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Background

Costasiella ocellifera is a small (up to 13 mm) species of sea slug, a shell-less marine gastropod mollusk in the family Costasiellidae[1]. Costasiella ocellifera, and other members of the Costasiellidae family are often mistakenly classified as nudibranchs because they superficially resemble other species of that clade, 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."[2] The Brazilian species, Costasiella liliana, is a synonym of C. ocellifera.[3][4]


Etymology

The name 'ocellifera'' comes from the Latin word for eye, ''ocellus'' and the Latin word "ifer" which means "to carry" and is in reference to the blue eyespot found on the top of Costasiella ocellifera’s head.[5]

Description

The body of C. ocellifera is a white, somewhat translucent color and speckled with small black dots. A majority of the upper surface of the body is covered in pointed cerata. Similar to the body, the cerata is also transparent, however, they contain digestive gland ducts, so it appears green because of the chloroplasts the sea slug has digested. The tips of the cerata are often white, but some can also have an orange-yellow colored ring towards the top of the cerata as well. The cerata is also speckled with small black, white and blue iridescent spots. The top of the head is an orange-yellow color, and it has two large horn-like rhinophores. The rhinophores are semi-transparent, but towards the tip they appear black due to large clusters of black dots. There are two distinct black eyes in between the rhinophores. The area around the eyes is almost always completely white and is sometimes described as resembling an eye-mask[6]. Directly behind the eyes and rhinophores is a blue eyespot that is distinguishing characteristic of this species.[1][7] These slugs, like all other sacoglossan slugs, only have a radula with one row of teeth that allow the slugs to skillfully punctures the cell wall of the algae, Avrainvillea.[4] These sea slugs average about 5mm in size, but can grow up to 13mm.[7]

Distribution/habitat

This species of Costasiella has only been found within the tropical/subtropical Atlantic Ocean region, but within that region it has been found in several places, including, the Bahamas, Barbados, Belize, Bermuda, Dominican Republic, Florida, Honduras, Jamaica, and some areas of Mexico.[1][8][9]

Costasiella ocellifera inhabits shallow coastal waters and is almost always found on the plant species Avrainvillea nigricans.[3] In fact, the distribution of this sea slug is interrelated with the distribution of the Avrainvillea algae[10].

Characteristics

Shell-less Sacoglossan sea slug are often preyed upon by small predatory fish, some nemerteans species, cnidarians, crustaceans, and even some carnivorous coral species.[11] In order to protect themselves from these predators, C. ocellifera was able to develop a chemical defense system by using secondary metabolites that come from the algae they feed on, Avrainvillea. Using TLC chromatography, scientists were able to identify the metabolite as avrainvilleol. This chemical defense is so effective that in a laboratory test, several slugs were placed into a tank filled with predatory fish (bluehead wrasses), and it was observed that whenever a sea slug was eaten by a fish it was almost immediately spit back out, unharmed.[12] In addition to the chemical defense mechanism, these sea slugs have also evolved an effective camouflage defense because when they digest the algae chloroplasts their cerata turn green in color which helps them blend in with the surrounding algae.[13][4]

Costasiella ocellifera also shows long-term retention of functional kleptoplasty, which means that they have the ability to ingest functioning chloroplasts from algae, and survive using photosynthesis for up to 65 days when starved.[14]

Kleptoplasty/feeding

Costasiella ocellifera is a strictly herbivores sea slug that feeds almost exclusively on the algae species, Avrainvillea. The unique thing about this sea slug’s eating habits is that they use their radula (teeth) to pierce into the algal cell wall, and suck out the cell content, including the functioning chloroplasts (hence the name “sap-sucking sea slugs”).[15][16] After sucking out the plant cell content, they are able to incorporate the plant plastids into specialized cells within their digestive diverticula which allows them to become photosynthetic.[17] This process is known as kleptoplasty. The word kelptoplasty is derived from the Greek word for thief, Kleptes, so the word kleptoplasty can be translated to mean “stolen plastids.”[10] By taking part in this process, these animals are able to establish a unique symbiosis with the plant plastids, known as photosymbiosis.[10][18]

