the rhinophores, is often present. Varies from very evident and intense opaque white 15 Aeolidia papillosa to unobtrusive beige or light brown, and may be partly covered by white or beige flecks 16 Aeolidia papillosa . [See appendix.]
4) Cerata, [often in neat, easily counted rows], are typically flattened, broader at their base, and often slightly hooked inwards 17 Aeolidia papillosa . This is the primary feature for identification (L. Carmona, pers. comm. 7 October 2022) [They may inflate a little to give a thicker cross section.]
5) Cerata usually [have much less surface pigment than on A. papillosa and] are usually lighter than the rest of the body 15 Aeolidia papillosa. [But some have dark cerata 18 Aeolidia papillosa.]
6) Apices of cerata are white, [often revealing large white cnidosacs 15 Aeolidia papillosa ].
7) Blunt, conical, smooth rhinophores are translucent whitish with opaque white or yellowish-white freckles which often concentrate to colour the distal quarter 19 Aeolidia papillosa . [Most also have brown spots of varying extent and intensity on the basal three-quarters 18 Aeolidia papillosa]
8) Internal eyes sometimes faintly visible at base of rhinophores in lighter specimens 19 Aeolidia papillosa.
9) [Distance between oral tentacles at base about three times thickness of tentacle base. 15 Aeolidia papillosa ]
Pre 2016 authors such as Alder & Hancock (1845-1855) 20 Aeolidia papillosa and Thompson & Brown (1984), illustrated their descriptions of A. papillosa with images of probable A. filomenae.

Aeolidiella alderi (Cocks, 1852) 21 Aeolidia papillosa , A. glauca (Alder & Hancock, 1845) 22 Aeolidia papillosa and A. sanguinea (Norman, 1877) 23 Aeolidia papillosa
1) Extreme maximum length 46 mm (A. sanguinea, others shorter).
2) Body translucent white or pale shade of other colour. Any opaque marks are scattered, small and not dark.
3) No white ‘Y’ or triangular mark on head.
4) Cerata not flattened, with uniform diameter for most of length
5) Cerata have more saturated colour than body.
6) Apices of cerata are white or pale.
7) Rhinophores translucent, no dark pigment marks.
8) Internal eyes visible at base of rhinophores
9) Distance between oral tentacles at base about same as thickness of single tentacle base (IFS pers. obs.).

Habits and ecology
Information in this section is mainly from Thompson & Brown (1984) who did not differentiate A. papillosa from A. filomenae, so it may apply to either one or both.
It lives sublittorally and on lower shores where there is some hard substrate, including estuaries down to 20‰ salinity and on muddy sand with isolated stones coated with sediment.
A. papillosa attacks and eats sea anemones, including Actinia equina and Metridium senile 02 Aeolidia papillosa . It is immune to the toxic nematocysts in their tentacles and exuded acontia 24 Aeolidia papillosa , and it ingests them and stores them in cnidosacs at the tips of its cerata for release when it is attacked. The effect is powerful enough in a dog’s mouth to make it drop the slug (IFS pers. obs.) but it does not prevent haddock, Gadus aeglefinus, from consuming it (Thompson & Brown, 1984). Other enemies include copepod parasites and Nucella lapillus which occasionally eats its spawn. When alarmed it can raise its cerata and roll into a ball resembling a sea anemone 25 Aeolidia papillosa . Faeces are irregular masses 01 Aeolidia papillosa & 04 Aeolidia papillosa .
A. papillosa is a simultaneous hermaphrodite. Its convoluted white, pink or purple cord of spawn, somewhat resembling a coiled spring, is attached spirally to hard substrate from January to August in Britain. Initially, the coil forms a compact disc 26 Aeolidia papillosa but, as it ages, it absorbs water and expands into a looser coil 27 Aeolidia papillosa . When several individuals spawn close together, a confused mass may result 28 Aeolidia papillosa .
Veliger larvae hatch from the spawn and live in the plankton before metamorphosis. Small juveniles are not often found on shore; they may spend their early life sublittorally (Thompson & Brown, 1984).

Distribution and status
A. papillosa sensu stricto is an amphiboreal species with maximum uncorrected p-distance of 1.6% between individuals (Carmona et al., 2013), which is common along the Atlantic coasts of Europe and North America 29 Aeolidia papillosa and from Washington State to Alaska in the in the north-eastern Pacific 30 Aeolidia papillosa . Kienberger et al. (2016) verified with molecular sequencing specimens from Sweden, Netherlands, Maine, Massachusetts, Alaska and Washington State. GBIF map www.gbif.org/species/2291938 . UK map NBN species.nbnatlas.org/species/NHMSYS0021312941

Acknowledgements
For use of images I gratefully thank Nils Aukan, Emil Burman, Roy Dahl, Jeff Goddard, Heine Jensen, Guillaume Lemonnier, Sutherland MacIver, Erin McKittrick, Malcolm Storey and Alex Wilson. For providing specimens to photograph I thank Simon Taylor. For information and advice I thank J. Lucas Cervera, Leila Carmona and Marta Pola, but any errors or omissions are my (IFS) responsibility.

