It is well established that many marine sponges are host to and have a symbiotic relationship with a wide variety of microorganisms. Often these bacteria live within the sponge mesophyl, though it varies whether this is intra- or extracellular. It is considered that in high-microbial-abundance-sponges (HMAS), microorganisms makeup about 40-60% of the total sponge biomass, the “bacteriosponge”, whereas this is much lower in low-microbial-abundance sponges (LMAS) (Khan et al, 2014).

Whilst this is a growing area of research, it remains difficult to harvest and cultivate the bacteria (Sipkema et al, 2011). Moreover, currently little is really known about the nature of this symbiotic relationship, and how sponges acquire and maintain the specific bacteria.

Sipkema et al, (2009) studied the bacterial symbionts of Haliclona gellius and concluded it is most likely a LMA sponge. LMAS are usually smaller and less dense than HMAS (Khan et al, 2014). Details of the specific bacteria and densities may be found in their study.

Sponge bacterial symbionts are of particular interest because of their production of potentially useful bioactive compounds, of which there is a vast array. They may have properties such as,antimicrobial, antiviral, antioxidant and antitumor (Faulkner, 2002). Khan et al, (2014) believe that species of Haliclona may be a rich source of ‘novel bacteria’. In their study they found bacteria from Haliclona sp. to be producing novel polyketides. Polyketides are a large family of structurally diverse natural products, which may be useful to the pharmaceutical industry (Khan et al, 2014).

Sponges have an important role to play in the recycling of dissolved organic matter (DOM) in what otherwise may be a nutrient poor oligotrophic coral reef ecosystem. Coral reef crevices and cavities are known to be major sinks of DOM but the microbial loop is insufficient to explain DOM removal on coral reefs.

Through their filter feeding, sponges are able to uptake DOM from the water column. Sponges respire only 42% of the carbon from their uptake, and it is believed that the remainder goes into a rapid tissue turnover.  Choanocyte cells divide every 5- 6 hours and thus this is accompanied by a rapid shedding of old choanocyte cells. This cell shedding produces particulate organic matter (POM), or detritus. This available detritus material in the water column is consumed by detritivores (e.g. small crustaceans) which thus provides an energy source for the higher tropic levels up the trophic web. This process has become known as the “sponge loop” and is depicted in Figure 2.  

(Goeji et al, 2013).

This process has not been documented for Haliclona gellius specifically, however it is a reef dwelling sponge and the choanocyte ultrastructure and basal apparatus has been described as almost constant across adult sponges (Woollacott and Pinto, 1995). Thus, it is likely that Haliclona gellius does have this functional role in nutrient recycling for coral reef ecosystems. Additionally although Haliclona gellius preferentially inhabits cold waters, the “spongeloop” has now since also been documented to occur in cold water coral reef ecosystems (Rix et al, 2016). 

The aquiferous system, characterizes sponges. It functions as their feeding, excretion, respiration, gamete release and transport systems. Flagellated collar cells (choanocytes), beat their flagella and draw water into inhalent canals through small pores called ostia. The water is eventually drawn into choanocyte chambers where suspended food particles and oxygen are trapped and filtered by particular cells. This filtered water is then passed out through a series of exhalent canals and eventually leaves the sponge through its oscula. The aquiferous system is flexible and can easily be rearranged (Ereskovsky, 2010).

As is the case for most sponges, Haliclona gellius has a leuconoid structured aquiferous system (Figure 9).This structure is the most complex, consisting of a net like structure of small-diameter incurrent and excurrent canals between choanocyte chambers of flagellated collar cells. Leuconoid sponges are densely packed with many choanocyte chambers. This structure allows sponges to grow large in size whilst still maintaining a high surface area to volume ratio for obtaining the nutrition they require for their size (Ruppert et al, 2004). 

The specific reproductive and development strategies for this specimen have not yet been described. However there have been some detailed studies on a few species of Haliclona. Additionally, the Australian coral reef sponge, Amphimedon Queenslandica (Degnan et al, 2015) has been extensively studied, and considered to be a close relative, based on 18s rDNA sequence analysis (Sipkema et al, 2009).

Most species within Haplosclerida are oviparous, with some being gonochorich, and others hermaphrodites. Sexual reproduction is most often alternated with asexual blastogenesis (gemmule production) throughout the Haploscerida life cycle (Ereskovsky, 2010). Both mechanisms are outlined below. 

Sexual

Spermatogenesis occurs via spermatocycts diffused within the choanosome by the same process that is common to most demospongae. It has not yet been studied from which cells male gametes are derived in marine Haplosclerids, but for their freshwater varieties and all other demosponges, (except carnivorous poecilosclerids), they derive from choanocytes within the choanocyte chambers. The newly formed spermatocysts fuse with exhalent canals, and once mature are released into the water column through their canal lumens.

