Feeding behaviour of broody female Octopus vulgaris

Anim. Behav ., 1978, 26, 8 03-813

FEEDING BEHAVIOUR OF BROODY FEMALE OCTOPUS VULGARIS By JEROME WODINSKY Department of Psychology, Brandeis University, Waltham, Massachusetts 02154 and Lerner Marine Laboratory, Bimini, Bahamas

Abstract . When female Octopus vulgaris reproduce, their feeding behaviour changes . Food intake decreases, on the average, by 70 % of normal intake per meal, and additionally by 65 % of the normal number of meals, a total decrease of about 90 %. The method of predation upon gastropod prey changes from boring a hole in the shell, secreting a toxin, and pulling out the affected snail, to pulling the living snail out by force, and ceasing to bore . The fact that the post-egg-laying female expends energy to extract the body of the snail which it then scarcely eats may be a unique pattern of feeding behaviour. The primary purpose of the present report is to describe changes in a specialized predatory feeding behaviour of female Octopus vulgaris Cuvier after the female lay eggs . Simultaneously, the quantitative changes in the amount of food eaten before and after eggs are laid is measured . When O. vulgaris feeds upon shelled molluscs, it bores a hole in the shell, secretes a toxin from its posterior salivary glands into the borehole, pulls the affected body of the mollusc out through the aperture of the shell and eats it (Fujita 1916 ; Pilson & Taylor 1961 ; Arnold & Arnold 1969 ; Wodinsky 1969) . However, the octopus may also, on occasion, pull out the body of the mollusc without first boring . Fujita (1916) reported that the octopus ate, on the average, 5 . 7 pearl oysters per day, of which only 2 . 6 (45-5y.) had boreholes. Pilson & Taylor (1961) reported that O. bimaculoides and O . bimaculatus can open a bivalve, or pull an abalone off the substratum, by force . Arnold & Arnold (1969) reported that O . vulgaris ate the gastropod Tonna maculosa without boring the shell . 1 have offered T. maculosa to O . vulgaris which ate them, sometimes with, and sometimes without, boring. There is some experimental evidence that the octopus tries force first before boring ; a few individual octopuses even prefer using force to boring, but all will use force occasionally (Wodinsky 1969) . Furthermore, when the experimenter covers the shell containing a living snail with a thick, hard coat of a chemically resistant substance such as epoxy, acrylic or polyester, all octopuses pull out the body of the snail almost 100% of the time without boring (Wodinsky 1973a). There are four indications that force has been used to extract the snail from its shell . (1) The absence of boreholes in the shells of conchs

Strombus gigas and S . raninus, the species used

in this report, is about 10 % . (2) Some boreholes do not penetrate into the interior of the shell, so that no secretion reaches the mollusc . In a randomly selected sample of S . gigas, eaten by octopuses in the laboratory, 20 of 112 shells (17-9%) had incomplete boreholes. For S. raninus, 23 of 141 shells examined (16-3%) had incomplete boreholes . (3) The octopus may bore in an ineffective location, such as the lip of the shell, so that any secretion would pass directly into the sea water and leave the mollusc unaffected (Wodinsky 1969) . (4) Boreholes produced in empty shells, the apertures of which were sealed, indicates that the octopus does not secrete into every completed borehole (Wodinsky 1969) . The octopus therefore has two methods for extracting the body of molluscan prey . The present report describes a change in the natural life cycle of the octopus that is correlated with the choice of feeding method . In brief, when a female O . vulgaris lays a clutch of eggs : (1) it works to obtain food, the criterion of work being that the living body of the mollusc is pulled out of its shell ; (2) very little of the food thus obtained is eaten, that is, there is a marked hypophagia ; and (3) there is a shift in the method of obtaining food, that is, the octopus changes from boring and then pulling, to pulling without boring . Methods Subjects. Fifteen specimens of O . vulgaris were observed, of which 11 laid eggs and four died with ovaries loaded with eggs . This latter is not uncommon in octopus (Lee 1875 ; Gravely 1908 ; Pickford & McConnaughey 1949 ; Wodinsky 1972 ; Van Heukelem 1973) . The 803



804

ANIMAL BEHAVIOUR, 26, 3

dates of capture, egg laying and death, and initial, maximum, and death weights are presented in Table I . The octopuses were maintained individually in opaque fibreglass aquaria, 56 x 41 x 25 cm, covered with 6 . 3-mm wire-mesh sealed tops, which were supplied with continuously running sea water . Standard food during captivity was living gastropods in the shell, most commonly the queen conch, Strombus gigas Linnaeus, and the hawk-wing conch, S. raninus Gmelin. Also included as food was the body of S. gigas removed from its shell by the experimenter and an occasional crab, Callinectes ornatus Ordway. Method. The method of extraction of the prey from its shell and the amount of food eaten was examined before and after the female laid eggs for 11 egg-laying females and for two eggbound females (numbers 40 and 49) prior to death. The food intake of snails removed from the shell by the experimenter was examined after egg-laying in one of these egg-laying females (No . 4) and for two additional egg-bound females (numbers 3 and 20) prior to death . Prior to egg-laying, each octopus was presented with living snails, S. gigas or S. raninus on an ad libitum basis . As soon as the eggs were laid, each octopus was given two conchs, one each of S. gigas and S. raninus, whose weights (shell and body) were recorded . After the octopus removed the body of a snail, the food was permitted to remain with it for at least 12 and usually 24 h, at which time it was removed, the uneaten remains weighed, and another prey specimen replaced . Fresh, living prey were thus available continuously . Empty shells were measured (height and weight) and examined for the presence of a borehole . All shells bored after egg-laying were cut to determine whether the borehole penetrated the interior of the shell . The amount of food that the octopus ate was obtained by weighing the shell and body of the snail prior to presenting it to the octopus and subtracting the weight of the empty shell after the octopus had eaten the snail . However, this is an inflated measure because the living snail retains water in the interface between its body and the shell . Therefore, a control was run, in which 71 S. gigas shells were weighed, height of shell measured, shell broken, and the complete body of the snail extracted and weighed . The least squares solution was computed for relating the body weight of the snail (Y) to the height of the shell (X) from a log-log transformation . The empirical equation is

Y = 6 . 38 x 10- 7 x

X3 . 70 .

