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Thenus australiensis

(Burton & Davie, 2007) Australian Slipper Lobster



Emma Grace Arnett 2018

Summary

Commonly known as a slipper lobster or a Moreton Bay bug, Thenus australiensis was mistaken for T. orientalis for many years (Burton& Davie, 2007). Morphologically the Thenus genus are almost identical, the only differences is that T. australiensis has a small spine is on the merus of the third maxilliped and a more rigid crista dentata (see Feeding Behaviour) (Burton & Davie, 2007). There is currently a lack of literature in regards to T. australiensis thus the species must be investigated further in order to gain insights into understanding their full ecological and economical importance. T. australiensis, along with other species of the Thenus genus, has a great commercial significance and is a fundamental component to the demersal trawling fisheries. T. australiensis can be found on the benthos in the shallow (~40m deep) tropical/subtropical Indo-West Pacific regions (Johnston & Yellowlees, 1998; Burton & Davie, 2007; Wakabayashi & Phillips,2016). 

T. australiensis is a nocturnal bottom dwelling crustacean which scavenges and feeds mostly on the soft flesh of organisms (Johnston & Yellowlees, 1998; Johnston & Alexander, 1999). Along with other Thenus species, their feeding behaviour and mouth adaptations are uniquely specialised to assist with the consumption of hard to access flesh. Being in the phylum Arthropoda, T. australiensis grow and develop by the means of ecdysis (moulting their exoskeleton). They have a complex pelagic-benthic life cycle with four pelagic larval stages before settling on the benthos and metamorphosing into a juvenile (Kizhakudan & Krishnamoorthi, 2014; Wakabayashi & Phillips, 2016). Furthermore, T. australiensis sexually reproduces and is a brooding species whereby the female carries and protect the brood of eggs (Jones, 1990; Kagwade & Kalbi, 1996; Tonks, Milton & Fry, 2011).


Physical Description

T. australiensis is a small crustacean which can grow up to approximately 25cm long (Department of Primary Industries and Fisheries, 2002). The body is encapsulated in an orange exoskeleton. T. australiensis has a dorsal-ventral flattened body plan with a clear cephalothorax (fused head and thorax), abdomen and telson segmentation (Figures 1, 2 & 3). The telson is more narrow than it is long, the anterior end of the telson is calcified and hard, whereas the posterior end is soft and flexible (Burton & Davie, 2007). The uropods extend from the posterior end of the telson. The abdomen has five segments where there are four pairs of pleopods attached to the ventral side of each segment except for the first (Jones, 1990; Burton & Davie, 2007). The carapace (thorax) is wider than it is long. There are five pairs of long, thin pereiopods attached to the ventral side of the thorax. The first to fourth pairs have adapted sharp dactyls whereas the fifth pair are biramous (Burton& Davie, 2007). The mouth is also located on the ventral side of the thorax anterior to the five pairs of pereiopods. The mouth has three maxillipeds, two maxillas and one mandible (see Feeding Behaviour). Antennae are present on the anterior end of the body where the second and fourth antennae segments are flattened. Antennules extend anteriorly from the ventral side of the body located just above the mouth(Burton & Davie, 2007). Two eyes are found deep within their orbits each located on the left and right anterior end of the carapace either side of the antennae.
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Figure 1
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Figure 2
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Figure 3

Ecology

Habitat

The adult form of T. australiensis are free-moving bottom-dwelling crustaceans which are found in deep coastal waters (~40m) in coarse or sandy substrate (Tonks, Milton & Fry, 2011). The larval form are free-swimming pelagic organisms which can be found at the surface of the water column moving with the water currents (Wakabayashi & Phillips, 2016). T. australiensis can be found in the coastal waters of tropical and subtropical Australia and Indo-West Pacific (see Biogeographic Distribution).

Ecosystem Interactions

There is no current literature which suggests T. australiensis has any symbiotic relationships with other organisms or contributes to any ecosystem services. 

