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Aspidosiphon muelleri (Diesing, 1851)


Harriet Goodrich 2015

Summary
Aspidosiphon muelleri is a species of peanut worm or Sipuncula, known to occupy empty mollusc shells, polychaete tubes, and also burrows that they dig out through both mechanical and chemical methods (Antonelli et al, 2015; Williams and Margolis, 1974). To protect themselves from predation and desiccation, Aspdosiphon muelleri use their  anal shield to cap and plug the openings of these burrows (Cutler, 1994). Typically, burrowing occurs in carbonatic substrata which means A. muelleri can be found inhabiting the coral reefs of both tropical and temperate waters.  Because of this, A. muelleri can be considered a main biodeteriogen that contributes to the erosion of these habitats (Trilbollet and Golubic, 2011). This species ability to live in such a range of different niches has allowed it to radiate globally, meaning it can be found in the waters off Australia, Italy, Costa Rica, West Africa and many more (Antonelli et al, 2015).  As such, differences in morphology coincide with where these animals choose to live, and variation in appearance between individuals and within the species does exist.  As a whole, A.muelleri is typically characterised by their bi-denante hooks that are arranged in rings on the anterior end of the introvert (Stephenand Edmonds, 1972; Cutler, 1994). 

While these differences are apparent, all individuals within the species A.muelleri share the same life cycle, anatomy and physiology.  Specific to their genus (Aspidosiphon) is the presence of  two pelagic larval stages in their life cycle, which are a product of external fertilization and spawning events (Ferrero-Vicentea et al, 2014). Alongside this, the continuous longitudinal musculature of A.muelleri is an important aspect that contributes to and facilitates  the feeding behaviour, digestion, locomotion and burrowing of this organism (Cutler 1994).  

While many would refer to A.muelleri as a species apart of the phylum Sipuncula, recent studies have highlighted that the sipunculids are actually nested within polychaete annelids (Struck et al, 2007). Constant debate revolves around the phylogeny of the Sipuncula, with many textbooks identifying them as their own phylum, but its now apparent that this groups stark resemblance to annelids may actually be more than just a resemblance. 

Physical Description

Sipuncula are unsegmented, coelomate worm-like marine invertebrates which range from 2mm to 70cm in length (Antonellia et al,2015).  The main anatomical feature of the Sipuncula is their highly muscularised introvert which serves not only as the main feeding apparatus of this group, but can also be used in locomotion (Ruppert et al, 2004).  The slender introvert can be completely retracted into the plump posterior or trunk of this organism, causing them to sometimes resemble a shelled peanut. This is why they are often referred to as‘peanut worms’. This retraction occurs through the use of one, two, three or four retractor muscles, with the number of muscles varying in accordance with species (Ruppert et al, 2004). The surface of the introvert can harbour hooks, papillae and other cuticular structures, while the anterior end of the introvert is flattened to form the oral disc, which is where the mouth, tentacles and the unpaired nuchal organs are found (Antonellia et al,2015; Cutler, 2014).  

Specifically, the family Aspidosiphonidae have an anal shield or calcareous cap that sometimes possess horns and grooves, which is characteristic of rock and coral boring peanut worms (Figure 2). The introvert also protrudes from the trunk at a 45-90 degree angle in all species aside from one (Cutler, 1994). Alongside this, animals within this family are generally quite small; ranging between 5-30mm in length (Cutler, 1994). The longitudinal musculature of the body wall can be either grouped into bundles or continuous (Stephen and Edmonds, 1972). This feature was first used by Stephen 1965 to distinguish between the genus’s Aspidosiphon and Paraspdosipon. 

Aspidosiphon possess longitudinal musculature that is continuous, but aside from this feature, Aspidosiphon share all their defining characteristics with Paraspidosiphon (Stephen and Edmonds, 1972). This fact makes them hard to distinguish from one another, which is only helped by the fact that peanut worms tend to contract and distort when fixed. 

