Pulling or drilling, does size or species matter? An experimental study of prey handling in Octopus...

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Journal of Experimental Marine Biology and Ecology

290 (2003) 165–178

Pulling or drilling, does size or species matter?

An experimental study of prey handling in

Octopus dierythraeus (Norman, 1992)

Mike A. Steer*, Jayson M. Semmens

School of Marine Biology and Aquaculture, James Cook University, Townsville, Queensland 4811, Australia

Received 23 September 2002; received in revised form 30 December 2002; accepted 27 January 2003

Abstract

The influence of both predator and prey size on the shift from a pulling to a drilling predatory

response was examined in the intertidal octopus Octopus dierythraeus, using an experimental

program. Additionally, selective drilling, where particular regions of the prey are targeted, was

examined for a variety of bivalve and gastropod prey. O. dierythraeus always initially attempted to

pull bivalves apart. Shells that were eventually drilled were always subjected to significantly more

pulling attempts than those that could be pulled apart, indicating that octopus are willing to expend

more energy to access the flesh quickly. There was no defined threshold where bivalve size caused

an octopus to switch from a pulling to a drilling response. Instead, there was a broad size range

where the octopus could adopt either handling method and it varied for each individual. Octopus

may only able to pull open bivalves before the molecular ratchet or ‘catch’ mechanism that many

bivalves possess is engaged. This might explain the lack of a relationship between either octopus

or bivalve size and the success of pulling, as it is likely that when the bivalves were presented to

individual octopus they were either setting the ‘catch’ mechanism, or had already engaged it. O.

dierythraeus demonstrated selective drilling on a variety of molluscan prey, with penetration sites

differing between prey species. O. dierythraeus targeted the valve periphery, which was the

thinnest part of the shell, therefore minimizing handling time. O. dierythraeus always drilled

gastropods, but did not target the thinnest regions of the shells, with drill site varying according to

the morphology of the prey. Elongate species with pronounced aperture lips were drilled in the

apical region, close to the columella on the side of the opercula whereas nonelongate species were

0022-0981/03/$ - see front matter D 2003 Elsevier Science B.V. All rights reserved.

doi:10.1016/S0022-0981(03)00076-5

* Corresponding author. Present address: Marine Research Laboratories, Tasmanian Aquaculture and

Fisheries Institute, University of Tasmania, Private Bag 49, Hobart, Tasmania 7001, Australia. Tel.: +61-3-

62277236; fax: +61-3-62278035.

E-mail address: [email protected] (M.A. Steer).

M.A. Steer, J.M. Semmens / J. Exp. Mar. Biol. Ecol. 290 (2003) 165–178166

drilled immediately above the aperture. The location of drilling sites may represent a trade-off

between targeting the most effective places to inject paralyzing secretions and the mechanically

simplest places to drill.

D 2003 Elsevier Science B.V. All rights reserved.

Keywords: Octopus; Predation; Drilling; Pulling; Bivalve; Gastropod

1. Introduction

Foraging predators must expend time and energy to search for, capture and consume

prey. How predators budget this time has received much attention in the literature and is

considered an important component in determining the energetic ‘cost’ of predation (see

Hughes, 1980 for a review). Octopus are versatile foraging predators, with morpho-

logical and behavioural adaptations enabling them to handle a diverse array of prey

(Hartwick et al., 1978), ranging from relatively defenceless polychaetes and fish to

heavily armoured bivalves, gastropods and crustaceans (see Nixon, 1987). Upon capture

of hard prey items an octopus will usually attempt to pull the prey apart using force

exerted by its muscular arms and suckers (McQuaid, 1994). If this fails, they are able to

subdue and access prey by drilling into soft tissue and injecting paralysing salivary

secretions (Nixon, 1979).

Unlike other armoured prey items, gastropods are typically drilled, as their

morphology makes them difficult to pull apart. Conversely, the pulling response is

always the first action inflicted on bivalves regardless of their size (Fiorito and

Gherardi, 1999). When small, bivalves are easily opened, however, they may reach a

critical size and strength at which they can resist being pulled apart. If an octopus

encounters a bivalve that resists its pulling attempts, it will change its tactics and

initiate a drilling response (Hartwick et al., 1978). Holes are drilled by the radula and

salivary papillae via a combination of mechanical and chemical abrasion through which

toxic salivary secretions are injected (Nixon and Boyle, 1982). These secretions

paralyse and partially digest the prey, allowing the octopus to pull it apart easily

(Grisley et al., 1996).