Life History and Behaviour

Life Cycle

Common among most marine invertebrates, T .australiensis has a pelagic-benthic biphasic life cycle with a larval stage to assist in dispersal. There are four stages of larval development which approximately lasts for 45 days (see Development) (Jones, 2006). The nisto recruit then settles on the substrate and undergoes  metamorphosis into the juvenile form. To develop into a reproductive adult, the juvenile undergoes ecdysis and moults (see Development). Once matured,the adults sexually reproduce and fertilisation of the eggs occurs externally in the water column (see Reproduction). These eggs are carried by the female in a brood until the larvae hatch (Wakabayashi & Phillips,2016). A simplified life cycle of T .australiensis is shown in Figure 4.

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Figure 4

Development

Larval Development

T. australiensis larvae are positively phototactic meaning they are attracted to light. This explains why the pelagic larvae during the first phase of the lifecycle can be found on the surface of the water column. There are four stages of larval development which approximately lasts for 45 days (Jones, 2006). The larvae in the first four stages are known as ‘phyllosoma’ and the individual in the post-larval stage is known as a ‘nisto’ (Kizhakudan & Krishnamoorthi, 2014; Wakabayashi & Phillips, 2016). In the first larval stage, the phyllosoma has an unsegmented uniramous antennule and unsegmented eyes, the first maxilliped and pleopods are absent, and the telson is undifferentiated.The phyllosoma is in the first larval stage for a duration of approximately seven days. In the second larval stage, the eyes are segmented, the antennules become biramous but are still unsegmented, uropods begin to develop, pleopods and gills are still absent, and telson is still undifferentiated. The phyllosoma is in the second larval stage for a duration of approximately five days. In the third larval stage, the antennules are biramous and have become unsegmented, the biramous antennae are unsegmented and flattened, the first maxilliped and pleopods start developing, uropods are well developed, gills are still absent, telson is differentiated. The phyllosoma is in the third larval stage for a duration of approximately seven days. In the fourth larval stage, the antennae become segmented, and the gills are present. The phyllosoma is in the fourth larval stage for a duration of approximately seven days. Finally, the post-larval stage is where the phyllosoma develop into a nisto. The post-larval stage is short lived (approximately four days) where the nisto is a non-feeding organism. It signals the end of the planktonic phase and the body plan resembles that of a translucent adult form. Thus, the nisto are sedentary and begin life on the benthos. Relatively soon after the larvae has transformed into the nisto, the nisto metamorphoses into a juvenile which is characterised by its now hardened exoskeleton and begins feeding (Kizhakudan & Krishnamoorthi, 2014; Wakabayashi & Phillips, 2016). Figure 5 shows a simplified four stage life of the larva.

Ecdysis

The phylum Arthropoda are a part of the superphylum Ecdysozoa. This means that development in arthropods occur through ecdysis as opposed to direct development. Ecdysis is the growth process where organisms, such as T. australiensis, moult their exoskeleton (chitinous cutile) in order to grow and develop (Mikami, 2005; Jones, 2006). There are three stages of moulting an exoskeleton: post-moult, inter-moult, and pre-moult. During the post-moult stage, the newly formed cuticle under the old exoskeleton is vulnerable and soft which soon will harden and develop into the new exoskeleton. The cuticle generally takes 48 hours to harden. The post-moult stage is the most vulnerable for the organism. Once the exoskeleton has become rigid the organism has now entered the inter-moult stage. The pre-moult stage is the most complex. First,the epidermis and cuticle begin to separate resulting in a wide “transparent zone”. When the transparent zone is wide enough new soft and irregular setae expand into the space. Once the setae become hard, a new layer of cuticle develops externally to the epidermis (Jones, 2006). Ecdysis is the actual moult activity of the exoskeleton after pre-moult. This is where the old exoskeleton is fully expelled off the body (Mikami, 2005).

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Figure 5

Reproduction

T. australiensis are a dioecious species meaning individuals are either female or male, not both (i.e. not hermaphroditic), thus sexual reproduction is the only means of reproduction in this species. Studies suggest that the T. australiensis are seasonal cyclic reproducers where spawning occurs during the months of August and October, i.e. the dry season (Tonks, Milton & Fry, 2011). T. australiensis are a brooding species where fertilisation of the egg occurs externally and the embryo undergoes embryogenesis in a brood of eggs attached to the pleopods on the ventral side of the female’s abdomen (Jones, 1990; Kagwade & Kalbi, 1996; Tonks, Milton& Fry, 2011). The female’s body has adapted in order to carry the brood of eggs and it characterised by having a wider abdomen and a longer telson which helps to protect the brood (Jones, 1990). Studies have shown that the female reaches sexual maturity when their carapace is approximately 59mm long (Tonks, Milton & Fry, 2011). Furthermore, females of this species are highly fecund meaning that they produce between 10,000-30,000 eggs during any one reproductive cycle (Kagwade & Kalbi, 1996; Tonks, Milton & Fry, 2011).