Species within the genus Aspidosiphon are usually sorted into organisms that have either single or double pointed hooks (Stephenand Edmonds, 1972; Cutler, 1994). Characteristic of Aspidosiphon muelleri (Diesing, 1851) is the latter. The double pointed, bi-dentate hooks are arranged in rings on the anterior part of the introvert (Figure 1), while the posterior of the introvert is covered with uni-denate spine like hooks (Figure 2) (Antonellia et al,2015). Typical of most Aspidosiphonidae is that the shield is much darker than the rest of the body, and in the case of this specimen, it means the anal shield is a darker shade of yellow/brown (Figure 2).

It is important to mention that the morphology of A. muelleri can and does vary, and that differences between individuals of this species is common. This can be related to the fact that A.muelleri is the most widespread of the genus Aspidosiphon.  Resultantly, the body plan of individuals has been adapted and manipulated over time, allowing the occupation of shelters specific to their niche (Antonellia et al,2015).
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Figure 1
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Figure 2

Ecology

Habitat and Predation:
A. muelleri is typically found occupying empty mollusc shells, but they are also a known boring species. This species has been seen to bore into carbonate substrata including dead coral, mollusc shells, hard rocks and finally chalk rocks (Antonelli et al, 2015). The opening of the burrow created through this activity can be plugged by the anal shield of this organism. Not only does this protect the animal from predation, but also reduces the risk of desiccation (Cutler, 1994). The problem of desiccation can also be combatted by mucus glands located in the epidermis that keeps their skin moist (Cutler, 1994).  As A. muelleri is found in depths ranging between 5-2900 meters (Antonelli et al, 2015), the risk of predation is much greater than the risk of desiccation. Sipunculids are known prey items of animals including fishes, crabs, anemones, cephalopods and humans, who use them as fish bait (Cutler, 1994).

Bioerosion:
Most of the work revolving around bioerosion focuses on biodeteriogens such as sponges, polychaetes and bivalves (Antonelli et al, 2015). While these taxa are responsible for the bioerosion of coral reefs, sipunculids (especially species that bore into carbonatic substrata) are still a major factor that contribute to the erosion and destruction of reefs (Trilbollet and Golubic, 2011). Peyrot-Clausade and Chazottes (2000) found that dead corals can harbour a rich population of sipunculids such as Aspidosiphon sp. This finding is supported by the work of Risk and Sammarco (1982), who identified that alongside boring sponges, sipunculids were responsible for most of the destruction and bioerosion of the staghorn coral that existed within territories defended by damselfish.

Boring in peanut worms can occur either mechanically or chemically. Mechanically, sipunculids rub their caudal shield on carbonatic substrata, which helps to dig out burrows that they are then able to occupy (Figure 3) (Rice, 1969). Accompanying  this, the eversion, retraction and peristalsis of the introvert also contributes to the burrowing ability in Aspidsiphon (Rupert et al, 2004). As such, the caudal shield and introvert is usually fitted with abrasive structures, grooves and hooks which assist in excavation.  The musculature system responsible for this burrowing behaviour is described and discussed in detail in the Life History and Behaviour section of this page. 

Chemically, sipunculids are thought to form burrows through the use of a chelating agent or by rapidly lowering the Ph of the solution between the organism’s epidermis and the coral skeleton (Williams and Margolis, 1974). While a specific chemical agent has not been identified, the presence of glands in the epidermis of boring sipunculids definitely supports chemical mechanisms as a means of boring into calcareous substrata.  

Symbiotic Relationships:
While this species is known to be a major force responsible for the bioerosion of corals, they are also known to share symbiotic relationships with them. It is apparent that A.muelleri shares a mutualistic relationship with solitary corals, and  Gill and Coates, (1977) suggest that these relationships have existed in Aspidosiphon since the early Neogene times. Currently, A.muelleri is the only known peanut worm to partake in mutualistic behaviour (Hoeksema and Best, 1991). 

Most commonly, A.muelleri can be found living in a spiral cavity located at the base of the coral Heteropsammia michelini. During feeding, the introvert is extended through a hole in this cavity, which actually moves the coral around. In doing so, the coral is transported to new feeding grounds, and is able to be kept upright (Beesley, 2000).