The rational basis for this equation is the well known relation that, in similar figures, volume (weight) increases as the cube of the linear dimensions (height). This correction was applied to each of the S. gigas snails as the initial body weight from which the uneaten remains were subtracted to obtain the values for the amounts eaten. The estimated weight of the snail obtained by both of the above methods was compared . A randomly selected sample of 128 S. gigas provided a mean estimated body weight of 103. 6 g obtained by subtracting the weight of the empty shell from the weight of the living snail in the shell . The mean estimated body weight of the same sample calculated from the height of the shell was 61 .2 g, only 59 % of that obtained by the first method . Water in the shell accounts for the difference . A further problem in precisely estimating the body weight of the snail arose and will be discussed later. The empirical equation for estimating the body weight of S. raninus was Y= 6 .85 x 10- 7 x

X3'88,

based upon a sample size of 30 . The estimate of the amount of food that the octopus ate required a further correction due to the fact that the body of the snail, out of its shell, changes weight . A separate control of leaving the body of S. gigas (N = 63) in sea water for 24 h indicates that there is a mean loss of 4 . 36 g or 7-2% of the initial body weight . This control has not been run either with fractional parts of the body or for shorter durations of time . Results The Shift From Boring to Pulling Table II indicates that 11 octopuses ate 384 snails before laying eggs, of which 375 (97 . 7 %) had boreholes . The lowest incidence of boring was by octopus 66 which bored 91-7% of its shells . After egg laying, the octopuses removed 134 snails from their shells, in which only 27 (20 . 1 %) had boreholes . The highest incidence of boring was by octopus 4 which bored 56 % of its shells . Every female, after laying eggs, bored less frequently than (1) it itself did before laying eggs, and (2) any female did before laying eggs .



WODINSKY : FEEDING OF BROODY OCTOPUS

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80 6

ANIMAL BEHAVIOUR, 26,

3

penultimate 10, which is comparable to the 17 indicated as normal in the Introduction section . In summary, the data indicate two points O . vulgaris removes snails from the shell after spawning ; and it shifts from boring to extracting the snail without boring, not only after laying eggs, but also as the egg laying episode approaches .

Examination of the interior of the cut shells revealed that 10 of the 27 boreholes (37%) made after egg laying were incomplete . This compares with an incidence of about 17% (see Introduction) based upon a random sampling of boreholes of 35 different octopuses . Hence, only 17 of the 134 shells (12 . 7 %) post-egg laying had complete boreholes . Table II also indicates that most of the boreholes were made immediately after egg laying . The last column of Table II shows that 23 of the 27 boreholes were made in the first four shells taken after spawning . Two octopuses, numbers 43 and 70, never bored after laying eggs . Borings occurred equally often in S. gigas (13) and in S. raninus (13), but there were many more of the larger S. gigas (78) removed without boring than S. raninus (28) . Table III presents data for two octopuses that died before laying eggs but whose ovaries were full of eggs . The last 20 shells taken by each octopus were cut and examined . A marked shift occurs in the incidence of incomplete boreholes and the absence of boreholes in the last 10 shells compared with the penultimate 10. In the last 10, 15 (75 %) either have no borehole or an incomplete one . Only three (15 %) occur in the

Amount Eaten Table IV presents results of food intake of these octopuses both before and after egg laying . The results presented are the amounts eaten of S. gigas, and are entirely comparable for S . raninus for which there is a much smaller sample . In each case, the body weight of the snail was estimated from the height of the shell by the empirical formula previously given . The mean amount of food left uneaten increases markedly after spawning (38 .2 versus 17 . 8 g), despite the fact that a smaller amount of food was available to the octopus . The octopuses ate, on the average, 18 .4 g per meal after laying eggs, compared to 51 . 6 g prior to egg laying, a mean decrease of 61 .2 % . Each octopus showed decreased food intake . There were only three meals by two octopuses in which more was eaten than in any pre-egg laying meal . These calculations do not

Table III. Incidence of Incomplete and No Holes in the Last Twenty Shells of Octopuses That Died Before Laying Eggs Penultimate ten shells Octopus number

No. snails eaten

No. shells bored

40 49

73 72

69 66

0 0

145

135

0

Last ten shells

No . No . incomplete no hole holes

No . no hole

No . incomplete holes

2 1

3 5

5 2

3

8

7

Table IV. Food Intake Data for Octopuses That Laid Eggs and for Those That Died Before Laying Eggs Octopuses that laid eggs Last feeding Before After before egg laying egg laying egg laying Mean height of shell in millimetres (measured) Mean weight of snail, complete body, in g (calculated) Mean weight of snail, without viscera, in g (calculated) Mean amount of food uneaten in g, (measured) Mean amount of food eaten in g, (calculated) N

