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DETERMINATION OF THE DIET OF OCTOPUS RUBESCENS BERRY, 1953 (CEPHALOPODA: OCTOPODIDAE), THROUGH EXAMINATION OF ITS BEER BOTTLE DENS IN PUGET SOUND

1 2 3 4 Roland C. Anderson , Paul D. Hughes , Jennifer A. Mather & Craig W. Steele

ABSTRACT

Den middens have been used to determine the diet of several species of octopuses, but are not available for the red octopus ( Octopus rubescens Berry, 1953). As a result, its diet in the wild is poorly known. To determine their diet, 0. rubescens were collected in beer bottle dens, evicted from the bottles for measurement, and released. The shell contents of the bottles were then sieved, identified and compared to those from bottles not containing octopuses. The shell con­ tents of bottles containing octopuses had significantly more species and significantly more shells than bottles without octopuses. In this mud/sand area, the octopuses were consuming predom­ inantly the gastropod Olive/la baetica. Beer bottle trash on the sea floor is a non-polluting den re­ source for 0 . rubescens, and is shown here to be a valuable tool for diet analysis. Key words: Octopus, diet, habitat, Puget Sound, beer bottles.

INTRODUCTION mation about feeding, because many octo­ puses leave middens of prey remains in front The small red octopus, Octopus rubescens of their dens (Mather, 1991 ; Hanlon & Mes­ Berry, 1953, is the most common octopus in senger, 1996). The dens of 0. rubescens the nearshore area on the west coast of the have only been inferred from their being United States (Hochberg & Fields, 1980), but trawled up in empty giant barnacle shells, its habits are not very well known. Several in­ beer bottles, and other hard containers of ap­ dications of prey preference have been given propriate size (Dorsey, 1976). A female guard­ for 0. rubescens, mostly from laboratory stud­ ing her eggs was even found in a cast-off ies. For example, Warren et al. (1974) delin­ shoe (Anderson, 1994). Other than beer bot­ eated its color changes while attacking prey, tles (Anderson, 1994, 1997), natural dens and Dorsey (1976) described its natural his­ have not been described for 0. rubescens tory and social behavior. Anderson (1997) and from observations in the wild. Octopuses Boyle (1991) described methods for its aquar­ have used discarded human trash as dens for ium husbandry and laboratory maintenance. millennia (Lane, 1957; Cousteau & Diole, Hochberg (1997) listed the diets observed in 1973). Fishermen have taken advantage of the laboratory, which included a variety of the octopuses' propensity to inhabit shelters species of molluscs and crustaceans. There is by lowering strings of jars; the octopuses little information on the feeding of 0. ru­ crawl into them and can be harvested when bescens in the wild, although Hochberg & the jars are retrieved. This behavior has been Fields ( 1980) stated that 0. rubescens prefers used to assess octopus populations by Voight small crabs, and Laidig et al. (1995) observed (1988), who placed 325 ml beer bottles on in­ them eating small euphausiids. This limited in­ tertidal sand flats as shelters. Such collection formation on the natural diet of 0. rubescens succeeded because octopuses prefer shelter inspired the present study. that is dark and has a small entrance (Mather, Many species of octopuses take refuge in a 1982; Aronson, 1986). A routine collection of den over a period of days or weeks (Mather, 0. rubescens in bottles revealed the shell re­ 1982, 1991; Ambrose, 1983; Hartwick et al., mains of likely prey items and suggested beer 1984; Voight, 1988; Cigliano, 1993). The dens bottles could serve a further purpose, as a of octopuses are a conspicuous aspect of tool for analyzing the previously unknown their natural history, and are a source of infor- prey choice of 0. rubescens.

1The Seattle Aquarium, 1483 Alaskan Way, Seattle, Washington 98101 , USA; [email protected] 2University of Washington, Seattle, Washington, USA 3University of Lethbridge, Lethbridge, Alberta, Canada 4 Edinboro University of Pennsylvania, Edinboro, Pennsylvania, USA 455 456 ANDERSON ET AL.