While it is apparent that A.muelleri is able to occupy such spaces within the coral, how it comes to move into this spiral cavity is quite unusual. It begins with the juvenile of this species taking shelter within a gastropod shell. Planula larvae of the coral then settle on the occupied shell, and over time, as the coral grows, it actually absorbs the shells material into its own tissues. As it does this, it creates a coiled space that A.muelleri is able to occupy (Cutler, 1994). 
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Figure 3

Life History and Behaviour

Reproduction and Development: 
Majority of the Sipuncula are gonochoristic, meaning that the sexes are separate and as such, the male and female reproductive organs occur in different individuals (Ruppert et al, 2004). The gonads of the organism can be found at the base of the introvert retractor muscles, and the gametes within them are released at an early stage into the trunk coelom where they develop and mature (Ruppert et al, 2004). Once the gametes are fully developed they are stored in the nephridial sacs. The gametes stay here until spawning, which occurs in the seawater. Ferrero-Vicentea et al (2014) investigated the reproductive biology of A.muelleri in the temperate waters of the western Mediterranean Sea, and found that spawning took place between August and September. This is when the water temperature reaches its annual maximum, thus highlighting the fact that spawning could be temperature dependent in A.muelleri. 

External fertilization follows these spawning events and results in a zygote that undergoes spiral cleavage and determinate development. Interestingly, at the 64-cell stage, the zygote resembles a typical molluscan cross (Figure 4)(Cutler, 1994). This development pattern is thought to be of potential evolutionary significance, highlighting a possible sister-taxon relationship of the Sipuncula to the Mollusca (Ruppert et al, 2004).

There are four development pathways that occur in the Sipuncula, each leading to metamorphosis into a reproductive adult (Figure 5). Little is known about the specific pathway used in A.muelleri, but it has been documented that the genus Aspidosiphon has two pelagic larval stages (Ferrero-Vicentea et al, 2014). As such, the genus Aspidosiphon possess a pelagic lecithotophic larvae which undergoes metamorphoses into a planktotrophic pelagosphera larva (Cutler, 1994). The pelagosphera larva lives in the water for a period between 1 and 6 months. During this time it increases dramatically in size until it metamorphoses to a vermiform juvenile, and later into a reproductive adult (Ferrero-Vicentea et al, 2014). 
Musculature Systems: Feeding, Digestion and Locomotion: 
The Sipuncula possess three main muscle systems; the body wall musculature, the introvert retractor muscles and finally the intestinal fasteners (Cutler, 1994). These muscle systems have been identified through fluorescent staining of sections taken from an A.muelleri specimen that was collected off of Heron Island Reef, Australia. The structure of these systems will be discussed in detail and related back to their roles in feeding, digestion, locomotion and burrowing.  As the musculature of the organism is an imperative part of the organisms feeding behaviour and movement it has been explored in this section of the webpage.

Specific to the genus Aspidosiphon is the presence of two introvert retractor muscles that may be almost completely fused (Figure 6) (Cutler, 1994). These muscles extend from the body wall of the trunk coelom and attach behind the cerebral ganglia, which is also the beginning of the esophagus (Cutler, 1994; Ruppert et al, 2004). Contraction of these muscles results in the retraction of the introvert. This retraction not only allows the organism to ingest food particles captured by its tentacles but also to anchor it in its burrow (Ruppert et al, 2004). The retraction of the introvert causes the trunk to swell and pressurize, and it is the increase in girth that follows which facilitates this behaviour. A.muelleri is known to occupy empty polychaete tubes, mollusc shells and burrow into hard substrata (Antonellia et al, 2015).  As such, the retraction of the introvert is an essential part of this organism’s ecology as is allows them to occupy such spaces (Figure 7). 