Octopuses 40 and 49 Earlier feedings

Last ten feedings

147 .5 69 .4 43 .3 17 .8 51 . 6

138 .7 55 . 7 34 .7 38 .2 18 .4

145 .8 66 .2 41 .3 45 .7 20 . 5

146 . 0 70 . 2 43 . 8 19 .8 50 .4

142 . 0 59 . 2 36 . 9 41 . 8 18 . 6

25

81

5

12

15



WODINSKY : FEEDING OF BROODY OCTOPUS

include the correction for spontaneous changes in the weight of the snail merely being in sea water. If the mean weight loss of 4 .36 g shown by the control measurements is deducted, the mean decrease in food intake is 70 . 3 % of the pre-egg laying intake. An attempt was made to determine when the reduction actually begins . Table IV includes data for five feedings that were the last meal eaten before eggs were laid . The amount eaten was similarly decreased . The food intake of octopuses 40 and 49 from 15 S . gigas eaten during the last 10 feedings was also decreased by a comparable amount relative to that from 12 snails eaten during earlier feedings . The above results refer to the amounts eaten during a 12- to 24-h period . The octopuses, on the average, extracted one snail every 2 . 7 days after laying eggs. Prior to egg laying, the average was slightly less than one snail per day . Therefore, not only is less food eaten per meal (29 .7 of normal), but the brooding octopus eats fewer meals irregularly spaced over longer periods of time (37 % of normal) . The food intake of the female after spawning is thus about 11 % of its intake before laying eggs . Whereas the approximately 90 % decrease relative to normal food intake of the females after spawning seems to accord with observations of feeding behaviour, the estimated absolute amounts eaten in grams (e .g . 50. 6 and 18 .4 g, Table IV) seem excessively large and in disagreement with other measurements of food intake . Indeed, in many cases, the body of the snail was extracted and appeared to be untouched, as indicated by the absence of beak marks . The weights of the apparently uneaten snails varied from quite close to the calculated weights to less than two-thirds of the calculated weights . Octopuses do not usually eat the viscera, eyes and proboscis of the snail . The viscera were removed from the control snails which formed the basis of the estimated body weights of snails (see Method section) . The least-squares solution for the weight of the body of the snail without the viscera (Y) as a function of shell height (X) was computed . The empirical equation for S . gigas was Y = 3 . 60 x 10- 7 x X3 . 72 . These values, which are 62 .4 % of the weight of the complete snail, are included in Table IV . The weight of the eyes and proboscis of S . gigas is about 3 g. Thus if the viscera, eyes and proboscis are not eaten, the mean amount eaten should not exceed, for example, 40 .3 g (before spawning). One hypothesis to explain the

80 7

apparent overestimation is that the viscera of the snail are punctured or torn when the octopus pulls them out of the shell, or when the octopus bites them, and the body fluids leak out thereby altering the net weight . Unfortunately, the amount that the octopus left was not divided into body and viscera and separately weighed, so that no correction factor can be introduced. With greater precision in future measurements the absolute amount eaten may be specified more accurately, but the relative decrease in food intake of egg-laying females should remain the same . We may note that whereas there are several ways to measure food intake, there seems to be only one method to chronicle the shift from boring to pulling . Other measurements of food intake indicate that the amount eaten by the octopus should be about 50 % of the values shown in Table IV . During the course of another study, to be reported elsewhere, 19 octopuses were each daily fed the body of S . gigas (without viscera) broken out of its shell in an attempt to measure the daily food intake . Octopus 4 (post-egg laying) and octopus 20 (pre-egg-laying) were included in that study . At the start of the experiment, the mean weight of the octopuses was 516 g . Octopus 20 weighed 182 g and octopus 4 weighed 1220 g (the next heaviest weighing 856 g) . Octopus 4 died on the 26th day of the experiment ; octopus 20 died 6 days after the end of the 28-day experiment, before laying eggs . The food intake of both was markedly, erratically and consistently below that of normal healthy feeding octopuses . The mean intake of the 17 normals was 555 . 2 g of food cumulated over the 28 days of the experiment, a mean daily intake of 19 .8 g . During the 24 days that it lived, octopus 4 ingested 160 g, a mean daily intake of 6 . 7 g or 28-8% of the normals, a decrease of 71-2% . Octopus 20 ingested a total of 133 g, a mean daily intake of 4 .8 g, or a decrease of 76 .0 of the normals . Octopus 3 showed a similar decrease in a comparable experiment conducted at a different time of year with a different control group, and its data are not presented . Two of the normal octopuses in this experiment weighed more than 900 g. Their mean daily intake averaged 28 g. These results, obtained with a more accurate method, support the conjecture that the amount eaten should be about 50 % of the values presented in Table IV . In summary, the data indicate that the female O . vulgaris does eat after laying eggs ; it decreases