MATERIALS AND METHODS prey species. We also compared the number of shell species in bottles with octopuses to Sixteen Octopus rubescens were found in those without, using a niche breadth index de­ "aged" 355 ml beer bottles with a mouth open­ veloped by Cardona (1991 ). This index looks ing size of 18.0 mm inside diameter by scuba at frequencies of occurrence of the different divers during the fall and winter of 1997 - 1998 prey species to calculate a niche breadth in 20-25 m deep water at Federal Way, 30 km index, and we considered unoccupied bottles south of Seattle, Washington State, USA. and occupied ones as representatives of two Long duration in the sea was indicated by a predator "species". dense covering of barnacles (Ba/anus crena­ tus) and/or sea anemones (Metridium gigan­ teum). Sixteen aged bottles unoccupied by RESULTS octopuses were also collected. Octopuses in their bottles were placed into zippered plastic All octopuses found at the site during the bags and transferred to the Seattle Aquarium day were within bottles, possibly because no using the methods of Anderson (1997). Octo­ suitable dens other than Polinices shells, al­ puses were removed from the bottles by hold­ ways occupied by hermit crabs (see Jensen, ing the bottles mouth downward over a pail of 1995), were available. Significantly more oc­ water. Remaining bottle contents were rinsed topuses were found in aged brown bottles (16 out thoroughly into the pail. The octopuses occupied, 7 unoccupied) than in clear ones (0 were sexed, weighed, measured for mantle occupied, 9 unoccupied) when tested with a length (ML), and released into the water near two-way Chi-square test (X2 = 16.358; p < the Aquarium, a known habitat for 0. ru­ 0.001 ). The octopuses' mean weight was 8.26 bescens (Jeff Christiansen, pers. comm.). g, and their mean mantle length was 19 mm. The contents of the bottles were then strained Possible prey remains consisted of mollus­ through a sieve with a 2.0 mm openings, and can shells and barnacle fragments and were the shells collected were kept and identified. found in nearly all bottles. They came from a The labels were removed from 30 new bot­ large number of species, but predominantly tles (short, brown 355 ml Budweiser® bottles, from the molluscs Olive/la baetica, Alia sp., with a mouth opening size 18.0 mm inside di­ Kurtziella sp., and Nassarius mendicus, and ameter) and they were painted black, because the barnacle Ba/anus crenatus (Table 1 ). octopuses prefer dark dens (Mather, 1982; Comparisons of number of shells between oc­ Voight, 1988). The bottoms of the bottles were cupied and unoccupied bottles could only be left unpainted so octopuses inside could be made for these five species because of the seen with the aid of a dive light. They were laid small numbers found of the other species. out on the bottom about 100 m from where the Chi-square analyses revealed that each of previous octopuses were collected. After 66 these five species were found significantly days, all bottles were retrieved and any octo­ more often in bottles that had been occupied puses inside were measured, weighed, and by an octopus (Table 2). released. Any shells inside were sieved, re­ The niche breadth index developed by Car­ trieved and identified. The taxonomy of some dona (1991) applied to the shells found in the of the small gastropods examined is in a state bottles (Table 3) uses occurrence frequen­ of flux (Ronald L. Shimek, pers. comm.), so cies, that is, in how many individuals collected they were not identified beyond genus, using of each species of shell a certain food type the guides of Abbott (1974), Kozloff (1987), was found. Cardona's index is an improve­ and Rice (1971 ). ment/extension of the Gladfelter-Johnson An 0. rubescens found in a bottle at the Index (Gladfelter & Johnson, 1983) in that it same site was taken to the Seattle Aquarium, looks at numbers of occurrence rather than where the interior of its bottle was cleaned out relative percentage of total volume or weight and the octopus allowed to re-occupy the bot­ of the collected food items. By using these tle. It was placed in an aquarium with 39 live niche-breadth calculations, we found a niche Alia sp., collected from the same area from breadth for the occupied bottles to be B' = eelgrass. The octopus was ejected from the 0.2417 and for the unoccupied bottles B' = bottle after 10 days and the bottle's contents 0.1275. The occupied bottles had about twice examined. the niche breadth of the unoccupied bottles, Comparisons of the number of likely prey which is a clear indication of octopus activity. species between occupied and unoccupied After 10 days, the octopus in captivity had bottles were made for the five most common consumed 14 of the 39 Alia sp. available in its 0 m -l m JJ -s: TABLE 1. Mean number of molluscan and crustacean prey remains per bottle found on mud/sand habitat in Puget Sound. z ~ Octopus-occupied old Unoccupied old - Octopus-occupied Unoccupied new 0 bottles (N = 16) bottles (N = 16) new bottles (N = 2) bottles (N = 28) z Olive/la baetica 27. 75 Olive/la baetica 5.625 Olive/la baetica 6 Olive/la baetica 0.5 0.,, barnacle fragments 7.06 Barnacle fragments 3.562 Nassarius mendicus 0.5 barnacle fragments 0.143 -l I Alia sp 4.125 Alia sp 0.9375 Alia sp. 0.5 Alia sp. 0.428 m Kurtziella sp 0.875 Nassarius mendicus 0.125 Eulima sp. 0.036 Nassarius mendicus 0.625 0 Clinocardium nuttallii 0.0625 Mopalia muscosa 0.036 m- Pododesmus macrochisma 0.31 Eulima sp 0.0625 -l Clinocardium nuttallii 0.25 Kurtziella sp. 0.0625 0 Chlamys hastata 0.1875 Lucinoma annulatum 0.0625 .,, Protothaca staminea 0.1875 Macoma nasuta 0.0625 0 (") Cancer oregonensis 0.125 Pododesmus macrochisma 0.0625 Crepipatella lingulata 0.0625 Polinices lewisii 0.0625 d Eulima sp 0.0625 Protothaca staminea 0.0625 c:\) Lucinoma annulata 0.0625 (/) Macoma nasuta 0.0625 :::0 Simomactra falcata 0.0625 Natica clausa 0.0625 ~ Odostomia sp 0.0625 m Polinices lewisii 0.0625 i CJ) m JJ JJ ~