Alongside the retraction of the introvert, to obtain food the introvert must also be everted. Eversion of the introvert occurs through the contraction of the body wall musculature (Figure 8). The body wall has two muscle layers, the outer layer has circular fibers, while the inner layer is made up of longitudinal fibers (Figure 9) (Cutler, 1994). The thickness of these layers depends on the size of the organism, which is this instance was <10mm in length. Specifically it is the contraction of the circular muscle fibers that elevates the pressure of the trunk, causing the introvert to evert (Ruppert et al, 2004).  Alongside eversion, alternation between contraction of circular and longitudinal fibers causes peristalsis of the introvert (Ruppert et al, 2004). It is the eversion, retraction and peristalsis of the introvert that allows organisms such as A.muelleri to burrow into substrates. As such, the body wall musculature is an essential component to the survival and wellbeing of this organism. Before the specimen was fixed and sectioned, video footage of the eversion and retraction of the introvert was recorded and can be viewed here: 


Introvert of Aspidosiphon muelleri

The third and final muscle system of the Sipuncula is the intestinal fasteners, which is made up of the spindle muscle and sometimes fixing muscles (Cutler, 1994). Both spindle and fixing muscles are present in A.muelleri, but could not be identified in this specimen.  This could be attributed to the smallness of this specimen, and the fine nature of these muscles.  Spindle muscles are long and thin and in A.muelleri, the spindle muscle extends along the rectum into the centre of the gut coil and continues on to the posterior end of the trunk (Figure 10) (Cutler, 1994).  The spindle muscle branches out and attaches to individual intestinal coils, which upon contraction, compress the intestinal coils and removes any kinks that could hinder digestion (Cutler, 1994: Ruppert et al, 2004). The fixing muscles attach these coils to the body wall of the animal, this allows the gut to be suspended in the trunk coelom and to assist in stirring intestinal content (Ruppert et al, 2004). 
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Figure 4
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Figure 5
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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

Anatomy and Physiology
The anatomy of Aspidosiphon muelleri has been described extensively in the book written by Cutler (1994). Here, the description and physiology of this species will be supported by diagrams and sections from a specimen collected off of Heron Island Reef, Australia. 

Anatomy: 
The body wall consists of continuous longitudinal musculature (Figure 9), and the species will generally possess two introvert retractor muscles that may be almost completely fused (Figure 6 & 10 ). Alongside this the spindle muscle attaches posteriorly, and the fixing muscle wraps around the ventral retractor muscle (Figure 10). A thorough analysis of the functional role of these muscles has been conducted in the Life History and Behaviour section of this webpage.

The unpaired ventral nerve cord runs along the centre of the animal, where it joins with the dorsal biolobed cerebral ganglion or brain. Excretion occurs through two nephridia in A.muelleri and digestion occurs in the intestine associated with the J shaped gut of this phylum (Figure 10).  Respiration involves transfer between the two ceolomic cavities of this organism. The anatomy and physiology involved with respiration, excretion, nerve transmission and digestion of this organism will be discussed in more detail below: 

Respiration and Gas Exchange:
Sipunculans possess two ceolomic cavities; a trunk and tentacular coelom. As sipunculans lack a hemal system, diffusion and ultrafiltration across the tentacle-trunk septum is responsible for transport between these two coeloms (Ruppert et al, 2004). Nutrients and gases are moved around the body by ceolomic fluid, which compensates for the lack of a hemal system and in turn the absence of blood vessels. The main coelomocyte responsible for oxygen transport in the Sipuncula, is the hemerthryocyte (Figure 11). Hemerthryocytes are effective oxygen carriers that exist in the ceoloms of sipunculans, polychaetes, priapulids and brachiopods (Klots et al, 1976).

A.muelleri typically live in burrows, and because of this, the tentacles are the main respiratory surface. As the animal extends its introvert outside the burrow oxygen is able to diffuse across the surface of the tentacles (Figure 7). This method is in contrast to sand burrowers whose whole body wall is a gill surface (Ruppert et al, 2004). A dermal canal system connects the epidermis of the organism with the trunk coelom. Coelomic fluid fills these canal systems, and as such, the hemerythrocytes within this fluid bind the oxygen diffusing across the tentacle epidermis, which can then be transported to the trunk coelom and the musculature (Ruppert et al, 2004). 

Excretion:
Excretion of nitrogenous wastes occurs through the metanephridia (Figure 10). Alongside this, the metanephridia are thought to play a role in osmoregulation and gamete storage and maintenance (Cutler, 1994; Ruppert et al, 2004). Whether the metanephridia of Sipuncula act as filtration or secretion kidneys is unknown, some argue that it is the former, which is based on the presence of podocytes in some species (Ruppert et al, 2004). If this is the case, sipunculans are said to possess a metanephridial system, which produces urine through ultrafiltration, modification and release (Figure 12) (Ruppert et al, 2004). 

