“The Sting’s the Thing”
Sea Slug Predators of Anemones and Hydroids
Have you ever inadvertently brushed past a stinging hydroid during a dive and some small part of your skin, being exposed, receives a searing sting? Or perhaps you have been enjoying the surf and a bluebottle’s tentacles have wrapped around your arm or chest and put a sudden and painful end to the day’s activities? It certainly beggars belief then, to learn, that there are animals that actually feed upon these, and related tormenting denizens of our marine world, ingesting those polyp’s stinging cells and all seemingly without repercussion. The tormentors are cnidarians and they belong to a large group that range from jellyfish to the reef-building corals.
The stinging or fire hydroid Macrorhynchia philippina. This species belies its seemingly innocuous feathery appearance and is well-known to deliver a sharp and severe wakeup call to the careless diver. Also a food source for the nudibranch Lomanotus vermiformis.
The Dendronotina nudibranch Lomanotus vermiformis, living its whole adult life upon and feeding on the fire hydroid Macrorhynchia philippina. It is well adapted for the lifestyle.
The sea slugs that prey upon soft and hard corals have been discussed in a previous NudiNote (see The Coral Eaters). There are other animal groups, also belonging to the cnidarians (Phylum Cnidaria), that sea slugs prey upon, including anemones, hydroids and siphonophores, that are discussed here.
Cnidarians and Nematocysts
A characteristic defining feature of all the cnidarians is the possession of cnidocytes. These are specialised single use cells that are chiefly concerned with: catching prey, or as a defence against predators, or even defending territory. They operate by forcefully ejecting a cnidocyst or nematocyst. Across the phylum there are approximately 30 types of nematocysts grouped into three main categories – penetrating, sticky and coiling. Those nematocysts that penetrate are hollow, usually barbed, and inject a toxin to immobilise their prey. These are the stinging cells. These nematocysts, according to the species that possess them, have a range of penetration power and also toxicity, the toxicity of course being dependent on the target’s susceptibility.
Sea Slug Cnidarian Predators
Almost all of the sea slugs that prey on cnidarians are cladobranch nudibranchs. Not all Cladobranchia however feed on cnidarians but the greater majority do. None of the Dorididea (dorid) nudibranchs feed on cnidarians. There is evidence that some species of the Pleurobranchoidea e.g. Pleurobranchaea spp, feed upon cnidarians. These sea slugs are generalist foragers not specialist feeders though, with the cnidarians being just one (but significant) of the wide range of animal types found within their stomach upon investigation.
The cladobranch Pleurolidia juliae spends its entire adult lifespan living and preying on the polyps of often just a single colony of the hydroid Solanderia fusca. Its body form and colouration ensure it is well camouflaged upon it.
The presence of Pleurolidia juliae can be betrayed however by its spawn, the white, yellow or pink egg spirals laid and wound around stems that have had all of their polyps stripped off and eaten.
An undescribed Pleurobranchaea species. The Pleurobranchaea spp. of the side-gilled Pleurobranchoidea order of sea slugs are generalist feeders known to consume cnidarian prey, the only sea slugs other than the cladobranchs known to do so.
Within the Cladobranchia:
The Aeolidina nudibranchs, all feed upon cnidarians of one type or another (except the oophagous Favorinus species) and we have previously dealt with those members preying on corals;
A small anemone that lives on algal fronds, in shallow waters with strong tidal currents or surge. It is one of the anemones hunted and preyed upon by the aeolid nudibranch Baeolidia moebii that moves through the dense algal growth searching them out. This encounter was captured in a photographic dish. Baeolidia moebii senses and approaches a small anemone, straddling it with its long oral tentacles. In the wild the anemone’s pedal disc is attached powerfully to an algal frond and is very difficult to dislodge. The anemone is secured by the oral tentacles of Baeolidia moebii, then drawn back towards the mouth and engulfed whole. In the wild the touching of the nudibranch’s oral tentacles causes the anemone to release its hold in order to escape but is then trapped by the overlapping tentacles.
Found wherever their prey hides. Cratena lineata can sometimes be found grazing on small hydroids growing on the underside of plate sponges such as shown here. At times there might be several feeding together.
Most of the Dendronotina too, are cnidarian predators and we have also discussed those members that prey on corals;
Left – A close-up of the dendronotinid Bornella anguilla feeding on Aglaophenia hydroids. In this image all the branches have been cropped off (arrowed) by its strong jaws as it moves up the stem of the hydroid.