Appendix
Kienberger et al. (2016) stated of A. papillosa, “A white Y–shaped or triangular mark extending from the oral tentacles to the pericardial area between the rhinophores may be present”. But the common practice of European recorders on iNaturalist and Facebook is to record all specimens with a white Y as A. filomenae.
As substantiation for their statement, Kienberger et al. refer to their Fig. 5B which shows a sequenced A. papillosa from the White Sea with a whitish mark on the head resembling a wine glass with the stem passing back between the rhinophores. Apart from it, the only European Aeolidia image with a wine glass mark found by IFS is one from the Mersey Estuary 31 Aeolidia papillosa . Whether the wine glass mark should be regarded as a form of white Y is an open question. Sometimes it is centrally faded with small lateral branches to resemble a Y, but the branches bend to meet at an obtuse angle of nearly 180° instead of the acute junction of the arms of a Y 13 Aeolidia papillosa & 29 Aeolidia papillosa .
Judging from the many images posted as A. papillosa on iNaturalist, and ‘Fig. 5F’ from Alaska in Kienberger et al. (2016), the wine glass mark is frequent on it in North America both in the Atlantic and Pacific. In the Pacific, it is often misidentified as A. loui Kienberger, Carmona, Pola, Padula, Gosliner & Cervera, 2016, especially in Washington and further north where there is no molecular evidence for A. loui ( L. Carmona, pers. comm. 7 October 2022).
Kienberger et al. differentiated A. papillosa and A. filomenae on the basis of molecular sequencing, and they described morphological features observed on the specimens studied which correlated with each species. It is possible that subsequent experience and photography of larger numbers have revealed more morphological variations but they need molecular sequencing for substantiation.
In June 2016, J. Lucas Cervera, co author with Kienberger, posted on Facebook Group N. E. Atlantic Nudibranchs to say that an in depth, focused study of UK and Irish specimens is still required to understand much better the diversity of this complex in that area, but that without material it is not possible. He would like collections to be made from different localities and then sent to him together in one or two packs, as if he receives the material scattered over time it is difficult to arrange students and material for a study focused on the issue. If you wish to help, please first email leila.carmona@uca.es for detail of how to preserve and send specimens.
Without further linked morphological and molecular study, morphological identifications of British and Irish Aeolidia species including those illustrated in this account are uncertain. Some specimens have some morphological features of each species 32 Aeolidia papillosa and cannot be confidently identified without molecular sequencing; they are best recorded as Aeolidia sp.

References and links
Alder, J. & Hancock, A. 1845-1855. A monograph of the British nudibranchiate mollusca. London, Ray Society. Family 3 Plate 9 [A. papillosa sensu lato includes A. filomenae ] www.biodiversitylibrary.org/item/131598#page/314/mode/1up

Carmona, L., Pola, M., Gosliner, T. M. and Cervera, J. L. (2013) A tale that morphology fails to tell: a molecular phylogeny of Aeolidiidae (Aeolidida, Nudibranchia, Gastropoda). PLoS ONE 8(5): e63000. journals.plos.org/plosone/article?id=10.1371/journal.pone…

iNaturalist www.inaturalist.org/observations

Kienberger, K., Carmona, L., Pola, M., Padula, V., Gosliner, T.M. and Cervera, J.L. 2016. Aeolidia papillosa (Linnaeus, 1761) (Mollusca: Heterobranchia: Nudibranchia), single species or a cryptic species complex? A morphological and molecular study. Zool. J. Linn. Soc., 177: 481–506. www.researchgate.net/publication/303953645_Aeolidia_papil…

Thompson, T.E. & Brown, G.H. 1984. Biology of opisthobranch molluscs 2. London, Ray Society.

Glossary
acontia = thread-like tissue containing numerous stinging nematocysts which are released by some sea anemones.
amphiboreal = living in the cold temperate boreal zone to south of Arctic on more than one side of the Atlantic and/or Pacific.

cerata = (sing. ceras, adj. ceratal) lobes on notum of some nudibranchs.
cleioproctic = (of anus) located on the notum to the right of the midline.
Cnidaria = hydroids, jellyfish, sea anemones etc. which possess cnidocytes.
cnidocytes = explosive stinging cells of Cnidaria. en.wikipedia.org/wiki/Cnidocyte
cnidosac = storage capsule at tips of cerata of Aeolidiidae for ingested cnidocytes.
digestive gland = large organ in gastropods which acts like the liver and pancreas in mammals to absorb food.

distal = away from centre of body or from point of attachment.
hermaphrodite, simultaneous = individual acts as both male and female at the same time with similar partner.

molecular sequencing = technique for determining the sequence of the bases adenine, guanine, cytosine, and thymine (A, G, C and T) in a DNA molecule.

notum = (of sea slugs) the dorsal surface of the body; the back.
partim = partly, in part, a part, some of, some.
pericardium = sac containing heart, sometimes visible as a raised pericardial mound behind rhinophores in sea slugs.
pleuroproctic = (of anus) located on side of body below the notal edge or cerata.
propodial tentacles = tentacular, lateral extensions on anterior of the foot.
rhinophore = chemo-receptor tentacle; many sea slugs have a pair on top of the head.
sensu lato = (abbreviation s.l.) in the wide sense, possibly an aggregate of more than one species.

sensu stricto = (abbreviation s.s.) in the strict sense, excluding species that have been aggregated or confused with it.

veliger = shelled larva which moves by action of cilia on a velum (bilobed flap). Stage may be passed in plankton or within liquid-filled egg-capsule.