Kleptoplasty, is common amongst several species of sacoglossan sea slugs, however the retention period, or in other words, the amount of time that an individual slug can survive off of photosynthesis alone, varies. Some sacoglossan species have non-retention (NR), meaning they are unable to incorporate the plastids and photosynthesize. Others have short-term retention (StR), meaning that these slugs can survive using photosynthesis for up to two weeks.[14] Lastly there are the sea slugs, such as C. ocellifera, who have long-term retention (LtR) which means they can stay alive from one to several months solely on photosynthesis. It has been found that C. ocellifera can survive for up to 65 days on photosynthesis alone, however, it is unknown why there are these differences in the retention periods.[19] It has been found that specific plant/algal species consumed does contribute to the differences in the ability to perform photosynthesis.[20] This is an evolutionary advantage because the sacoglossan slugs are able to choose which method of feeding they use, so if there is a shortage of algae the sea slugs can switch from active-feeding to photosynthesis.[19] Although these slugs can photosynthesize, they are not photoautotrophic because the plant plastids are not passed from the parental slugs onto their offspring. Newly hatched sea slugs must feed on algae for a certain amount of time before they are able to photosynthesize.[18]


Life cycle/reproduction

This species of sea slug, along with all other sacoglossan species, are simultaneous hermaphrodites[9]. Meaning, they possess the reproductive organs of both sexes, and produce both types of gametes. They reproduce through internal fertilization, and then spawn their eggs in a unique spiral pattern on the plants that they eat, Avrainvillea nigricans[21]. This species is unique because they are poecilogony, which means they have two different types of larval development[22]. In several studies it was shown that C. ocellifera can have both lecithotrophic (aplanktonic) and planktotrophic larval development. Lecithotrophic larvae feed from the egg reserves, such as the yolk sacs. Planktotrophic larvae, on the other hand, feed on plankton in the water column[22]. For approximately a month after hatching, the planktotrophic larvae are free-swimming, while the lecithotrophic larvae go through their metamorphoses process while in their eggs.[23][9]


Phylogeny

Results of a study based on the analysis of almost 3,000 base pairs of DNA from four genetic loci which suggest the following evolutionary relationships of the Costasiella species[24]:

