Life history and den ecology of Octopus briareus Robson in a marine lake

J. Exp. Mar. Biol. Ecol., 1986, Vol. 95, pp. 37-56

37

Elsevier

JEM 609

LIFE HISTORY A N D D E N ECOLOGY OF OCTOPUS BRIAREUS Robson IN A MARINE LAKE

RICHARD B.

ARONSON 1

Department of Organismic and Evolutionary Biology, Harvard University, The Biological Laboratories, Cambridge, MA 02138, U.S.A. (Received 3 June 1985; revision received 25 July 1985; accepted 8 October 1985)

Abstract: Sweetings Pond, a saltwater lake on Eleuthera Island, Bahamas, supported a high-density population of Octopus briareus Robson. Females spawned throughout the year in 1982-83, but spawning peaked in February-March. A number of females spawned early and unsuccessfully in August, 1982. This event was followed in October by a reduction in adult density, and it may have caused late recruitment the following summer. Under natural conditions in Sweetings Pond, O. briareus occupied cavities underneath a variety of benthic formations. In field choice experiments with artificial dens, adult O. briareus displayed minimum cavity length and diameter requirements. Restricted entrances were not preferred, perhaps due to the availability of material with which O. briareus could block their den entrances. A tactile examination of the cavity was important in selection, but visual discrimination was also involved; translucent dens were completely avoided in favor of opaque ones. Certain sponge species were rarely occupied by O. briareus because they lacked sufficient cavity space underneath. When artificial dens were placed underneath these sponges they were occupied. Den defense was examined with a nearest neighbor experiment in which three pairs of artificial dens were placed in a study area. Dens were set 0, 15 and 50 cm apart and the frequency with which both dens of a pair were simultaneously occupied was recorded. The contiguous dens were never simultaneously occupied, whereas the other two pairs were simultaneously occupied with approximately equal frequency. Direct observations of intraspecific interactions confirmed the small size of the defended area. Abundant predatory fishes probably limit Octopus populations off the Eleuthera coast, and the absence of such fishes from Sweetings Pond may account for the high O. briareus density there. Though not subject to interspecific predation, lake O. briareus required the protection of dens due to cannibalism. Only a small minority of benthic formations in the lake were consistently occupied in 1982-83, and enriching areas with artificial dens increased local density. This suggests that dens were limiting in Sweetings Pond. With suitable cavities so widely spaced, den defense probably did not influence density apart from limiting occupation to one octopus per cavity. No Octopus occupied artificial dens in a coastal enrichment experiment, implying that dens were not limiting off the coast.

Key words: Bahamas; den ecology; life history; marine lake; Octopus briareus INTRODUCTION

Octopuses are an economically significant food resource throughout much of the world, yet only in recent years have ecologists begun to study them in the field. Many researchers have been deterred by the difficulties inherent in working with such elusive and highly mobile animals. Octopuses are found in a variety of coastal habitats where they face severe competition and predation pressure from fishes; nevertheless, they are Present address: Department of Pure and Applied Zoology, University of Reading, Whiteknights, Reading RG6 2AJ, U.K. 0022-0981/86/$03.50 © 1986 Elsevier Science Publishers B.V. (Biomedical Division)

38

RICHARD B. ARONSON

themselves important predators in a number of coastal benthic communities (Yarnall, 1969; Packard, 1972; Fotheringham, 1974; Simenstad et al., 1978; Ambrose & Nelson, 1983; Fawcett, 1984). The determinants of octopus density are largely unknown, with the result that geographic variations are currently beyond our explanatory power. Equally elusive are the causes of occasional octopus "plagues" in the English Channel (Rees, 1950) and the octopus population explosion off Peru associated with the 1982-83 E1 Niflo event (Arntz, 1984). Having lost the external shell of their ancestors and thus achieved high mobility in the face of the Mesozoic marine vertebrate radiations (Packard, 1972), benthic octopods must rely on naturally-occurring cavities, or dens, for protection from predation. Therefore, it is essential to their survival that they have the behavioral capability to choose dens that will actually afford good protection. Although shelter preferences have been investigated for various marine crustaceans (Serene, 1954; Hazlett, 1962, 1981; Cobb, 1971; Reaka, 1980; Scully, 1983), the only detailed studies of Octopus den selection are those of Butterworth (1982) and Mather (1982a) on O. joubini. Most of their experiments employed natural dens - mollusk shells in this case. The experiments reported here made extensive use of artificial dens, in which single dimensions and other physical characteristics could be carefully controlled. Decreasing the availability of high-quality shelters might increase the frequency and intensity of agonistic interactions between octopuses, as it does in hermit crabs (Vance, 1972; Scully, 1983) and stomatopods (Dingle, 1983). Researchers have explored the possibility of octopus territoriality for a number of years, but the results have been inconclusive. Woods (1965) and Cousteau & Diol6 (1973) present anecdotal observations of territorial behavior by O. vulgaris in the Mediterranean; however, Altman (1967) and Kayes (1974) found no evidence for such interactions. A study ofO. dofleini off Vancouver Island, British Columbia (Hartwick et al., 1978a) revealed that their dens were spaced more evenly than expected in a random distribution. This result, combined with an observation of intraspecific fighting over a den (Kyte & Courtenay, 1977), supports the commonly held view that the species is territorial (Hartwick et al., 1978a). On the other hand, Hartwick et al. (1978b) observed two O. dofleini in a single den. The requirement of a large feeding area may have caused the observed overdispersion of O. cyanea dens off Hawaii, even though feeding territories were not defended (Yarnall, 1969). Under aquarium conditions, investigators have found linear, size-based dominance hierarchies in octopods (Mangold& Boucher-Rodoni, 1973; Dorsey, 1976; Van Heukelem, 1977; Boyle, 1980; Mather, 1980). Such hierarchies may have been due to artificial crowding of normally territorial animals. Bovbjerg (1956), for example, discusses this effect with respect to crayfish, and Mather (1982b) explicitly raises the issue for O. joubiniunder laboratory conditions. By contrast, O. bimaculoides are very tolerant of crowded aquarium conditions, and it is not unusual for two or more animals to occupy a single length of plastic pipe (Hanlon & Forsythe, 1985; pers. comm.). Yarnall (1969) examined the behavior of O. cyanea in artificial ponds (seminatural conditions)

