title for limpet section of the Odyssey
   
  Defenses & predators
 

Defenses of limpets include attachment strength, shell, escape crawling, and camouflage (both visual and chemical). Chief predators are crabs, fishes, and sea stars when the tide is in, and birds when the tide is out. There is overlap between defenses and predators. For example, attachment strength is useful against predation by both sea stars and birds, and shells provide protection against both crabs and fishes. For this reason, defenses and predators are intermixed in this overall section.

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  Defenses of keyhole limpets
  The topic of defenses of keyhole limpets is considered in this section, and topics of ATTACHMENT-STRENGTH PROTECTION, SHELL PROTECTION, ESCAPE-CRAWLING FROM SEA STARS, PREDATION BY BIRDS, and DEFENSIVE CHEMICALS, CAMOUFLAGE, are considered in other sections. Defenses of keyhole limpets include camouflage, mantle response, and (sometimes) aggressive defensive activities of a symbiotic polychaete.
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Camouflage

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Research study 1
 

photograph of keyhole limpet Diodora aspera with tunicates growing on its shellphotograph of keyhole limpet Diodora aspera with different types of tunicates growing on its shellKeyhole limpets Diodora aspera are often richly adorned with growths of colonial tunicates, sponges, and bryozoans.  Whether this is for visual or chemical camouflage is not known. The individual in the photo on the Right seems visually camouflaged (to our eyes), but not the one on the Left.

  Here are 3 more examples of Diodora aspera with possibly camouflaging growths. All photos are of specimens living on current-swept promontories on islands in Barkley Sound, British Columbia. Diodora grows to sizes in excess of 6cm shell length:
  photograph of keyhole limpet Diodora aspera with different types of tunicates growing on its shell
With growths of colonial tunicates, mostly Distaplia occidentalis
photograph of a keyhole limpet Diodora aspera with tunicates, sponges (at the anterior end; Right), and sea anemones growing on its shell
With tunicates, sponges (at the anterior end; Right), and sea anemones
photograph of a keyhole limpet Diodora aspera with miscellaneous stuff, but mostly bryozoans, possibly Hippodiplosia insculpta, growing on its shell
With miscellaneous growths, but mostly bryozoans, possibly Hippodiplosia insculpta
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Mantle response

 
Research study 1
 

drawing of mantle response of keyhole limpet Diodora aspera from Margolin 1964 Anim Behav 12: 187photograph of a keyhole limpet Diodora aspera that has initiated its mantle response without  apparent contact with a sea star Orthasterias koehleriA unique defensive response is employed by keyhole limpets Diodora aspera against attack by sea stars.  Within moments after contact with a predatory sea star the limpet rises to twice its normal height and extends part of its mantle up and over the shell and another part downwards to curtain the side of the foot.  Additionally, the limpet extends its siphon up and out of the hole.  Probing tube feet of the sea stars appear to be unable to gain a hold on the mantle tissue and may even be chemically repelled by it.  About 20min after being stimulated the limpet recovers and the mantle is withdrawn. Contact is not required to initiate the behaviour, suggesting the involvement of some kind of water-soluble substance. Margolin 1964 Anim Behav 12: 187.

NOTE as seen in the sequence of images above, the rising-up response is not always so obvious as described here

A Diodora aspera has initiated its mantle response without
apparent contact with a sea star Orthasterias koehleri. Note
the extension of the posterior mantle tentacles by the snail

 

Some views of the mantle response of Diodora aspera:

  photograph of a keyhole limpet Diodora aspera with mantle response just beginning
Mantle response beginning. Note the siphon protruding out of the hole at the top 0.6X
photograph of a keyhole limpet Diodora aspera showing mantle response nearing completion
Mantle response nearing completion. The anterior end of the snail is at the Left 0.6X
photograph close view of a keyhole limpet showing mantle during extension
Close view of the extended mantle showing how it is drawn out into sensory "fingers" 4X
 
 
photograph of a keyhole limpet responding with mantle extenstion to touch of a sea star Orthasterias koehleri

CLICK HERE to see a video of a keyhole limpet Diodora aspera responding to touch by a sea star Orthasterias koehleri.

NOTE the video replays automatically

 
Research study 2
 

Studies at Friday Harbor Laboratories, Washington show that 9 of 17 species of sea stars tested induce a mantle response in Diodora aspera.  Is there a “commonality” to these species, perhaps phylogenetic, or dietary, or habitat? The 17 species are arranged in the first 2 columns below in colour-coded taxonomic categories of ORDERS, separated as to whether they induce a response (POSITIVE) or not (NEGATIVE):

 
POSITIVE
Pisaster ochraceus
Pisaster brevispinus
Pisaster giganteus
Leptasterias aequalis
Evasterias troschelii
Orthasterias koehleri
Pycnopodia helianthoides

Hippasteria spinosa
Asterina miniata
NEGATIVE
Mediaster aequalis
Dermasterias imbricata
Luidia foliata