The action of pulling is energetically demanding, and in Octopus vulgaris is

calculated to be 1.29 times more costly than that of drilling (McQuaid, 1994). Pulling,

however, is considerably quicker, with each pull lasting a few seconds, consequently

minimising prey handling time. The switch from pulling to drilling may be a

compromise between valuable handling time, which could be utilised to find and feed

on additional prey, and energetic cost (McQuaid, 1994). It is also possible that this

compromise may not necessarily be an issue of energetics, but may relate to the prey’s

ability to resist a pulling action.

Once an octopus has elicited the drilling response, it may target particular areas

of the prey (Nixon and Macconachie, 1988). Selective drilling is also observed in

predatory gastropods (see Kabat, 1990 for a review), with these animals consuming

the prey via the drill hole. Some gastropod species drill directly over the digestive

M.A. Steer, J.M. Semmens / J. Exp. Mar. Biol. Ecol. 290 (2003) 165–178 167

gland and gonads of the prey maximising calorific yield (Palmer, 1988). Other

species target the thinnest parts of the shell, minimising drilling time (Hart and

Palmer, 1987). As octopuses do not consume prey via the drill hole, selective

drilling in these animals has been attributed wholly to the physiology of their prey

(Runham et al., 1997). Some octopus species target the region of adductor muscle

attachment directly weakening the union between the two valves (e.g., O. vulgaris,

Nixon and Macconachie, 1988; O. mimus, Cortez et al., 1998), while others target

the thin pallial edge (O. vulgaris, Ambrose and Nelson, 1983). Drill holes in

gastropods are often located on the apical spire (Nixon and Macconachie, 1988;

Runham et al., 1997). There is, however, variation both within and between species

of predators and prey that suggest that drilling behaviour is not consistent across the

octopod genera.

The causal mechanisms underlying the shift from a pulling to a drilling mode of

feeding are unknown and few studies have investigated selective drilling for a variety

of prey species. Whether predator or prey size influences the pulling or drilling

response was examined in captive Octopus dierythraeus, which occurs in inshore

waters of subtropical and tropical Australia (Norman, 1992). Additionally, selective

drilling by O. dierythraeus was examined for a variety of bivalve and gastropod prey

species.

2. Materials and methods

2.1. Pulling vs. drilling

Three O. dierythraeus individuals (104.2, 174.5, 532.2 g) were captured on the

coral/rocky reef flats at Cockle Bay, Magnetic Island, Queensland, Australia

(19j10VS, 146j49VE). Octopus were flushed from their lairs, during periods of low

tide ( < 0.8 m), using a weak copper sulphate solution and transported to the

aquarium facilities at James Cook University in Townsville. Each animal was housed

in separate 380-l opaque tanks, attached to an 80,000-l recirculating system,

containing a dead coral head and a 30-cm pipe for shelter. Tanks were half-filled

and securely covered with a shade-cloth lid. Animals were allowed time to habituate

to their new environment before the experimental program began, during which time

they fed ad libitum on various crustacean, bivalve and gastropod species found in

surrounding coastal waters.

Formal observations of prey manipulation commenced approximately 1 week after

capture, where each octopus was starved for 24 h then fed a total of four cockles

(Gafrarium pectinatum) or oysters (Pinctata maculata) daily for 1 month, with 2 weeks

for each prey type. These species were chosen, as they were common in the midden

contents found at the entrance of O. dierythraeus lairs and easily collected from the reef

flats. During feeding, bivalves were added one at a time and the handling time, which is

the time taken to open and consume the prey, was recorded to the nearest second. The

number of pull attempts was also recorded. Each pulling attempt was clearly recognised

by defined tensioning of the arms. Rejected clean valves were retrieved and examined


macroscopically for drill holes. From this it could be established whether the bivalves

were either pulled apart or drilled open.

