Sacoglossa

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Sacoglossa
Temporal range: Eocene – present [1]
Elysia clarki, Florida.jpg
Elysia crispata , a shell-less species in the family Placobranchidae
Oxynoe viridis cropped.jpg
Oxynoe viridis , a shelled sacoglossan in the family Oxynoidae
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Animalia
Phylum: Mollusca
Class: Gastropoda
Subclass: Heterobranchia
Infraclass: Euthyneura
Superorder: Sacoglossa
H. von Ihering, 1876 [2]
Diversity [3]
284 species
Synonyms

Ascoglossa Bergh, 1876

Sacoglossa are a superorder of small sea slugs and sea snails, marine gastropod mollusks that belong to the clade Heterobranchia known as sacoglossans. There are 284 valid species recognized within this superorder. [3] Sacoglossans live by ingesting the cellular contents of algae, hence they are sometimes called "sap-sucking sea slugs". [4] Some sacoglossans simply digest the fluid which they suck from the algae, but in some other species, the slugs sequester and use within their own tissues living chloroplasts from the algae they eat, a very unusual phenomenon known as kleptoplasty, for the "stolen" plastids. [5] This earns them the title of the "solar-powered sea slugs", and makes them unique among metazoan organisms, for otherwise kleptoplasty is known only among single-celled protists. [6]

Contents

The Sacoglossa are divided into two clades - the shelled families (Oxynoacea) and the shell-less families (Plakobranchacea). [7] The four families of shelled species are Cylindrobullidae, Volvatellidae, Oxynoidae, and Juliidae, the bivalved gastropods. The shell-less Plakobranchacea are grouped in six families, divided between two clades ("superfamilies"), the Plakobranchoidea and the Limapontioidea. All sacoglossans are distinguished from related groups by the presence of a single row of teeth on the radula. The teeth are adapted for the suctorial feeding habits of the group. [8]

Appearance

Many of these gastropods (e.g. Elysia spp.) resemble winged slugs with a pair of cephalic tentacles. In photosynthetic members of the group, the wings, or parapodia, can be unfurled to maximise the area of the organism that is struck by sunlight. [9] In others (e.g. Placida spp.), cylindrical cerata extend from the dorsal surface. The majority of sacoglossans are 1–3 cm in length; they are typically uniform in color because the chloroplasts they ingest end up installed in their own cells. [1]

Distribution

Sacoglossa species are found worldwide in tropical and temperate oceans, but most live in the central Pacific Ocean, where they frequent the shorelines of tropical islands; diverse tracts of species are also known in the Caribbean and Indo-Pacific. These three areas have distinct ranges of species, indicating a high degree of biogeographic separation. Where sacoglossans are present further from the equator, in places such as Australia or Japan, diversity is lower, and the species present are typically tropical species that have a higher tolerance for temperature variation. Their temperate distribution closely corresponds to the distribution of their important food source, Caulerpa spp. [3] They typically live at very low population densities, making scientific study of the group difficult. [1]

Use of ingested cellular material

The sacoglossans can use the chloroplasts of the algae on which they feed, which they keep alive for hours to months after their ingestion. They maintain the cells and metabolise the photosynthetic products; [10] this process is termed kleptoplasty, and the sacoglossans are the only animals to employ it; some ciliates and foraminifera (protists) also employ the strategy. [9] Sacoglossans have been known to survive for months living solely on the photosynthetic products of their acquired plastids. [9] This process is somewhat mystifying, as the upkeep of chloroplasts usually requires interaction with genes encoded in the plant cell nucleus. This seems to suggest that the genes have been laterally transferred from algae to the animals. [9] DNA amplification experiments on Elysia chlorotica adults and eggs using Vaucheria litorea derived primers revealed the presence of psbO, an algal nuclear gene. [11] These results were likely an artefact, as most recent results based on transcriptomic analysis [12] and sequencing of genomic DNA from the slug's eggs [13] reject the hypothesis that lateral gene transfer supports kleptoplast longevity. Sacoglossans are able to choose which method of feeding they use. The switch from active feeding to photosynthesis in sacoglossans is triggered by the shortage of food resources, and typically not preferred. If food is readily available, the animal will actively consume it. Starvation periods (with photosynthesis and no active feeding) vary between species of sacoglossans from less than a week to over four months, and photosynthesis is used as a last-resort mechanism to avoid mortality. [14] Another unclear step in the process is how the chloroplasts are protected from digestion, and how they adapt to their new position in animal cells without the membranes that would control their environment in the algae. [9] However it is achieved, kleptoplasty is an important strategy for many genera of Placobranchacea. One species of Elysia feeds on a seasonally calcifying alga. Because it is unable to penetrate the calcified cell walls, the animal can only feed for part of the year, relying on the ingested chloroplasts to survive whilst the foodstuff is calcified, until later in the season when the calcification is lost and the grazing can continue. [9]