+loo (J1 -...J 458 ANDERSON ET AL.

2 TABLE 2. Results of Chi-square tests (x ) , with Yates' correction, on the five most-com­ mon shell remains in red octopus occupied and unoccupied beer bottles.

Number in Number in Shell item occupied bottles unoccupied bottles x2 O:< Olive/la baetica 444 90 233.35 0.001 Barnacle fragments 113 57 17.79 0.001 Alia sp. 66 15 30.86 0.001 Kurtizella sp. 14 1 9.60 0.005 Nassarius mendicus 10 2 4.08 0.05

TABLE 3. Niche breadth indices (B') of red octopus occupied and unoccupied beer bottles.

Occupied Bottles Unoccupied Bottles *Frequency of "Frequency of Shell item occurrence O/o occurrence O/o Olive/la baetica 13 81.25 11 68.75 Barnacle fragments 15 93.75 12 75.00 Alia sp. 11 68.75 8 50.00 Kurtizella sp. 7 43.75 1 6.25 Nassarius mendicus 6 37.50 2 12.50 Pododesmus macrochishma 2 18.75 1 6.25 Clinocardium nuttalli 4 25.00 1 6.25 Protothaca staminea 3 18.75 1 6.25 Eulima sp. 1 6.25 1 6.25 Lucinoma annulata 1 6.25 1 6.25 Macoma nasuta 1 6.25 1 6.25 Polinices lewisii 1 6.25 1 6.25 Chlamys hastata 3 18.75 0 0.00 Cancer oregonensis 1 6.25 0 0.00 Crepipatella lingulata 1 6.25 0 0.00 Simomactra falcata 1 6.25 0 0.00 Natica clausa 1 6.25 0 0.00 Odostomia sp. 1 6.25 0 0.00 Niche breadth indices: B' = 0.2417 B' =0.1275

*Frequency of occurrence: In how many of the 16 bottles in each category a species was found.

