NOTES

OBSERVATIONS OF SEA OTTERS DIGGING The Alaskan otters "dug out with their FOR CLAMS AT MONTEREY HARBOR, forepaws while maintaining a head downward position" in intertidal and shallow subtidal water. However, Shimek's (1977) description is the only Although the feeding behavior of the sea·otter, detailed underwater observation of sea otters Enhydra lutris, is frequently observed from the foraging on soft substrate~ Detailed observations surface, few underwater observations offoraging of sea otters taking prey from soft substrates are sea otters have been published. Faro (1969) and more difficult than those on rock, because the ot­ Houk and Geibel (1974) described the underwater ter's disturbance of the bottom often results in behavior and tool use of sea otters when they re­ clouds ofsediment obscuring further vision. In the moved from rock substrates. Shimek present account, we describe underwater ob­ (1977) observed a foraging for and servations of sea otters digging clams in a silty presumably other invertebrates by patting the sand substrate and present information about the surface of rocks and feeling into cracks. Shimek impact of this foraging on the distribution and also described a sea otter digging up the echiuroid abundance ofsubtidal clams at Monterey Harbor, worm, Urechis caupo, from a silt and cobble sub­ Calif. strate. Further deductions about underwater foraging behavior have been made from collec­ Observations tions ofabalone shells with the characteristic "ot­ ter break" hole in the middle (Wild and Amesl ) In 1976-77 we observed sea otters eating large and from observations ofaluminum beveragecans numbers ofthe Washington , nut­ bitten by otters to remove (McCleneghan talli, primarily in two specific areas of Monterey and Ames 1976). Some sea otters can be enticed Harbor (A and B ofFigure 1). From vantage points underwater to take food offered them (pers. obs). alongthe floating boatslips and elevatedwharves, However, these latter observations ofunderwater we observed sea otters at the surface feeding on food manipulation are oflimitedvalue because the 211 prey items: S. nuttalli (88.6%); the crabs otters also take items unpalatable to them (e.g., Pugettia producta (4.2%) and Cancer sp. (3.3%­ the holothuroid Stichopus californicus), and be­ probably C. antennarius or C. productus, but not cause the otters were clearly interacting with the C. magister); the rock jingle bivalve Pododesmus diver observer. These accounts of underwater cepio (1.4%); and unidentified items (2.4%). Dur­ foraging indicate thatseaotters use primarily tac­ ing spring 1976, as many as four sea otters were tile sensitivity of the forelimbs to locate and cap­ foraging at one time in the harbor vicinity, but an ture prey, whereas all other marine mammals average ofabout one sea otter was observed on 38 (pinnipeds and cetaceans) use their jaws to cap­ counting trips made to the area. ture prey. Radinsky (1968) hypothesized that the The underwater path of foraging sea otters sea otter evolved forelimb tactile sensitivity sepa­ could often be observed from the surface by follow­ rately from the aonychoid otters. ing the trail of air bubbles escaping from their The large impact of sea otters on Pismo clam, compressed fur. The paths offoraging dives made Tivela stultorum, populations in California has in the inner harbor were often contorted, 50-60 m been documented (Stephenson 1977; Miller et or more long, and lasted 45-80 s. These dives usu­ al,2), and in PrinceWilliam Sound, Alaska, 81% of ally produced no prey, but the prey taken were the food items taken by sea otters were bivalves, mostly crabs and rarely clams. On those dives that especially Saxidomus gigantea (Calkins 1978). resulted in the capture of kelp crabs, sea otters usually (eight out of nine dives) finished their search with a swim under 10-20 m of the floating IWiId, P. W., and J. A. Ames. 1974. A report on ~he sea otter, Enhydra lutris L., in California. Calif. Dep. FISh and docks intheinnerareaoftheharbor. Duringscuba Game Mar. Resour. Tech. Rep. 20,93 p. dives in this area, we repeatedly observed kelp 'MilIer, D. J., J. E. Hardwick, and W. A. Dahl­ strom. 1975. Pismo clams and sea otters. Calif. Dep. Fish crabs on the undersides of these floats and rarely Game Mar. Resour. Tech. Rep. 31,49 p. elsewhere. It was difficult to observe the paths of FISHERY BULLETIN: VOL. 78. NO.1. 1980. 