Marine Invertebrates of Bermuda The Undertaker (Aplysia morio) By Liana Coviello with James B. Wood and Melissa Parr (Eds) Abstract Taxonomy  Habitat  Ecology  Recent Research  Commercial Importance  Bermuda Laws  Personal Interest  References  Links

Abstract


Aplysia morio is commonly known as the Undertaker or as the sooty sea hare due to its black coloration. When witnessed, they exude a dark, mysterious appearance, and they disappear almost as quickly as they were seen. Aplysia are sparsely seen throughout the year in the intertidal zones of northern Bermudian waters or in waters ranging up to 40 m. These organisms are hermaphroditic and lay their eggs in beds of Laurencia, a type of algae, to protect their young from predation. They eat green, yellow, and red algae, specifically Laurencia sp. Aplysia secrete a toxic purple ink that is thought to be used for predator avoidance, as a warning signal, and for waste removal. Because of their well understood neural circuit that is comprised of 1500 neurons, Aplysia are commonly used in medical research.

Taxonomy


Phylum: Mollusca<
  Class: Gastropoda
    Subclass: Opisthobranchia
      Order: Anaspidea
        Family: Aplysiidae


While the presence of a protective shell is a synapomorphy for the phyla mollusca, Aplysia have evolved towards losing their shells. Aplysia have indistinct internal shells that are poorly calcified and are located within the mantle (Bezerra, 2006). Opisthobranchs have two tentacles on their mouths and a pair of rhinopores on their heads (Sterrer, 1986). They also have separated podia like those of the family Aplysiidae.

Habitat


Aplysia morio are found in Bermuda, the Eastern United States, and Texas, but are most abundant in Florida (Miller, 1999; Rudman, 2006). They can live at depths up to 40 m, but are typically found in shallow intertidal areas (Sterrer, 1986). Aplysia prefer living in areas abundant in algae (Bablanian, 1980). Some of these areas include regions of low wave disturbance and sandy, rocky substrates. Aplysia morio prefer habitats with low wave shock because of their poor grasping abilities; thus, when a strong storm stirs up their habitats, Aplysia are usually washed ashore (Rudman, 2006). They are usually found clinging to hard substrates or hiding in crevices (Bablanian, 1980).

Ecology


Aplysia morio can be up to 30 cm in length as adult and are typically dark brown to black in color, which gives rise to their common name “Sooty sea hare” (Sterrer, 1986). The shell plate, which is poorly calcified, is inside the organism and is contained within the mantle (Sterrer, 1986). Aplysia morio have large, rabbit-ear shaped tentacles that contain numerous nerve cells and they also have mantle flaps for swimming (Miller, 2007). Aplysia use their radula or odontophore to grasp algae and bring it to their jaw (Sutton et al., 2004). They typically feed on red, green, yellow, and red-green types of Laurencia. Juveniles prefer to eat green Laurencia over any other type of Laurencia, and they rarely ingest red Laurencia. Even though these organisms live in an area rich in algal species, adult Aplysia exclusively consume Laurencia and Rhodymenia palmate and not any of the other algal species which include: Ulva, Bryopsis, Dictyota, Galaxaura, and Padina (Bablanion, 1980). In Bermuda, Aplysia feeding patterns are not correlated with diurnal or tidal periods because they feed and move throughout the entire day (Bablanion, 1980). These organisms only cease movement when there is bad weather or lower water temperatures (Bablanion, 1980). Aplysia have unique feeding behaviors that include crawling on the sea floor, lifting their heads, and then consuming there food source (Bablanion, 1980).

The swimming behavior of Aplysia may be connected to feeding. The swimming abilities of Aplysia are impaired as a result of the consumption of sand (Carefoot & Pennings, 2003). Due to algae’s location on rocky or sandy substrates, Aplysia often consume sand along with algae. The influx of sand makes the organism much heavier, and therefore reduces its ability to swim (Carefoot & Pennings, 2003). Swimming may also be correlated with looking for food. Well fed sea hares swim less often than hungry sea hares (Carefoot & Pennings, 2003). Aplysia also swim when they are avoiding predation (Carefoot & Pennings, 2003; Sterrer, 1986). Because they have a reduced shell, Aplysia have fewer defenses against predators and must rely on swimming and inking to escape. When Aplysia are stimulated or scared, they swim longer than individuals who have not been disturbed (Carefoot & Pennings, 2003).

