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The hidden Sacoglossa, Stiliger smaragdinus


Patrick Green 2016

Summary

The Sacoglossa are a highly specialised order of sap-sucking Gastropods (Jensen, 2015). While previously were believed to be a monophyletic group under the subclass of Opisthobranchia, they have now been moved under the new classification of Heterobranch Gastropods due to recent phylogeny (Jörger et al., 2010). Within the family Limapontiidae under Sacoglossa, there lies a very unique seaslug, the Stiliger smaragdinus (Jensen, 2007), commonly referred to as the ‘the Emerald seaslug’ (Figure 1) and often mistaken for a nudibranch.  One of the unique aspects that belong to this Sacoglossa is that of it’s perfect camouflage making it almost invisible to spot on its algae food source, Caulerpa racemose (Figure 2) (Rudman, 1998). It achieves this by replicating the exact size and shape of C.racemose bulbs as cerata on its dorsal side. This type of camouflage is often referred to as nutritional homochromy (Jensen, 1997). While little direct research has been conducted into this relatively unknown species, it still remains a very unique and interesting species.


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Figure 1
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Figure 2

Physical Description

Similar to other Heterobranch Gastropods, S.smaragdinus has lost its external hard shell. The soft body Gastropod ranges in size, typically from 20-40mm (Jensen, 1996) and up to 50mm in length (Grove, 2015). It has white tipped rhinophores and cerata along the dorsal side that mimic it’s food, C.racemose (Figure 3).  The rhinophores are a chemosensory organs that act as the scent and taste receptors (Cummins et al., 2009). Like all Sacoglossa, it has a strong muscular foot that it uses to move around (Video 1). S.smaragdinus also has green translucent skin that contain chloroplasts collected from its food.

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Figure 3

Ecology

While sightings of S.smaragdinus are still uncommon, they have been found in such locations of sandy/ inner reef zone (as collected from) and tide pools at rocky/ reef crest sites (Pittman & Fiene, 1994) (Figure 4). S.smaragdinus have also been found up to depths of 12 meters (Hervé, 2007). Though it is  normally found around high abundant of C.racemose, due to both the protection it provides from the mimicry and and it being S.smaragdinus only source of food. 
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Figure 4

Life History and Behaviour

Feeding:
With S.smaragdinus being a specialist herbivore and a sap-sucking Sacoglossa,  it is found to only eat the chlorophyll of the C.racemose (Baumgartner et al., 2009). It achieves this by piercing the algae with its radula and sucking out the cell cytoplasm and chlorophyll (Jensen, 1997) (Video 2).  Upon feeding on the C.racemose, it is almost unspottable (Figure 5).

Reproduction:
Similar to most Heterobranch Gastropods, S.smaragdinus are hermaphroditic. With only one documented case of reproduction, they observed that the egg mass forms an irregular spiral  and that the eggs are densely crammed within the egg mass (Jensen, 1995).  Prior to hatching the embryos are fairly large compared to the capsules and that there is a dark spot on the right side of the embryos that is believe to possibly be the larval kidney (Jensen, 1995). While no other details have been recorded, other Sacoglossa once hatch go into the water column as planktotorphic larvae (Clark, 1975).

Defences:
Most Gastropods possess a shell that is used as the primary organ for defence upon predation and environmental conditions. Though upon lost the shell means greater freedom is gained for the individual, it comes with less defence and a greater risk of predation. From this, many soft bodied Gastropods have developed unique and interesting ways to protect themselves. Some use toxins to deter predation and others will use different types of colours and patterns to protect themselves. This can range from warning displays, changing colours, counter shading or like the S.smaragdinus, camouflage (Rudman, 1998). It achieves this by kleptoplasty (Maeda et al., 2010). This is the process to retain intact chloroplasts from food algae and incorporate it into its own cells (Maeda et al., 2010). Within the Metazoans, Sacoglossa are the only group noted to do this (Maeda et al., 2010). Research into kleptoplasty has found two types of it, photosynthetically functional kleptoplasty and non-functional kleptoplasty (Maeda et al., 2010). In the photosynthetically functional kleptoplasty, the active chloroplasts can be kept functionally working for one to seven months (Maeda et al., 2010). In the non-functional kleptoplasty they are only able to incorporate the cells for up to several hours. While S.smaragdinus are only able to utilise non-functional kleptoplasty, it is still able to not only help camouflage themselves, but also by producing food for themselves (Maeda et al., 2010).
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Figure 5

Anatomy and Physiology

Like many of its sister taxons, Sacoglossa have undergone detorsion, which is an evolutionary reversal of the half revolution torsion of their immediate ancestors (Jensen, 1995). Along with this, Sacoglossa have also lost their defensive shells over time, giving them more freedom in their bauplan. Overtime Sacoglossa have also developed bilateral symmetry and are a coelomate animal with a haemocoel cavity (Ruppert et al. 2004). Once the Sacoglossa pierces the algae with its radula (see below), the cytoplasm and chlorophyll follows through into the buccal mass (Figure 7 & 8), oesophagus, stomach and then to the anus to form the digestive system (Figure 6). Along the epithelium tissue, respiration occurs.

