The Journal of Experimental Biology

The Journal of Experimental Biology

Sponges are primarily bacterivores – few suspension feeders other

than flagellates specialize in capturing food less than 1 μm in size.

The filter consists of microvilli that are linked laterally by a fine

glycocalyx mesh 40–70 nm in diameter (e.g. Fjerdingstad, 1961;

Leys et al., 2011; Mah et al., 2014). In sponges, and in some

colonial choanoflagellates, neighbouring collars are also joined near

the upper end by a second mucus mesh or by cells (Weissenfels,

1992). The tightness of the resulting filter means that filtration is

efficient, and direct measurements of water filtered by sponges show

up to 100% removal of bacteria (Maldonado et al., 2012). The

sponge must therefore filter any particles that are in the water around

it, including inorganic detritus such as fine sediments disturbed by

fish or storms. Although the organic portion of resuspended material

might be used by the sponge as food, sponges are irritated by

concentrations greater than ~10 mg l

−1

(Gerrodette and Flechsig,

1979; Tompkins-MacDonald and Leys, 2008) and contract ostia

and/or canals during resuspension events, or in response to storms.

The main behaviour of sponges, apart from filtering, is to prevent

uptake of unwanted particles that might damage the filter: this

occurs either by contractions of canals or, in the case of glass

sponges, by arrest of the flagella pumps.

Sponges in all four classes – Calcarea, Demospongiae,

Homoscleromorpha and Hexactinellida – contract (Nickel, 2010),

and whereas contractions of the whole body take anywhere from

15 min to several hours, many sponges are constantly in motion,

contracting portions of their body and relaxing others (Bond, 2013)

(S.P.L., unpublished data). Contractions are usually triggered by

storm events (turbulent water) and increased sediment in the water,

but seasonal temperature changes (which are associated with

changes in many water column properties) also cause reduced

pumping and in some instances one species will stop pumping in

response to a spawning event by another species (Reiswig, 1971).

The greatest range of behaviour has been documented for

freshwater sponges, from contractions of the osculum only (McNair,

1923) to a periodic contraction of the whole sponge called a

‘condensation rhythm’ (Weissenfels, 1990), as well as a behaviour

that has been termed a ‘sneeze’ because of the biphasic inflation and

then contraction of the aquiferous system to expel unwanted

particles (Elliott and Leys, 2007). Larval behaviour is the other main

activity known from sponges: larvae change swimming direction

within seconds of a change in light intensity, some in response to

gravity and other stimuli (reviewed in Maldonado and Bergquist,

2002). Sponge larval responses are not very different to responses

seen by other invertebrate larvae that have nerves. How are they

carried out? And how do adult sponges detect and respond to

changes in water quality?

Neural toolkits

Sensory systems and conduction pathways

‘Systems’ and ‘pathways’ are terms that typically refer to a

constant morphological structure: tissues. Understanding that

sponges have ‘tissues’, which are groups of cells that are organized

together to carry out a particular function - is essential to be able

to consider and interpret evidence of the function of neural-like

elements. There are at least 16 different cell types in sponges

(Simpson, 1984) and whereas the function of some is well-known,

many have a name but unknown function and yet others, such as

archaeocytes, have subtypes whose function can only be identified

by their behaviour or gene expression (e.g. Funayama et al., 2010).

A number of types of sponge cells are organized and function

together as tissues, as in other animals. For example choanocytes

together with endopinacocytes form a highly effective, non-leaky,

filtration unit. Epithelia are formed by many subtypes of

pinacocytes, which form stable interactions. Those on the exterior

of the sponge (exopinacocytes) have been shown to possess

sealing junctions which allow the sponge to control the ionic

milieu of its extracellular matrix, as in other animals (Prosser,

1967; Adams et al., 2010). Transport pathways in Aplysina are so

distinct they can be lifted out of the sponge like a tendon (Leys

and Reiswig, 1998), and in many sponges the cortex is such a

distinct tissue of spicules, cells and ostia, it is termed a ‘rind’

(Boury-Esnault and Rützler, 1997). The most obvious tissue of a

sponge is the epithelium, which has the sensory cells and is

thought to be the conducting pathway.

Sensory cilia in the osculum

The osculum – excurrent chimney – is the most easily identified

structure in all sponges. It also seems to be the main organ for

sensing stimuli from the environment and triggering responses by

the whole animal. Short (4–6 μm long), non-motile, ‘primary’ cilia

have been found to line the inside of oscula in all sponges studied

so far by scanning electron microscopy (Fig. 2A–D) (Nickel, 2010;

Ludeman et al., 2014). Primary cilia are found on all cells in

vertebrates and many cells in invertebrates, and are involved in

sensing gradients of chemicals, light and flow (vibration) via ion

channels of the transient receptor potential (TRP) family (Singla and

Reiter, 2006).

Primary cilia in sponges are thought to function in a similar manner

to the balancer cilia in ctenophores, or the sensilla of crustaceans, or

the cilia on mammalian kidney epithelia by sending a signal, via a

calcium wave, in response to a change in position of the cilium

(Singla and Reiter, 2006). In sponges, primary cilia label with FM 1-

43, a steryl dye, and also with a conjugate to the antibiotic neomycin

sulphate, both non-specific calcium channel blockers (Ludeman et al.,

2014; Fig. 2E,F), as do primary cilia in the lateral line of fish and

inner-ear hair cells (Ou et al., 2009). The cilium is non motile and

lacks a central pair of microtubules (Ludeman et al., 2014; Fig. 2G,H).

Our understanding of the sensory role of primary cilia in animals and

unicellular flagellates such as Chlamydomonas comes from

behavioural assays (Fujiu et al., 2011). In the sponge, removing the

whole osculum, or removing the cilia using chloral hydrate, eliminates

the ability to respond to triggers of the ‘sneeze’ behaviour, the

stereotypical inflation–contraction response that freshwater sponges

use to rid themselves of wastes (Elliott and Leys, 2007). This links

both the osculum and the cilia in the osculum with the sneeze

behaviour. Furthermore, neomycin sulphate, FM 1-43 and gadolinium

all reduce or block the ability of the sponge to carry out a ‘sneeze’ and

the effect is reversible (Ludeman et al., 2014). The fact that cilia

appear at the osculum of all sponges studied so far (even

hexactinellids), suggests that this is a common sensory organ in

Porifera.

Sensory cells in the larva

Sponge larvae come in a great range of forms, but are largely

ciliated propagules, up to 3 mm in length; they often have

differentiated anterior–posterior ends and may swim or crawl,

usually rotating as a result of the metachronal beat of short cilia

(Fig. 2I; Maldonado and Bergquist, 2002). In laboratory

environments they are typically short-lived, settling within 12 h to

3 days, but in situ they may live much longer. Sponge larvae show

phototaxis and geotaxis (Maldonado and Bergquist, 2002).Where

phototaxis has been studied in depth, directional swimming has been

shown to occur by a combination of rotation of the larva around its

anterior–posterior (A–P) axis and the shading by pigment of a

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REVIEW

The Journal of Experimental Biology (2015) doi:10.1242/jeb.110817

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