CERATA

Part 2 – The Multiple Functions

In Part 1, an overview of cerata was given together with some examples of what are, and what are not, considered to be cerata and which sea slug taxa possess them. A list of their diverse roles was included. Here in Part 2 those roles (excluding defence – Part 3) will be discussed. But first, a review of which sea slugs have cerata.

A quick run down on which taxa of sea slugs bear cerata.

Gaseous exchange (Respiration)
The nudibranchs of the Aeolidina do not have that true naked gill from which the order Nudibranchia derives its name. There is no rosette or arc or line of gills on their dorsum to facilitate gaseous exchange. Instead, it is their cerata that act as secondary gills by providing an immense thin-walled surface area interfacing with their watery environment externally and the circulating haemolymph fluid internally. By holding their shape, jutting up into the water column, the cerata are able to function with some efficiency. They are supported by the surrounding water and also by the internal hydrostatic pressure of the haemolymph that also serves to maintain their shape. The movement of water causes the cerata to also move thus constantly refreshing the water in contact with their external surface. All of the Aeolidina use cerata as secondary gills for respiration.

This composite image, and the two below, serve to demonstrate the variety in Aeolidina cladobranch cerata shape, size, adornment and deportment. Regardless of these differences they are all employed as secondary gills.
Clockwise from top left:
Crowded dorsum: Baeolidia moebii has a profusion of cerata crowded down the length of the dorsum.
Sparse: This undescribed Eubranchus sp. has a sparse arrangement of cerata in comparison, alternating on each side down the length of the dorsum.
Held erect: Samla bilas carrying its cerata in an erect manner.
Held flat: Cerberilla annulata holds its cerata flat against the notum, a characteristic probably expected in a species that burrows through the substrate in search of its prey.

More Aeolidina cladobranch cerata characteristics.
Clockwise from top left:
Inflated: Like most of the Eubranchus, Eubranchus inabai possesses inflated or swollen cerata.
Lean: The very lean or narrow cerata of Sakuraeolis nungunoides.
Curled: The curled cerata presentation of Phyllodesmium opalescence is frequently observed in species of Phyllodesmium and is even more pronounced in those that host zooxanthellae thereby increasing exposure to ambient sunlight.
Straight: Tenellia sibogae has cerata that are sturdy and straight.
The examples chosen are done so to highlight a particular feature however we should remember that no one adjective properly describes a type of cerata – for example here the cerata of Sakuraeolis nungunoides could be described as long, lean, erect, straight, smooth and crowded upon the dorsum.

Another composite of cerata variation in the Aeolidina cladobranchs.
Clockwise from top left:
Translucent: The digestive diverticulum is readily visible in the cerata of this undescribed Flabellina sp. 04.
Pigmented: Four pigment colours are displayed in bands on the cerata of this undescribed Tenellia sp. 44.
Tuberculate: The cerata of Phyllodesmium crypticum bears tubercles along their edges.
Smooth: Flabellina exoptata has smooth cerata.

In the Dendronotina, the Tritonia, Tritoniopsis, Marionia and Dendronotus species, for example, the cerata are many-branched, often finely so, whereas in Bornellidae they act as protective structures and supports for tufts of gills emanating medially at their bases. Similarly, some of the Dotidae have small gills (pseudobranchs) attached at the base of their cerata. Tethydidae e.g. Melibe, bear fine dendritic gills on the medial surface of their large paddle-like cerata. Lomanotidae on the other hand have much reduced cerata presenting as small lobed appendages on an often undulating notal ridge.

Examples of the cerata or secondary gills of non-aeolidina cladobranchs.
Upper row: Dendronotina – The Bornellidae species, Bornella anguilla, has feathery secondary gills lying inside the protective lateral appendages.
Lower row: Dendronotina – The Tritoniidae species – left – an undescribed Marionia sp. and right – a close-up of the finely branched terminals of the cerata of Marionia pustulosa.

More examples of the cerata or secondary gills of non-aeolidina cladobranchs.
Upper row: Dendronotina – The Tritoniidae species – Tritoniopsis elegans and a close-up of its lace-like cerata.
Lower row: Dendronotina – The Tethydidae species – Melibe viridis and a close-up of its large paddle-like cerata.