aquarium and had left all the empty shells in­ Pagurus armatus. Natural den space was lim­ side its bottle den. None of the shells were ited and may be competed for by other ani­ drilled. mals (Mather, 1982), such as P. armatus, which is invariably found in Polinices shells in this area (Jensen, 1995). It was obvious the DISCUSSION octopuses preferred darker brown bottles and those obscured with marine growth. Thus, the It is not surprising that a small octopus octopus-occupied bottles were preferred species like Octopus rubescens occupies dens and contained more shells than unoccu­ beer bottles, because a number of other Oc­ pied bottles, which may have been occupied topus species utilize man-made items for their by octopuses on a transitory basis and hence dens. In fact, beer bottles may allow 0 . had fewer shells in them. The experiment in rubescens to utilize the sand/mud habitat, as the aquarium confirmed 0. rubescens keeps cockle shells do for 0. joubini in the sea-grass its prey remains in its bottle dens. beds of Florida (Mather, 1982). Few other den It is perhaps a bit surprising to find an octo­ sites were available. There were only the oc­ pus that leaves its food remains in its den, casional clam shells Tresus capax, Panopea since 0. vulgaris, 0 . dofleini, and 0. cyanea all abrupta and Clinocardium nuttallii, and the eject prey remains (studied by Mather, 1991 ; large moon snail Polinices lewisii, which was Hartwick et al., 1978; and Yarnall, 1969, re­ usually occupied by the large hermit crab spectively). There are possible advantages DETERMINATION OF THE DIET O F OCTOPUS RUBESCENS BERRY 459 and disadvantages to this behavior. The pos­ could have consumed the barnacles. If so, the sible disadvantage is that food wastes may barnacle-covered bottles would have pro­ foul the den. The advantage is that the den site vided both homes and a food source. will not be "advertised." Scuba divers have Octopuses consume hermit crabs in mol­ long used den middens to spot an octopus lusc shells (lribarne et al. , 1991 ), and it is pos­ (High, 1976) and likewise a hungry fish or seal sible that 0 . rubescens were eating hermit might use a midden to detect its potential oc­ crabs in Alia sp. shells found in the shallow topus prey, as suggested by Ambrose (1983). eelgrass beds. Few hermit crabs were seen at This population of small 0. rubescens ap­ the depths where the octopus-occupied bot­ pears to be feeding mostly on gastropod mol­ tles were found, and no hermit crab remains luscs. The diet of 0. rubescens may indicate were found in the bottles. It is possible that habitat-specific prey selection similar to that crab remains might pollute the interior of the of 0 . bimaculatus, which prefers crabs but bottles more than molluscan remains and consumes predominantly the molluscan prey hence be ejected by the octopus, but the most widely available in its habitat, such as snails, common shell found inside the bottles, chitons or bivalves (Ambrose, 1986). Olive/la Olive/la baetica, has a narrow aperture un­ baetica is very common in Puget Sound suitable for occupation by local hermit crabs. (Shimek, 1992), and its presence in the prey Thus, the 0. baetica were probably directly remains indicates the octopuses were taking consumed by the octopuses. advantage of its wide availability in the sand. This unusual kind of animal/human interac­ Although crabs may be a preferred food, oc­ tion, with octopuses using our discarded topuses have been described as "generalist trash, has offered us an interesting research predators" (Ambrose, 1986) and flexible prey opportunity. If an octopus species does not choice is indicated here. The number of Alia discard its food remains in front of its den, sp. in the bottles may also indicate octopuses prey choice assessment is difficult. The shape can go a considerable distance to forage, as and color of beer bottles have made them an these Alia sp. live in the eelgrass beds in shal­ appropriate shelter for small octopus species low water and they were approximately 100 m (Mather, 1982; Voight, 1988). Food remains of inshore of the octopus collection location octopuses in different climates may pollute (pers. obs.); this is similar to the results found the interior of their bottle dens and hence the by Hartwick et al. ( 1981) for 0. dofleini. remains may be ejected, but in this case the The octopuses inhabiting bottles at the time bottles have allowed us to "capture" prey re­ of this study (November 1997-January 1998) mains of 0. rubescens that would otherwise were juveniles. Octopus rubescens can grow be scattered by scavengers or removed by to 400 g (Hochberg, 1998), although females water currents. We encourage other re­ can spawn at just 23 g (Osborn, 1995). An oc­ searchers to examine the bottle dens of other topus of a mean weight of 8.26 g is occupying species of octopus to look for what Dodge & just 2.3°/o of a 355 ml beer bottle. The small Scheel (1997) called "the remains of the prey." size of these octopuses represent one stage of the life cycle and hence these prey items may only be eaten by juveniles. Octopus rubes­ ACKNOWLEDGMENT cens up to 99 g have been found in beer bot­ tles (Seattle Aquarium, unpubl. data), and We thank Ronald L. Shimek, Eugene V. Coan larger animals may be eating different prey or and Elsie Marshall for assistance in identify­ may not be leaving their food remains in the ing the small molluscs and acknowledge the bottles. support of the Seattle Aquarium in this project. More than one explanation is possible for We gratefully acknowledge the diving support the presence of the barnacle fragments in the of John Hughes, Patrick Almeda and volun­ bottles. Octopuses have been known to eat teer divers from the Seattle Aquarium. barnacles (Nixon & Maconnachie, 1988), but we cannot be sure they are doing so in this LITERATURE CITED case. The barnacles on many of the bottles examined were dead, possibly eaten by sea ABBOTT, R. T. , 1974, American seashells. Van stars, a major barnacle predator (Mauzey et Nostrand Reinhold, New York. 663 pp. al., 1968). The barnacle shells might then AMBROSE, R. F. , 1983, Midden formation by octo­ have been held by the octopuses as barriers puses: the role of biotic and abiotic factors. 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