Bibliography

[edit]
  • Functional kleptoplasty in a limapontioidean genus[14]
  • Sacoglossa (Mollusca: Gastropoda: Heterobranchia) from northern coasts of Singapore[15]
  • Selective consumption of sacoglossan sea slugs (Mollusca: Gastropoda) by scleractinian corals[11]
  • Functional chloroplasts in metazoan cells - a unique evolutionary strategy in animal life[19]
  • Crawling leaves: photosynthesis in sacoglossan sea slugs[16]
  • Specialist herbivores reduce their susceptibility to predation by feeding on the chemically defended seaweed[12]
  • A review of taxonomy and phylogenetic relationships in the genus Costasiella[24]
  • Polymorphic adaptations in metazoans to establish and maintain photosymbioses[10]
  • Saccoglossa (Opisthobranchia) from the Ryukyu Islands[6]
  • Costasiella coronata, new species, and a revised diagnosis for the family costasiellidae[3]
  • Chemical Studies of Caribbean Sacoglossans[8]
  • Reduced genetic diversity and increased reproductive isolation follow population‐level loss of larval dispersal in a marine gastropod[9]
  • Costasiella ocellifera (Simroth, 1895)[1]
  • Poecilogony and Population Genetic Structure[22]
  • Identification of sequestered chloroplasts in photosynthetic and non-photosynthetic sacoglossan sea slugs[20]
  • Costasiella ocellifera (Simroth, 1895)[7]
  • Plastid-bearing sea slugs fix CO2 in the light but do not require photosynthesis to survive[18]
  • Comparison of Biochemical Composition and Developmental Mode in Two Populations of Costasiella[23]
  • Plastid survival in the cytosol of animal cells[2]
  • The making of a photosynthetic animal[17]
  • Sacoglossa[21]
  • Planet Catfish[5]
  • Sap-sucking Slugs (Sacoglossa)[4]
  • Ceras[13]
  • Costasiella ocellifera (Simroth, 1895)[25]
  1. ^ a b c d "Costasiella ocellifera (Simroth, 1895) | Cataloging Diversity in the Sacoglossa". sacoglossa.myspecies.info. Retrieved 2021-02-17.
  2. ^ a b de Vries, Jan; Christa, Gregor; Gould, Sven B. (June 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.
  3. ^ a b c Swennen, C. (31 August 2007). "Costasiella coronata, new species, and a revised diagnosis for the family costasiellidae (Mollusca : Opisthobranchia : Sacoglossa)". The Raffles Bulletin of Zoology. 55(2): 355–362.
  4. ^ a b c d "Snails and Slugs (Gastropoda)". www.molluscs.at. Retrieved 2021-04-03.
  5. ^ a b "Synodontis ocellifer • Mochokidae • Cat-eLog". www.planetcatfish.com. Retrieved 2021-03-23.
  6. ^ a b Ichikawa, Marina (November 1993). "Saccoglossa (Opisthobranchia) from the Ryukyu Islands". Publications of the Seto Marine Biological Laboratory. 36 (3): 119–139. doi:10.5134/176229. ISSN 0037-2870.
  7. ^ a b c jurisdiction=New South Wales; corporateName=Australian Museum; author=Rudman, W. B. (2010-07-15). "The Sea Slug Forum - Costasiella ocellifera". www.seaslugforum.net. Retrieved 2021-02-17. {{cite web}}: |last= has generic name (help)CS1 maint: multiple names: authors list (link)
  8. ^ a b Gavagnin, Margherita; Mollo, Ernesto; Montanaro, Domenico; Ortea, Jesus; Cimino, Guido (2000-07-01). "Chemical Studies of Caribbean Sacoglossans: Dietary Relationships with Green Algae and Ecological Implications". Journal of Chemical Ecology. 26 (7): 1563–1578. doi:10.1023/A:1005526526884. ISSN 1573-1561.
  9. ^ a b c d Ellingson, Ryan A.; Krug, Patrick J. (2016). "Reduced genetic diversity and increased reproductive isolation follow population-level loss of larval dispersal in a marine gastropod". Evolution. 70 (1): 18–37. doi:10.1111/evo.12830. ISSN 1558-5646.
  10. ^ a b c d Clavijo, Jenny Melo; Donath, Alexander; Serôdio, João; Christa, Gregor (2018). "Polymorphic adaptations in metazoans to establish and maintain photosymbioses". Biological Reviews. 93 (4): 2006–2020. doi:10.1111/brv.12430. ISSN 1469-185X.
  11. ^ a b Mehrotra, Rahul; Monchanin, Coline; Scott, Chad M.; Phongsuwan, Niphon; Gutierrez, Manuel Caballer; Chavanich, Suchana; Hoeksema, Bert W. (2019-04-29). "Selective consumption of sacoglossan sea slugs (Mollusca: Gastropoda) by scleractinian corals (Cnidaria: Anthozoa)". PLOS ONE. 14 (4): e0215063. doi:10.1371/journal.pone.0215063. ISSN 1932-6203. PMC 6488191. PMID 31034493.{{cite journal}}: CS1 maint: PMC format (link) CS1 maint: unflagged free DOI (link)