Solaster stimpsoni
Solaster dawsoni
Pteraster tesselatus
Crossaster papposus

Henricia leviuscula


ORDERS
Order Forcipulatida
Order Valvatida
Order Velatida
Order Spinulosida

 

schematic showing morphological phylogeny of sea stars from Margolin 1964 Anim Behav 12: 187
How does this “Diodora-derived” classification accord with asteroid evolutionary relationships?  Well, in 2 phylogenies derived from morphological and combined morphological/molecular characters, respectively, the forcipulatids and schematic showing morphological/molecular phylogeny of sea stars from Lafay et al. System Biol 44: 190velatids/spinulosids) are placed in distant relationship while the valvatids are placed closer to the velatids/spinulosids, which accords to some extent with the Diodora-escape data. The splitting of the valvatids into both "positive" and "negative" response-columns, however, is awkward to resolve. Margolin 1964 Anim Behav 12: 187.

 



NOTE  of the 7 commonly recognised Orders of asteroids, the Forcipulatida is one of the largest and includes many common west-coast representatives. Approximate numbers of species in each of the 4 main Orders are as follows:

Forcipulatida: about 300 species in 68 genera, distinguished by their forcipulate (i.e., forceps-like) pedicellariae

Valvatida: about 400 species in 165 genera, often distinguishable by the presence of marginal ossicles, but the Order is quite diverse morphologically

Velatida: about 200 species in 25 genera, often characterised by thick bodies and large central discs

Spinulosida:  about 120 species in 9 genera


A final molecular phylogeny adds little, if anything, to what we have seen from the previous depictions:

  What about DIETARY AFFINITY? This seems promising, as all of the spinulosids in the "POSITIVE" column (with the exception of Pisaster brevispinus) would be expected to prey on keyhole limpets. However, of the 2 valvatid "POSITIVES", Hippasteria spinosa eats sea pens and Asterina miniata is an omnivorous scavenger of plant and animal matter (although it is recorded as preying on sea urchins Lytechinus anamesus and bryozoans in south- and mid-California, respectively). Of the species in the "NEGATIVE" column above, only Crossaster papposus is recorded as consuming snails, and then only a minor dietary component of populations in Alaska. The other velatids are fairly specialised on holothurians (Solaster stimpsoni), sea stars (Solaster dawsoni), and sponges/anemones/ascidians (Pteraster tesselatus). The spinulosid Henricia leviuscula is a ciliary plankton feeder that may also eat sponges/bryozoans. So, other than the odd-ball valvatids in the "POSITIVE" column, dietary affinity seems promising and may be deserving of closer scrutiny.
   
  Finally, what about HABITAT AFFINITY? The premise here is that keyhole limpets are more likely to respond to sea stars that they normally encounter in their day-to-day activities. There is actually so much overlap between habitats of Diodora aspera and these sea stars that only the sea stars NOT usually found sympatric with the keyhole limpet are highlighted ( light blue) in the columns below:
 
POSITIVE
Pisaster ochraceus
Pisaster brevispinus
Pisaster giganteus
Leptasterias aequalis
Evasterias troschelii
Orthasterias koehleri
Pycnopodia helianthoides
Hippasteria spinosa
Asterina miniata
NEGATIVE
Mediaster aequalis
Dermasterias imbricata
Luidia foliata
Solaster stimpsoni
Solaster dawsoni
Pteraster tesselatus
Crossaster papposus
Henricia leviuscula

The separation is somewhat arbitrary, and varies depending upon location, but it does show that there is little support for the "habitat affinity" idea. Species highlighted are ones that generally live on sand or mud, or that are found deeper tha Diodora.

One would expect habitat affinity to accord with dietary affinity, as it is unlikely that a particular sea star would evolve a "taste" for species never, or only rarely, encountered.

 

TAKE-HOME MESSAGE:  strongest support for the options offered comes from the “phylogenetic affinity” idea.  Clarification of this will benefit from identification of the chemical factor(s) produced by sea stars that induce the mantle response, and of the factor(s) produced by Diodora that repel the predators.  
 
NOTE  this topic is considered elsewhere in the ODYSSEY in relation to swimming responses of the sea anemone Stomphia spp. to different species of sea stars:  LEARN ABOUT SEA ANEMONES & RELATIVES: DEFENSES: SWIMMING

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Aggressive defensive activities of a symbiotic polychaete

 
Research study 1
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photograph of a keyhole limpet Diodora aspera with its symbiotic scaleworm Arctonoe vittata courtesy Dave Cowles, Walla Walla University, WashingtonKeyhole limpets Diodora aspera often carry a polychaete worm Arctonoe vittata within the mantle cavity between the foot and the outer shell margin.  It is commonly termed a “commensal” (i.e., gains benefit without harming the host) but, because its presence must incur costs to the host (occlusion of ctenidial gas-exchange surfaces, extra mass to carry, excretory and fecal contamination, possible food-robbing, etc.), it could also be thought of as a parasite.  However, the observation that the worm comes out to bite at tube feet of potential sea-star predators (with positive effect), its designation as a “mutual” might be more correct.  Photograph courtesy Dave Cowles, Walla Walla University, Washington rosario.wallawalla.edu.