80 8

ANIMAL BEHAVIOUR, 26, 3

its food intake about 70 % per meal and about 63 % of the number of meals, a total decrease of about 90 % of its normal pre-egg laying amounts ; the decrease appears 1 to 2 weeks prior to the actual occurrence of egg laying ; and it is correlated with the change in the instrumental behaviour in obtaining food and reward previously reported, namely, the shift from boring to pulling . Qualitative Observations on Feeding During the second week preceding spawning there is a precipitous decline in the food intake of female O . vulgaris. This drop is perfectly correlated both with the cessation of sexual receptivity and, 2 weeks later, with spawning (Wodinsky 1973b) . This decrease has also been reported for O . cyanea (Van Heukelem 1973) . It is during this second week preceding spawning that the incidence of incomplete and no boreholes suddenly increases . During the week immediately preceding egg laying, almost no food is eaten, nor are the continuously available snails extracted from their shells . Immediately after egg laying, snails are pulled out and the low level of feeding begins. The complete body of the snail, including the viscera, usually was removed from the shell without the columellar muscle having been torn . These snails were alive and contracted vigorously when touched . Sometimes, however, the snail was torn out of its shell, the columellar muscle ripped, and the viscera left inside the shell . On occasion the snails were dead, sometimes when removed from the shell, sometimes while still inside, prior to being extracted . The relative frequencies of each of these results were not recorded, but numerous cases of each were observed . The octopus may kill the snail while in its shell (without boring) in a manner unknown at this time ; it will also extract the living snail . Beak marks were clearly visible where the octopus nibbled at the snail's body . In many cases no such beak marks were evident, indicating, in conjunction with weight measures, that the octopus had not eaten . The experimenter often placed the body of the snail in contact with the octopus . With one exception, the octopus immediately rejected the food and pushed it away with an arm or with a jet of water from its siphon . These same individuals regularly came and took food out of the experimenter's hand before laying eggs . If the prey were left in the aquaria, the octopuses ate them several hours later, or overnight, or even a week

later. The almost invariable immediate rejection of food is not necessarily the only valid index of consumatory feeding behaviour . The crab C. ornatus was always killed . Sometimes it was untouched, and sometimes the meat was nibbled, but it was never completely cleaned and eaten in the fashion typical of a healthy, normal, feeding octopus . Table I indicates that three of the 11 clutches of eggs were fertilized . The octopuses typically remained on the clutch . They did leave the eggs, on occasion, to seize the prey . In one case, the octopus started to lay eggs, stopped, and laid the remainder of the eggs in the opposite side of the tank . Thereafter, the octopus was seen brooding both clutches of eggs alternately, with young hatching from both . These observations indicate that the female is not inflexibly tied to one location during brooding . Unfertilized eggs were scattered after about 5 or more days throughout the aquarium. Often the octopuses blew the eggs out of the water onto the wire mesh covers. These observations indicate that the behaviour of the post-egg laying female is not dependent upon copulation, fertilized eggs, or even the continued presence of eggs . Table I indicates the dates that eggs were laid . Egg laying has been reported during each month of the year (Wodinsky 1972) . Since the behaviour described occur in all cases, the prespawning and post-spawning decrease in food intake is not correlated with a temperature drop . Borer (1971) has shown, for O . briareus, a 50 reduction of food intake with a 10 C drop in temperature . The weight losses sustained during the reproductive episode are indicated in Table I . Taki (1944), Wells & Wells (1959), Wells (1960), and Mangold-Wirz (1963) have maintained that female O . vulgaris is not sexually mature under a body weight of 1000 g . Table I indicates the maximum weights recorded, the mean weight of the 15 octopuses being 712 g (749 . 5 g for those that laid eggs ; 608 . 5 g for the other four) . The heaviest weighed 1389 g and the lightest 182 g. The four octopuses that died prior to laying eggs contained egg masses weighing 56, 21, 46 and 21 g for the respective body weights at death of 967, 141, 520, and 343 g . Sakaguchi (1968) reported that the mean body weight of O. vulgaris after spawning was 475 g with a range from 450 g to 620 g. Even with the assumption that the gonads, at the maximum, may account for 20 % of the total body weight of a ripe female (Wells & Wells 1959), these values are only



WODINSKY : FEEDING OF BROODY OCTOPUS

60% of those reported . Van Heukelem (1973) has reported a similar discrepancy for O . cyanea, and has hypothesized that age, not body weight, influences the maturation of the gonads . He has combined the age hypothesis with an hypothesis of abundance of food to account for sexual maturity of low weight individuals . Laboratory lighting conditions (daylength and intensity) may accelerate the onset of sexual maturity . However, no studies have been reported of the effects of lighting on any octopod . There may also be geographical differences (Wodinsky 1972) . The loss of body weight preceded egg laying . This loss is indicated not only by three of the four octopuses that died before laying eggs, but also by those cases where data are available for octopuses that did lay eggs (numbers 22, 24, 26 and 71) . Particularly impressive are the data for numbers 40 and 49 . Octopus 40 weighed 696 g on 31 July, before the eggs were noticed. At death, 11 days later, its weight was 520 g, a loss of 176 g (25-3y.), an average daily loss of 16 g . Similarly, number 49 weighed 444 . 5 g on 30 July, and 343 g on 13 August, a loss of 101 .5 g (22-8y.), an average loss of 7 .2 g per day. These average daily losses compare with those of normal, food-deprived octopuses of 1 . 8 g per day (Nixon 1966) . This pre-spawning loss of body weight has also been documented for O . cyanea (Van Heukelem 1973). Three of the octopuses that laid eggs lost more than 50 % of their maximum body weight ; one lost more than 40 % ; three lost more than 30 and two lost more than 20 % . Similar losses are reported for O . cyanea (Van Heukelem 1973) . There is a slight suggestion in the data that the higher the maximum weight, the longer the octopus lived after egg laying, and the greater the percentage of body weight loss . Table I indicates that the mean life expectancy after laying eggs was 36 . 2 days, ranging from 17 to 58 days at temperatures ranging from 21 .1 to 33 .3 C . The incubation times at these temperatures range from 24 to 34 days (Wodinsky 1972). Vevers (1961) reported that O. vulgaris died from 45 to 61 days after laying eggs . Van Heukelem (1973) reported for O . cyanea a mean life expectancy of 35 days, with a range of from 22 to 50 days, after egg laying . Therefore, female octopuses may live up to about 3 . 5 weeks after hatching of the eggs . The present data indicate that death follows egg laying in approximately the same time, regardless of the continued presence of eggs. Because the water temperature was the same for simultaneously brooding