In addition, a further five O. dierythraeus ranging from 104.2 to 1125 g were used in a

second experiment investigating the switch from a pulling to a drilling response based on

prey size. Prey handling times were not recorded for these octopus, as only the switch from a

pulling to a drilling response was of interest. These animals were fed approximately 5–8 G.

pectinatum of known sizes every second day for 3 weeks, giving the animals approximately

Fig. 1. The time (min) taken for Octopus dierythraeus to open and consume the oyster, Pinctata maculata, and the

cockle, Gafrarium pectinatum. Symbols represent prey handling methods; bivalves successfully (o) pulled, (.)drilled open and (w) drill holes located at the junction of the two valves.


48 h to consume the prey without any observer influence. All prey remains were collected

and categorised as being either pulled apart or drilled. The relationship between bivalve size

and handling method was analysed using a series of logistic regression analyses.

2.2. Selective drilling

A total of 55 O. dierythraeus lair midden accumulations were collected from the

coral/rocky reef flats at Cockle Bay and Pioneer Bay, Orpheus Island (18j36VS,146j29VE). Each prey item was identified to species level and inspected for drill holes.

In addition, three captive O. dierythraeus were fed the mud-whelks Telescopium

telescopium and Terebralia palustris and the bivalve G. pectinatum ad libitum for 2

Fig. 2. Probability of drilling calculated via a series of logistic regression analyses for each octopus. Horizontal

line represents the 50% probability level.

Table 1

Summary of drill hole locations made by O. dierythraeus for examined bivalve species

Prey species n % drilled

pallial edge

% drilled

adductor scar

% drilled

umbo region

No. holes

incomplete

Repeat

attempt

Valve

pref p0.05

G. pectinatum 84 79.8 11.9 0.0 2.0 0.0 0.52

A. antiquata 59 84.8 3.4 0.0 0.0 1.0 0.52

B. amygdalumtostum 19 57.9 21.0 5.3 0.0 0.0 0.50

S. bilocularis 47 63.8 19.2 2.1 0.0 0.0 0.47


weeks. The gastropods used in this laboratory-based component were abundant and

easily collected from the surrounding coastline. Although these species were not found

in O. dierythraeus’ natural diet, gastropods of similar morphology (e.g., Cerithium

lifuensis) were.

The most frequently drilled prey items collected from middens at Cockle and Pioneer

Bays (including bivalves: Anadara antiquata, Barbatia amygdalumtostum, Septifer

bilocularis; and gastropods: Lambis lambis, Turbo haynesi) and gastropods and cockle

debris from captive animals (including those cockle shells from the pulling vs. drilling

Fig. 3. Site-specific drilling in (a) Gafrarium pectinatum, (b) Anadara antiquata, (c) Barbatia amygdalumtostum

and (d) Septifer bilocularis (. = complete, � = incomplete drill hole). Dashed circles represent areas of adductor

muscle attachment. Scale bar equals 10 mm.


experiment) were pooled. The position of drill holes for each prey species was recorded

on a scaled illustration, with the drilling sites normalised for the left and right valves of

the cockles. Valve preference was statistically quantified using paired sample t-tests. To

determine whether the position of drill holes were randomly distributed around the

periphery of bivalve shell, each valve was ‘‘sectorized’’ and analysed via a series of

nonparametric goodness of fit chi-square tests. The valve peripheries of G. pectinatum,

A. antiquata and B. amygdalumtostum were equally divided into three sectors: posterior,

anterior and ventral edges; whereas S. bilocularis was divided into posterior and ventral

sectors.

Five replicates of each drilled prey item were sectioned longitudinally using a

water-cooled, diamond circular saw. Bivalves were characterised into three zones:

valve margin, adductor muscle scar and umbo region. Gastropod species were

similarly characterised into three zones: apical spire, mid-body region and first

body whorl. Shell thickness for each of these zones was measured to the nearest 0.1

mm using digital vernier callipers and an average of five measurements taken.

Differences in shell thickness of each region for each species were statistically

Fig. 4. Each bivalves’ relative shell thickness (F SE) graphs are presented. Horizontal bars encompass

nonsignificantly different means, determined via Tukey’s HSD post hoc test.


analysed using one-way ANOVAs, incorporating a post hoc Tukey’s HSD test to

highlight differences amongst means. Data transformations were performed where

necessary.