Central Nervous system:
The central nervous system of the Sipuncula is made up of the brain, circumenteric connectives and a ventral nerve cord (Cutler, 1994; Ruppert et al, 2004).  Specifically the brain is dorsal and bilobed, and the ventral nerve cord is unpaired and has no segmentation (Cutler, 1994). Ger et al (1977) conducted experimentation on a Phascolosoma specimen, and found that 46 µg of acetycholine was present for each gram of wet weight. This finding suggests that nerve transmission in the Sipuncula is cholinergic and in turn similar to what occurs in the brains of molluscs, arthropods and mammals. 

Sensory cells are abundant all over the animals’ body, but heavily centred on the end of the introvert. This is due to the fact that the animal uses this apparatus to investigate and examine its surrounding environment (Ruppert et al, 2004). Alongside this, peanut worms are able to sense their environment through the use of a nuchal organ which may act as a chemoreceptor (Radashevsky and Migotto, 2006).  Most sipunculids are also said to possess eyespots or ocelli. The ocelli are embedded in the dorsal surface of the brain, are usually paired, pigmented and play a role in photoreception (Cutler, 1994; Ruppert et al, 2004). Investigation of the pelagosphere larvae of Sipuncula by Radashevsky and Migotto (2006), found that the pelagospheras possess one pair of transparent, spherical bodies on the anterior part of the head. These structures where thought to bear a resemblance to the the unpigmented ocelli in Spionidae larvae. As such, they may be important photoreceptive organs used by the planktotrophic pelagosphera larvae to locate food sources or light during the 1-6 month period they spend in the plankton. 
 

Digestive System: 
The sipuncula do not target a specific food source, and can be termed non selective suspension or deposit feeders (Ruppert et al, 2004). Food and inorganic matter is collected on the tentacles and ingested as the introvert is retracted into the trunk (Ruppert et al, 2004). Digestion occurs in the long intestine which is tightly coiled into a double helix (Cutler, 1994). The coiled intestine leads to the rectum and the anus which is locatered anteriorly on the trunk, and is where waste products are released (Ruppert et al, 2004). Jeuniax, (1969) found the enzyme chitinolytic polysaccharidase in the species Phascolion strombus and Sipunculus nudus, which could mean it plays a role in the digestion of particulate matter in this phylum.  
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Figure 11
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Figure 12

Evolution and Systematics
Classification:
Kingdom: Animalia
Phylum: Sipuncula
Class: Phascolosomatidea
Order: Aspidosiphoniformes 
Family: Aspidosiphonidae
Genus: Aspidosiphon 
Subgenus: Aspidosiphon
Species: Aspidosiphon muelleri


Ancestry and the Fossil Record:
There is no definite fossil sipunculid, but many have speculated that the mud dwelling worm Otto prolifica(Figure 13), which possess a retractable proboscis could be a potential candidate (Cutler, 1994).

Alongside this organism, one possible ancestor for the peanut worms could be the hyoliths (Figure 14) that were globally distributed during the Palaeozoic (Kouchinsky, 2000). Runnegar et al (1975), proposed that the hyoliths were in fact the closest relatives of the Sipuncula. This statement stems down to the fact that many features present in sipunculids bear a resemblance to structures present in the Hyolitha. The collagenous fibre bundles in the cuticle of sipunculids is similar to the arrangement of hyolith fibres, although having said that, the Sipuncula fibres are much thinner and come in numerous layers (Kouchinsky, 2000).  Again, the hydrostatic skeleton used by the hyoliths to evert the head of the animal is similar to the retraction of the introvert that is characteristic of the Sipuncula (Cutler, 1994). Finally is the presence of the anal shield in all Aspidosiphon. It has been suggested that the microstructure of calcareous Aspidosiphon shields may be similar to the cone shaped exoskeleton of the hyoliths (Kouchinsky, 2000; Cutler, 1994). While this connection could be possible, lack of investigation into the microstructure of the anal shields in sipunculids makes it hard to state that they could be a remnant of the hyolith’s calcareous exoskeleton. 

