The Journal of Experimental Biology

The Journal of Experimental Biology

586

calligraphy ink. Ink clogs the canals and it takes the sponge some

hours to remove it, but the effect of ink is informative because the

repeated inflation–contraction events eventually push the undigested

and mucus-coated clumps of particles out of the osculum to litter the

bottom of the dish. Whereas shaking causes the osculum to contract,

70–80 μmol l

−1

L

-Glu causes the osculum to contract vigorously and

triggers the full stereotypical inflation–contraction (‘sneeze’)

behaviour in Ephydatia muelleri (Fig. 3B,C) (Elliott and Leys,

2007). Higher concentrations caused such a vigorous contraction

that the top of the sponge tore, although the canals continued

through their full inflation and contraction.

Two glutamate receptor inhibitors, AP3 (a competitive inhibitor)

and kynurenic acid (Kyn, a non-competitive or allosteric inhibitor)

both blocked the sneeze behaviour in a concentration-dependent

manner (Elliott and Leys, 2010) (Fig. 3D). These experiments

suggested that clogging of chambers with dye must trigger stretch

receptors or reduce flow enough to make the sensory cells in the

osculum (Ludeman et al., 2014) respond and cause the osculum to

contract; the hypothesis is that glutamate receptors lie at the base of

the osculum and along the entire epithelium of the sponge incurrent

canal system. Transmission is presumed to be by localized release

from cells into the mesohyl, then binding mGluR receptors, which

triggers calcium to enter neighboring cells, which in turn release

glutamate, much as envisioned by Nickel (Nickel, 2010). There are

at least three mGluR candidates for this in the sponge (Sakaraya et

al., 2007). GABA applied directly causes the sponge to flinch, but

incubation in GABA (1 mmol l

−1

) for 10 min prevents any sneeze

when stimulated either by shaking or by 

L

-Glu (70–80 μmol l

−1

)

(Elliott and Leys, 2010).

Many molecules are known to trigger contractions of the osculum,

ostia or whole body of sponges (Emson, 1966; Prosser, 1967;

Ellwanger et al., 2004; Ellwanger and Nickel, 2006). Tethya wilhelma

has pacemaker-like activity with repeated innate contractions every

hour to several hours depending on the individual. Contractions can

also be triggered by a suite of chemicals including caffeine, AchE,

nicotine, nitric oxide, cAMP and serotonin (Ellwanger and Nickel,

2006). Although no molecules prevent contractions in Tethya and

most trigger an immediate contraction, some molecules have an

interesting modulating effect – for example, NOC-12 a nitric oxide

donor and caffeine both reduce the amplitude and period of the

contractions (Ellwanger and Nickel, 2006). Bath application of

chemicals can also have very different effects on different sponge

species: in Tethya, for example, both glutamate and GABA clearly

trigger abrupt contractions of the sponge (Ellwanger et al., 2007),

whereas in Ephydatia, GABA distinctly inhibits contractions (Elliott

and Leys, 2010). We do not yet know the role of aspartate, histamine

or ATP in sponges and this is where continued research should focus.

The role of biogenic amines (e.g. catecholamines dopamine,

epinephrine and norepinephrine) in signalling in the sponge is

unclear. Bath application of both dopamine and epinephrine causes

contractions (Prosser, 1967; Ellwanger and Nickel, 2006) and

portions of the catecholamine synthesis pathway were found in

most, but not all, of eight sponge transcriptomes, yet the complete

pathway was not found in any sponge transcriptome or genome

(Riesgo et al., 2014). It is possible that some of these molecules are

so divergent that they remain undetected with BLAST searches.

Neuropeptides have not yet been found in sponges, although as

with catecholamines, some enzymes of the synthesis pathways are

REVIEW

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

75

70

80

90

60

100

40

50

30

Time (min)

Canal diameter

(relative change)

B

Time 

Responsiveness

25 µmol l

–1

50 µmol l

–1

100 µmol l

–1

150 µmol l

–1

10 s

10 s

Osculum

Choanosome

Time

Area

A

C

D

0

10

20

30

ASW

ASW

Sr

2+

(CaM-free)

Mg

2+

(Ca

2+

-free)

CaM-free

K

+

(no Na

+

)

20% Na

+

Na

+

-free

[Kyn]

Fig. 3. Ionic basis of contractions in freshwater

sponges. (A) Substitution of sodium (top panel) and

calcium and magnesium (bottom panel) in marine

sponges (after Prosser, 1967). Solid line (both

panels): ASW control. Top panel: dotted blue line,

80% reduction in sodium (sodium replaced with

sucrose); dashed green line, no sodium, 100%

sucrose; dash-dotted red line, potassium instead of

sodium. Bottom panel: dotted blue line, magnesium

but no calcium; dashed green line, neither calcium

nor magnesium; dash-dotted red line, strontium

instead of calcium and magnesium. (B) Contraction

of the osculum (left) and choanosomal region with

feeding chambers (right) of Ephydatia muelleri with

tracings showing the time of both events below.

(C) Concentration-dependent effect of glutamate on

the inflation–contraction behaviour of E. muelleri. A

full ‘sneeze’ is triggered by 75 μmol l

−1

L

-Glu; lower

concentrations generate localized contractions and

higher concentrations cause the surface of the

sponge to tear, whereas the canals continue a full

inflation–contraction event (from Elliott and Leys,

2010). (D) Concentration-dependent effect of

glutamate blocker kynurenic acid on contractions in

E. muelleri. Longer incubation in Kyn reduces

responsiveness to 

L

-Glu, even at lower

concentrations of the inhibitor. High concentrations of

the inhibitor block all contractions.

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