It is believed that female gametes, by the process of oogenesis are derived in nucleated ameobocytes or choanocytes diffused in the choanosome. A distinguishing feature for Haplosclerida oogenesis, is the presence of “nurse cells” (or “trophocytes”).  These are somatic cells and provide the yolk source for oocytes during vitellogenesis. This “nurse cell” presence indicates a higher level of oogenesis specialization within Haplosclerida.

Most haplosclerids are oviparous, with internal fertilization. However, little is known about the cleavage process for marine Haplosclerida as, with the eggs and blastomeres full of yolk granules (from the “nurse cells”), dividing nuclei and blastomere borders are concealed from view.

After cleavage is the morula stage, and differentiation of cells for larval structure formation. Often in haplosclerids sclerocytes are the first cells to differentiate and begin functioning.  

(Ereskovsky, 2010) 

The larvae settle, anterior pole first, attach to the substrate and under go metamorphosis, which is completed by their development of a functioning aquiferous system (Ereskovsky, 2010).

Chalidinae larva is paranchymella and it may be uniformly ciliated or have extended cilia on its posterior (Hooper and weidenmayer, 1994). Paranchymella larva have all or some of the spicule types seen in its adult form (Simpson, 1984). 
Interestingly it has been suggested that larval morphology may be a useful character in determining sponge taxonomy (Levi,1956). In a study of Haliclona indistincta (Stephens et al, 2013) they were able to distinguish the larvae as H.indistincta because of their sticky characteristic, and they suggest this may be a useful feature within sponge taxonomy. Moreover, Haplosclerida larva have a number of distinguishing features (Figure3) which can be diagnostically useful; absence of ciliated cells in the posterior pole, which is encircled by cells of elongated cilia, a skeleton of densely bundled oxeas in posterior portion, and a concentration of pigment cells at the posterior end, either within the long ciliated cells or the non-ciliated cells (Ereskovsky, 2010). This reflects how there is a wide range of taxonomic features that may be useful in sponge identifications. These could be especially useful in this case, where it is not possible to use the usual features (e.g. ectosomal skeleton) due to the juvenile nature of the sponge. However Stephens et al, (2013) do note that further morphological data on larva is required and thus indicate the infancy of which much sponge research remains and perhaps why sponge taxonomy is so challenging.

Asexual

Asexual reproduction in sponges can be via gemmule production, fragmentation, or budding, however budding is generally not considered a characteristic in Haploscerida and thus is not documented here.

Fragmentation occurs mostly when a sponge has been damaged in wave or current action and fragments break off. Dislodged fragments can reattach to the substrate and re-order itself into a functional sponge (Ruppert et al, 2004).

Gemmules are produced by some marine Chalinidae and occurs occurs after the completion of sexual reproduction.

Gemmule trophocytes, archaeocytes and spongocytes migrate and densely aggregate in specific parts of the mesophyl. Archaeocytes begin phagocytosing trophocytes and yolk plates develop, consisting of flattened archaeocytes internally, and flattened spongiocytes externally. A Gemmule envelope then begins to form spreading from one pole to the other. Prior to hatching, thesocytes synthesize collagen ready for substrate attachment. After hatching the gemmule attaches to the substrate and differentiation of totipotent thesocytes begins.

Gemmule germination may be triggered by a range of external factors, such as temperature, humidity, illumination and ionic composition of water etc. Though in cold climates germination can only occur after a certain lapse of time, diapause.

Gemmules are well adapted to extreme environments, for instance they are capable of germinating after 2 months of exposure to -80°C and -100°C. Additionally 25% of gemmules have shown the ability to survive 4 months at +5°C out of the water.

(Ereskovsky, 2010). 

Gellius oxeas are usually long and stout with hastate (narrow/spearhead) ends. Microslceres, are not always present, but may be, sigmas, toxas or raphides (or a mixture) (Hooper and Van Soest, 2002). Usually microscleres are easily distinguished by their size and morphology, and megascleres, although less easily identified, can be done so based on morphology (Simpson, 1984). 


This specimen has...

Thank you to Anita George from the Queensland Museum for helping to provide spicule identifications and many of the photos of this specimen. 

Haplosclerida have a siliceous skeletal structure that may include either or both a choanosomal skeleton and ectosomal (surface) skeleton.The study species here is a juvenile and thus has not yet developed the ectosomal skeleton which is so crucial for species level identification within this group (Fromont, 1993).

The skeletons of Haplosclerida are delicate and usually a simple unispicular reticulation, connected by spongin or a network of fibers in which spicules are incorporated (Fromont, 1993).

The choanosomal skeleton of Chalinidae is described as a confused, isodyctyal (triangular patterned) structure consisting of pauci- to multispicular primary lines that are connected irregularly at nodes of collagenous spongin (Hooper and Wiedenmayer, 1994) by unispicular lines (Hooper and van Soest, 2002). More specifically Gellius has an anisotrophic, ladder-like structure, consisting of uni- or paucispicular ascending primary lines. They may regularly or less regularly be connected by unispicular secondary lines (Hooper and Van Soest, 2002).