Phylogeny: 
The phylogeny of Sipuncula continues to be a topic of debate among invertebrate biologists, and it revolves around two very separate views. The first being that Sipuncula are actually derived Polychetes and in turn sit within the phylum Annelida. The second poses that the sipunculids are in fact their own phylum, sitting more basal in the evolutionary tree. 

Next to the crustaceans, annelids can be thought of as the most dominant phylum in the oceans. With over 16,500 described species, their effective segmented bauplan has allowed this phylum to radiate throughout both terrestrial and marine environments, and can even be deemed the leading macrofauna of the deep sea (Struck et al, 2007).  

Many struggle to associate the Sipuncula with the annelids for the fact that one of the main defining characteristics of the phylum is that they are segmented, which is not the case in the Sipuncula. While the Sipuncula body plan can be split into the anterior introvert and posterior trunk, they do not possess the repeated sections that are present in the Annelids.  

While their position has been refuted for quite some time, phylogenetic analysis of nuclear genes suggests that not only the Sipuncula, but the Echiurans, Siboglinidae and Clitellatans are actually nested within polychaete annelids (Struck et al, 2007).
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Figure 13
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Figure 14

Biogeographic Distribution
 A. muelleri is the most widespread of the genus Aspidosiphon and as such has been found to inhabit locations such as the north-eastern Atlantic, Azores, Canary Islands, Red Sea,West Africa, western Pacific Ocean (from Japan to Australia), Chile, Brazil,Costa Rica, Alboran, Spain, Algeria, France, Italy (Tyrrhenian Sea, Liguria,Sicily), Adriatic and Aegean Sea (Antonelli et al,2015).

Characteristic of this species is their ability to bore and construct burrows intohard substrates such as dead coral, the shells of other organisms and also chalk rocks (Fonsecaet al, 2006; Cutler, 1994; Por, 1975). This factor means that majority of A.muelleri are distributed in areas where carbonatic substrata is available, such as coral reefs and even submerged artefacts (Antonelli et al,2015).
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Figure 15

Conservation and Threats
The sipunculids have not been used as an  indicatory species of environmental deterioration, but having said that, some species of peanut worm have been  seen to be affected by, or even completely removed from areas because of anthropogenic disturbances (Cutler, 1994).

Specific to A.muelleri is the factor of shelter availability. A.muelleri are known to occupy spaces such as empty polychaete tubes, gastropod shells, and have even been known to bore into hard carbonatic substrata (Antonelliet al, 2015; Cutler 1994). Gastropod shells are important to the life cycle of A.muelleri as the occupation of gastropod  shells usually occurs by the juveniles of this species (Beesley, 2000). 

Work conducted by Ferrero et al (2013), found that sample plots with shelter had an abundance of A.muelleri ten times greater than sample plots without shelter.  This highlights the importance of shelter availability to this species, and inturn demonstrates that environmental disturbances that limit the availability of this resource could have a large impact on A.muelleri.

References

Antonellia, F., Perassoa,C., Riccib, S., and Petriaggib, B. (2015). Impact of the sipunculan Aspidosiphon muelleri Diesing, 1851 on calcareous underwater Cultural Heritage. International Biodeterioration & Biodegradation 100, 133-139.

Beesley, P. (2000). Polychaetes & Allies: The Southern Synthesis, CSIRO Publishing, Australia.

Cutler, E. (1994). The Sipuncula, Their Systematics, Biology and Evolution, Comstock Publishing Associates, Cornell University Press, New York.

Ferrero-Vicente, L.M., Marco-Méndez, C., Loya-Fernández, A., and Sánchez-Lizaso, J.L. (2013). Limiting factors on the distribution of shell/tube-dwelling sipunculans. Journal of Experimental Marine Biology and Ecology 446, 345-354.

Ferrero-Vicentea, L.M., Marco-Méndeza,C., Loya-Fernándeza, A. and Sánchez-Lizasoa, J.L. (2014). Observations on the ecology and reproductive biology of the sipunculan worm Aspidosiphon muelleri in temperate waters. Journal of the Marine Biological Association of the United Kingdom 94, 8:1629-1638.

