Feeding & growth
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Prey handling & drilling

  The section on feeding & growth is divided into prey handling & drilling, considered here, and DIETS, PREY CAPTURE, and GROWTH, considered in other sections. 
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Research study 1

photograph of borehole in butter clam Saxidomus giganteus made by an octopus Enteroctopus dolfleiniIt may be a surprise to learn that octopuses can drill their shellfish prey and inject a toxin. Drilling by octopuses is first described on our coast for Californian Octopus spp. preying on abalone Haliotis fulgens, and on other molluscs including mussels, chitons, and Chlorostoma (Tegula) snails.  An octopus’s arms and suckers are greatly outmatched by the clamping forces of an abalone’s foot.  Still, it takes about 3h for an octopus to drill a 0.6mm conical hole in the shell, through which a toxic salivary-gland secretion is then injected.  Experimental injection of small volumes of prepared octopus toxin into abalone and crabs lead to quick, convulsive, death.  Although the authors note “hard wear” on the central cusps of the radulae of the octopuses used in the California study, often to a state of being worn completely flat, later studies by other authors on the drilling process show that the radula is not actually involved in the drilling.  Pilson & Taylor 1961 Science 134: 1366. Shell for photograph kindly provided by Brian Hartwick, Simon Fraser University, British Columbia.

NOTE  worldwide, the behaviour was earlier described for Octopus spp. preying upon pearl oysters in Japan and is reviewed generally for the Atlantic species O. vulgaris byFujita 1916 Dobytsugaku Zusshi 28: 250 and Wodinsky 1969 Am Zool 9: 997

Research study 2

photograph of a moon snail-drilled littleneck clam Protothaca stamineaCollections of dead shells of littleneck clams Protothaca staminea and black turban snails Chlorostoma (Tegula) funebralis in the North Reef area near San Diego reveal that about two-thirds of each are drilled by octopuses.  Fotheringham 1974 Limnol Oceanogr 19: 84.

Littleneck clam Protothaca staminea drilled in the umbo region.
This hole, however, is caused by a moon snail Euspira lewisii.
Not only is it much larger in comparison with a hole produced
by an octopus, but it has the countersunk appearance characteristic
of moon-snail attack 3X. CLICK HERE for more on moon-snail drillings

Research study 3

drawing of radula/salivary papilla of an octopusphotograph of a drill hole made by octopus Enteroctopus dolfleini in a shell of a cockle Clinocardium nuttallii“Drilling” is not the correct term to use.  Rather, the octopus applies the tip of its paired salivary papillae to the prey.  There are small teeth at the end of the papilla as well as within its inverted end.   A duct joins the papilla tip with the posterior salivary glands.  When the tip of the papilla is in position, perhaps aided by gripping with the small teeth, the octopus releases a small dribble of salivary secretion that contains both a calcium-carbonate dissolving agent and deadly tetrodotoxin.  As the secretion works its way into the shell of a bivalve, photograph of a borehole in a bivalve shell made by an octopusperhaps aided by rasping of the small teeth, it creates a conical opening starting at about 1mm in diameter and terminating on the inner shell at less than half that size (see photographs).  The economy of the operation is testimony to the effectiveness of the toxin.  Once the shell integrity is breached, death of the prey is virtually instantaneous.  Nixon 1980 J Zool, Lond 190: 53. Shells with boreholes made by Enteroctopus dolfleini kindly provided by Brian Hartwick, Simon Fraser University, British Columbia.

NOTE  this work is done on the European Octopus vulgaris, and is presented here to generate ideas on research to be done on our west-coast species

NOTE  this is likely to be enzymatic rather than acidic, possibly carbonic anhydrase.  Calcium carbonate is the principal component of mollusc shells and also comprises about 65% of crustacean exoskeleons

study 4

Octopuses open shellfish prey by breaking the shells or carapaces of snails and crustaceans, pulling apart the valves of clams, and by pulling the bodies of snails from their shells.   Each of these methods may be accompanied by a hole being drilled and toxin being injected. Numerical estimates on the methods used by octopuses can be obtained by collection and analysis of prey items from den middens.  Of 905 items collected in one such study of giant octopuses Enteroctopus dofleini at sites on Vancouver Island, British Columbia, 223 (25%) are crabs Cancer spp., and most of the remainder are bivalves (<1% are gastropods, made up entirely of moon snails Polinices lewisii).  Of the bivalves, 387 (43% of the total of 905) are cockles Clinocardium nuttallii, with 9 other species making up the remaining 31% (295 items) of the prey items found.  Examination of the prey shows that bivalves are mostly pulled apart (78%) or broken (18%).  Moon snails are mostly drilled and their bodies pulled out of the shell.  Cockles are mostly not drilled (only 1%), while the next most abundant bivalve prey, littleneck clams Protothaca staminea, are 20% drilled.  This likely relates to difference in force required by the octopus to open a littleneck clam by pulling apart the shell valves in comparison with that required for a cockle.  In some instances drilled, but live, prey are found, indicating that toxin is not always injected or that not enough toxin is injected to be lethal.  Hartwick et al. 1978 Mar Behav Physiol 5: 193.