Sacoglossans can also use antiherbivory compounds produced by their algal foodstuffs to deter their own would-be predators, in a process termed kleptochemistry. [10] This may be achieved by converting algal metabolites to toxins, [15] or by using algal pigments for camouflage in a process termed nutritional homochromy. [9] [16]

Oxynoacea

Around 20% of sacoglossan species bear a shell. The Oxynoacea contains three shelled families, and all feed solely on algae of the genus Caulerpa. [1] None of these organisms benefits from the photosynthesis of the ingested chloroplasts, but the chloroplasts may have been retained to perform a camouflaging function. [9] The shells of the Volvatellidae and Oxynoidae somewhat resemble those of the cephalaspid bubble snails. The Juliidae are extraordinary in that they are shelled, bivalved gastropods. They have a shell in two pieces, which resemble the valves of a minute clam. Living members of this family have been known since 1959,[ citation needed ] and had previously only been known to science as fossils (which had been interpreted as bivalves).[ citation needed ]

Plakobranchoidea

The majority of sacoglossans are shell-less, consequently, the Plakobranchoidea are commonly described using the vernacular term "sea slugs", which can lead to their confusion with the only very distantly related nudibranchs. However, the plakobranchoid Elysia (and undoubtedly others) do develop a shell before hatching from their egg. [17] Indeed, at least the Elysiidae, Limapontiidae, and Hermaeidae all bear larval shells, which are spiral, and possess between three-quarters and one complete whorl. [18]

The plakobranchoids have a more diverse feeding range than the Oxynoacea, feeding on a wider range of green (and sometimes red) [9] algae, and even, in three cases, being carnivorous. [1]

Evolution

The ancestor of the Sacoglossa is presumed to have fed on a now-extinct calcifying green alga in the Udoteaceae. [1] The first fossil evidence of the group comes from bivalved shells dating to the Eocene, and further bivalved shells are known from later geological periods, although the thin nature of the shells and their high-erosion habitat usually make for poor preservation. [1] The corresponding fossil record of algae points to an origin of the group deeper in time, perhaps as early as the Jurassic or Cretaceous. [1]

The loss of the shell, which was apparently a single evolutionary event, opened up a new ecological avenue for the clade, as the chloroplasts of the green algae on which they fed could now be retained and used as functioning chloroplasts, which could generate energy by photosynthesis. [1]

Taxonomy

The suborder name comes from the Greek words σάκοςsákos "shield" and γλώσσαglóssa "tongue" because the species have single toothed radulas. [19]

2004 taxonomy

This taxonomy follows Marin 2004. [20]

2005 taxonomy

In the taxonomy of Bouchet & Rocroi (2005), [21] the clade Sacoglossa is arranged as follows:

In this taxonomy, the family Elysiidae Forbes & Hanley, 1851 is considered a synonym of the family Placobranchidae Gray, 1840, and the families Oleidae O'Donoghue, 1926and Stiligeridae Iredale & O'Donoghue, 1923 are synonyms of the family Limapontiidae Gray, 1847.

The family Cylindrobullidae belongs to the superfamily Cylindrobulloidea in the sister "group" Cylindrobullida. [22]

2010 taxonomy

Jörger et al. (2010) [23] moved Sacoglossa into the Panpulmonata.