OCTOPUS ECOLOGY

39

and describes a dominance hierarchy based on size as well. However, O. cyanea did defend their dens, and smaller den occupants sometimes won in encounters with larger intruders. A few field studies have been conducted on the ecology of den selection in geographically disparate populations of O. vulgaris (Altman, 1967; Kayes, 1974; Tauchi & Matsumoto, cited in Mottet, 1975). More recently, detailed investigations have focused on the den ecology of single populations of three other species (O. joubini: Butterworth, 1982; Mather, 1982a,b; O. dofleini: Hartwick & Thorarinsson, 1978; Hartwick et al., 1978a,b, 1984; O. bimaculatus: Ambrose, 1982). Studies by E.B. Hartwick and associates have made the most progress toward determining whether there is a relationship among den selection, territoriality and dens as a limiting resource. They found a positive relationship between O. dofleini size and den cavity volume. When the octopuses were removed from an area, some of the vacant dens were occupied by incoming animals similar in size to the previous occupants. Both of these results suggest the importance of suitable physical dimensions to den selection (Hartwick et al., 1978a). Individuals were spaced evenly but territoriality did not influence density, as dens did not appear to be limiting (Hartwick et al., 1984). This paper concerns a dense natural population of Octopus briareus Robson in a saltwater lake in the Bahamas. I have suggested elsewhere (Aronson, in press) that the high Octopus density was a consequence of release from predation (absence of predatory fishes). Here I discuss the population biology and den ecology of O. briareus in the lake, and consider the interrelationship among den selection, den defense and den limitation. The importance of den limitation and predator limitation to a coastal Octopus population are also evaluated.

STUDY AREAS

Sweetings Pond, the saltwater lake, lies at the north end of Eleuthera Island, Bahamas (25°21'35"N : 76°30'40"W). It is 1.69 km long with a surface area of 0.92 km 2 and a maximum depth of 15.3 m. The lake apparently communicates with the nearby west coast of Eleuthera through one or more restricted subterranean passages. Within a depth range of 2-8 m, the benthos of Sweetings Pond was characterized by a "patch zone" of discrete sponge, Xestospongia, Halicometes, Suberites and Reniera; bivalve clump, chiefly Arca imbricata Brugirre; and coral, Porites astreoides Lamarck and P. porites (Pallas), both with Arca, formations. They either rested atop or were loosely buried in the sandy-to-silty sediment. Octopus briareus were found in cavities under the formations. The patch zone, although extensive in 1980, was restricted in area in 1982-83 (Fig. 1) by growth during the intervening period of a filamentous green alga, Cladophora crystallina (Roth). This alga formed large mats, which overgrew and smothered all sessile invertebrates. The Cladophora mats began to die back after June, 1982 and patch zone destruction ceased. While Octopus briareus occupied formations

40

RICHARD B. ARONSON

500

rn

Fig. 1. Map of Sweetings Pond, showing patch zone areas (dark) in 1983, including areas A and B: stippling represents sparse patch zone; diagonal shading indicates patch zone areas overgrown by Cladophora crystallina after May, 1982.

in other parts of the lake (limestone boulders near shore, dead coral heads exposed following Cladophora die-off), their greatest concentration was in the patch zone. One den limitation experiment was conducted off the west coast of Eleuthera. This coast is characterized by shallow ( < 5 m deep) coves, with sand or turtlegrass (Thalassia testudinum Koenig) bottoms. The two coves used were Annie Bight and Old Daughters Bight, a few kilometers northwest of Sweetings Pond and 1.6 km apart. In 1982-83, Sweetings Pond and Annie Bight water were similar in temperature, pH, dissolved oxygen content and salinity. Visibility was almost always lower in Sweetings Pond. Aronson (in press) presents a detailed description of the limnology, benthic biota and fish fauna of Sweetings Pond, as well as an account of its Octopus briareus population. This community, which also contained superabundant ophiuroids, had persisted for at least 10 yr by the time this study was conducted (Aronson & Harms, 1985). METHODS POPULATION BIOLOGY

Monthly censuses of the Sweetings Pond O. briareus population were taken from March, 1982 to July, 1983. Density estimates were obtained, beginning in April, 1982, from surveys of Study Plot 2, a 30 x 27 m portion of patch zone area A gfidded into 3-m squares with nylon line (Fig. 1; depth range 3.4-7.0 m). Surveys consisted of methodical SCUBA swims through the plot, during which divers carefully overturned and scrutinized every formation for O. briareus. When an animal was located, the formation in which it was found was noted and the octopus was measured (mantle length; Aronson, 1982; in press), sexed and examined for injuries (scars and severed or regenerating arms). The individual was then placed back in its den.