Scalelworm Arctonoe vittata peeking out of the
mantle cavity of a keyhole limpet Diodora aspera

 
Research study 2
 

The first published account of Arctonoe’s unusual behaviour in coming to the defense of its host keyhole limpet appears to be from work done at Friday Harbor Laboratories, Washington.  On contact with tube feet of 3 sea-star species Pisaster ochraceus, Evasterias troschelii, and Pycnopodia helianthoides the limpet raises its mantle within 15sec, and the worm soon appears.  The worm inspects a tube foot for a moment, then bites at it.  A sea star usually responds to being bitten by withdrawing its tube feet and bending its arm away from the worm.  Interestingly, when isolated from its Diodora host and in the presence of a sea star, the worm does not bite at the tube feet.  The response does not seem to be a feeding one, because the tube feet are not bitten off, and when offered an isolated tube foot in a feeding experiment, Arctonoe does not eat it.  The fidelity of the biting response is species specific.  Thus, photograph showingcClose view of Diodora aspera in the process of raising its mantlein 10 tests with P. ochraceus, the worm appears and bites 8 times; however, in 10 tests with each of E. troschelii and P. helianthoides, the worm appears and bites only 2 times at each predator.  The authors suggest that an identifying chemical may be be involved, possibly one associated with the mantle response.  They also raise the question that if the behaviour is truly defensive and mutualistic, then why is there not a more “vigorous” response by the worm to attacks by Pycnopodia helianthoides which, of the 3 species tested, is the one most able to catch and eat a keyhole limpet?  Of the 3 species tested, it is also the one most likely to contact a keyhole limpet in its sublittoral habitat.  Clearly further work is needed on this interesting subject. Dimock & Dimock 1969 Veliger 12: 65.

 

 

Close view of Diodora aspera in the process of raising its mantle
taken from the photo in Research Study 1 above. But where is the
worm? If, indeed, the worm is there but not responding, it may
be because there has not yet been physical contact with a tube foot 1X

 
Research study 3
 

drawing of Y-tube apparatus used in tests of host fidelity with the worm Arctonoe vittata and keyhole limpet Diodora aspera from Gerber & Stout 1968 Physiol Zool 41: 169drawing of head of worm Arctonoe vittata from Gerber & Stout 1968 Physiol Zool 41: 169The worm is an obligatory symbiont with Diodora aspera, as well as with numerous other mollusc and echinoderm hosts.  Thus, it is the worm that is likely to be the one that seeks out a suitable host and not vice versa. An account of the relationship, done in Puget Sound, Washington, includes experiments to determine the organs of chemical perception being used by Arctonoe vittata to find its host.  In Y-tube choice experiments with Diodora aspera in one arm of the tube and Arctonoë vittata in the stem (see diagram), the worm is able to select the host-containing arm of the Y-tube with 100% fidelity (host arm: 20 vs. empty arm: 0, in 20 trials; see Table on lower Right). It is therefore obvious that some part of the worm is perceptive to a chemical1 emanation from Diodora, but which one?  The head bears 3 antennae, 2 pairs of tentacles, a pair of palps, and 2 pairs of eyes (see drawing upper Right). The protocol involves removing2 each set of organs in turn, followed by removing combinations, then testing in the Y-tube. 

table showing choice frequencies of worms Arctonoe vittata to host keyhole limpets Diodora aspera with parts of the worms extirpatedFirst is a check on effects of removal of the prostomial scales, which overlap some of the other sensory parts and therefore must be removed first to get access to these other organs. As shown in the Table above, the results are 20:0*, indicating highly significant3 selection of the host-containing arm of the Y-tube.  Thus, the prostomial scales appear NOT to be involved in host selection.  Removal of either palps or tentacles also does not significantly affect a worm's ability to find its host. However, removal of the antennae leads to a loss of this ability. To be sure, the researchers now remove combinations of sensory parts, including the antennae in each case. Note that removal of palps, tentacles in combination with the antennae, and removal of all 3 sets of organs, leads uniformly to a loss in ability of the worm to find the keyhole limpet. The antennae, therefore, are the most likely candidates to be the organs of chemical perception. Perhaps some mock extirpations could have been done as controls, but the data appear to support the author’s conclusion that the antennae are the organs responsible for perception of its host.  Gerber & Stout 1968 Physiol Zool 41: 169.

NOTE1  vision is not likely to be involved, as the eyes are only light-sensing – still, they should probably have been tested, just to be sure

NOTE2 after parts are extirpated, the worms are left alone for 8h to recover before being tested

NOTE3  significant Chi-square ratio for this sample size is 15:5 and greater (i.e., values closer to 20:0), indicated by * in the Table

 
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