Aplysia that are less than 10 cm in size are commonly eaten by Aglaja inerxnis, a carnivorous opisthobranch (Pennings, 1990). Aplysia are also eaten by sea turtles, the sea spider Anoplodactylus evansi, labrid fishes, and wrasses (Rogers, 2001). Aplysia have few predators because they contain toxic, algal metabolites in their digestive glands, their skin, and in their mucous coating. Some of these toxins are thought to be neurotoxins and can cause liver damage and respiratory failure (Rogers, 2002).

Aplysia are hermaphroditic organisms whose only complex social behavior is that of fornication. Each individual has a penis that is located outside of its mouth and a vagina on their back. While these organisms are hermaphroditic, an Aplysia that has few or no eggs acts only as a male to ensure reproductive success within the community (Miller, 1979). During paired fornication, one Aplysia acts as a male and the other as a female, or they both can switch roles for reciprocal fornication (Miller, 1979). If multiple organisms fornicate together, multiple males may fertilize one female at a time or a line of fertilization may be formed where the leading organism functions as a male, the middle organism functions as both female and male, and so on. Numerous Aplysia will mate with one another in a mass spawning when in laboratory conditions (Miller, 1979). Studies were done to determine why Aplysia mass spawn and how they communicate with one another to increase the size of the aggregation (Miller, 1979). Signaling for mass spawning is attributed to a single female laying her eggs. When females lay their eggs, they release a chemical from their accessory genital mass that is carried by water flow and attracts other Aplysia (Miller, 1979). When the eggs hatch, larvae spend at least a month in the planktonic phase before they settle onto Laurencia where they eat and grow into adults (Kriegstein et al., 1974).

Recent Research


Because Aplysia have reduced shells, they need a method of protection to increase their rate of survival against predators. When disturbed, Aplysia release purple ink from their Blochmann’s gland (Bezerra et al., 2006). This ink is thought to be a predator avoidance response. The purple ink may serve as a smoke screen so that Aplysia can distract or disorient their predator for long enough to escape (Eales, 1921); however, the ink would become diluted fairly quickly in areas of increased wave shock and the sea hare would soon be rediscovered (Carew & Kandel, 1977). The ink is also toxic and signals to the predator that the Aplysia is not palatable (Chapman & Fox, 1969). While the ink is used for visual predator avoidance, it has also been suggested that the ink is a way to remove unwanted toxins from the organism’s body (Chapman & Fox, 1969); it is a warning for other Aplysia (Ambrose et al., 1979); and it affects the predator in such a way that the predator losses its appetite (Carefoot et al., 1999).

There are numerous ink filled vesicles that are dispersed throughout the Blochmann’s gland (Bezerra et al., 2006). These vesicles contain different colors of ink depending upon the food that Aplysia consume (Bezerra et al., 2006). Aplysia that eat red algae mostly have purple filled vesicles, but also have some clear and some granular vesicles (Bezerra et al., 2006). Aplysia that eat green algae only have clear vesicles and therefore have no ink; hence, ink coloration and presence is attributed to the diet of Aplysia and higher survival rates are attributed to organisms that have ink as compared to those who do not (Bezerra et al., 2006).

In a laboratory study by Chapman & Fox (1969), Aplysia were fed brown and red algae to determine if their ink would be replenished. Because ink was only replenished when red algae was consumed, it is believed that Aplysia extract the biliprotein chromophores, a complex of protein and bile pigments, from the red algae and store them in their Blochmann’s glands (MacColl et al., 1990). By using thin layer chromatography (TLC), the ink was separated into three colors that migrated at different speeds: purple, the fastest migrater, blue, the middle migrater, and red, the slowest migrater (MacColl et al., 1990). Gel filtration yielded similar results to those of the TLC experiment in that the red color was first seen, then purple and lastly blue (MacColl et al., 1990). The appearance of these three pigments shows that Aplysia ink is derived from three algal biliprotein chromophores (MacColl et al., 1990).

Commercial Importance


Because Aplysia have a well understood and mapped out neural circuit, they are commonly used in medical research to study learning behaviors. The gills and siphons of these organisms are observed under varying amounts of stress for different amounts of times (Levy & Weller 1994). Aplysia found in intertidal zones have reduced stress responses, such as gill and siphon withdrawal more compared to those found in calm water (Calin-Jagerman & Fischer, 2003). This neural response indicates that Aplysia are able to adapt to the different stresses in their natural environments.

Bermuda Laws


There are no Bermuda laws pertaining to Aplysia morio.

Personal Interest


I had been perplexed about choosing a Bermudian organism since these organisms are all very new and exciting to me. It was not until a good friend of mine, Kim Zeeh, suggested I take a look at the Undertaker. Being intrigued by the name itself, I began researching sea hares, specifically Aplysia morio. Much to my surprise, there has been very little research on this organism, but quite a bit has been done on other members of the genus. Because there was so little information regarding this organism, I became enthralled with the challenge of learning more about this species.