A molecular phylogeny analysis by Maeda et al. (2010) [24] confirmed the placement of Cylindrobulla within the Sacoglossa. [24]

2017 taxonomy

Bouchet et al. (2017) moved Sacoglossa from Panpulmonata to the subterclass Tectipleura. [25] [26]

Autotomy

Extreme autotomy has been observed on two species, Elysia marginata and E. atroviridis , studied in vitro. [27] [28] Over the course of the study, some individuals decapitated themselves, a behavior known as autotomy. The neck wound usually closed within one day, and the heads, especially in younger specimens, began to feed on algae within hours. Twenty days later, an entirely new body had regrown, while the discarded bodies never regrew heads. In E. atroviridis, three of 82 studied individuals autotomized, and two of the three eventually grew new bodies. All of these animals were infected with small crustaceans known as copepods. In another group of 64 without parasites, none self-decapitated, leading the researchers to hypothesize that animals cast off their bodies as a means to get rid of parasites. Another possibility is that the slugs autotomized to escape predators, but when the researchers tried to mimic an enemy's attack by pinching and cutting the creatures, none cast off their bodies. The process itself takes several hours, which the scientists say would make it ineffective as means of escape.

How the slugs survive without a heart and other vital organs for nearly a month remains a mystery. Mitoh and her colleagues suspect it may be tied to their ability to survive using the photosynthetic algae in their diet while other energy sources are unavailable.

Related Research Articles

<span class="mw-page-title-main">Kleptoplasty</span> Form of algae symbiosis

Kleptoplasty or kleptoplastidy is a process in symbiotic relationships whereby plastids, notably chloroplasts from algae, are sequestered by the host. The word is derived from Kleptes (κλέπτης) which is Greek for thief. The alga is eaten normally and partially digested, leaving the plastid intact. The plastids are maintained within the host, temporarily continuing photosynthesis and benefiting the host.

<i>Elysia chlorotica</i> Species of gastropod

Elysia chlorotica is a small-to-medium-sized species of green sea slug, a marine opisthobranch gastropod mollusc. This sea slug superficially resembles a nudibranch, yet it does not belong to that clade. Instead it is a member of the clade Sacoglossa, the sap-sucking sea slugs. Some members of this group use chloroplasts from the algae they eat for photosynthesis, a phenomenon known as kleptoplasty. Elysia chlorotica is one species of such "solar-powered sea slugs". It lives in a subcellular endosymbiotic relationship with chloroplasts of the marine heterokont alga Vaucheria litorea.

<i>Elysia viridis</i> Species of gastropod

Elysia viridis, the sap-sucking slug, is a small-to-medium-sized species of green sea slug, a marine opisthobranch gastropod mollusc in the family Plakobranchidae.

<span class="mw-page-title-main">Limapontiidae</span> Family of gastropods

Limapontiidae is a taxonomic family of small to minute sacoglossan sea slugs. These are marine opisthobranch gastropod mollusks.

<i>Elysia</i> (gastropod) Genus of gastropods

Elysia is a genus of sea slugs, marine gastropod molluscs in the family Plakobranchidae. These animals are colorful sea slugs, and they can superficially resemble nudibranchs, but are not very closely related to them. Instead they are sacoglossans, commonly known as sap-sucking slugs.

<i>Elysia crispata</i> Species of gastropod

Elysia crispata, common name the lettuce sea slug or lettuce slug, is a large and colorful species of sea slug, a marine gastropod mollusk.

<i>Elysia timida</i> Species of gastropod

Elysia timida is a species of sacoglossan sea slug, a marine opisthobranch gastropod mollusk. Found in the Mediterranean and nearby parts of the Atlantic, it is herbivorous, feeding on various algae in shallow water.

<i>Elysia pusilla</i> Species of gastropod

Elysia pusilla is a species of small sea slug, a marine gastropod mollusk in the family Plakobranchidae. It is a sacoglossan.

<span class="mw-page-title-main">Juliidae</span> Family of gastropods

Juliidae, common name the bivalved gastropods, is a family of minute sea snails, marine gastropod mollusks or micromollusks in the superfamily Oxynooidea, an opisthobranch group.

<i>Plakobranchus ocellatus</i> Species of gastropod

Plakobranchus ocellatus is a species of sea slug, a sacoglossan, a marine opisthobranch gastropod mollusk in the family Plakobranchidae. It is found in shallow water in the Indo-Pacific region.

<span class="mw-page-title-main">Plakobranchacea</span> Family of gastropods

The Plakobranchacea are a clade of sea slugs, marine gastropod molluscs in the clade Sacoglossa.

