Tag Archives: sea slugs

Door #19: Photosynthetic vs solar-powered sea slugs

I think we can all agree that sea slugs are amazing creatures. Some species contain toxins that are useful for cancer research and others are photosynthetic! There are a few species of sea slugs that have the ability to photosynthesize. But beware; the ability for them to do the thing that plants and algae are good at (photosynthesis), doesn’t always mean they are solar-powered. And I will explain you in the next few lines what I mean with that.

There are two families of sea slugs known to have a few species within them that can photosynthesize; it’s within the family of Facelinidae and the family of Sacoglossa.

Within the family of Facelinidae we have the genus Phyllodesmium; and all species in this genus are considered solar-powered, meaning that they get a part of their daily energy intake via photosynthesis. At the moment the theory goes that they are able to do so as they contain photosynthetic zooxanthella stolen from their feeding source (soft corals), and they continue to ‘farm’ these zooxanthellae in their own bodies. The species Phyllodesmium longicirrum masters this trade and is best known as the solar-powered Phyllodesmium

Solar-powered Phyllodesmium longicirrum by Jason R. Marks

The other family does things quite differently but nevertheless as impressive; those are the Sacoglossa.

A few representatives of the photosynthetic sea slugs within the Sacoglossa

Unlike Phyllodesmium, they don’t farm zooxanthella but they steal the photosynthetic cell organelles (chloroplasts or plastids) from the algae they feed on; also known as kleptoplasty (Kleptes (κλέπτης) Greek for thief). Approximately 140 years ago these sea slugs were first described by de Negri and de Negri, who discovered that these sea slugs were green colored due to foreign ‘bodies’ that were reminiscent to those known from plants. It took at least another 100 years before the ‘granule bodies’ were identified to be chloroplasts from the algae the slugs feed on. Sacoglossa are also known as sap-sucking sea slugs because of the way they eat their algae; at first, the sea slugs pinch a whole in the algae wall with their special teeth, called the radula. Then they suck out the cytosolic content of the algae (hence the name sap sucking sea slugs). Finally, the cytosol content is being digested in the digestive tract that perforates the entire body and within some species the chloroplasts are being sequestered and continue to photosynthesize in the animal’s digestive cells

Sap-sucking slug sequestering chloroplasts from the algae it feeds on (figure from Rauch et al. 2015)

Although the sea slugs are famous for their ability of stealing chloroplasts, they only represent a minority within the Sacoglossa. In fact, only 6 out of 300 described species, can keep the chloroplasts fully functional for long term, or long-term retention species; that is the chloroplasts are photosynthetic active for longer than 21 days after sequestration. The gross majority are either short term retention species (with functional chloroplasts up to 14 days or more) or cannot retain the chloroplasts at all (called non-retention species). This means that the chloroplasts are immediately being digested like the rest of the algae content.

So why are Sacoglossa photosynthetic but not solar powered like Phyllodesmium? Well this is because numerous studies observed how the sea slugs died as soon as they were being starved (meaning they couldn’t eat their algae food anymore) even though they had photosynthetic active chloroplasts in their cells. Besides, based on CO2 fixating measurements, it turned out that 99% of the sea slug has to live from normal ingested food, like all other animals do. This could very well explain why only 6 out of the 300 described species are able to sequester chloroplasts long-term, and apparently for reasons other than carbon fixation!

The take home message is that this case of photosynthetic and solar-powered sea slugs is a great example of how good science is about resisting the pull of easy conclusions. When something seems right at first, it should still be testified!

Furthermore
Interested in photosynthetic sea slugs? You can read more in the following papers that are also used as source for this blog:

  1. A sea slug’s guide to plastid symbiosis (2015) J De Vries, C Rauch, G Christa, SB Gould, Acta Societatis Botanicorum Poloniae 83 (4)
  2. Why it is time to look beyond algal genes in photosynthetic slugs (2015) C Rauch, J Vries, S Rommel, LE Rose, C Woehle, G Christa, EM Laetz (…), Genome biology and evolution 7 (9), 2602-2607
  3. On being the right size as an animal with plastids (2017) C Rauch, P Jahns, AGM Tielens, SB Gould, WF Martin, Frontiers in plant science 8, 1402
  4. Mitochondrial Genome Assemblies of Elysia timidaand Elysia cornigera and the Response of Mitochondrion-Associated Metabolism during Starvation (2017) C Rauch, G Christa, J de Vries, C Woehle, SB Gould, Genome biology and evolution 9 (7), 1873-1879
  5. The ability to incorporate functional plastids by the sea slug Elysia viridisis governed by its food source (2018) C Rauch, AGM Tielens, J Serôdio, SB Gould, G Christa, Marine Biology 165 (5), 82

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Door #11: Just a white blob?

Colobocephalus costellatus repainted from M. Sars (T.R. Oskars)

Colobocephalus costellatus repainted from M. Sars (T.R. Oskars)

When researching small, obscure sea slugs you are bound to run into surprises. Partly because it often takes a long time between discovery and identification, and also because a lot of the really interesting stuff is first revealed when new methods become widely available.