The original Chalinidae definition by Gray (1867), was based only on the choanosomal skeleton, however (Weerdt, 1986) later revised this to include an ectosomal description in this definition (Fromont, 1993). Characteristics of the ectosomal skeleton have been useful in family level classification. This really highlights, not only the importance of skeletal structure, but also the changing nature of sponge taxonomy.

Weerdt’s (1986) definition for the ectosomal skeleton was, ‘if present, a unispicular tangential reticulation’. For Chalinidae if present, Hooper and Van soest (2002) describe it to be either a tangential, unispicular, isotrophic reticulation, or to consist of irregularly strewn, tangentially orientated spicules. 

Cross sections depicting the specific cell structure of the study specimen here are displayed in Figures 16-22. 

Demosponges have two epithelial cell layers, pinacoderm and choanoderm.

It is of some debate as to whether these cell layers may be considered as “true” epithelial layers. The traditional definition for epithelium requires there to be the presence of a basal lamina and junctions between the epithelial cells (Stephens et al, 2013). However, more modern definitions recognize that the sponge epithelial layer forms a very similar function as those deemed as “true” epitheliums in other animals and thus must be considered as such. This of course may have an impact on the phylogeny of sponges within the metazoan lineages.

Pinacoderm is formed from pinacocytes (flattened cells) which make up the external layer of the aquiferous system and some of the internal cavities. Choanoderm, consisting of the flagellated collar cells (choanocytes) lines the choanocyte chambers. Between the outer layer of the pinacocytes and the aquiferous system, is the mesophyl (Ereskovsky, 2010).

The mesophyl, an extracellular matrix between the internal pinacoderm layer and flagellated collar cells is a dynamic cell layer, with the capacity to constantly remodel itself. It is highly variable and contains a vast variety of cell types for different functions, many of which have yet to be determined (Simpson, 1984). The functions of these cells collaboratively create major parts of the skeleton, including minerals, collagen and ground substance (Simpson, 1984). Some of the most significant mesophyl cell types have been outlined below. 

Archeocytes – Polyblasts – Thesocytes

These cells all have a very similar structure and function. It is actually considered that they do not have a specific function, but generally it is said they are involved with the storage and processing of nutrients. Interestingly, they are pluripotent or have an embryonic nature meaning they can potentially develop into any sponge cell type e.g. for growth or gamete formation. However the specific cells that they develop into varies for each sponge species, and unfortunately this has not been studied for the study species here (Simpson, 1984).  

Lophocytes                                                                                                                                         
Considered to have archeocyte type properties and functions, there is no complete agreement on the function of this cell type. Some consider it to be a transient stage of an archeocyte, whilst others believe lophocyctes to specifically function as cells to biosynthesize collagen (Simpson, 1984).

Trophocytes                                                                                                                                             
These function as a source of nutrients for archeocytes during gemmule production in asexual reproduction. Additionally they are involved with providing nutrients for developing oocytes, as mentioned in the reproduction section. However in that case they can be considered as “nurse cells’ in order to avoid confusion (Simpson, 1984).

Sclerocytes                                                                                                These cells are responsible for secreting the mineralized megascleres and microscleres (Ruppert et al, 2004).                                                                                                                                      
Spongocytes                                                                                                                                           
These cells secrete collagen that polymerizes into thick fibre, called sponging (Ruppert et al, 2004).                                                                                                                                                 
Choanocytes                                                                                                  Otherwise known as flagellated collar cells, they generate the water flow through the sponge aquiferous system (see‘Life History and Behaviour’) with their pumping flagellum (Ruppert et al, 2004). 

The solution, in order to place the Australian species, was to use an amalgamation of previous Chalinidae revisions, even with the knowledge that Haliclona itself is an ‘unmanageable and heterogeneous’ genus (Hooper and Wiedenmayer, 1994). Taxonomic characteristics, such as larval morphology have been suggested as useful diagnostic tools to aid the classifications (Levi, 1956; Ereskovsky, 2010). However this of course requires an in depth knowledge and data on sponge larva morphologies, which is still being developed. 

Langenbruch and Jones (1990) further the disagreements by demonstrating that even the order, Haplosclerida is not polyphyletic and contains sponges suggested to be of poecilosclerid origin. Unlike most demosponges, in the majority of haploscredia the choanocytes do not touch the mesohylar tissue and are mostly directly covered with pinacocytes of the incurrent canal walls. However Lengenbruch and Jones (1990) show that this is not the case in Haliclona indistincta, whereby the choanocytes are in contact with the mesohyl on their outer surface and thus suggest a polyphyletic order.