159 In spring 1976, we conducted an underwater .,. survey ofmost ofthe bottom ofthe inner and outer N harbor, noting variations in the substrate and I counting protruding clam siphons in haphazardly tossed 14 m2 quadrats. Depths intheharbor ranged from 2 to 8 m, with area A being 4.5 m and area B Outer 2-3 m (Figure 1). The substrate in much of the enclosed inner harbor was black mud and silt, and Harbor most of the rest of the harbor (including areas A and B) was silty sand. The two areas where otters fed extensively on clams had high densities of clam siphons: for area A, x = 13.5/m2 , SD = 8.9, n = 19; for area B,x = 9.3/m2 , SD = 7.2, n = 16. The area under Wharf No.2 adjacent to area A had 2 even higher densities ofsiphons: x = 17Alm , SD = 11.9, n = 18. However, other areas ofthe harbor had siphon densities < 1.0/m2 , and the black mud of the inner harbor had densities <0.04/m2 • We inserted a slender rod down siphon holes in the substrate until the rod contacted the clam shell, and, with considerable difficulty, we used a stream offreshwater from a garden hose to obtain a few 8-14 em long clams from area A. We used these specimens to distinguish the two species present FIGURE I.-Monterey Harbor, Calif. High densities of clams by the morphology ofthe protruding siphons. The were foraged by sea otters in areas A and B. 1 = Fisherman's species composition in areas A, B, and under Wharf; 2 =WharfNo. 2; 3 =north andeastseawails ofthe inner WharfNo. 2 were the same: 95% wereS. nuttalli, harbor; 4 = breakwater for the outer harbor. (Traced from an aerial photograph in Haderlie and Donat 1978.) 5% were the gaper clam, nuttallii. In this way we also determined that the clams were lo­ cated 10-50 em into the substrate and that larger dives made in the Illiddle ofthe outer harbor, but individuals of both species tended to occur at the sea otters usually surfaced without prey 50 m or deeper end of this range in the sediment. We re­ morefrom thestartofthedive. However, the paths corded the densities of clam siphons in area A and offeeding dives in the two locations where clams also in the adjacent area ofhighest density under weretaken in abundance wereusuallyquiteshort, WharfNo. 2 atapproximately bimonthly intervals only 10 m or less. from February 1976 to March 1977. The densities Theusual sequence ofdives in theharborregion and proportions ofthe two species ofclams did not began with otters making one to three 50-90 s change (ANOVA, P>0.05). dives that producedno prey. After about 10-20 s on The bottom in the two areas where sea otters the surface and a little grooming, the otters usu­ took large numbers of clams was littered with ally dove again to the same spot. A series ofshort hundreds ofshells, both on the surface and mixed (25-40 s) dives followed the initial dives, and each into the sediments. About 58% ofthe shells did not ofthese invariably resulted in a single S. nuttalli have pairs of connected valves, and about one­ about 10 em long. The otters took 30-90 s to open third ofthe valves were broken. Of89 shells sam­ and eat the clams before diving to the same spot. pled, 99% wereS. nuttalli and 1% wereT. nuttallii. Sometimes they pounded the clams on a rock anvil The bottom topography was hummocky in these on their chest; other times they simply twisted or areas, and there were many craters 0.5-1.0 m pried the clams open with their teeth. An average across and 10-15 em deep. The bottom under of6 andas many as 19clams were taken in a single Wharf No.2, where the density of clam siphons series of these dives. Following such a series, ot­ was highest, was mixed with debris consisting of ters usually spent up to 30 min grooming before chunks ofasphalt apparently from resurfacing of they swam away, sometimes to forage in a new the road on the wharfand ofclumps oflarge bar­ location. nacle, Balanus nubilus, tests which had fallen 160 from themassive barnacles encrustingthepilings. lateral digging with the front paws continued There were considerablyfewer craters in this area again for about 30 s until anotherclam was caught compared with the adjacent area A, and our at­ and the activity suddenly stopped. Thehole at this tempts to dig into the substrate under the wharf time was over 0.5 m deep and the otter's body was proved difficult as a result ofthe debris embedded entirely below the level of the substrate surface in the sediment. while digging. The otter used this process oflat­ Sea otters were in the process of foraging on eral digging on three more dives lasting about 30 s clams during several