<i>Vaucheria litorea</i> Species of alga

Vaucheria litorea is a species of yellow-green algae (Xanthophyceae). It grows in a filamentous fashion. V. litorea is a common intertidal species of coastal brackish waters and salt marshes of the Northern Atlantic, along the coasts of Europe, North America and New Zealand. It is also found in the Eastern Pacific coasts of Washington state. It is found to be able to tolerate a large range of salinities, making it euryhaline.

<i>Costasiella kuroshimae</i> Species of mollusc (sea slug)

Costasiella kuroshimae—also known as a "leaf slug", or "leaf sheep"—is a species of sacoglossan sea slug. Costasiella kuroshimae are shell-less marine opisthobranch gastropod mollusks in the family Costasiellidae. Despite being animals they indirectly perform photosynthesis, via kleptoplasty.

<i>Julia exquisita</i> Species of gastropod

Julia exquisita is a small species of sea snail with a green bivalve shell. It is a marine gastropod mollusk in the family Juliidae.

<span class="mw-page-title-main">Panpulmonata</span> Clade of gastropods

Panpulmonata is a taxonomic clade of snails and slugs in the clade Heterobranchia within the clade Euthyneura.

<i>Costasiella ocellifera</i> Species of gastropod

Costasiella ocellifera is a small (5–13 mm) species of sea slug, a shell-less marine gastropod mollusk in the family Costasiellidae. Costasiella ocellifera, and other members of the Costasiellidae family are often mistakenly classified as nudibranchs because they superficially resemble other species of that group, but they are actually a part of the Sacoglossa superorder of sea slugs, also known as the “sap-sucking sea slugs,” "crawling leaves" or the "solar-powered sea slugs." C. ocellifera was discovered by Simroth in 1895, and was initially classified as Doto ocellifera. The Brazilian species, Costasiella liliana, is a synonym of C. ocellifera.Costasiella ocellifera shows long-term retention of functional kleptoplasty.

<i>Elysia marginata</i> Species of sea slug

Elysia marginata is a marine gastropod in the family Plakobranchidae. It is known for its ability to regenerate its whole body and heart after autotomizing it from its head.

<i>Costasiella nonatoi</i> Species of mollusc (sea slug)

Costasiella nonatoi is a species of sacoglossan sea slug in the genus Costasiella. It is one of few species in the genus that is not photosynthetic. The description of this species was based on two specimens which were serially sectioned and designated as the holotype. The species was named after Dr. Edmundo Nonato, a professor at the Oceanographic Institute of the University of São Paulo.

<i>Elysia atroviridis</i> Species of sea slug

Elysia atroviridis is a benthic species of sea slug belonging to the family Plakobranchidae native to the northwest pacific. E. atroviridis slugs live up to three meters deep, and are generally dark green in skin colour with small, black spots all around the body. E. atroviridis is a member of the superorder Sacoglossa, and thus possesses the ability to perform kleptoplasty. E. atroviridis and Elysia marginata are notable for possessing the ability to completely autotomize their bodies and grow them back within 20 days.