NOTE  the toxin, known originally as maculotoxin, is now confirmed to be a type of tetrodotoxin, also found in pufferfishes, some amphibians, and a few reef fishes.  It is a potent neurotoxin causing paralysis and ultimately death if administered in sufficient quantity.  Tetrodotoxin is the active “ingredient” in fugu or photograph showing shell remains of prey around an octopus's den Enteroctopus dolfleiniJapanese sashimi pufferfish.  Specially licensed chefs prepare fugu in such a way as to avoid the most toxic parts, the liver and gonads, while cutting slivers of muscle tissue from as near to these organs as possible.  Fugu patrons pay exorbitant prices in order to have their lips and fingertips tingling after a meal, but not, of course, to be killed.  A few deaths occur each year from consumption of improperly prepared fugu

NOTE  an early study of the toxin in Enteroctopus dofleini shows that it is a peptide of molecular mass 23,000 Daltons and that boiling it for 10min destroys its effects.  When injected into crayfishes through an arthrodial membrane into the hemocoel, the crustaceans become flaccid, lose the ability to right themselves, and eventually die.  The toxin is a neurotoxin that interferes with sodium-channel function.  At concentrations of toxin about one-third that causing death, a crayfish becomes lethargic and loses its righting ability, but can recover from the effects in 3-12h.  Songdahl & Shapiro 1974 Toxicon 12: 109.

Shell remains around the den of octopus Enteroctopus dofleini 0.33X
Research study 5

photograph of a borehole made by the octopus Enteroctopus dolfleini in a butter clam Saxidomus giganteusIf the radula is removed surgically, the octopus can still drill holes in its prey, and the holes are similar in shape and size to those done by control, intact octopuses.  However, if the salivary papillae are removed, no drilling is possible.  The radula functions as in other molluscs, as a rasp to tear flesh from prey once the beak and/or salivary papillae have done their jobs.  Ambrose et al. 1988 J Zool, Lond 214: 491.

An incomplete borehole made by an octopus Enteroctopus
in a butter clam Saxidomus giganteus.  
The walls are smooth-sided and tapered 40X

Research study 6

photograph of a pouncing octopus Enteroctopus dolfleiniJust prior to capturing a prey, Enteroctopus dofleini may extend the first pair of arms in a splayed-out fashion, with the tips in contact with one another.  An attack may culminate in “parachuting”, where the arms splay along the body, the web is extended outwards between the arms, and the octopus jets towards its prey. Mather 1998 J Comp Psychol 112: 306.






Parachuting attack by octopus
Enteroctopus dolfleini in an aquarium tank 0.1X

Research study 7

schematic drawings showing borehole disposition on crab carapaces made by octopuses Enteroctopus dolfleini in Prince William Sound, AlaskaCrabs are also drilled.  Drill-hole locations are commonly in the posterior part of the carapace, abdominal flaps, and claws.  Although the octopus has to dismember the crab anyway to eat it, drilling and injection of toxin may be a way for the octopus to quell its prey’s biting, especially as it may transport several crabs at once within its web. Most drill holes in crabs are over the region of the heart and major vessels (see drawings on Right), and in bivalves over the adductor muscles that hold the shell valves together or in the umbo region that contains the heart and guts.  Drill location may not matter much in the case of crabs as the toxin is potent and the crab’s hemolymph circulation is quite fast. Of 177 crab remains collected from octopus dens in Prince William Sound, Alaska, 33 are drilled, and most of these (64%) are into one species, Cancer oregonensis, that has a relatively hard carapace.  In comparison, the crab species found to be eaten most, the helmet crab Telmessus cheiragonus, has a much softer carapace and is hardly drilled at all (6%).  Octopuses may find it easier to bite into or rip apart this helmet-crab species than the other harder-bodied species. Dodge & Scheel 1999 Veliger 42: 260.