809

octopuses, differences in longevity may be a function of the initial body weight, and how well the octopus can withstand the tremendous weight loss that reproduction seems to entail . Octopuses weighing more than 600 g survived 40 or more days, whereas those weighing less lived 17 to 28 days after laying eggs . Discussion A series of apparently irreversible events begins about 2 weeks before female O . vulgaris lays eggs. These include a decreased food intake and a change in the technique for obtaining molluscan food from boring to extracting the body of the snail without boring . As a consequence, the female loses a large proportion of its body weight . These changes commence as egg laying nears, prior to the actual spawning, and persist thereafter, even in the absence of the eggs themselves . During the week immediately preceding spawning, almost no feeding occurs . For the moment, we may view the factors involved in boring and its cessation as separate from the question of the determinants of the amount of food eaten . We may then briefly consider three hypotheses, two non-food and one food-related, to account for the removal of the snail from its shell (and the killing of crabs) . The first non-food related hypothesis is that the brooding female kills to defend the eggs . Since gestating females prior to egg laying, females who have discarded infertile eggs, and females from which the experimenter has removed the eggs all show the pattern, the eggs as environmental stimuli are not necessarily implicated . No defensive postures or coloration were observed. The increase in time for extracting the snail from about one per day to one every 2 . 7 days, on the average, questions why the defence took so long. No snails are extracted during the week preceding egg laying . The second non-food related explanation is that the octopus extracts the snail as part of its well-known habit of manipulating and exploring objects in its environment . However, other evidence collected at this laboratory does not support this possibility . During the course of maintaining several hundred octopuses for protracted periods of time (up to 1 year), several, in non-reproductive condition, have suddenly and permanently ceased eating for 2 or 3 months prior to death . Although snails were continuously available, they were not extracted, nor were the shells bored .



810

ANIMAL BEHAVIOUR, 26, 3

A food-related hypothesis, which has some experimental support, is that the octopus's toxic secretion is inhibited, in some way, thereby necessitating the use of force . This would also serve an adaptive function of protecting the eggs against possible deleterious effects from the posterior salivary secretion . The next section explores this hypothesis further. The Shift From Boring to Pulling Barlow et al . (1974) ligated the posterior salivary duct, in the walls of which run secretory and efferent nerves from the superior buccal hole of the brain to the posterior salivary glands, and reported that there was an accumulation of neurosecretory products (noradrenaline and 5-hydroxytryptamine) on the brain side of the ligature . I have ligated the duct from the posterior salivary glands in normal, nonreproductive, octopuses . They killed and ate crabs without the toxin (Young 1965) . More interestingly, there was an immediate and permanent cessation of boring . Thereafter, all snails were pulled out of the shell and eaten . If we may extrapolate this result to the onset of reproduction, it suggests that there may be a specific inhibitory effect of an (gonadotrophic?) hormone either upon the posterior salivary glands directly or indirectly via the brain lobes controlling its secretion . The gradual decline of boring as spawning nears and the fact that 23 of the first 27 shells that were bored, after egglaying, were within the first four shells taken, supports this interpretation . Several functions : poisoning, digestive and excretory, have been attributed to the secretion from the posterior salivary glands (Arvy 1960). To these we may add a possible, though unlikely role as a decalcification agent in softening or dissolving the calcium carbonate shell during boring. Sakaguchi (1968) found a 96 .2 decrease in the proteolytic activities of the posterior salivary glands' extract from O . vulgaris after spawning relative to virgin octopuses . Although this suggests an inhibition of posterior salivary gland activity after spawning, it remains to be assessed whether there is a concomitant reduction of the toxic secretion, and whether the remaining 4 % of the secretion is sufficient for poisoning prey. The above-reported result, namely, that snails are extracted after ligation of the salivary duct, eliminates the necessity of hypothesizing that, where there is no borehole under normal feeding, the posterior salivary secretion may be

put directly into the aperture of the shell to affect the snail . The octopus clearly possesses the strength to pull the snail out by force alone (Parker 1921 ; Dilly et al. 1964 ; Dilly & Nixon 1965 ; Trueman & Packard 1968) . The present data, however, do not constitute an explanation of the previously reported finding that some non-reproductive octopuses prefer to use force to boring, either occasionally or predominantly (Fujita 1916 ; Pilson & Taylor 1961 ; Arnold & Arnold 1969 ; Wodinsky 1969) . Consumatory and Instrumental Feeding Responses of the Brooding Octopus The literature regarding the brooding female's feeding behaviour is extremely contradictory . In the first modern observation, Lee (1875) reported, for 0 . vulgaris, `Aristotle asserted that while the female is incubating she takes no food . This is incorrect' . Table V lists all of the reports of post-spawning feeding that I have found. Egg laying, brooding, and death of the female are reported in interesting observations of 0 . ocellatus (Yamamoto 1941) and for 0 . variabilis typicus (Yamamoto 1942), but no information about the food intake of the female is provided . Van Heukelem (1973) reported that female 0 . cyanea killed and dismembered, but did not eat, crabs . Two females, however, ate their eggs . Both of these findings are common . Most of the entries in Table V represent casual observations based upon an accidental occurrence of egg laying, more than half of these reports being based upon a sample size of one . Where contradictory reports on the same species exists, greater probative weight must be given to positive observations. At the present time the existence of possible differences between species must be acknowledged . This is particularly true of Hapalochlaena maculosa which holds the eggs with its suckers unlike almost all other reported species which attach the eggs to some substratum. The only quantitative data are those of Borer (1971) for eight female 0. briareus and of Joll (1976) for one specimen of 0 . tetricus . Borer (1971) reported that female O . briareus reduced its food intake by about 50 % of the normal amount beginning about 2 weeks before, and continuing for the first 3 weeks following, egg laying . During the 64 post-spawning days that it lived . the single female 0 . tetricus ate about 74 % less food than during the 48 prespawning days (Joll 1976) .