OCTOPUS E C O L O G Y

41

Similar surveys were made of the rest of area A starting in June, 1982. Parts of other patch zone areas (Fig. 1, diagonal shading) were surveyed from March-May, 1982; these latter areas were subsequently overgrown by Cladophora. A total area of 23 000 m 2 was thus censused monthly from March, 1982 to July, 1983. Surveys were conducted in the morning, when virtually all Octopus briareus in Sweetings Pond were in dens (Aronson, in press). Sex was determined by the presence of the hectocotylized third right arm in males and its absence in females. The groove and hectocotylus were discernible in males down to a mantle length (ML) of 3.5 cm. Dissections revealed that animals smaller than 4.5 cm ML were never mature, and these were lumped as "juveniles" (Aronson, 1982; in press). The few individuals that escaped before they could be examined thoroughly were still classifiable as adults or juveniles. DEN SELECTION

Octopus spp. readily occupy a variety of manmade objects, such as clay pots, bottles and old tires (Wolterding, 1971 for O. briareus; Cousteau & Diol6, 1973; Lane, 1974; Mottet, 1975; High, 1976). The artificial dens used in these experiments were constructed of clear acrylic tubing (0.32 cm wall thickness); the dimensions and entrance diameters tested are discussed on pp. 46, 47. For dens in which the entrance diameter was smaller than the tube inner diameter (ID), a solid cap was placed at one end of the tube and a cap with the desired entrance hole at the other (the front). Dens in which the entrance and tube diameters were equal were fitted at the front with a false cap lip and at the back with a cap-and-plug assembly that filled twice the tube volume of a single cap (single width: 0.81 cm; Fig. 2). Thus, it was possible to construct dens of the same outer and inner lengths, but with different entrance diameters. All parts were roughed with abrasive cloth ("blending") pads.

A

B Fig. 2. Exploded diagrams of acrylic dens: A, den in which entrance diameter is smaller than tube diameter; components, left to right: backing cap, tube, and entrance cap (with entrance hole); caps fit into tube; B, den of the same internal volume with open entrance; components, left to right: entrance cap, filler plug, tube, and false cap rim; filler plug fits into entrance cap to form double-width backing cap; false cap rim fits over outside of tube.

42

RICHARD B. A R O N S O N

Choice experiments were conducted at 3.7 m depth in the patch zone. Three or four dens were placed in random order at even intervals on the circumference of an imaginary 40-cm diameter circle on the substratum. The dens were covered with sandbags and their entrances faced the center of the circle. Experiments were checked daily in the morning. O. briareus often blocked their den entrances with small objects, and such blocking material was removed from unoccupied dens daily. Because 96~o of O. briareus encountered under natural conditions in Sweetings Pond were in dens in the morning, and because this population was highly mobile (Aronson, in press), empty, blocked dens indicated occupations of < 24 h. When one or more dens were occupied, the occupant(s) were measured, sexed and examined for injuries. Octopuses were released 50 m away. After an occupation, all dens in the experiment were cleaned and reset in new random positions (see pp. 46, 47 for sample sizes). Only adult O. briareus were considered in the den dimension experiments (mean ML 6.0 cm + 0.8 SD). To determine the effect of den opacity on suitability for occupation, two artificial dens of the same dimensions were used (600 cm 3, 5.1 cm ID, 30.5 cm long, 5.1 cm entrance diameter, chosen according to the results of the den dimension experiments). One den was blackened with electrical tape and the other left translucent (the tubes, again, were roughed). The procedure was the same as for the den dimension choice experiments except that the dens were not sandbagged, but were anchored with lead fishing weights. An acceptable datum was a case in which only one den of a choice experiment was occupied, by a naive octopus. All multiple occupation and repeat occupant data were rejected. Individuals were recognized on the basis of size, sex and injuries. SPONGE SELECTION EXPERIMENT

Two species of pancake-shaped, orange-colored sponges (Suberites sp. and Halicometes sp.) were common in the patch zone of Sweetings Pond, but were rarely used as dens by Octopus briareus (see p. 49). These sponges had a fiat morphology and, it was conjectured, did not in general have cavities under them of sufficient size for O. briareus occupation. To test this hypothesis, 10 pairs of Suberites sp. were located at the deep end of the patch zone (5.8-7.9 m depth), where they were most abundant (Aronson, in press). These sponges ranged in length from 17.5-37.0 cm and in width from 15.5-31.0 cm. A 600-cm 3, 5.1-cm ID acrylic den was pushed into the sediment beneath one sponge of each pair (determined at random), with the entrance protruding slightly from the sponge perimeter and facing the other sponge. The control sponge was disturbed to a similar degree but no den was placed underneath. Experimental and control sponges were 80-175 cm apart. Sponge pairs were checked every 3-4 days in the morning with an underwater light and blocking was removed from vacant dens. DEN D E F E N S E

A nearest neighbor experiment was conducted using 600-cm 3, 5.1-cm ID white polyvinyl chloride (PVC) tubes. These were capped tightly on one end with clean,