Feeding Behaviour

T. australiensis is a carnivorous specialised predator who scavenges the benthos for marine invertebrates (Johnston & Yellowlees,1998; Johnston & Alexander, 1999). They prey upon bivalves, other small crustaceans and polychaetes by searching and digging through the substrate (Johnston & Yellowlees, 1998; Johnston & Alexander, 1999). The foraging and ingesting behaviour of this species is highly complex for their mandibles are not evolved for crushing (Figure 6). Thus, T. australiensis have highly specialised oral appendages and digestive system which synchronise to assist in consuming large and rigid prey items (see Digestive System).

Foraging behaviour

At night T. australiensis hunt for their prey buried in the substrate by using one of two processes: digging or probing (Johnston & Yellowlees, 1998). Digging occurs when the organism expands its third, fourth and fifth pereiopods and inserts them into the benthos. While inserted in the benthos, the organism excavates the substrate by moving the pereiopods inward and up towards the centre of its body. As the pereiopods are moving upwards, the organism jumps while moving to the side. The pereiopods expand again and are reinserted into the benthos repeating this process. This is compared to the probing process where the organism uses the first and second pereiopods to probe the benthos. First, the organism lowers its body to ground using its third, fourth and fifth pereiopods. Then the first and second pereiopods continuously probe the ground in front of the body as it slowly walks forward. If the organism is successful in locating a prey item using either of the two above techniques, then it will lower its body even further, place its antennae on the ground and continuously probe the prey item. The organism will then capture its prey using its pereiopods (Johnston &Alexander, 1999).

Accessing prey

As mentioned above, the mandibles are not able to crush through the hard exoskeletons of its prey. Therefore, T. australiensis have developed a process to assist in the acquisition of the soft flesh. If they encounter a prey item, such as a bivalve, the organism must first position itself over the prey item. It then inserts the third pereiopods between the two shells and pries them open. Utlising the first and second pereiopods the organism then detaches and removes the prey item from the shell valves (Johnston & Yellowlees, 1998). The prey item is now ready for ingestion.

Ingesting behaviour

Once the prey has been located and accessed, the organism must place the food item into the oral cavity. Still holding the prey item, the first and second pereiopods move the food towards the mouth. The crista dentata, propodus and dactylus located on the third maxillipeds (Figure 7) grasp the prey item and move it towards the mandible. The mandibles then grip onto the prey item in a shearing motion. The third maxillipeds then pull and stretch the prey item away from the mandible. The second maxillipeds (Figure 8) then use their propodus and dactylus to cut the prey item between the mandible and the third maxilliped. The first maxilla (Figure 9) then help to shovel the prey gripped by the mandibles into the oesophagus. Simultaneously, the third maxillipeds open its crista dentata, propodus and dactylus to rearrange the remaining of prey item in preparation for the next insertion into mandibles (Johnston & Alexander, 1999).

Note, that the second maxilla and first maxillipeds are not used during the feeding process (Figures 10 & 11 respectively). The second maxilla help regulate water movement over the gills (see Respiratory and Circulatory System).

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Figure 6
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Figure 7
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Figure 8
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Figure 9
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Figure 10
11
Figure 11