In 2011 a team of researchers from the Invertebrates collection were sampling specimens in Aurlandsfjorden for the Invertebrate collections and range data for the Norwegian Biodiversity Information Centre (Artsdatabanken). Among other interesting critters they found a 2 mm long white blob. While not initially impressive this small blob turned out to be the enigmatic cephalaspidean sea slug Colobocephalus costellatus (Cephalaspidea: Heterobranchia) described by Michael Sars from Drøbak in 1870. At the time of its re-discovery it was thought that this species, which is unique for Norway, had not been seen or collected since M. Sars first laid hands on it 145 years ago (more (in Norwegian) here). However, you continuously discover more information in the course of scientific work. During their work on the enigmatic slug Lena Ohnheiser and Manuel Malaquias found in the literature that the species had in fact been discovered a couple of times since 1870, first by Georg Ossian Sars in Haugesund some years after his father, and more recently by Tore Høisæter of Bio UIB in Korsfjorden outside Bergen.

Still, no in-depth analyses have been done on this species since M. Sars until Nils Hjalmar Odhner of the Swedish Natural History Museum drew the animal from the side showing some of the organs of the mantle cavity.

Most authors have had real difficulties to place this slug within the cephalaspids, and M. Sars even thought is possible that the slug might not be an opisthobranch. Some placed it within Diaphanidae based only on the globular shell, a family that has been poorly defined and often used as a “dump taxon” for species that hare hard to place. Yet others thought it might even be the same as the equally enigmatic Colpodaspis pusilla, which has been suggested to be a philinid sea slug (flat slugs digging around in mud and sand).

What was unique about the most recent find was that this was the first time it was collected alive and photographed with high magnification. The material was also so fresh that Lena and Manuel could dissect the animal and study its internal organs. In their 2014 paper “The family Diaphanidae (Gastropoda: Heterobranchia: Cephalaspidea) in Europe, with a redescription of the enigmatic species Colobocephalus costellatus M. Sars, 1870” they tried to resolve the relationships between these globe shelled slugs. What they found was that Diaphanidae was likely not a real grouping of species, containing at least three distinct groups, where one group was Colobocephalus and Colpodaspis, which were closely related to each other, but also quite distinct.

Colobocephalus costellatus M. Sars, 1870. Photo Lena Ohnheiser, CC-BY-SA. Also featured on http://www.artsdatabanken.no/File/1292

Colobocephalus costellatus M. Sars, 1870. Photo: Lena Ohnheiser, CC-BY-SA. Also featured on http://www.artsdatabanken.no/File/1292

Another new development with the sampling in Aurlandsfjorden was that the slugs were preserved in alcohol rather than formalin. Formalin is good for preserving the morphology of animals, but it destroys DNA. On the other hand, alcohol is perfect for preserving DNA. This lead to C. costellatus to be included in a 2015 DNA based phylogenetic analysis of cephalaspidean sea slugs.

Modified Tree from Oskars et al. (2015)

Modified Tree from Oskars et al. (2015)

This resulted in that the slug was found to be indeed an Opisthobranchia, and as Lena and Manuel thought, Colobocephalus and Colpodaspis were placed in their own family, Colpodaspididae. Whereas the traditional “Diaphanidae” was split apart. Even weirder was the sea slugs that were shown to be the closest relatives of Colpodaspididae, which were neither the philinids or the diaphanids. The closest relatives turned out to be slugs that are equally as weird and unique as Colpodaspididae, namely the swimming and brightly colored Gastropteridae (sometimes called Flapping dingbats) and the Philinoglossidae, which are tiny wormlike slugs that live in between sand grains.

*Cousin Meeting*  - "You sure we are related?"  - "Well, the scientists seem to think so. I see no reason to waste a good party!"

*Cousin Meeting*
– “You sure we are related?”
– “Well, the scientists seem to think so. I see no reason to waste a good party!”

So it took 145 years from its discovery before Colobocephalus became properly studied and its family ties revealed, but it is still mysterious as we do not know much about their ecology or diet.

Suggested reading:

Colobocephalus costellatus: http://www.biodiversity.no/Pages/149747

Colpodaspis pusilla: http://www.biodiversity.no/Pages/149766

Philinoglossa helgolandica: http://www.biodiversity.no/Pages/149915

Høisæter, T. (2009). Distribution of marine, benthic, shell bearing gastropods along the Norwegian coast. Fauna norvegica, 28.

Gosliner, T. M. (1989). Revision of the Gastropteridae (Opisthobranchia: Cephalaspidea) with descriptions of a new genus and six new species. The Veliger, 32(4), 333-381.

Odhner, N.H. (1939) Opisthobranchiate Mollusca from the western and northern coasts of Norway. Kongelige Norske Videnskabers Selskabs Skrifter, 1939, 1–92.

Ohnheiser, L. T., & Malaquias, M. A. E. (2014). The family Diaphanidae (Gastropoda: Heterobranchia: Cephalaspidea) in Europe, with a redescription of the enigmatic species Colobocephalus costellatus M. Sars, 1870. Zootaxa, 3774(6), 501-522.

Oskars, T. R., Bouchet, P., & Malaquias, M. A. E. (2015). A new phylogeny of the Cephalaspidea (Gastropoda: Heterobranchia) based on expanded taxon sampling and gene markers. Molecular phylogenetics and evolution, 89, 130-150.

Sars, M. (1870) Bidrag til Kundskab om Christianiafjordens fauna. II. Nyt Magazin for Naturvidenkaberne, 172–225.

-Trond