OCTOPUS ECOLOGY

43

yellow-painted metal jar caps (which did not rust appreciably). Three pairs of artificial dens were placed in the patch zone at 3.7 m depth. The pairs were arranged in an equilateral triangle, 8 m on a side. In one pair, the dens were 0 cm apart, and in the other two they were placed 15 and 50 cm apart (referred to as the 0-, 15-, and 50-cm dens, respectively). The tubes of each pair were set parallel to each other, with entrances facing in the same direction. The direction in which each pair faced was determined independently and at random from among eight possible compass directions, and the positions of the three pairs were randomized as well. Lead fishing weights anchored the PVC tubes, and the 0-cm dens were held together by two tan-colored rubber bands. For control, two rubber bands were also placed around each den in the other two pairs. The experiment was monitored daily in the morning. Again, blocking was removed from empty dens. When both dens of a pair were simultaneously occupied, the whole experiment was removed. Animals were measured, sexed and examined for injuries. The two octopuses from the same den pair were released 700 m away, in another part of the lake, to avoid their entering the experiment again; records of individuals confirmed the success of this procedure. Any other den occupants from that day were released near the experimental area. The latter release procedure was followed since no attempt was made to control other, unknown Octopus briareus that entered and left the experiment. This approach ensured that no animal occurred in more than one recorded double occupation. All tubes and caps were cleaned and dried, and the experiment was reset 24 h later, with den pair positions randomized again. A second den defense experiment allowed divers to observe interactions between individuals directly. In each of 18 trials, a SCUBA diver captured an O. briareus in the patch zone and measured and sexed it. Carrying the animal in one hand, he swam to a nearby occupied (natural) den, assessing occupancy by gently and slightly lifting the formation. The diver then placed the octopus he had been carrying (the "intruder") on the substratum ~ 0.5 m from the den and nudged it in that direction. The immediately ensuing interaction was recorded. The diver then captured, measured and sexed the occupant. A different, naive occupant was used in each trial (3.0-8.0 cm ML). All occupied dens used in this experiment had more than one passage into and out of them since formations were not attached to the substratum.

DEN LIMITATION

The frequency distribution of natural formation occupations was obtained from the monthly surveys of Study Plot 2. Frequency was defined as the number of times that a formation was occupied by different O. briareus during the 16 months of surveys. If a formation contained what might have been the same animal in consecutive months (on the basis of size, sex and injuries), the possible duplicate counts were eliminated from the data set. In each of four den enrichment experiments, 15 600-cm 3, 5.1-cm ID PVC tubes were placed in a 15 × 15 m plot, which was gridded into 3-m squares. The tubes were capped

44

RICHARD B. ARONSON

at one end and anchored with lead fishing weights. They were placed in the centers of randomly chosen squares, with a maximum of one tube per square. The direction in which each artificial den faced was also random. Gridded plots of the same size without artificial dens served as controls. Experiments ran for 15 days, and the experimental and control plots were censused before and after the den enrichments. In the first two experiments, the control and experimental plots were 100 m apart in area A, and in Experiments 3 and 4 the control was in area A and the experimental was 625 m away, in area B (Fig. 1). The depth range of the plots was 2.4-4.6 m. At the end of each experiment, occupants of the artificial dens were released in the experimental plot and the PVC tubes removed. No individual was recorded in more than one experiment. A coastal den enrichment experiment was identical in design and duration. Dens were added to a plot in the center of Old Daughters Bight (sand bottom) and examined after 15 days. The control site was a sandy area of Annie Bight. Bottom depth ranged from 3.5-4.3 m in these plots.

RESULTS POPULATION BIOLOGY

Sweetings Pond contained Octopus briareus at high density; the 1982-83 mean for Study Plot 2 (Fig. 3) was 7.9 ind/1000 m 2 + 3.6 SD. Divers encountered octopuses 775 times during 393 SCUBA and snorkel dives. By contrast, only four octopuses were sighted in 166 dives during the same 17 months off the west coast of Eleuthera

13II-

~E 9-i 0 -

,' /i

CO 7 -

Z

I T T - T

f

T

I

I

[ -I~

A M J d A S 0 N D J F M A M d J 1982 1983

MONTH Fig. 3. Monthly Octopus briareus density variation in Study Plot 2 (O): A, additional surveys of the same area.

OCTOPUS ECOLOGY

45

(three O. briareus a n d one O. macropus Risso, all in Annie Bight). The highest density ever r e c o r d e d in the lake was 15.2 ind/1000 m 2 + 2.8 SD, b a s e d u p o n three surveys of a 30 x 30 m p a t c h zone plot in July, 1980. In July, 1982, the m e a n was similar (ll.7ind/1000m2+0.9SD, N=2); however, a m a r k e d l y lower density of 3.7 ind/1000 m 2 was o b t a i n e d in July, 1983. Octopus briareus was the only c e p h a l o p o d in Sweetings Pond. Fig. 4 A shows the p r o p o r t i o n o f females that were b r o o d i n g eggs each month. Peaks

1.00- ~ Females with eggs

0.60b

0.20 50

20

I0 f-

"S

C o Females

r~ 15 E Z I0-

_

1982

1983

Fig. 4. Results of monthly Octopus briareus surveys over 23000 mz of Sweetings Pond patch zone: A, fraction of females that were brooding eggs; note that no females were found at all in April, 1982; B, number of adults (A) and juveniles (A); C, number of females (O) and males (m).