Rose diagrams were utilised to determine whether octopus preferred to drill gastro-

pods in a particular sector. Zero degrees (0j) was categorised as the plane where the

apex of the shell intercepts the aperture lip (following Wodinsky, 1969; Runham et al.,

1997).

Fig. 5. Site-specific drilling in (a) Terebralia palustris, (b) Telescopium telescopium, (c) Lambis lambis and (d)

Turbo haynesi (. = complete, � = incomplete drill hole). Scale bar equals 10 mm.


3. Results


Immediately after capture, the bivalve was orientated under the octopus’s interbranchial

web so that the valve margin faced its buccal mass. Once the bivalve was in this position the

octopus always attempted to pull the valves apart, with each pull lasting approximately 5 s. A

linear relationship between handling time and prey size was evident.P. maculatawas always

successfully pulled open within 4.1F 0.2 (meanF SE) attempts and consumed within 10

min (Fig. 1).G. pectinatum could be opened within 7.7F 0.4 attempts and consumed within

15 min; however, larger individuals, which subsequently required drilling, experienced

significantly more pulling attempts (14.8F 0.5; F1,127 = 148.7; p < 0.001). In preparation for

drilling, the octopus rotated the bivalve 90j from its pulling orientation. Upon completion of

drilling, the bivalve was returned to its original position and easily pulled apart, with the

entire process taking approximately 60 to 90 min. In a few cases, G. pectinatum was drilled

at the junction of the two valves and consumed within 40 min (Fig. 1).

The switch from pulling to drilling was not a defined response for O. dierythraeus fed

G. pectinatum, as there was a broad size range of cockles where both pulling and drilling

was used (Fig. 1). It was hypothesised that the bivalve size, at which there is a 50% chance

of drilling occurring, increases with increasing octopus size. This, however, was not

observed to be the case, with no obvious relationship between prey size at which a drilling

response would be initiated and octopus size (Fig. 2).

3.2. Site-specific drilling

O. dierythraeus primarily targeted the valve margins of all bivalves, particularly those

of G. pectinatum and A. antiquata, with no preference for left or right valves (Table 1).

Drill holes on G. pectinatum were primarily concentrated on the posterior valve margin

(v2 = 62.2, df = 2, p < 0.001), whereas those on A. antiquata were aggregated on the ventral

edge (v2 = 21.6, df = 2, p < 0.001). Drill holes were randomly located around the valve

periphery in B. amygdalumtostum (v2 = 2.9, df = 2, p = 0.23) and S. bilocularis (v2 = 3.5,df = 1, p< 0.06) (Fig. 3). The valve margins were the thinnest region in all species (Fig. 4).

B. amygdalumtostum and S. bilocularis are relatively thin-shelled species with even their

thickest regions thinner than the valve margins of the robust G. pectinatum and A.

antiquata. As such, these species displayed a higher relative proportion of drill holes in

both the adductor muscle scars and umbo areas (Table 1). Two G. pectinatum specimens

Table 2

Summary of drill hole locations made by O. dierythraeus for examined gastropod species

Prey species n % drilled

apical

% drilled

mid-body

% drilled

first body whorl

No. holes

incomplete

Repeat

attempt

L. lambis 28 78.6 17.9 3.6 0.0 1.0

T. haynesi 15 0.0 20.0 80.0 0.0 0.0

T. telescopium 24 53.6 46.4 0.0 2.0 3.0

T. palustris 62 69.3 30.7 0.0 0.0 3.0


displayed incomplete drill holes on the thick mid-body section and in each instance were

accompanied by a complete hole on the thinner valve margin (Table 1, Fig. 3).