Top right – A different hydroid, Pennaria sp., being preyed on by Bornella anguilla. I have observed at least four different species of hydroid being eaten by this Dendronotina nudibranch.
Lower right – Here the strong jaws of Bornella anguilla are visible clamped together within the buccal cavity. Most Aeolidina and Dendronotina nudibranchs that prey upon hydroids use their jaws to crop or slice off pieces for ingestion.
Above: Bornella anguilla eating hydroids. At one point the jaws of the nudibranch can be seen to be working upon the polyps.
Above: This video clip shows the jaw action of Bornella anguilla, gripping the hydroid branches and dragging them into the mouth for stripping by the radula.
The Scyllaeidae nudibranchs belong to the Dendronotina. Here, a member of that family, Notobryon wardi, hunts across the substrate for epiphytic hydroids, that is, small hydroids living on algal and seagrass fronds. Some of the family have a pelagic lifestyle on algae drifting in the open ocean.
Of the remaining group, the Arminina, we have discussed those members that feed on corals and sea pens and none of the remaining prey on other cnidarians.
Avoiding Harm
As to be expected, those that prey on anemones and hydroids need to have developed ways and means to avoid the potential harm, that crawling over and ingesting animals that possess such powerful toxic stinging cells, would engender.
– Those nudibranchs that prey on hydroids have a narrow body and foot that enables them to grip and move along the polyp-free stem or on the opposite side to the polyps on a branch, a combination of anatomy and behaviour that serves to minimise contact with those surfaces that have the reactive stinging cells.
An undescribed aeolid species, Eubranchus sp., living and feeding its whole adult lifespan on a hydroid colony, sustaining itself by consumption of the polyps. Here it is caught in the process of laying its small spiral of eggs upon the hydroid stem. The narrow body and foot are adaptations for moving along a thin hydroid stem or branch.
– Conversely those, like the Cerberilla, that burrow into the sand hunting for the likes of cerianthids (tube anemones) have a broad foot for that purpose and long oral tentacles for tactile sensing, but smallish rhinophores for water sampling.
– The buccal cavity and oesophagus of many nudibranchs that prey upon cnidarians have a hard cuticle covering for protection of the underlying epithelium.
– Mucus secretions not only assist the movement of food particles through the digestive system but can also act as a barrier against epithelial contact by essentially just smothering the nematocysts. It has been shown that the nudibranch’s mucus can also be augmented with compounds that are able to inhibit or reduce nematocyst discharge through a process of acclimation to a specific prey’s nematocysts. So if the targeted prey changes so too does the inhibitory chemistry of the mucus.
– Although many nudibranchs are in possession of them some aeolids in particular have a high concentration of intracellular ovoid discs, called spindles, within their outer skin and stomach epithelium. Upon receiving a discharge of nematocysts the spindles, composed of “granular” chitin, are released entangling the nematocyst’s tubules thus impeding their progress and reducing their effect. This is analogous to the reactive armour on modern military tanks that explodes outwards upon detecting an incoming projectile. Once again, nature is way ahead of us.
Feeding Methods
Nearly all of the Aeolidina and many of the Dendronotina use their jaws to slice or crop off segments of their cnidarian prey, the radula being used to drag those pieces further into the oesophagus. Species of Doto, belonging to the Dendronotina, however, feed by a different method, slashing open the stalks of the hydroids and sucking out the internal fluids.
The aeolid nudibranch Cratena lineata moves in to feed on a hydroid polyp (just out of focus) on its stem anchored in the substrate. The polyp will be lopped off and ingested.
The Dendronotina nudibranch Doto rosacea, feeds by slicing open the stalks and branches of its hydroid prey and sucking out the internal fluids. Species of Doto lack cnidosacs. Their method of eating denies them the ability to sequester nematocysts.
To generalise, those that hunt across the substrate for anemones and small hydroids tend to have longer oral tentacles the better to cover and sample a broader swathe of territory while those that live on large hydroids, that is, residing and spending their whole adult lifespan on their prey, may have oral tentacles that are quite short. Compare, for example, the oral tentacle lengths of Cerberilla ambonensis with Lomanotus sp., both pictured here.