46

RICHARD B. ARONSON

of brooding activity occurred in March, 1982 and February-March, 1983, these peaks being followed by precipitous declines in the frequency of egg-brooders (Fig. 4A) and adults generally (Fig. 4B), and by increases in the number of juveniles (Fig. 4B). There was also a smaller reproductive peak in August, 1982. This was followed in October by a drop in the number of adults, with no rise in the number of juveniles (Fig. 4B). Total density thus dropped dramatically that month (Figs. 3, 4B), and after the drop it never again reached the high level of the previous summer. Juvenile numbers peaked considerably later in 1983 than they did in 1982 (Fig. 4B). The 1983 decrease in brooding females was more shallow, and this was accompanied by a shallower subsequent rise in juvenile abundance (Fig. 4A, B). The July ratio of adults to juveniles was significantly different between the two years (Z 2 = 10.44, df = 1, P < 0.005). Surveys in July, 1980 yielded 29 adults and 5 juveniles, not significantly different from July, 1982 (Z 2 = 0.025, P > 0.50), but significantly different from July, 1983 (Z 2 = 11.83, P < 0.005). The adult sex ratio was not significantly different from unity in July, 1980 (15 males and 13 females), nor was it in 1982-83 except for March, 1982 (1 male and 12 females; P = 0.003, two-tailed binomial test; Fig. 4C). Juveniles did not deviate significantly from a 1 : 1 sex ratio in April, 1982 (Aronson, in press). DEN SELECTION

In two experiments in which tube volume was held at a constant 600 cm s and inner diameter varied, the 31.2-cm long, 5.1-cm ID tube was preferred (Table IA). Tubes 16.4 cm long of variable ID (2.5, 5.1, 10.2, and 14.6 cm) were not occupied in 17 days in Sweetings Pond. Of four 31.2-cm long artificial dens tested (Table IB), the 2.5-cm ID one was avoided and the other three were occupied with frequencies not significantly different from an even distribution. Among these latter was a 600-cm 3, 5.1-cm ID den. When 5.1-cm ID tubes of varying lengths were tested (Table IC), the 600- and 1200-cm 3 ones were preferred and were occupied with frequencies not significantly different from each other. Since 600-cm 3, 5.1-cm ID tubes were occupied readily in the above experiments, they were employed in all subsequent artificial den experiments. Given the choice between a 5.1-cm diameter entrance and a smaller entrance size, O. briareus neither preferred nor avoided a 2.5-cm entrance diameter (occupation ratio 5 : 5, P = 1.00; two-tailed binomial test) and avoided a 1.3-cm entrance completely (10:0, P = 0.002). Observations revealed that the 1.3-cm entrance was avoided because the octopuses could not fit through them easily. Animals confined in 5.1-cm ID tubes with 1.3-cm diameter entrances freed themselves with varying degrees of success. Two 5-cm ME individuals became stuck and apparently died of asphyxiation while attempting to escape. A 7.5-cm animal remained overnight in such a den. On the other hand, three individuals of mantle lengths 3.0, 4.5, and 5.0 cm escaped. In the den opacity experiment, only the opaque den was occupied in 10 out of 10 trials (P = 9.8 x 10-4; one-tailed binomial).

OCTOPUS ECOLOGY

47

TABLE I Results of den selection experiments with adult Octopus briareus:ID, inner diameter; a tube outer length (see text); b two-tailed binomial test. A. Constant volume (600 cm 3)

Tube ID (cm)

Tube length a (cm)

2.5 5.1

119.1 31.2

5.1 10.2 14.6

31.2 9.0 9.0

Frequency of occupation 0 11 I 9.8 × 10

P 4,1,

19 ~ <0.005; ~(2 = 38.00, 0 0 ~ df= 2

B. Constant length (31.2 cm)

Tube ID (cm)

Tube volume (cm 3)

2.5 5.1 10.2 10.2 with 5.1 entrance

150 600 2400 2400

Frequency of occupation 0 4 ~ >0.50; 6 X2 = 2.80,[ 10 ~ df = 2 j

P

<0,025;

Z2

= 10.40, df = 3

C. Constant ID (5.1 cm)

Tube length (cm)

Tube volume (cm 3)

9.0 16.4 31.2 60.8

150 300 600 1200

Frequency of occupation

P

0 | 1 ~ <0.025; ([ Z 2=<0"005;17.20, 11 / 0.648b j- g 2 = 7.90, df 3 8 ~ df = 2

/

SPONGE SELECTION EXPERIMENT

The experimental sponges (tubes added) were occupied 10 out of 10 times; the controls were never occupied (P = 9.8 × 10-4; one-tailed binomial). DEN D E F E N S E

In the nearest neighbor experiment, the 15- and 50-cm dens were simultaneously occupied at approximately the same frequency, but the 0-cm dens were never simultaneously occupied (Table II). A goodness-of-fit test with all occupant categories combined revealed a significant deviation of frequencies of simultaneous occupation from an even distribution (Z 2 = 7.60, df = 2, P < 0.025). A one-tailed binomial test showed that the 0-cm dens were simultaneously occupied at a frequency significantly lower than expected on a random basis (P = 2.3 × 10-3). This was also true for the

48

RICHARD B. ARONSON TABLE II

Results of nearest neighbor experiment with Octopus briareus, showing breakdown of simultaneous occupations by sex and life stage: a den pair designations: "x-cm dens" refers to a pair x cm apart. Number of simultaneous occupations by den paira Den occupants

0-cm dens

15-cm dens

50-cm dens

Total

Adult male, adult female Two adult males Two adult females Adult male, juvenile male Adult male, juvenile female Adult female,juvenile female

0 0 0 0 0 0

3 1 1 1 0 2

3 0 0 1 3 0

6 1 1 2 3 2

Total

0

8

7

15

0-cm dens when double occupations by animals of opposite sexes were considered alone (zero out of nine simultaneous occupations in the 0-cm dens; P = 0.026). Most likely, a larger sample size would have produced the same result for same-sex simultaneous occupations (zero out of six in the 0-cm dens; P = 0.088). All diver-created interactions (Table III) occurred within or a few centimeters from the den of the occupant. Occupants smaller than the intruder were more likely to evacuate the den, and larger occupants were more likely to remain (P = 0.0047; Fisher's exact test, using the first two lines of Table III).