WODINSKY : FEEDING OF BROODY OCTOPUS

Sakaguchi (1968) found a marked decrease in the proteolytic activities of the posterior salivary glands and the hepato-pancreas after spawning . Extracts of these glands from females that had spawned exhibited only 3 . 8 % and 8 . 1 respectively of the proteolytic activity of extracts from virgin octopuses . It should be noted, on the one hand, that this decrease in the proteolytic activity of the digestive process affects the Table V. Reports of Post-Spawning Feeding in Octopus

Species 0. vulgaris

Feed while brooding Yes

No 0. joubini

Yes

No 0 . briareus

Yes

0 . apollyon

No Yes No

0. dofleini martini 0 . bimaculoides

Yes Yes No

0. maorum 0 . hummelincki

Yes Yes

0. tetricus Eledone cirrosa Hapalochlaena Sp . (prob . lunulata) H. maculosa

Yes Yes Yes

0. cyanea

No

0. bimaculatus 0. aegina

No No

0. luteus 0. maya 0 . dollfusi 0. rubescens Robsonella australis

No No No No No

No

Reference

Lee (1875), Lo Bianco (1909), Wells & Wells (1959), Vevers (1961), Mangold-Wirz (1963), Sakaguchi (1968), Mangold & Boletzky (1973) Grimpe (1928), Heldt (1948), Wood (1963) Boletzky & Boletzky (1969), Thomas & Opresko (1973), Opresko & Thomas (1975), Wodinsky, Mather & Fraser (Unpublished observation) Mather (1972), Bradley (1974) Wolterding (1971), Borer (1971), Opresko & Thomas (1975) Messenger (1963) Fisher (1923) Fisher (1925), MacGinitie & MacGinitie (1968) Gabe (1975), Okubo (1973) Wodinsky (Unpublished observation) MacGinitie & MacGinitie (1968) Batham (1957) (Unpublished Wodinsky observation) Joll (1976) Mangold et al. (1971) Overath & Boletzky (1974) Dew (1959), Sutherland & Lane (1969), Tranter & Augustine (1973) Dew 1959), LeSoeuf & Allen (1933, 1937), van Heukelem (1973) Fox (1938) Eibl-Eibesfeldt & Sheer (1962) Arakawa (1962) Walker et al . (1970) Sarvesan (1969) Warren et al . (1974) Brough (1965)

81 1

ingestion of amount of food . On the other hand, Sakaguchi (1968) reported that the proteolytic activity is quite high as compared with fish such as yellowtail and mackerel, and that the octopus, even after spawning, shows higher activity than these fishes . It may therefore be premature to conclude, as Van Heukelem (1973) has done, that the octopus is unable to digest its smaller meal . The present report clearly indicates that all observed 0 . vulgaris females about to lay eggs, and after laying eggs, eat. The ratio of the amount eaten during the reproductive period to the normal period preceding it varied from 13 % to 72 % per meal, with a mean ratio of about 35 % per meal . Thus, by the consumatory measure of food intake, there is a reduction of food intake during the reproductive period . This suggests that the octopus is less motivated for food . On the other hand, it is clear that effort is required to extract the living snail from its shell . No data exist which measure the energy (forcetime function) required to pull the living snail out of its shell, but human attempts to do so indicate that great effort is necessary . Effort is also required for the octopus to bore a hole in the shell . Thus, by the instrumental response measure of work, or energy expended, the brooding octopus appears highly motivated to obtain food . The octopus may be increasingly hungry, exaggerated by (1) the energy expended to extract the snail or to bore the shell ; (2) the continuing enormous body weight loss ; (3) the energy expended in increased ventilation rate (Vevers 1961) perhaps to aerate the eggs ; and (4) the reduction of food intake . The data therefore indicate a combination of effort expended to obtain food with a concomitant reduction of food intake . Recent evidence supports the hypothesis of direct effects of female hormones upon feeding centres in the mammalian brain . Wade & Zucker (1970) found that the majority of rats given oestrogen into the ventromedial-arcuate region showed a 10 to 20 % decrease in food intake . The broody octopus shows a mean decrease of about 70 per meal . The feeding behaviour of the broody female octopus may be a unique natural phenomenon . A decrease in hunger, or the inhibition of ingestion, may have the evolutionary adaptive function of attaching the female to the lair and eggs, of guaranteeing aeration of the eggs, of defending the eggs against predators and of