In some species of Lomanotus I have observed a number of singular, thin tendrils, bright red in colour, emanating from some of these small lobes, that appear capable of extension and withdrawal. These may possibly be respiratory in function, however I have found no reference to them in the literature thus far. (Personal observation/opinion)

Another composite of cerata variation of non-aeolidina cladobranchs.
Upper row: Arminina – left – the Madrellidae species Madrella ferruginosa, and right – the Janolidae species Janolus flavoanulatus. (Note how the cerata run right around the anterior edge, in front of the rhinophores.)
Lower row: Dendronotina – The Lomanotidae species – left – Lomanotus vermiformis with many simple, small, much-reduced cerata, and right – Lomanotus sp. 04 with the thin red retractable tendrils, arrowed, that possibly have a respiratory function.

Examples of ceratal respiration in the Arminina include species in the genera Janolus, Caldukia, Madrella and Dirona.

The cerata of those of the Sacoglossa that possess them, whether leaf-shaped or fusiform, function for the same purpose.

Some examples of the cerata of the Sacoglossa that are employed as secondary gills.
Clockwise from top left:
The translucent, puffy, cushion-like cerata of Cyerce elegans.
The thin, leaf-like cerata of Cyerce nigra.
This undescribed Limapontiidae slug – Stiliger sp. has long fusiform cerata.
An undescribed species of Hermaeidae – Hermaea sp. 02 has large translucent fusiform cerata, some in the process of regeneration.

Digestion
The major site for digestion, that is, the breakdown, via both extracellular and intracellular, and the subsequent uptake of ingested food at the molecular level, is the appropriately named digestive gland. In most sea slugs this is the largest gland of the digestive system and consists of many “blind” tubules connected to the stomach. In most sea slugs it is a large mass located in the body proper. However, in the aeolids, and some of their other cladobranch relatives, and some of the ceras-bearing sacoglossans, the digestive gland is not located in the main body but instead each ceras receives a branch of the digestive gland as a tube penetrating for almost the entire length (often termed digestive diverticulum). It may be straight (most species), undulating, branched, thin or thick. Often, if it can be observed through the wall of the ceras, it takes on the colouration of the sea slug’s recently ingested prey. In brief and to generalise, food is moved from the stomach into the lumen of the digestive gland penetrating each ceras. The digestive cells lining the lumen secrete the necessary compounds for extracellular digestion and take up the resulting substances in vesicles for intracellular digestion.

Types of digestive diverticula found in sea slugs bearing translucent cerata.
Clockwise from top left:
Flabellina sp. 04 has a straight tubes.
Phyllodesmium undulatum has undulating tubes as indicated in its name.
Phyllodesmium koehleri has highly branched tubes that penetrate the ceratal tubercles.
Phyllodesmium poindimiei has finely branched tubes.

More variation in digestive diverticula found in sea slugs bearing translucent cerata.
Clockwise from top left:
Eubranchus sp. has quite thin tubes.
Eubranchus sp. has relatively thick tubes.
Hermaea sp. 02 a sacoglossan, has cruciform tubes
Tenellia sp. 23 has tubes that fill the cerata volume almost entirely.

Here are two examples of ceratal colour differences within the same species as a result of the different colour of food sources:
Upper row; Favorinus japonicus – white and pink.
Lower row: Favorinus tsuruganus – yellow and orange.

The cerata of many, but not all, Aeolidina species have a terminal sac, the cnidosac, able to open to the exterior at the very tip of each ceras, that contains undischarged nematocysts (stinging cells), obtained through consumption of their cnidarian prey, and used for their own defensive purposes (more in Part 3).

Farming of zooxanthellae
Some species, for example some of those aeolids that prey on soft corals or anemones, will take advantage of the large ceratal surface area and the exposure they can provide to sunlight for “farming” of zooxanthellae (Symbiodinium) that they have sequestered from that prey. These aeolids have come to be termed “solar-powered slugs” because of the considerable nutritional benefits derived through this symbiotic association.