TABLE III Summary of direct interaction experiment trials: all Octopus briareus sex categories have been combined. Frequency Result

Occupant s m a l l e r

Occupant larger

Occupant evacuated den Occupant remained, intruder retreated Intruder would not enter den Fight occurred (see text) Occupant evacuated, intruder retreated Intruder entered opposite end of den: no interaction

7

0

1 1 1 1 1

5 0 1 0 0

12

6

Total

Two fights are listed in Table III. In the first, both the intruder and the occupant were males, 6.0 and 5.0 cm ML, respectively. The intruder entered the den, and the o c c u p a n t struck at the intruder's arms. A short struggle ensued and the o c c u p a n t then evacuated the den. In the second fight, the intruder was a 4.0-cm juvenile female and the occupant

OCTOPUS ECOLOGY

49

an 8.0-cm female. The intruder entered and then recoiled suddenly. It was pulled in, struggling, by the occupant and one of its arms was torn offin the process. The intruder lost two more arms before the observer rescued it. This juvenile certainly would have been killed, and possibly would have been eaten, by the occupant. The nearest neighbor and direct interaction data agree with other observations made in Sweetings Pond. Of >450 dens examined, only one contained more than one O. briareus, and these were two fighting males. In another natural interaction, two O. briareus were observed copulating in the patch zone. This pair at one point moved near a coral head (Porites astreoides) which contained the den of a third animal. When the copulating octopuses were within a few centimeters of the coral, the third Octopus briareus suddenly shot two arms out of its den, causing the pair to move away. In both of these natural interactions, the human observers were completely ignored. This appeared to be true for the interactions created by divers as well but, although they support the nearest neighbor results, the direct interaction data should be viewed with some caution. DEN LIMITATION

Certain formations in Study Plot 2 were used consistently as dens by O. briareus, more so than expected if den occupations were distributed randomly over the formations. Comparison of the den occupation frequency data to Poisson distributions yielded significant differences for Xestospongia sp., Porites astreoides heads with Arca, and total formations (Table IV). Orange sponge (Halicometes and Suberites) occupations did not differ significantly from a Poisson distribution. The small sample size obtained in 16 months of surveys was due to the unsuitability of these sponges as dens for

O. briareus. TABLE IV Comparison of Study Plot 2 den occupation data to Poisson distributions: expected occupation frequencies (from Poisson distribution of occupations over the number of available formations) are compared to observed frequencies by Z2 goodness of fit tests; df = 2 in all cases; modified from Aronson (in press). Total occupations

Formations available

Formations occupied

~(2

p

Orange sponges

38 34 5

82 62 98

23 14 5

4.73 10.26 0.14

< 0.05 <0.005 > 0.90

Total

77

242

42

17.23

< 0.005

Formation type

Xestospongia P. astreoides/Arca

Combining the results of the four enrichment experiments, the addition of artificial dens had a significant effect on local density (Table V). Noteworthy also is the significant result of Experiment 1 alone. The sharp decline in the control plot density was apparently a manifestation of the general drop in O. briareus population density in

50

R I C H A R D B. A R O N S O N TABLE V

Results of the den enrichment experiments: probabilities by one-tailed Fisher's exact test; combined probability by Fisher's method (Sokal & Rohlf, 1969); a includes individuals in natural dens. Total number in plot a Control Expt. 1 2 3 4

Starting date 14 8 26 26

September, December, January, May,

1982 1982 1983 1983

Experimental

Start

Finish

Start

Finish

5 2 I 2

0 1 1 1

2 0 0 2

5 6 6 6

P 0.027 0.083 0.25 0.28

Combined probability: Z2 = 17.52, df = 8, P < 0.05.

October, 1982 (Figs. 3, 4). Octopuses found in the PVC tubes ranged in size from 2.8 to 7.0 cm ML. In the coastal den enrichment experiment, begun 23 January, 1983, there were no Octopus found before or after the enrichment in either the control or the experimental plot. However, 13 of the 14 PVC tubes remaining in the experimental plot after 15 days were occupied by two species of fish. These were the bridled goby, Coryphopterus glaucofraenum Gill (Gobiidae) and the blackfin cardinalfish, Astrapogon puncticulatus (Poey) (Apogonidae). Ten of the dens contained one Astrapogon, two had one Coryphopterus and one had one of each. By contrast, no fishes occupied the artificial dens in the first three Sweetings Pond experiments, and one den in the fourth contained a banded blenny, Paraclinus fasciatus (Steindachner) (Clinidae). A comparison of Sweetings Pond Experiment 3 (begun 26 January, 1983) with the coastal enrichment revealed this difference to be significant (Z 2 = 6.78, df = 1, P < 0.05; of the 15 PVC dens placed in the Sweetings Pond plot, 9 were not occupied by octopuses and were thus available to fishes; one den disappeared from the Annie Bight plot, leaving 14 available).