References

  1. 1 2 3 4 5 6 7 8 9 Jensen, K. R. (1997). "Evolution of the Sacoglossa (Mollusca, Opisthobranchia) and the ecological associations with their food plants". Evolutionary Ecology. 11 (3): 301–335. Bibcode:1997EvEco..11..301J. doi:10.1023/A:1018468420368. S2CID   30138345.
  2. ↑ Ihering H. v. (1876). "Versuch eines natürlichen Systemes der Mollusken". Jahrbücher der Deutschen Malakozoologischen Gesellschaft 3: 97-148. Sacoglossa is on the page 146.
  3. 1 2 3 Jensen, Kathe R. (November 2007). "Biogeography of the Sacoglossa (Mollusca, Opisthobranchia)" (PDF). Bonner zoologische Beiträge . 55 (3–4): 255–281. Archived from the original (PDF) on 5 October 2013.
  4. ↑ Tan, Rina (December 2008). "Sap-sucking slugs". Wild Singapore. Retrieved 12 January 2010.
  5. ↑ de Vries, Jan; Christa, Gregor; Gould, Sven B. (2014). "Plastid survival in the cytosol of animal cells". Trends in Plant Science. 19 (6): 347–350. doi:10.1016/j.tplants.2014.03.010. ISSN   1360-1385. PMID   24767983.
  6. ↑ Händeler, K.; Grzymbowski, Y. P.; Krug, P. J.; Wägele, H. (2009). "Functional chloroplasts in metazoan cells - a unique evolutionary strategy in animal life". Frontiers in Zoology . 6: 28. doi: 10.1186/1742-9994-6-28 . PMC   2790442 . PMID   19951407.
  7. ↑ Handeler, K.; Grzymbowski, Y. P.; Krug, P. J.; Wagele, H. (2009). "Functional chloroplasts in metazoan cells - a unique evolutionary strategy in animal life". Front Zool. 6 (1): 28. doi: 10.1186/1742-9994-6-28 . PMC   2790442 . PMID   19951407.
  8. ↑ Barnes, Robert D. (1982). Invertebrate Zoology. Philadelphia, PA: Holt-Saunders International. p. 377. ISBN   0-03-056747-5.
  9. 1 2 3 4 5 6 7 8 9 Rumpho, M. E.; Dastoor, F. P.; Manhart, J. R.; Lee, J. (2007). "The Kleptoplast". The Structure and Function of Plastids. Advances in Photosynthesis and Respiration. Vol. 23. pp. 451–473. doi:10.1007/978-1-4020-4061-0_23. ISBN   978-1-4020-4060-3.
  10. 1 2 After Marín, A.; Ros, J. N. (2007). "Chemical defenses in Sacoglossan Opisthobranchs: Taxonomic trends and evolutionary implications" (PDF). Scientia Marina. 68 (Suppl. 1): 227–241. doi: 10.3989/scimar.2004.68s1227 .
  11. ↑ Rumpho, M. E.; Worful, J. M.; Lee, J.; Kannan, K.; Tyler, M. S.; Bhattacharya, D.; Moustafa, A.; Manhart, J. R. (2008). "Horizontal gene transfer of the algal nuclear gene psbO to the photosynthetic sea slug Elysia chlorotica". Proc Natl Acad Sci U S A. 105 (46): 17867–71. doi: 10.1073/pnas.0804968105 . PMC   2584685 . PMID   19004808.
  12. ↑ Wägele, H.; Deusch, O.; Händeler, K.; Martin, R.; Schmitt, V.; Christa, G.; Pinzger, B.; Gould, S. B.; Dagan, T.; Klussmann-Kolb, A.; Martin, W. F. (2011). "Transcriptomic evidence that longevity of acquired plastids in the photosynthetic slugs Elysia timida and Plakobranchus ocellatus does not entail lateral transfer of algal nuclear genes". Mol Biol Evol. 28 (1): 699–706. doi:10.1093/molbev/msq239. PMC   3002249 . PMID   20829345.
  13. ↑ Bhattacharya, D.; Pelletreau, K. n.; Price, D. C.; Sarver, K. E.; Rumpho, M. (2013). "Genome analysis of Elysia chlorotica Egg DNA provides no evidence for horizontal gene transfer into the germ line of this Kleptoplastic Mollusc". Mol Biol Evol. 30 (8): 1843–52. doi:10.1093/molbev/mst084. PMC   3708498 . PMID   23645554.
  14. ↑ Middlebrooks, M. L.; Pierce, S. K.; Bell, S. S. (2011). "Foraging behavior under starvation conditions is altered via photosynthesis by the marine gastropod, Elysia clarki". PLOS ONE. 6 (7): e22162. Bibcode:2011PLoSO...622162M. doi: 10.1371/journal.pone.0022162 . PMC   3140505 . PMID   21799783.