Fonseca, A.C., Dean, H.K, Cortes, J. (2006). Non-colonial coral macro-borers as indicator of coral reef status in the south Pacific of Costa Rica. Revista de Biologia Tropical 56, 101-115.

Ger, B.A., Zeimal, E.V., Kratskin I.L. and Lavrenteva, V.V. (1977). Cholinergic mechanisms in the central nervous system of the sipunculid Physcosoma japonicum. Journal of Evolutionary Biochemistry and Physiology 13, 2: 152-156.

Gill, G.A. and Coates, A.G. (1977). Mobility, growth patterns, and substrate in some fossil and recent corals. Lethaia 10, 119-134. 

Hoeksema, B.W. and Best, M.B. (1991). New Observations on scleractinian corals from Indonesia. 2. Sipunculan-associated species belonging to the genera Hetercyathus and Heteropsammia. Zoologische Mededelingen (Leiden) 65, 15: 221-245. 

Jeuniax, C. (1969). Nutrition and Digestion. In: Florkin, M. and Scheer, B.T. (Eds.), Chemical Zoology, Academic Press, London, 88-89.

Klots, I.M., Klippenstein, G.L. and Hendrickson, W.A. (1976).  Hemerythrin: Alternative Oxygen Carrier. American Association for the Advancement of Science 192, 4237: 335-344.

Kouchinsky, A.V. (2000). Skeletal microstructures of hyoliths from the Early Cambrian of Siberia. Alcheringa: An Australasian Journal of Palaeontology 24, 2: 65-81.


M.E. and Todorovic, M. (Eds.), Proceedings of the International Symposium on the Biology of the Sipuncula and Echiuravol,  Naucno Delo Press, Belgrade, 1, 301–304


Peyrot-Clausade M, Chazottes V. (2000). La Bioérosion récifale et son rôle dans la sédimentogénèse à Moorea (Polynésie française) et à la Réunion. Océanis 26, 275–309.

Por, F.D. (1975). Boring species of Aspidosiphon (Sipuncula) on the coasts of Israel. In: Rice, M.E. and Todorovic, M. (Eds.) Proceedings of the International Symposium on the Biology of the Sipuncula and Echiura. Naucno Delo Pres, Belgrade, 301-304. 

Radashevsky, V.I. and Migotto, A.E. (2006). Photoreceptive organs in larvae of Spionidae (Annelida) and Sipuncula. Journal of Zoology 268:4, 335-340. 

Rice, M.E. (1969). Possible boring structures of Sipunculids. American Zooogist 9, 803-812.

Risk, M.J. and Summarco, P.W. (1982). Bioerosion of Corals and the Influence of Damselfish Territoriality: A Preliminary Study. Oecologia 52, 376-380.

Runnegar, B., Pojeta, J.Jr., Morris, N.J., Taylor, J.D., Taylor, M.E. and McClung, G. (1975). Biology of the Hyolitha. Lethaia 8, 181-191.

Ruppert, E.E., Fox, R.S. and Barnes, R.D. (2004). Invertebrate Zoology: A Functional Evolutionary Approach,7, Brookes/Cole, USA.

Stephen, A., and Edmonds, S. (1972). The Phyla Sipuncula and Echiura, 1, The British Museum (Natural History), London.  

Struck, T., Schult, N., Kusen, T., Hickman, E., Bleidorn, C., Mchugh, D. and Halanych, K. (2007). Annelid phylogeny and the status of Sipuncula and Echiura. BMC Evolutionary Biology 7:57, 1-11.

Trilbollet, A., and Golubic, S. (2011).  Reef Bioerosion: Agents and Processes. In: Dubinsky, Z and Stambler, N. (Eds.), Coral Reefs: An Ecosystem in Transition, 1, Springer, New York, 435-449.

Williams, J.A. and Margolis, S.V. (1974). Sipunculid Burrows in Coral Reefs: Evidence for Chemical and Mechanical Excavation. Pacific Science 28, 4: 357-359.