DISCUSSION P O P U L A T I O N BIOLOGY

All coleoid cephalopods examined thus far are semelparous, with the exception of

Octopus chierchiae (and possibly two other Pacific species; Rodaniche, 1984). Some benthic octopods reproduce seasonally, although there is considerable variation among species and among populations within species (Wodinsky, 1972; Mangold & Froesch, 1977; Hanlon, 1983a,b; Mangold, 1983). Studies in southeastern Florida, reviewed by Hanlon (1983a), point to seasonality of O. briareus reproduction, with egg-brooding occurring from January through April. In Sweetings Pond, brooding females were found

OCTOPUS ECOLOGY

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throughout the year, but peak activity occurred in February and March. A large increase in juveniles in April and May (1982) agrees with the approximately 60-day development time measured for Sweetings Pond O. briareus eggs (Aronson, in press; cf. 50-80 day development time documented in Hanlon, 1975, 1983a). As in other populations of this species (Hanlon, 1983a), successfully breeding males and females lived for ~ 1 yr. A number of females brooded eggs early and unsuccessfully in August, 1982. Whether this was an anomalous occurrence is unknown, but the depressed density in 1983, the asynchrony of spring, 1983 female spawning and the peculiar recruitment pattern in the summer of that year (as compared to 1980 and 1982) may have been causally connected. The similarity of population structure in July, 1980 and July, 1982 indicates that patch zone destruction by Cladophora (see p. 39) was not responsible.

DEN SELECTION

Octopus briareus in Sweetings Pond occupied a variety of natural formations. With the exception of brooding females (see below), the animals were mobile, residing in a given den for no more than a few days (Aronson, in press). Adult O. briareus displayed certain minimum den cavity requirements. Volume per se was not important, but cavity length and diameter, taken separately, were. O. briareus, like other species of Octopus (Lane, 1974), rest in their dens in a protective posture, with the body and head toward the blind end and the arms facing the entrance. Too shallow a cavity would endanger the arms; indeed, most individuals in the 31.2-cm long tubes were located in the rear two-thirds when first observed. A minimum diameter (Table IA, B) is necessary to allow gill ventilation. Mantle expansion was most likely restricted by 2.5-cm ID tubing. This diameter was obviously large enough for adults to fit through since 2.5-cm entrances were not avoided compared to 5.1-cm ones. The den dimension experiments did not determine the maximum cavity diameter acceptable, although presumably there was some diameter above which the cavity was not perceived as a potential den. It appears that there was no maximum tolerable cavity length. Two juveniles were found (on separate occasions) in a ll9.1-cm long tube (2.5-cm ID; Table IA experiment), but each was only one half to one body length from the tube entrance when discovered. Since dens with smaller entrances should provide greater protection, the fact that such artificial dens were not preferred to tubes with 5.1-cm entrances was contrary to expectation. This lack of preference may be attributable, in the case of the 2.5-cm entrance, to the availability of blocking material (small clumps of bivalves, shells, pieces of coral) with which O. briareus could reduce den entrance size. In contrast, O. joubini preferred gastropod shells and acrylic tubes with small entrances in aquarium studies (Mather, 1982a). The 1.3-cm entrance diameter was avoided because adult O. briareus could not always fit through it. The failure of three adults to slip through a 1.3-cm hole deflates considerably the vaunted reputation of octopuses for escaping from tightly closed containers (see Lane, 1974).

52

RICHARD B. ARONSON

O. briareus selected dens primarily on the basis of a tactile examination of the cavity with their arms. It is likely that they were assessing cavity dimensions and also checking cavity occupancy. In one instance an individual was observed crawling from formation to formation in the patch zone, inserting its arms into the cavities and then withdrawing and moving on. It finally chose a sponge and slid underneath (pers. obs.). Honeybee (Apis mellifera) scouts measure the insides of potential nest cavities as well but, unlike Octopus briareus, they select on the basis of volume rather than lower order dimensions (Seeley, 1977). American lobsters (Homarus americanus) do select for lower order dimensions; dens lower than they are wide are preferred (Cobb, 1971). Different species of hermit crabs use internal volume, weight, width, aperture size and shape, and a number of other features in various combinations in gastropod shell selection (Hazlett, 1981; Scully, 1983). There is also a visual component to Octopus briareus den selection. Bierens de Haan (1926) concluded that den selection by O. vulgaris did not involve vision, since transparent dens were occupied readily in his laboratory experiments. Under natural conditions, my den opacity results suggest that O. briareus conceal themselves from view. Mather (1982a) found in the laboratory that O. joubini weakly preferred (nonsignificant result) intact gastropod shells to ones with clear acrylic apices. Unfortunately, this experiment lacked the proper control (opaque acrylic apices). Entranceblocking, while functioning to increase directly the physical protection afforded by the den, may also decrease visibility into and inside the cavity. The sponge selection results confirm the importance of a suitable cavity to formation selection. In patch zone surveys, O. briareus were occasionally found under Halicometes and Suberites (Table IV). In all such cases, there were obvious troughlike cavities under the sponges. These either existed prior to occupation or had been excavated by the occupant (Aronson, in press). Xestospongia sponges, which had much more threedimensional structure, were commonly occupied (Table IV; Aronson, in press). DEN ECOLOGY