  15. ↑ Gavagnin, M.; Marin, A.; Mollo, E.; Crispino, A.; Villani, G.; Cimino, G. (1994). "Secondary metabolites from Mediterranean Elysioidea: origin and biological role". Comparative Biochemistry and Physiology B. 108: 107–115. doi:10.1016/0305-0491(94)90170-8.
  16. ↑ Clark, K. B.; Jensen, K. R.; Stirts, H. M. (2009). "Survey for Functional Kleptoplasty among West Atlantic Ascoglossa (= Sacoglossa) (Mollusca, Opisthobranchia)". Veliger. 33 (4): 339–345.
  17. ↑ Thompson, T. E.; Salghetti-Drioli, U. (1984). "Unusual features of the development of the sacoglossan Elysia hopei in the Mediterranean Sea". J. Molluscan Stud. 50 (1): 61–63. Archived from the original on 2005-07-10.
  18. ↑ THOMPSON, T. E. (1961). "The Importance of the Larval Shell in the Classification of the Sacoglossa and the Acoela (Gastropoda Opisthobranchia)". J. Molluscan Stud. 34 (5): 233–238. doi:10.1093/oxfordjournals.mollus.a064867.
  19. ↑ Maggenti, Mary Ann Basinger; Maggenti, Armand R.; Gardner, Scott (2005). "sacoglossa". Online Dictionary of Invertebrate Zoology. Harold W. Manter Laboratory of Parasitology. p. 800.
  20. ↑ Marín, A.; Ros, J. N. (2007). "Chemical defenses in Sacoglossan Opisthobranchs: Taxonomic trends and evolutionary implications" (PDF). Scientia Marina. 68 (Suppl. 1): 227–241. doi: 10.3989/scimar.2004.68s1227 .
  21. ↑ Bouchet, Philippe; Rocroi, Jean-Pierre; Frýda, Jiri; Hausdorf, Bernard; Ponder, Winston; Valdés, Ángel & Warén, Anders (2005). "Classification and nomenclator of gastropod families". Malacologia . 47 (1–2). Hackenheim, Germany: ConchBooks: 1–397. ISBN   3-925919-72-4. ISSN   0076-2997.
  22. ↑ Discussion in the Seaslug Forum : Ascobulla, Cylindrobulla [ permanent dead link ].
  23. ↑ Jörger, K. M.; Stöger, I.; Kano, Y.; Fukuda, H.; Knebelsberger, T.; Schrödl, M. (2010). "On the origin of Acochlidia and other enigmatic euthyneuran gastropods, with implications for the systematics of Heterobranchia". BMC Evolutionary Biology . 10 (1): 323. Bibcode:2010BMCEE..10..323J. doi: 10.1186/1471-2148-10-323 . PMC   3087543 . PMID   20973994.
  24. 1 2 Maeda, T.; Kajita, T.; Maruyama, T.; Hirano, Y. (2010). "Molecular Phylogeny of the Sacoglossa, With a Discussion of Gain and Loss of Kleptoplasty in the Evolution of the Group". Biological Bulletin . 219 (1): 17–26. doi:10.1086/bblv219n1p17. PMID   20813986. S2CID   27608931.
  25. ↑ Bouchet, Philippe; Rocroi, Jean-Pierre; Hausdorf, Bernhard; Kaim, Andrzej; Kano, Yasunori; Nützel, Alexander; Parkhaev, Pavel; Schrödl, Michael; Strong, Ellen E. (2017). "Revised Classification, Nomenclator and Typification of Gastropod and Monoplacophoran Families". Malacologia . 61 (1–2): 1–526. doi:10.4002/040.061.0201. ISSN   0076-2997.
  26. ↑ Bouchet P, Gofas S (2018-02-02). Bieler R, Bouchet P, Gofas S, Marshall B, Rosenberg G, La Perna R, Neubauer TA, Sartori AF, Schneider S, Vos C, ter Poorten JJ, Taylor J, Dijkstra H, Finn J, Bank R, Neubert E, Moretzsohn F, Faber M, Houart R, Picton B, Garcia-Alvarez O (eds.). "Sacoglossa". MolluscaBase. World Register of Marine Species . Retrieved 2018-05-15.
  27. ↑ Mitoh, Sayaka (2021). "Extreme autotomy and whole-body regeneration in photosynthetic sea slugs". Current Biology. 31 (5): PR233–R234. Bibcode:2021CBio...31.R233M. doi: 10.1016/j.cub.2021.01.014 . PMID   33689716. S2CID   232145105.
  28. ↑ Shultz, David (8 March 2021). "This sea slug cut off its own head—and lived to tell the tale". Sciencemag. Retrieved 22 April 2021.

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