These sea slugs include species of Phyllodesmium, Pteraeolidia and Spurilla. The photosynthesis process by the hosted zooxanthellae produces waste products such as sugars and amino acids, even oxygen, that are of benefit to the nudibranch host. In return the zooxanthellae receive a protective habitat plus the waste carbon dioxide and nitrogen compounds, among others, produced by the nudibranch, that they require. Some of these aeolid species may very often be found off their prey, it being conjectured that they do not need to feed as often as those aeolids that don’t host zooxanthellae. In fact these nudibranchs have been known to survive for months on the nutritional products produced by the thriving, dividing and photosynthesising  zooxanthellae.

The way zooxanthellae are exploited fall into two major groups. On the one hand there are those species that have a rapid turn over of the zooxanthellae and on the other where long term retention of zooxanthellae illustrates a well-developed, nurturing, symbiotic relationship. These relationships are reflected in the anatomical appearance of the cerata. The more highly developed of these “solar-powered” nudibranchs are well adapted for this “farming” of zooxanthellae by having modified cerata, in some cases flattened and broadened, and with a highly branched digestive gland within. In some instances they have developed larger cerata, and correspondingly, a smaller number of cerata to reduce shading from neighbours. Pteraeolidia on the other hand continues to add row after row of cerata growing into quite a long animal over time. These morphological adaptations by the nudibranch, bring improved housing and distribution and therefore greater solar exposure of zooxanthellae, thereby increasing efficiency. In some instances this has led to still further structural adaptations that in some species creates uncanny mimicry of their host (see Defence: Mimicry/crypsis – Part 3).

In some species the zooxanthellae are not only housed in the cerata but small gut tubules are seen ramified into the skin of the dorsum, the foot and even the rhinophores, oral tentacles and the head, almost any tissue exposed to direct sunlight, e.g. Phyllodesmium macphersonae, Phyllodesmium magnum and also Pteraeolidia.

Hosting of zooxanthellae is believed to have evolved many times across the Nudibranchia order.

Zooxanthellae hosting in nudibranchs.
Clockwise from top left:
Phyllodesmium magnum has modified cerata to improve the efficiency of the photosynthesis of the hosted zooxanthellae. The zooxanthellae are in the cells of the digestive gland lining the duct that is very finely branched. Notice how they are also on the dorsum of the body, the head and even into the rhinophores and oral tentacles.
Phyllodesmium macphersonae exhibits similar organisation, but as small brown spots.
Phyllodesmium longicirrum has larger, broader cerata and fewer to avoid shading. The zooxanthellae are hosted in clusters – the brown patches on the anterior surface (the outer curve) of the cerata.
A feeding scar on the soft coral Sarcophyton sp. produced by Phyllodesmium longicirrum.

Kleptoplasty and chloroplast maintenance
Some species of the Sacoglossa sea slugs (the sap-suckers) do not immediately digest all the contents they have sucked out of their algal prey. These species have developed branches of their digestive tract that ramify into the body wall, as well as the parapodia and cerata (depending on which they possess) in which they maintain the algal plastids, including chloroplasts, in a functioning state, to reap the benefits of their solar powered production. The removal, uptake and maintenance of the plastids for their own use has been termed kleptoplasty (theft of plastids). The length of time the plastids, at this point called kleptoplasts, are viable depends upon both the sea slug species and the algal species. Some sacoglossans are known to be long-term retentionists and others short-term retentionists. Whilst functional kleptoplasty (a quite complex process with many steps) is well recorded in the parapodia-bearing sacoglossans (some authors propose that it is limited to those species) it is not as well known in the cerata-bearing members. However the presence over several weeks of functional kleptoplasts in some species of the cerata-bearing Limapontiidae (e.g. Costasiella and Stiliger) and even some Caliphyllidae (e.g. Caliphylla) has been documented. It is also suggested that the kleptoplasts not only operate as a producer of nutrients but that they additionally, store manufactured products (polysaccharides) until drawn upon by a sea slug in want. The exact modus operandi by which the kleptoplasts survive, are controlled and function in the digestive tract of certain sea slugs is still in contention, but there is no doubt that these too are “solar-powered slugs”.