Drill holes for the gastropods, T. palustris, T. telescopium and L. lambis, were

located between 330j and 20j in relation to the aperture lip. Holes were tightly

aggregated at the apex of the apical spire for T. palustris and L. lambis, but were

evenly distributed along the spire in T. telescopium (Fig. 5). The majority of drill-holes

Fig. 6. Each gastropods’ relative shell thickness (F SE) graphs are presented along with circular histograms

representing penetration sites in relation to the aperture lip. Horizontal bars encompass nonsignificantly different

means, determined via Tukey’s HSD post hoc test.


in T. haynesi were located on the first body whorl adjacent to the aperture, around the

190j position (Table 2, Fig. 6). As was observed for the bivalve species, O.

dierythraeus targeted the thinnest region in L. lambis, however, this was not the case

for the other gastropods (Fig. 6). Multiple drilling was observed in T. telescopium, T.

palustris and L. lambis with holes located next to each other in the apical spire region.

Incomplete drill holes were only observed in T. telescopium and were always

accompanied by a successful drill hole (Table 2).

4. Discussion


Both bivalve species used in this study were preyed upon by O. dierythraeus. The

relatively fragile oyster, P. maculata, was consumed quickly and easily, as O. dierythraeus

always successfully pulled them apart. The cockle, G. pectinatum, however, is a more

robust species possessing two heavily calcified, interlocking shells and often resisted the

octopus’ pulling attempts and were subsequently drilled. It is noteworthy that drilled

cockles were initially subjected to significantly more pulling attempts indicating that

octopus are willing to expend more energy to access the flesh quickly, rather than drill.

Studies have shown that when fed ad libitum, captive O. vulgaris select the largest

bivalves that can be pulled open and reject those that require drilling (Smale and Buchan,

1981). However, when unlimited prey items are not available, as in the case of this study

and in the wild, cockles that cannot be pulled apart are drilled out of necessity.

In previous studies the switch from pulling to drilling has been directly linked to

bivalve size and strength (McQuaid, 1994; Fiorito and Gherardi, 1999). However, in this

study, the size and strength of G. pectinatum only partly explained changes observed in the

prey-handling techniques by individual O. dierythraeus. This was established purely on

the basis that bivalves on the smaller end of the size spectrum were usually pulled open,

where larger ones were less likely to be opened by this method. There was not a defined

threshold where bivalve size caused an octopus to switch from a pulling to a drilling

response. Instead, there was a broad size range where the octopus could adopt either

handling method and it varied for each individual. McQuaid (1994) found similar results

for O. vulgaris, as individual octopus differed in the ease with which they could open the

mytilid mussel, Perna perna. This suggests that there are other factors contributing to the

switch from a pulling to a drilling response.

Smaller octopus may be more dexterous in handling smaller bivalves, with their

comparatively smaller suckers enabling them to gain a greater purchase on the bivalve

shell. As a result, they may exert a greater cumulative pulling force than larger octopus that

may not be able to grip the valves effectively. When food is not limited, large octopuses

are likely to reject these bivalves as they are not energetically worthwhile and are difficult

to manipulate. However, when food is limiting, as was the case in these captive

experiments, larger octopuses will resort to drilling these smaller bivalves.

Another possible explanation for an undefined switch from pulling to drilling may

relate to the bivalve musculature. It has been documented that many bivalves possess two


types of muscles within their collective adductor muscle region: fast and slow fibres (see

Hoyle, 1964 for a review). The slow muscles possess a molecular ratchet mechanism, the

‘Sperrung’, or ‘catch-mechanism’, which maintains a state of tension with little energy

expenditure (Johnson and Szent-Gyorgyi, 1959). The catch has been suggested to set itself

automatically following excitation and adductor contraction, which may be triggered by

manipulation from a predator (Hoyle, 1964). These catch muscles are very slow to react

and in mytilid mussels they have been found to reach maximum tension 15 s after

excitation (Abbott and Lowry, 1956). This tension can be sustained for a number of hours

without any signs of fatigue and has been estimated to resist pulling forces up to 2 kg

cm� 3, keeping the valves tightly closed (Wilkie, 1954). It is feasible that octopuses are

only able to pull open bivalves before the slow ‘catch’ mechanism is engaged, after which

they can only access the soft prey tissue by drilling. This might explain the discontinuity

observed in this study, as it is possible that when bivalves were presented to individual

octopus they were either in the process of setting the ‘catch’ mechanism, or had already

engaged it. This may explain why some octopuses were not able to pull open relatively

small bivalves while others could. To further investigate the causal factors influencing the

shift from pulling to drilling, research must focus on the relative pulling forces for a range

of octopus sizes and the relative pulling forces that bivalves can resist, paying close

attention to the presence of the ‘catch’ mechanism.