812

ANIMAL BEHAVIOUR,

preventing cannibalism of the eggs . The fact that the broody female seems to work to obtain food, leaves the eggs, and may eat the eggs, seems to be at variance with this adaptive function . We have demonstrated that the broody female 0. vulgaris shows a reduction in food intake and a change in its method of feeding upon molluscan prey. However, we should stress that the results are obtained under artificial conditions where the octopus need not leave its eggs to forage . What occurs in a more natural condition is not known . The only information which this investigator has is provided by an observation reported by Dr H. Moeller and Mr P. Knight that they discovered a clutch of unattended octopus eggs in the field . However, it may be, of course, that the female started to lay and then changed location, or that a predator killed the female. It may also be that the female left the eggs to forage for food . Acknowledgments This research was supported by grants from the U.S . Public Health Service MH 18250-01 and from National Institutes of Health Institutional Grant 7044-04 to Brandeis University . It was conducted at the Lerner Marine Laboratory, Bimini, Bahamas, a field station of the American Museum of Natural History . I thank the Director, Mr Robert F . Mathewson . REFERENCES Arakawa, K . Y. 1962. An ecological account on the breeding behavior of Octopus luteus (Sasaki) . Venus, 22, 176-180 . Arnold, J. M . & Arnold, K . O. 1969. Some aspects of hole-boring predation by Octopus vulgaris. Am. Zool., 9, 991-996. Arvy, L. 1960 . Histoenzymological data on the digestive tract of Octopus vulgaris Lamarck (Cephalopoda) . Ann. N. Y. Acad. Sci., 90, 929-949 . Barlow, J. J ., Juorio, A . V. & Martin, R . 1974. Monoamine transport in the octopus posterior salivary gland nerves . J. comp . Physiol., 89, 105-122 . Batham, E . J. 1957 . Care of eggs by Octopus maorum . Trans. Roy. Soc. New Zealand, 84, 629-638 . von Boletzky, S . & von Boletzky, M . V. 1969 . First results in rearing Octopus joubini Robson, 1929 . Verhandl. Naturf. Ges. Basel., 80, 56-61 . Borer, K. T. 1971 . Control of food intake in Octopus briareus Robson. J. comp . physiol. Psychol., 75, 171-185. Bradley, E . A . 1974 . Some observations of Octopus joubini reared in an inland aquarium . J. Zool. Lond., 173, 355-368 . Brough, E. J. 1965. Egg-care, eggs and larvae in the midget octopus, Robsonella australis (Hoyle) . Trans. Roy. Soc . New Zealand, Zool., 6, 7-19. Dew, B . 1959. Some observations on the development of two Australian octopuses . Proc. Roy . Zool. Soc. New So. Wales, 1957/1958, 44-52 .

26, 3

Dilly, N. & Nixon, M. 1965 . Further observations on forces exerted by Octopus vulgaris . Pubbl. staz. zool. Napoli, 34, 340-345 . Dilly, N., Nixon, M . & Packard, A . 1964 . Forces exerted by Octopus vulgaris. Pubbli staz . zool. Napoli, 34, 86-97. Eibl-Eibesfeldt, I . & Scheer, G . 1962. Das Brutpflegeverhalten eines weiblichen Octopus aegina Gray. Z. Tierpsychol., 19, 257-261 . Fisher, W. K . 1923. Brooding-habits of a cephalopod . Ann. Mag . Nat. Hist., 12,147-149 . Fisher, W . K. 1925. On the habits of an octopus. Ann . Mag . Nat. Hist., 15, 411-415 . Fox, D . L. 1938 . An illustrated note on the mating and egg-brooding habits of the two-spotted octopus . Trans . San Diego Soc . Nat. Hist., 9, 31-34. Fujita, S. 1916 . On the boring of pearl oysters by Octopus (Polypus) vulgaris Lamarck. Dobytsugaku Zasshi, 28, 250-257. (In Janapese.) Gabe, S . H . 1975. Reproduction in the giant Octopus of the North Pacific, Octopus dofleini martini . Veliger. 18(2), 146-150 . Gravely, F . H . 1908. Notes on the spawning of Eledone and on the occurrence of Eledone with the suckers in double rows . Mem. Proc . Manchr. lit . phil. Soc., 53, 1-14 . Heldt, J. H . 1948 . Observations sur une ponte d'Octopus vulgaris Lmk . Bull. Soc. Sci. nat. Tunis, 1, 87-90. Joll, L. M. 1976. Mating, egg-laying and hatching of Octopus tetricus (Mollusca : Cephalopoda) in the laboratory. Mar . Biol., 36, 327-333 . Lee, H . 1875 . The Octopus. London : Chapman & Hall . Le Soeuf, A . S . & Allen, J. K . 1933 . Habits of the Sydney Octopus (Octopus cyaneus) in captivity . Aust. Zool., 7, 373-377 . Le Soeuf, A . S . & Allan, J. K . 1937. Breeding habits of a female octopus . Aust. Zool., 9, 64-67. Lo Bianco, S . 1909 . Notizie biologiche riguardanti specialmente it periodo di maturita sessuale degli animale del Golfo di Napoli . Mitt. zool . Stn. Neapel, 19, 513-761 . MacGinitie, G. E . & MacGinitie, N . 1968 . Natural History of Marine Animals. New York : McGrawHill . Mangold, K ., Boletzky, S . von & Frosch, D . 1971 . Reproductive biology and embyronic development of Eledone cirrosa (Cephalopoda : Octopoda) . Mar . Biol., 8, 109-117 . Mangold, K. & Boletzky, S. von 1973 . New data on reproductive biology and growth of Octopus vulgaris. Mar. Biol., 19, 7-12 . Mangold-Wirz, K. 1963 . Biologie des cephalopodes benthiques et nectoniques de la Mer Catalane . Vie Milieu (Suppl .), 13, 1-285 . Mather, J . A . 1972. A preliminary study of the behavior of Octopus joubini Robson, 1929 . M.A. thesis, Florida State University. Messenger, J. B . 1963 . Behaviour of young Octopus briareus Robson, Nature, Lond., 197, 1186-1187 . Nixon, M. 1966. Changes in body weight and intake of food by Octopus vulgaris . J. Zool. Lond., 150,1-9 . Okubo, S . 1973. The hatching of eggs of the giant pacific octopus, Paroetopus dafleini dofelni. J. Jap . Assoc . Zool. Gardens & Aquar., XV, No . 1 . (In Japanese .) Opresko, L. & Thomas, R . 1975 . Observations on Octopus joubini: Some aspects of reproductive biology and growth. Mar . Biol., 31, 51-61 .