Cerberilla ambonensis hunts across and burrows through the substrate, mostly at night, in search of cerianthids – tube anemones. It is highly adapted for the lifestyle. In this sequence it can be seen to dive beneath the silt and sand in pursuit of its prey that lives there. It disappears and re-emerges. This is a fascinating process to watch and not often observed.
An undescribed species of Dendronotina, Lomanotus sp., its narrow foot gripping the hydroid stem. The criss-cross pattern on its body serves to make it quite cryptic in amongst the tangled stems of a hydroid colony. Note the small oral tentacles. Species of the Lomanotidae family lack cnidosacs.
A highly adapted aeolid genus is Glaucus. They have adapted to the pelagic lifestyle by swallowing and maintaining an air pocket in their stomach thus making them buoyant to float, upside down as it happens, on the surface and feed on the floating siphonophores such as Physalia – Bluebottles, Velella – By-the-wind sailors and Porpita – Blue buttons.
The pelagic Glaucus bennettae nudibranch floats on the ocean surface together with its prey of siphonophores such as Physalia – the common stinging Bluebottle. As the bluebottle is devoured the nudibranch sequesters the stinging nematocysts for its own defensive use in cnidosacs at the tips of its cerata. Photographed here floating in the beach shallows having been blown inshore and washed up by strong and persistent onshore winds.
Kleptopredation
A recently described phenomenon that should be mentioned here is kleptopredation. Research on the feeding process of the aeolid nudibranch Cratena peregrina indicates that it is stimulated to feed upon polyps of its hydroid prey that have recently captured and are handling plankton. This plankton digestion is estimated to form at least half of the nudibranch’s diet. Additionally, this method of predation may afford a second benefit to the aeolid nudibranch in that the prey has just expended its nematocysts on a recent capture. The nudibranch is thus avoiding, or at least reducing, their effect upon them. This process has yet to be further investigated to ascertain if it applies to a wider species population.
Sequestration of Nematocysts
In dining on cnidarians most of the aeolids have not only evolved to manage the hypersensitive nematocysts to avoid being stung or injured but to also co-opt these stinging cells for their own defensive use. While this is a complex process, the detail of which is grist for a future NudiNote, a little information here will help place this strange capability into perspective. The nudibranch is able to sort the ingested nematocysts, selecting the type and maturity that are suitable for their purpose. Research has shown that immature nematocysts that are, as yet, incapable of discharging are selected for sequestration. This sequestration then involves transport through the digestive system and out to the tips of their cerata and storing in a cnidosac within special cells, called cnidophages, wherein they mature and are held ready for defensive use. At this point they are technically referred to as kleptocnides (which could be translated as “stolen stinging cells”). A “typical” aeolid cnidosac contains about 3,000 kleptocnides, so the defensive potential is significant. Muscles in the cnidosac contract and force the kleptocnides out of their cnidophages and the cnidosac where, resulting contact with seawater causes them to discharge. Not all are discharged at once allowing for more than one release. Interestingly, some research has indicated that certain aeolids are capable of altering the type of nematocyst they sequester through their diet, in response to the type of threat they detect in the region.
The aeolid nudibranch Spurilla braziliana feeds on anemones. The opaque white tips of its cerata indicate the location of the defensive cnidosacs that hold the stinging cells sequestered from their prey.
Flabellina (Coryphellina) lotos, its narrow foot gripping the hydroid stem, closes in upon a polyp that has withdrawn its tentacles in alarm. The many dozens of cerata each possess a cindosac that in turn carry many thousands of kleptocnides creating a massive defensive battery. A great deal of organisation is required to create and maintain this defensive system.
The possession of and therefore the availability of these stinging cells in the cerata for defensive purposes is complemented by behaviour to increase their effectiveness. Many nudibranchs with charged cnidosacs will suddenly erect and direct their cerata towards a perceived threat. This sudden startling action itself is termed deimatic or warning behaviour and depending upon species can be further enhanced by the possession of bold colouration and pattern on the cerata. The directing of the apex of the cnidosac-charged cerata towards the threat maximises the discharged concentration of the kleptocnides if extruded through the cnidopore.
Form and behaviour combining to produce both a warning and defense. A specimen of Unidentia erects and bristles its kleptocnide-charged cerata tips towards a perceived threat – deimatic behaviour. It can back up that threat by delivering a discharge of thousands of those kleptocnides into an attacker.