Research study 8

phtograph of octopus Enteroctopus dolfleini in its denOctopuses attack bivalves in 3 ways: pulling the valves apart with their arm suckers, chipping the edges of the valves with their beaks, and drilling and injecting toxin.  Studies at the Seattle Aquarium show that giant octopuses Enteroctopus dofleini have different preferences for different bivalve species, possibly in accordance with the difficulty they have in opening them.  When offered a choice in the lab of live and intact Manila clams Venerupis philippinarium, mussels Mytilus trossulus, and littleneck clams Protothaca staminea, either singly or together, the preference hierarchy for each species is 2.8, 1.7, and 1.0, respectively, indicating that Protothaca is much less preferred than the other species. However, if the bivalves are opened by the experimenter and then offered to the octopuses, the preference hierarchy is 0.7, 0.2, and 1.0, indicating that Protothaca is now preferred.  The explanation for the 2 sets of data may lie in the thicker shell valves and greater valve-closing strength of P. staminea, and in its possibly greater tastiness or energy content as compared with the other species.  In fact, Protothaca is drilled about 4-7 times more frequently than the other species, which are mostly broken (18%), chipped (33%), or pulled apart (45%).  Drilling seems a “last resort” for the octopus, perhaps because it is time-consuming and thus costly in time and energy. 

photograph of scallop shells in an octopus's midden Enteroctopu dolfleiniDrilling of Protothaca is done not in the thinnest part of the shells, but in the centre of the shell (see diagram lower Left).  This is actually thicker than other areas (e.g., over the adductor muscles), but is close to the heart, perhaps representing a compromise between drilling time and effectiveness of the injected toxin.  Manila clams Venerupis are mostly pulled apart (60%).  If, however, their valves are wired shut so that they cannot be pulled apart, the octopus changes its tactics and resorts to chipping or breaking with the beak, or to drilling.  The authors discuss the significance of this.  Early research on learned behaviour in octopuses has emphasised a general reliance on visual input, rather than a tactile-proprioceptive input from arm and sucker position.  In the circumstance of a wired-up Venerupis, the octopus cannot see its bound prey, but appears to be modifying its behaviour using trial-and-error learning based solely on tactile and proprioceptive input.  Anderson & Mather 2007 J Comp Psychol 121: 300.

NOTE  response to taste in an octopus, as in other animals, is immediate; in contrast, response to energy or nutrient content will be post-ingestive, that is, occurring some time after the meal.  The octopus associates the taste of what it is eating with a previous post-ingestive experience (in humans this could range from a feeling of well-being to one of nausea), and then continues to eat the food or rejects it

Stash of mostly scallop shells Chlamys spp. outside of a den
of Enteroctopus dolfleini. Note that the shells are unbroken

Research study 9

photograph of inner side of shell valve of Japanese littleneck clam Venerupis philippinarum to show adductor-muscle scarsAn investigation of drill-hole disposition by octopuses Octopus rubescens at the Seattle Aquarium reveals a significant preference for drilling into the 2 adductor-muscle sites.  A preferential targeting of these muscles is of strategic advantage, as these are the ones that hold the shells together.  In an experiment with 10 octopuses, 171 holes are drilled into shells of clams Venerupis philippinarum, with 64% of these being drilled into one or other of the 2 muscles, with a preference for the anterior adductor muscle.  Together, the 2 muscle scars comprise only 6% of the available shell area.  Interestingly, another 187 clams are eaten by the predators during the 1mo experiment, but are not drilled.  The authors note the potential effectiveness of injection of venom directly into the adductor muscle masses.  The mechanism used to locate these areas of the shell is not known.  Anderson et al. 2008 Veliger 50: 326.

NOTE  the drill holes are about 1.4mm in diameter.  With respect to venom injection into one of the muscles, one wonders if a single functional adductor is enough to hold the shells together, at least for a time.  If so, perhaps the targeting of of a muscle is not just to incapacitate that particular muscle, but to ensure that the venom reaches a part of the body rich in hemolymph supply so that the other muscle will be more quickly affected

Research study 10
  Photographs provided by a research student at Walla Walla University, Washington show various drill-hole positions in arthropods and molluscs created by octopuses, mostly Octopus rubescens. Onthank 2008 MSc Thesis, Walla Walla University, 91pp.
photograph of drill-holes in crab claws made by octopuses, probably Octopus rubescens photograph of drill-hole in whelk Nucella lamellosa made by Octopus rubescens photograph of drill-hole in scallop Chlamys hastata made by Octopus rubescens
Claws of crabs Lophopanopeus bellus (central, black tip) and Petrolisthes eriomerus. Note precise drilling spots Shell of whelk Nucella lamellosa collected from midden of octopus Octopus rubescens Right valve of scallop Chlamys hastata collected from midden of Octopus rubescens
photograph of drill-hole in varnish clam Nuttallia obscurata made by Octopus rubescens photograph of drill-hole in quahog clam Mercenaria mercenaria made by Octopus rubescens close view of chew-marks in valve edge of quahog Mercenaria mercenaria caused by beak of Octopus rubescens
Valve of varnish clam Nuttallia obscurata drilled by Octopus rubescens in the laboratory Left valve of quahog Mercenaria mercenaria drilled twice (incompletely) by O. rubescens. Note chewed valve edge Close view of chew-marks on quahog shell. Note the vertical grooves caused by the octopus' beak 3.7X