Much to my dismay, I still know very little about this organism because they are so sparse. Despite my disappointment, I was enthralled to learn about this genus as a whole. Sea hares went from being something I had never heard of or seen to being something that truly has sparked my interest. They are magnificent creatures in that they have very simple neural layouts and yet they can undergo complex tasks like retracting their gills and siphons when disturbed. Their mating patterns are quite unusual but also amazing. All in all, I am very happy that I chose this subject because Aplysia are extremely interesting and I hope to spread my affinity for these organisms to all who read this page.

References


Ambrose, H.W. Givens, R.P. Chen, R. and Ambrose, K. 1979. Distastefulness as a defense mechanism in Aplysia brasiliana (Mollusca: Gastropoda). Mar. Behav. And Phys. 6: 57-64

Bablanian, G. 1980. Distribution, substrate selection, and feeding behavior of Aplysia dactylomela in Bermuda.

Bezerra, L. Josè, R.F. Silva, A. Carvalho, F.U. and Melo, V. 2006. Histological description of the ink gland of the tropical sea hare Aplysia dactylomela Rang, 1828. Acta Zoo. (Stockholm). 87: 203-7

Calin-Jagerman, R. and Fischer, T. 2003. Temporal and spatial aspects of an environmental stimulus influence the dynamic of behavioral regulation of the Aplysia siphon-withdraw response. Behav. Neuro. 117(3): 555. Accessed 5 November 2007

Carefoot, T.H., Pennings, S.C. and Danko, J.P. 1999. A test of novel function(s) for the ink of sea hares. J. of Exp. Mar. Biol. And Eco. 234: 185- 197

Carew, T.J. and Kandel, E.R. 1977. Inking in Aplysia californica I. Neural circuit of an all-or-none behavioral response. J. Neurophysiol. 40:692-707

Chapman, D.J. and Fox, D.L. 1969. Bile pigment metabolism in the sea hare Aplysia.. J. of Exp. Mar. Biol. And Eco. 4: 71-8

Eales, N.B. 1921. Aplysia LMBC Memories. Liverpool, U.K. 84

Kriegstein, A. R. and Castellucci, V. Kandel, E. R. 1974. Metamorphosis of Aplysia californica in laboratory culture. Proc. natn. Acad. Sci. 71: 3654-8

Levy, M. and Weller, A. 1994. Learned changes in the rate of respiratory pumping in Aplysia fasciata in response to increases and decreases in sea water concentration. Behav. Neuro. 108(1): 161. Accessed 5 November 2007

MacColl, R. Galivan, J. Berns, D.S. Nimec, Z. Guard-Friar, D. and Wagoner, D. 1990. The chromophore and polypeptide composition of Aplysia ink. Biol. Bull. 179: 326-31

Miller, J. 1979. Sex and the sea hare. Science news. 116(13):218-9. Accessed 28 October 2007.

Miller, M.D. 1999. The Slug Site. Past Opisthobranchs of the week. http://slugsite.us/bow/nudwk174.htm accessed 2/25/2004

Rogers, C., 2001. Pycnogonids - Sea Slug predators [Message in] Sea Slug Forum. Accessed 13 November 2007. http://www.seaslugforum.net/find.cfm?id=3407

Rogers, C., 2002. Re: Sea Hare poisoning [Message in] Sea Slug Forum. Accessed 13 November 2007. http://www.seaslugforum.net/find.cfm?id=6390

Rudman, B. 2006. Aplysia morio near St. Petersburg, Florida. [Message in] Sea Slug Forum.Accessed 13 November 2007. http://www.seaslugforum.net/display.cfm?id=16913

Rudman, B. 2006. Aplysia morio from Miami, Florida. [Message in] Sea Slug Forum.Accessed 13 November 2007. http://www.seaslugforum.net/display.cfm?id=12465

Sterrer, W. 1986. Marine Fauna and Flora of Bermuda. A Wiley-Interscience Publication. 438, 444-446

Sutton, G. Mangan, E. Neustadter, D. Beer, R. Crago, P. and Chile, H. 2004. Neural control exploits changing mechanical advantage and context dependence to generate different feeding responses in Aplysia. Biol. Cybern. 91: 333-45. Accessed 5 Novermber 2007

Links

The Sea Slug Forum
Sea Hare poisoning
Aplysia
Aplysia Resource Facility at UM