Anatomy and Physiology

Digestive System

The digestive system of T. australiensis is an internal tube that is made up of three primary sections: the foregut, the midgut and the hind gut (Johnston & Alexander, 1999; McGaw & Curtis, 2013). The foregut is made up of the cardiac and pyloric chambers which are specialised for both extracellular and mechanical digestion. First, the ingested food enters the cardiac chamber and undergoes mechanical digestion with the aid of the gastric mill apparatus. The gastric mill possesses specialised teeth which assist in the breakdown of particles. The gastric teeth of T. australiensis are not as calcified as the gastric teeth of other carnivorous decapods. With the aid of the foregut muscles and the gastric mill, the broken down food then moves through the pyloric chamber into the midgut. These foregut muscles and the gastric mill movements are regulated by the stomaogratric ganglion (see Nervous System). The pyloric chamber filters the food particulates out of the digestive system allowing only liquid forms of food to enter the hepatopancreas in the midgut. The midgut of T. australiensis is fairly short (~3-5mm). The hepatopancreas is the site of intracellular digestion of food. Once all nutrients have been taken from the food, the hindgut disposes of a peritrophic membrane which contains the metabolic waste. The hind gut is essentially a long cuticle extending down the length of the abdomen to the anus on the ventral side of the body anterior to the telson. With the aid of longitudinal and circular muscles the waste is disposed of into the surrounding environment (Johnston & Alexander, 1999; McGaw & Curtis, 2013). Figure 12 shows a simplified diagram of the digestive system in T. australiensis.

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Figure 12

Respiratory and Circulatory System

Gas exchange in T. australiensis occurs via gill ventilation. This means that as water moves over the gills oxygen is taken in and carbon dioxide is expelled, hence why it is called ‘gas exchange’. The gills are protected by the branchial chambers (Figure 13) and the second maxilla (Figure 10) assists in water movement over the gills (Wilkens, 1981). Most decapods are able to ‘reverse pump’ water over gills which aids in flushing detritus particulates out of the gills (Wilkens, 1981).

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Figure 13

Nervous System

The nervous system of T. australiensis is made up of different ganglion. Ganglion are a conglomerate of nerves. In this species, the most important are the supraesophageal and the subesophageal ganglions which regulate the mouth movements. The stomatogastric is another important ganglion which regulates the musculature activity in the foregut and gastric mill (see Digestive System) (Daur, Nadim & Bucher, 2016).

Biogeographic Distribution

Burton and Davie (2007) identified that literature had been mistakenly classifying five different species as T. orientalis. They recognised that there was a species endemic to Australian and Indonesian waters and thus suggested a new species T. australiensisT. australiensis are commonly found off tropical and subtropical coastlines in the Indo-West pacific regions. It is further suggested that specimens can be found as far north as Singapore (Burton & Davie, 2007). While Thenus species have a wide geographic distribution, T. australiensis can be found from as far south as Hervey Bay, Queensland up to the Torres Strait, and as far west as Shark Bay on the west coast of Australia (Figures 14 & 15) (Butler et al., 2011).
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Figure 14
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Figure 15

Evolution and Systematics

Scientific Classification

Kingdom: Animalia

Superphylum: Ecdysozoa

Phylum: Arthropoda

Subphylum: Crustacea

Class: Malacostraca

Subclass: Eumalacostraca

Superorder: Eucarida

Order: Decapoda

Suborder: Pleocyemata

Infraorder: Achelata

Family: Scyllaridae

Subfamily: Theninae

Genus: Thenus

Species: Thenus australiensis

Phylogeny

Up until 2007 T. orientalis was believed to be the only species in the Thenus genus. Thus all studies conducted before this time were assumed to be on the one species, however, Burton and Davie (2007) identified that previous literature were mistakenly classifying five different species as T. orientalis. These five species are extremely similar and are closely related as each species possess their own combination of alleles, however, some can be found in either one or more of the other species. From this, Burton and Davie (2007) were able to suggest a possible phylogenetic tree, as seen in Figure 16, where the last common ancestor is polymorphic. Furthermore, this supports the hypothesis that the speciation event in the Thenus genus occurred recently.



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Figure 16

Conservation and Threats

The IUCN website states that there is a current lack of literature regarding T. australiensis population, ecology and habitat data, thus the species has not yet been categorised into a conservation threat-level (Butler et al., 2011). 

However, in northern Australia some prawn fisheries, where T. australiensis is a by-product, have already put some conservation efforts in place. For instance, there are legal restrictions on the minimum carapace size of an individual (75mm wide x 52mm long), and a complete ban on the harvesting of females who are egg-bearing. These restrictions aim to conserve populations by allowing individuals to reach maturity and reproduce at least once in their life time before being harvested. The restrictions were chosen from current biological data available in order to optimise the yield (Tonks, Milton & Fry, 2011).