4.2. Selective drilling

O. dierythraeus demonstrated selective drilling on a variety of molluscan prey, with

penetration sites differing between prey species. In other octopus species the most

common penetration site is in the vicinity of the adductor muscle (e.g., O. vulgaris,

Nixon and Macconachie, 1988; O. mimus, Cortez et al., 1998; O. bimaculoides, Casey,

1999). Drilling in this area has been linked to the octopuses paralysing saliva initiating a

direct action on the adductor muscle (Cortez et al., 1998). O. dierythraeus did not display a

tendency to selectively drill in this region, instead it was observed to target the valve

periphery. Penetrating the adductor muscles must therefore not be necessary to weaken the

union between the two valves. It seems likely that the salivary papillae need only to

nonspecifically pierce the flesh of the prey item to initiate paralysis (Nixon, 1980).

Ambrose and Nelson (1983) observed similar results for O. vulgaris, with drill holes

mostly occurring around the margins of the bivalves Venus verrucosa and Pitaria chione.

They attributed this nonrandom distribution as being the most efficient place to drill as a

product of the octopus’ preferred grip. Other studies suggest that octopus target these

regions as they are the thinnest part of the shell, therefore minimising handling time

(Leighton et al., unpubl., in Ambrose et al., 1988). This was observed to be the case for O.

dierythraeus.

O. dierythraeus was not observed to target the thinnest regions on gastropod shells.

Instead, it was observed to preferentially drill in the apical region, close to the columella

on the opercula side of large gastropod species. These results are consistent with those

found by Arnold and Arnold (1969) and Nixon and Macconachie (1988) for O. vulgaris.

Arnold and Arnold (1969) related this selective drilling to the octopus’ preferred

orientation of the prey using the aperture lip as a landmark. This, however, may only


relate to morphologically elongate prey like T. palustris and L. lambis with pronounced

aperture lips. T. telescopium demonstrates an elongate morphology but lacks a prominent

aperture lip, potentially explaining why drilling sites were not as tightly aggregated

compared to the other gastropods.

When octopus capture gastropods they tend to insert an arm into the aperture to confirm

that the shell is occupied (Wodinsky, 1969; pers. obs.). This action has been described as

‘customary behaviour’ (Wodinsky, 1969) and may stimulate the gastropod to retreat

further into its shell. Drilling higher up on the shell may increase the octopus’ chance of

penetrating the gastropod’s flesh. Penetration sites did not reflect this in the turban shell, T.

haynesi, as drill holes were located on the body whorl adjacent to and immediately above

the aperture. Because T. haynesi possesses a relatively short columella and large aperture,

it may not be able to retract very far into its shell and as a consequence octopus have been

observed to pull similar ‘top-shaped’ gastropods out of their shells without resorting to

drilling (Wodinsky, 1978; Loch, 1988). Similar penetration sites have been found on Turbo

undalatus, drilled by the Common Sydney Octopus, O. tetricus (incorrectly described as

O. cyaneus, Norman pers. comm.) (Loch, 1988) and the top shell Gibbula magnus, drilled

by O. vulgaris (Nixon and Macconachie, 1988).

It is possible that certain locations represent more effective places to inject paralysing

secretions than others and this may vary between prey species. Alternatively, the observed

distributions may reflect the mechanically simplest places to drill (Ambrose and Nelson,

1983). Further studies are required to investigate whether selective drilling is directly

correlated to particular areas of the prey’s underlying physiology or whether octopus are

simply drilling particular areas as a result of a preferred grip.

Acknowledgements

The authors wish to thank J. Collins and M. Norman for constructive criticism and

support throughout the study. Comments made by R. Alexander (Rider University) greatly

improved the manuscript. Thanks must also be extended to field volunteers, in particular

N. Urrie who also contributed greatly to the design and maintenance of laboratory

facilities. This study complies with the current collection laws and code of ethics of

Australia. This paper is contribution no. 19 of the Marine Invertebrate Group at JCU. [SS]

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Pulling or drilling, does size or species matter? An experimental study of prey handling in Octopus...

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