Radula:
S.smaragdinus feeds by using its uniseriate radula composed of an ascending (dorsal) limb, a descending (ventral) limb and an ascus containing used teeth rolled into a spiral still attached to the radular ribbon (Jensen, 1997; Jensen, 2015) (Figure 9). By feeding on the C.racemose, it retains the rich green colour in the digestive system and uses it in the bulb like bladders on its back making it incredibly difficult to spot (Jensen, 1997; SURG, 2014).


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Figure 6
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Figure 7
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Figure 8
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Figure 9

Biogeographic Distribution

While originally found in Sagami Bay, Japan in 1949 (Baba, 1949), S.smaragdinus has been documented all over the Indo-Pacific region. Including Hawaii and along the south Australian and New Zealand coast (Hervé, 2007; Jensen, 1995; Jensen 2015; Jörger et al., 2010; Pittman & Fiene, 1994; Rudman, 1998; SURG, 2014) (Figure 10). This follows the distributed of C.racemose in shallow temperate and tropical regions (Klein & Verlaque, 2008). 
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Figure 10

Evolution and Systematics

S.smaragdinus are Molluscs found in the class of Gastropoda. While previously monophyletically grouped under the subclass of Opisthobranchia, as of 2010 have been moved under the new classification of Heterobranhia due to recent phylogeny (Jörger et al., 2010) (Figure 11). Here they are found under the family of Limpaontiidae and in the clade of Sacoglossa. This clade is full of marine gastropod molluscs  that have undergone detorsion (Jensen, 1995) and that are found to be able to utilize within their own tissues living chloroplasts from the algae they eat, kleptoplasty (Maeda et al., 2010).

Due to the close associations between the S.smaragdinus and their food plant, C.racemose , it was originally believed to be a form of co-evolution (Jensen, 1997). However, no evidence for co-evolution has been presented (Jensen, 1997).
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Figure 11

Conservation and Threats

Being adapt at camouflaging to its algal food source, the S.smaragdinus is near impossible to spot. With this and it wide distribution or it’s food, C.racemose, there is little known about its abundance. Only random spottings over 60 years across the indo-pacific region. This could perhaps indicate a low abundance, though further research would be needed to prove this. Since it is reliant on only one food source, upon an event that might degrade or destroy it, it is believed that the abundance of S.smaragdinus are likely to be affected (Baumgartner et al., 2009).

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Figure 12

References

Baba, K. (1949). Opisthobranchia of Sagami Bay. Iwanami Shoten, Tokyo. 211

Baumgartner, F. A., Motti, C. A., De Nys, R., & Paul, N. A. (2009). Feeding preferences and host associations of specialist marine herbivores align with quantitative variation in seaweed secondary metabolites. Marine Ecology Progress Series, 396, 1-12.

Clark, K.B. (1975). Nudibranch life cycles in the Northwest Atlantic and their relationship to the ecology of fouling communities. Helgolander wiss Meereesunters. 27, 28-69

Cummins, S. F., Erpenbeck, D., Zou, Z., Claudianos, C., Moroz, L. L., Nagle, G. T., & Degnan, B. M. (2009). Candidate chemoreceptor subfamilies differentially expressed in the chemosensory organs of the mollusc aplysia. BMC Biology, 7, 28-28.

Grove, S.J. (2015). A Guide to the Seashells and other Marine Molluscs of Tasmania web-site and database.

Hervé, J.-F., (2007). (Sep 13) Stiliger smaragdinus? from New Caledonia. [Message in] Sea Slug Forum. Australian Museum, Sydney.

Jensen, K. R. (1995). Sacoglossa (Mollusca, Opisthobranchia) From the Darwin Harbour Area, Northern Territory, Australia. Zoological Museum, Universitetsparken.

Jensen, K.R. (1996). Phylogenetic systematics and classification of the Sacoglossa (Mollusca, Gastropoda, Opisthobranchia). Philosophical Transactions of the Royal Society of London, 351, 91-122.

Jensen, K. R. (1997). Evolution of the sacoglossa (Mollusca, Opisthobranchia) and the ecological associations with their food plants. Evolutionary Ecology, 11, 301-335.

Jensen, K.R. (2007). Biogeography of the Sacoglossa (Mollusca, Opisthobranchia). Bonner Zoologische Beiträge, 55, 255–281.

Jensen, K. (2015). Sacoglossa (Mollusca: Gastropoda: Heterobranchia) from northern coasts of Singapore. Raffles Bulletin of Zoology, 31, 226-249.

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, 323-323.

Klein, J., & Verlaque, M. (2008). The caulerpa racemosa invasion: A critical review. Marine Pollution Bulletin, 56, 205-225.

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, 17-26.

Pittman, C. & Fiene, P (1994). Stiliger smaragdinus Baba, 1949, Sea Slugs of Hawa’i.

Rudman, W.B. (1998). (October 14) Stiliger smaragdinus Baba, 1949. [In] Sea Slug Forum. Australian Museum, Sydney.

Ruppert, E.E., Fox, R.S. and Barnes, R.D. (2004). Invertebrate zoology: a functional evolutionary approach. (7th Ed). Belmont, CA, USA: Brooks/Cole.

SURG. (2014) Stiliger smaragdinus (Baba, 1949). Solitary Island Underwater Reasearh Group Inc.