Australian Population Threats

Approximately 300 tonnes of T. australiensis biomass is harvested every year on the Great Barrier Reef (Zeller & Larcombe, 2014; Wakabayashi & Phillips, 2016). It is evident that harvesting poses the biggest threat to this species, although the stock status deems the current Great Barrier Reef population as sustainable (Wakabayashi & Phillips,2016). This is probably due to the legal restrictions currently in place.  
 

Global Population Threats

Although the Australian population is deemed sustainable, there is an ever growing concern of the decreasing populations due to overfishing in Asian countries (Zeller & Larcombe, 2014). To reduce this threat similar legal restrictions to the Australian ones should be put in place and regularly monitored in the areas affected by overfishing.

References

Burton,T. & Davie, P. (2007). A revision of the shovel-nosed lobsters of the genus Thenus (crustacea: decapoda: scyllaridae), with descriptions of three new species. Zootaxa, 1429, pp. 1 – 38.

Butler,M., Chan, T., Cockcroft, A., MacDiarmid, A., Ng, H. & Wahle, R. (2011). Thenus australiensis. The IUCN Red List of Threatened Species 2011.

Daur,N., Nadim, F. & Bucher, D. (2016). The complexity of small circuits: the stomatogastric nervous system, Current Opinion in Neurobiology, 41, pp. 1 – 7.

Department of Primary Industries and Fisheries (2002). Fish Guide. Saltwater, Freshwater and Noxious Species. Brisbane: The Great Outdoors Publications.


Johnston,D. & Yellowless, D. (1998). Relationship between dietary preferences and digestive enzyme complement of the slipper lobster Thenus orientalis (decapoda: scyllaridae). Journal of Crustacean Biology, 18(4), pp. 656 – 665.

Johnston, D. & Alexander, C. (1999). Functional morphology of the mouthparts and alimentary tract of the slipper lobster Thenus orientalis (decapoda: scyllaridae). Marine Freshwater Research, 50, pp. 213 – 23.

Jones, C. (1990). Morphological characteristics of Bay lobsters, Thenus Leach species(decapoda, scyllaridae) from north-eastern Australia. Crustaceana, 59 (3), pp. 255 – 275.

Jones, C. (2006). Biology and fishery of the Bay lobster, Thenus spp. In Lobsters:biology, management, aqua- culture and fisheries. Oxford: Blackwell.

Kagwade,P. & Kabli, L. (1996). Reproductive biology of the sand lobster Thenus orientalis (Lund) from Bombay waters, Indian Journal of Fisheries, 43(1), pp. 13 – 25.

Kizhakudan, J. & Krishnamoorthi, S. (2014). Complete larval development of Thenus unimaculatus Burton & Davie, 2007 (decapoda, scyllaridae), Crustaceana, 87(5), pp. 570 – 584.

Mikami, S. (2005). Moulting behaviour responses of Bay lobster, Thenus orientalis, to environmental manipulation, New Zealand Journal of Marine and Freshwater Research, 39, pp. 287 –292.

McGaw, I. & Curtis, D. (2013). A review of gastric processing in decapod crustaceans, Journal of Comparative Physiology B, 183, pp. 443 – 465.

Tonks, M., Milton, D. & Fry, G. (2011). Reproductive characteristics of slipper lobster, cuttlefish and squid species taken as byproduct in a tropical prawn trawl fishery, Fisheries Science, 77, pp. 741 – 756.

Wakabayashi, K. & Phillips, P. (2016). Morphological descriptions of laboratory reared larvae and post-larvae of the Australian shovel-nosed lobster Thenus australiensis Burton & Davie, 2007 (decapoda, scyllaridae). Crustaceana, 89(1), pp. 97 – 117.

Wilkens, J. (1981). Respiratory and circulatory coordination in decapod crustaceans, In Locomotion and Energetics in Arthropods, New York: Plenum Press.

Zeller, B. & Larcombe, J. (2014). Moreton Bay Bug Thenus australiensis, In Status of Key Australian Fish Stocks (Fisheries Research And Development Corporation, Can- Berra, Act).