  12. ^ a b Hay, Mark E.; Dufy, J. Emmett; Paul, Valerie J.; Renaud, Paul E.; Fenical, William (1990). "Specialist herbivores reduce their susceptibility to predation by feeding on the chemically defended seaweed Avrainvillea longicaulis". Limnology and Oceanography. 35 (8): 1734–1743. doi:10.4319/lo.1990.35.8.1734. ISSN 1939-5590.
  13. ^ a b jurisdiction=New South Wales; corporateName=Australian Museum; author=Rudman, W. B. (2010-07-15). "The Sea Slug Forum - Cerata (ceras) in aeolids". www.seaslugforum.net. Retrieved 2021-04-03. {{cite web}}: |last= has generic name (help)CS1 maint: multiple names: authors list (link)
  14. ^ a b c Christa, Gregor; Gould, Sven B.; Franken, Johanna; Vleugels, Manja; Karmeinski, Dario; Händeler, Katharina; Martin, William F.; Wägele, Heike (2014-12-01). "Functional kleptoplasty in a limapontioidean genus: phylogeny, food preferences and photosynthesis in Costasiella, with a focus on C. ocellifera (Gastropoda: Sacoglossa)". Journal of Molluscan Studies. 80 (5): 499–507. doi:10.1093/mollus/eyu026. ISSN 0260-1230.
  15. ^ a b Jensen, Kathe (10 July 2015). "Sacoglossa (Mollusca: Gastropoda: Heterobranchia) from northern coasts of Singapore" (PDF). The Raffles Bulletin of Zoology. 31: 226–249.
  16. ^ a b Cruz, Sónia; Calado, Ricardo; Serôdio, João; Cartaxana, Paulo (2013-10-01). "Crawling leaves: photosynthesis in sacoglossan sea slugs". Journal of Experimental Botany. 64 (13): 3999–4009. doi:10.1093/jxb/ert197. ISSN 0022-0957.
  17. ^ a b Rumpho, M. E.; Pelletreau, K. N.; Moustafa, A.; Bhattacharya, D. (2011-01-15). "The making of a photosynthetic animal". Journal of Experimental Biology. 214 (2): 303–311. doi:10.1242/jeb.046540. ISSN 0022-0949. PMC 3008634. PMID 21177950.{{cite journal}}: CS1 maint: PMC format (link)
  18. ^ a b c Christa, Gregor; Zimorski, Verena; Woehle, Christian; Tielens, Aloysius G. M.; Wägele, Heike; Martin, William F.; Gould, Sven B. (2014-01-07). "Plastid-bearing sea slugs fix CO 2 in the light but do not require photosynthesis to survive". Proceedings of the Royal Society B: Biological Sciences. 281 (1774): 20132493. doi:10.1098/rspb.2013.2493. ISSN 0962-8452. PMC 3843837. PMID 24258718.{{cite journal}}: CS1 maint: PMC format (link)
  19. ^ a b c Händeler, Katharina; Grzymbowski, Yvonne P.; Krug, Patrick J.; Wägele, Heike (2009-12-01). "Functional chloroplasts in metazoan cells - a unique evolutionary strategy in animal life". Frontiers in Zoology. 6 (1): 28. doi:10.1186/1742-9994-6-28. ISSN 1742-9994. PMC 2790442. PMID 19951407.{{cite journal}}: CS1 maint: PMC format (link) CS1 maint: unflagged free DOI (link)
  20. ^ a b Christa, Gregor; Händeler, Katharina; Schäberle, Till F; König, Gabriele M; Wägele, Heike (2014). "Identification of sequestered chloroplasts in photosynthetic and non-photosynthetic sacoglossan sea slugs (Mollusca, Gastropoda)". Frontiers in Zoology. 11 (1): 15. doi:10.1186/1742-9994-11-15. ISSN 1742-9994. PMC 3941943. PMID 24555467.{{cite journal}}: CS1 maint: PMC format (link) CS1 maint: unflagged free DOI (link)
  21. ^ a b "Sacoglossa". OPK Opistobranquis. 2012-05-14. Retrieved 2021-04-03.
  22. ^ a b c Vendetti, Jann E.; Trowbridge, Cynthia D.; Krug, Patrick J. (2012-07-01). "Poecilogony and Population Genetic Structure in Elysia pusilla (Heterobranchia: Sacoglossa), and Reproductive Data for Five Sacoglossans that Express Dimorphisms in Larval Development". Integrative and Comparative Biology. 52 (1): 138–150. doi:10.1093/icb/ics077. ISSN 1540-7063.
  23. ^ a b Miles, Cecelia M.; Clark, Kerry B. (August 2001). "COMPARISON OF BIOCHEMICAL COMPOSITION AND DEVELOPMENTAL MODE IN TWO POPULATIONS OF COSTASIELLA [OPISTHOBRANCHIA: ASCOGLOSSA (= SACOGLOSSA)]". Journal of Molluscan Studies. 68 (2): 101–109. doi:10.1093/mollus/68.2.101. ISSN 1464-3766.
  24. ^ a b Jensen, Kathe R.; Krug, Patrick J.; Dupont, Anne; Nishina, Masayoshi (December 2014). "A review of taxonomy and phylogenetic relationships in the genus Costasiella (Heterobranchia: Sacoglossa), with a description of a new species". Journal of Molluscan Studies. 80 (5): 562–574. doi:10.1093/mollus/eyu048. ISSN 0260-1230.
  25. ^ "WoRMS - World Register of Marine Species - Costasiella ocellifera (Simroth, 1895)". www.marinespecies.org. Retrieved 2021-02-17.
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