Of the aeolids, the oophagus Favorinus, the octocoral predators Phyllodsemium (Phyllodesmium jakobsenae apart) and the hard-coral predators Phestilla, whilst possessing cnidosacs, lack the kleptocnide content. There are other exceptions among the various genera that lack kleptocnides including Bulbaeolidia alba for example. A number of non-Aeolidina cladobranchs also possess cnidosac-like structures but only members of the Dendronotina family Hancockiidae have been recorded with kleptocnides present within.
The small aeolid Bulbaeolidia alba hunts small anemones on the substrate. It exhibits a distinctive rocking motion of its head as it moves forward. This species has residual cnidosacs at the ceratal tips but they lack the defensive kleptocnides.
David A. Mullins – August 2021
References:
– Thompson, T. E. & Bennett, I. (1970). Observations on Australian Glaucidae (Mollusca: Opisthobranchia). Zoological Journal of the Linnean Society 49, 187–197, pls. 1–2.
– Willan, R. C. (1984). A review of diets in the Notaspidea (Mollusca: Opisthobranchia), Journal of the Malacological Society of Australia, 6(3-4): 125-142
– Cattaneo-Vietti, B., Burlando, B. & Senes, l. (1993) Life history and diet of Pleurobranchaea meckelii (Opisthobranchia: Notaspidea). Journal of Molluscan Studies. 59, 309-313.
– Frick, K. (2003). Response in nematocyst uptake by the nudibranch Flabellina verrucosa to the presence of various predators in the Southern Gulf of Maine. Biological Bulletin, 205: 367–376.
– Greenwood, P. G., Garry, K., Hunter, A. & Jennings, M. (2004). Adaptable defense: a nudibranch mucus inhibits nematocyst discharge and changes with prey type. Biological Bulletin, 206: 113.
– Behrens, D. W. (2005). Nudibranch Behaviour. New World Publications, Florida, USA.
– Aguado, F. & Marin, A. (2007). Warning coloration associated with nematocyst-based defenses in aeolidoidean nudibranchs. Journal of Molluscan Studies, 73: 23–28.
– Greenwood, P. G. (2009). Acquisition and use of nematocysts by cnidarian predators. Toxicon.54:1065–70.
– Churchill C. K. C., Valdés Á. & Ó Foighil, D. (2014). Molecular and morphological systematics of neustonic nudibranchs (Mollusca : Gastropoda : Glaucidae : Glaucus), with descriptions of three new cryptic species. Invertebrate Systematics, 28, 174–195.
– Shipman, C. & Gosliner, T. (2015). Molecular and morphological systematics of Doto Oken, 1851 (Gastropoda: Heterobranchia), with descriptions of five new species and a new genus. Zootaxa 3973:57-101.
– Goodheart, J. A. & Bely, A. E. (2016). Sequestration of nematocysts by divergent cnidarian predators: mechanism, function, and evolution. Invertebrate Biology 136(1): 75–91.
– Goodheart, J. A., Bazinet, A. L., Valdés, Á., Collins, A. G., & Cummings, M. P. (2017). Prey preference follows phylogeny: evolutionary dietary patterns within the marine gastropod group Cladobranchia (Gastropoda: Heterobranchia: Nudibranchia). BMC Evolutionary Biology. 17(1).
– Willis, T. J., Berglo ̈f, K. T. L., McGill, R. A. R., Musco, L., Piraino, S., Rumsey, C. M., Ferna ́ndez, T. V. & Badalamenti, F. (2017) Kleptopredation: a mechanism to facilitate planktivory in a benthic mollusc. Biology Letters. 13: 20170447.
– Gosliner, T. M., Valdés, Á. & Behrens, D. W. (2018). Nudibranch and Sea Slug Identification: Indo-Pacific – 2nd Ed. New World Publications, Jacksonville, Florida.
– Goodheart, J. A., Bleidißel, S., Schillo, D. et al. (2018). Comparative morphology and evolution of the cnidosac in Cladobranchia (Gastropoda: Heterobranchia: Nudibranchia). Frontiers in Zoology 15, 43.
– Ponder, W. F. & Lindberg, D. R., with illustrations by Ponder, J. M., (2020). Biology and Evolution of the Mollusca, Volume One & Two. CRC Press, Taylor & Francis Group.
– This NudiNote has been modified from a previously published article in Dive Log Magazine’s – NudiNotes Column, Issue: #388 (June 2021): 44-46 by David A. Mullins.