The nearest neighbor and direct interaction results, along with some incidental observations, indicate that Octopus briareus defended "territories" in the sense of excluding conspecifics from an area, but that those areas were small, extending no more than a few centimeters from the den itself. Animals defend territories for the purposes of feeding, reproduction and/or shelter (Wilson, 1975). The function of "territoriality" for these O. briareus was apparently to provide the latter; they foraged and mated away from the den in Sweetings Pond. Females brooded eggs for the duration of development and defended their eggs, their dens and a few centimeters of surrounding substratum (pers. obs.). "Den defense" is thus a more appropriate descriptor for these behaviors. Size was important in determining outcome in the direct interaction trials. Body size influences the results of agonistic encounters in a variety of animals (Brace & Pavey, 1978; Caldwell & Dingle, 1979; Clutton-Brock etaL, 1979; Austad, 1983). For pairs

OCTOPUS ECOLOGY

53

of O. vulgaris in a large aquarium, Boyle (1980) reports an arm alignment interaction which, he suggests, functions in the establishment of relative sizes. In a few cases in this study a smaller occupant won the encounter (Table III), and this may have been due to a "home advantage". O. briareus can modify their den cavities to some degree by blocking and excavation; however, the 1982-83 pattern of occupation in Study Plot 2 establishes that only a few of the many formations were suitable as dens. Had areas of the patch zone contained more suitable dens, they could have supported higher densities than occurred naturally in Sweetings Pond. With suitable dens so few and far between, it is doubtful that den defense played a role in determining density, apart from limiting occupation to one individual per den. In fact, nearest neighbor analyses of data collected in 1980 showed no deviations from random spacing of occupied dens (Aronson, in press). Vance (1972) and Hazlett (1981) discuss the problem of migration in enrichment experiments. Density increases in the short-term treatments of this study were due to immigration, and so do not alone establish that dens were globally limiting. The crucial experiment would involve large-scale, long-term enrichment, but the two pieces of evidence presented here (i.e., occupation frequencies plus enrichment results) suggest that den availability limits population size in Sweetings Pond. Dens were apparently limiting to O. joubini in a soft sediment community off Florida (enrichment experiments; Mather, 1982b), but not to rocky subtidal populations of O. bimaculatus and O. dofleini off the west coast of North America (Hartwick et al., 1978a; 1984; Ambrose, 1982). Global den limitation has been demonstrated in only one published report of which I am aware. Thousands of artificial dens were added to an O. vulgaris fishing ground off Japan, and this increased the catch substantially (Tauchi & Matsumoto, cited in Mottet, 1975). Dens are more likely to be limiting on soft bottoms, where there are fewer cavities available, than in rocky areas (Ambrose, 1982). Ifinterspecific predation pressure on O. briareus was nil in Sweetings Pond (Aronson, in press), one might expect individuals that were forced into poor-quality dens to have survived nonetheless. However, O. briareus, like other species of Octopus, are cannibalistic. The high density in Sweetings Pond increased the frequency of intraspecific encounters, possibly raising the per capita rate of cannibalism. Intraspecific predation was observed on a number of occasions (Aronson, in press). Furthermore, it was impossible to distinguish den-defensive from cannibalistic components in the observed intraspecific encounters. Even if dens are not limiting in coastal habitats, the risks of cannibalism (by the intruder) and predation involved in evacuating a den and searching for another may have selected for defense of the den against other Octopus. Whether the den-defensive interactions described in this paper occur in less dense, coastal O. briareus populations has yet to be determined. The coastal enrichment experiment did not support a den limitation hypothesis. Octopuses were too rare to appear in the den-enriched plot, but in their absence the den resource was exploited by two species of fish. Abundant large, predatory fishes such

54

RICHARD B. ARONSON

as serranids, lutjanids a n d sphyraenids p r o b a b l y limit Octopus p o p u l a t i o n s off the west c o a s t o f Eleuthera ( A r o n s o n , in press). Studies o f coastal O. briareus populations will provide information on the ecology and ethology o f den selection under a radically different set o f natural conditions.

ACKNOWLEDGEMENTS I am indebted to K . P . Sebens, W . H . Bossert a n d R . D . Turner. I also t h a n k R . F . A m b r o s e , A. Brussel, R . L . Caldwell, M . E . Day, R . T . H a n l o n , C . A . H a r m s , B. HOlldobler, L . S . K a u f m a n , J . A . Mather, E . M . Pollak, Jr., J. W o d i n s k y and two a n o n y m o u s reviewers. G. C. M a t t r a n o f the U . S . E m b a s s y in N a s s a u and D. T h o m p s o n of Gregory Town, Eleuthera provided logistical support. H. A r o n s o n and D. T h o m p s o n drew Fig. 2. F u n d i n g was provided by a Fulbright G r a n t , an N S F Dissertation I m p r o v e m e n t A w a r d (DEB-8114684), an N S F G r a d u a t e Fellowship and grants from the L e r n e r - G r a y F u n d (American M u s e u m o f N a t u r a l History), the R i c h m o n d F u n d ( H a r v a r d University), the Explorers Club, Sigma Xi and the H a w a i i a n Malacological Society. Field research was c o n d u c t e d under a permit from the B a h a m a s D e p a r t m e n t o f Fisheries. This p a p e r forms part of a doctoral dissertation submitted to the D e p a r t ment o f Organismic and Evolutionary Biology, H a r v a r d University.

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