WODINSKY : FEEDING OF BROODY OCTOPUS Overath, H. & Boletzky, S . von 1974 . Laboratory observations on spawning and embryonic development of a Blue-ringed Octopus. Mar. Biol., 27, 333-337 . Parker, G. H . 1921 . The power of adhesion in the suckers of Octopus bimaculatus Verrill. J. exp . Zoo!., 33, 391-394 . Pickford, G . E. & McConnaughey, B. H. 1949 . The Octopus bimaculatus problem, a study in sibling species . Bull. Bingham oceanogr. Coll., 12,1-66. Pilson, M . E . Q . & Taylor, P. B . 1961 . Hole drilling by octopus . Science, N. Y., 134,1366-1368 . Sakaguchi, H . 1968. Studies on digestive enzymes of devilfish . Bull. Jap. Soc . sci. Fish ., 34, 716-721 . (In Japanese.) Sarvesan, R. 1969. Some observations on parental care in Octopus dollfusi Robson (Cephalopoda : Octopodidae) . J. Mar. Biol. Ass. India, 11 (1 and 2), 203-205 . Sutherland, S. K. & Lane, W . R . 1969. Toxins and mode of envenomation of the common ringed or bluebanded octopus. Med. J. Aust ., 1, 893-898 . Taki, 1 . 1944 . Studies on Octopus 2 . The sex and genital organs. Jap. J. Malac ., 19, 267-310. (In Japanese .) Thomas, R. F. & Opresko, L. 1973 . Observations on Octopus joubini: Four laboratory reared generations. Nautilus, 87, 61-65. Tranter, D . J . & Augustine, O. 1973 . Observations on the life history of the blue-ringed octopus, Hapalochlaena maculosa. Mar . Biol., 18,115-128 . Trueman, E. R. & Packard, A . 1968. Motor performances of some cephalopods . J. exp. Biol., 49,495-507 . Van Heukelem, W . F . 1973 . Growth and life-span of Octopus cyanea (Mollusca : Cephalopoda) . J. Zoo!. Lond., 169, 299-315 . Vevers, H. G. 1961 . Observations on the laying and hatching of octopus eggs in the society's aquarium . Proc. zool. Soc. Lond.,137, 311-315. von Grimpe, G . 1928 . Pfiege, Behandlung and Zucht der Cephalopoden fdr zoologische and physiologische Zwevke. In : Handbuch der biologischen Arbeitsmethoden . Vol . 9 (Ed . by E. Abderhalden), pp . 331-402. Berlin : Urban and Schwarzenberg .

813

Wade, G . N. & Zucker, I. 1970. Modulation of food intake and locomotor activity in female rats by diencephalic hormone implants. J. comp . physlol. Psycho!., 72, 328-336 . Walker, J . J ., Longo, N. & Bitterman, M . E . 1970 . The octopus in the laboratory : Handling, maintenance, training . Behav. Res. Meth . Instru ., 2,15-18. Warren, L . R ., Scheier, M . F. & Riley, D . A . 1974. Colour changes of Octopus rubescens during attack on unconditioned and conditioned stimuli . Anim . Behav., 22, 211-219. Wells, M . J . 1960. Optic glands and the ovary of Octopus. Symp . zool. Soc. Lond., 2, 87-107. Wells, M . J. & Wells, J . 1959. Hormonal control of sexual maturity in Octopus . J. exp . Biol ., 36, 1-32 . Wodinsky, J . 1969 . Penetration of the shell and feeding on gastropods by Octopus . Am . Zool., 9, 997-1010. Wodinsky, J. 1972 . Breeding season of Octopus vulgaris . Mar. Biol., 16, 59-63 . Wodinsky, J . 1973a. Mechanism of hole-boring in Octopus vulgaris. J. gen . Psychol., 88, 179-183 . Wodinsky, J. 1973b. Ventilation rate and copulation in Octopus vulgaris . Mar. Biol., 20, 154-164 . Wolterding, M . R . 1971 . The rearing and maintenance of Octopus briareus in the laboratory, with aspects of their behavior and biology . M .A . thesis, University of Miami. Wood, F . G. 1963 . Observations on the behavior of octopus. Int. Congr..,16, Zoo! 73 . Yamamoto, T . 1941 . The breeding habits of Octopus ocellatus Gray, with observations on its hatched young. Botany and Zoo!., 9. 9-14 . (In Japanese .) Yamamoto, T. 1942 . On the ecology of Octopus variabilis typicus (Sasaki) with special reference to its breeding habits . Venus, 12, 9-20 . (In Japanese.) Young, J . Z. 1965 . The nervous pathways for poisoning, eating and learning in Octopus . J. exp . Biol., 43, 581-593 . (Received 17 July 1972 ; revised 20 April 1973 ; 2nd revision 6 June 1974 ; 3rd revision 5 April 1977 ; MS . number : A1354)