Kleptoplasty in Limapontiidae sacoglossans with cerata.
Many species exhibit kleptoplasty but only a few have been recorded to delay their digestion of them and in doing so keep the plastids functioning for a variable length of time.
Clockwise from top left:
Placida fralila has finely branched digestive diverticula in its cerata.
This undescribed species, Costasiella sp., has plastids in patches.
Costasiella formicaria with highly modified cerata – flattened and broadened to maximise sunlight exposure.
Another Costasiella sp. with crowded fusiform cerata on the dorsum.

Some unusual cerata adaptations
Because they lack a true heart and pericardium the haemolymph circulation within the Alderia species (Limapontiidae) of Sacoglossa is achieved by rhythmic pulsations of its cerata on alternating sides of the body, performing therefore as secondary hearts.

Species of the aeolid genus Pruvotfolia have some highly modified cerata situated around the genital orifice that play an active role related to positioning during copulation.

Undescribed species of Pruvotfolia. The gonopore is surrounded by modified cerata that play a role in copulation.

The roles cerata play in the defence of sea slugs are covered in Part 3.

(Note: where an sp. number is used in this NudiNote it refers to a species shown on this site.)

David A. Mullins – January 2022

References:
– Rudman, W. B., (1981). The anatomy and biology of alcyonarian feeding aeolid opisthobranch molluscs and their development of symbiosis with zooxanthellae. Zoological Journal of the Linnean Society, 72: 219-262.

– Clark, K. B., Jensen, K. R. & Starts, H. M., (1990). Survey for functional kleptoplasty among West Atlantic Ascoglossa (Sacoglossa, Mollusca: Opisthobranchia). The Veliger, 33: 339-345.

– Rudman, W. B., (1991). Further studies on the taxonomy and biology of the octocoral-feeding genus Phyllodesmium Ehrenberg, 1831 (Nudibranchia: Aeolidoidea). Journal of Molluscan Studies, 57(2): 167-203.

– Rudman, W. B., Willan, R. C. & Burn, R., (1998). Opisthobranchia. Pp. 915-1035 in Beesley, P. L., Ross, G. J. B.and Wells, A. (eds.), Mollusca: The Southern Synthesis. Fauna of Australia. 5, Part B. CSIRO Publishing, Melbourne.

– Rudman, W. B., (1998, October 11). Solar-powered sea slugs. [In] Sea Slug Forum. Australian Museum, Sydney. Available from http://www.seaslugforum.net/factsheet/solarpow and associated messages.

– Rudman, W. B., (1999, July 1). Cerata (ceras) in aeolids. [In] Sea Slug Forum. Australian Museum, Sydney. Available from http://www.seaslugforum.net/factsheet/cera

– Marin, A. & Ros, J., (2004). Chemical defenses in Sacoglossan Opisthobranchs: Taxonomic trends and evolutive implications. Scientia Marina 68(supply. 1): 227-241

– Rudman, W. B., (2005, March 22). Alderia modesta (Loven, 1844). [In] Sea Slug Forum. Australian Museum, Sydney. Available from http://www.seaslugforum.net/find/aldemode

– Rauch, C., et al, (2015). Why It Is Time to Look Beyond Algal Genes in Photosynthetic Slugs. Genome Biology and Evolution 7(9): 2602-2607.

– Laetz, E. M. J., Moris, V. C., Moritz, L., Haubrich, A. N. & Wagele, H., (2017). Photosynthate accumulation in solar- powered sea slugs – starving slugs survive due to accumulated starch reserves. Frontiers in Zoology 14:4.

– Lobo-da-Cunha, A., (2019). Structure and function of the digestive system in molluscs. Cell and Tissue Research 377:475–503.

– Ponder, W. F. & Lindberg, D. R., with illustrations by Ponder, J. M., (2020). Biology and Evolution of the Mollusca, Volume One & Two. CRC Press, Taylor & Francis Group.