ofthe scuba dives in area A. each with 40-60 s surface intervals, before the Although these otters were not bothered by our observer ran out ofair and surfaced. The trench at presence under water, attempts to observe pre­ that time was over 1.5 m long and remained about cisely how they were capturing clams usually 0.5 m wide and deep. The otter terminated the failed because they stirred up large clouds ofsedi­ series of feeding dives with one additional dive ment that obscured all oftheir activity. When the while the observer was at the surface. It paid no otters stopped foraging and the clouds ofsediment apparentattention to the observer's close presence dispersed, a large hole up to 1.0-1.5 m across and during the entire series. Simultaneous observa­ 0.5 m deep had obviously resulted from their dig­ tions by the second author from the surface indi­ ging. The sides ofthese holes were initially nearly cated that none of the first three dives (including vertical, but collapsed within minutes. two dives at the first spot) produced a clam, but Details of a sea otter digging for clams were that each ofthe six subsequent dives resulted in a observed by the first author on a single occasion on single clam. Theotterdid notuse a rock to open the 30 March 1977, when a strong current rapidly clams. dispersed the clouds of sediment. Upon observing a young male otter begin a typical sequence of Discussion foraging dives in areaA, the observermoved along the bottom and approached the digging site from In 1966, prior to the return ofsea otters to Mon­ an upstream direction. The otter was clearly visi­ terey Harbor, Calif., Department of Fish and ble at a distance of 5 m and was just leaving the Game divers made qualitative surveys ofthe bot­ bottom after completing the second longer dive of tom and used a garden hose to remove several the series. He returned to the bottom within 20 s clams from the substrate for identification. The but abandoned the initial digging site, leaving a bottom topography was smooth, clams were abun­ small hole about 0.5 m across and 25 cm deep. dant, and T. nuttallii was the dominant species Instead, on this third dive, he moved immediately removed from as deep as 50 cm in the substrate to a new spot about 4 m away and began to dig (Ebert3 ). Follow-up survey dives soon after the rapidly with his front paws in a fashion very much return ofsea otters indicated that clams were less like a dog, producing a large conical cloud ofsedi­ abundant and the bottom topography was hum­ ment extending downstream. Digging lasted mocky (Ebert, see footnote 3). Although definitive about 45 s, followed by a 20 s surface interval. all, quantitativedata are not availablefor that period, the fourth dive the otter resumed digging in the and although construction and dredging opera­ same spot, and as during all digging periods, he tions in the inner marina portion of the harbor faced into the current. The observer was able to may have had important impact on clam popula­ approach< 1 m from the seaotter by creepingup in tions, information in the present report indicates a prone position on the bottom while the otter that sea otters may have limited the abundance substantially enlarged the hole to a short trench and distribution ofS. nuttaZli and T. nuttaZlii and about 1 m long, 0.5 m across, and 25 cm deep by that T. nuttallii is now only a minor species. The digging rapidly with both front paws. His back cause ofthis apparent shift in dominance from T. flippers were moving at a slower rate, which prob­ nuttaZlii toS. nuttaZli is unclear. Ourlimited mea­ ably helped maintain his position and also ap­ surements ofthe depths ofthese clams in the sub­ peared to assist in digging. Toward the end of the strate indicated that larger individuals were digging on this dive the otter began to roll re­ found deeper (to about 50 cm), but that neither peatedly from side to side to enlarge the front end of the trench laterally, until he apparently en­ "E. E. Ebert, Director, Marine Culture Laboratory, California countered a clam and suddenly surfaced for 45 s. Department of Fish and Game, Granite Canyon, Coast Route, all, the fifth dive this rapid process of rolling and Monterey, CA 93940, pers. commun. June 1979. 161 species had a depth refuge from by sea knows that it is relatively easy to enlarge a hole, otters, which excavated deeper than 50 em. Tresus and it would be advantageous to do this rather nuttallii attains larger size than S. nuttalli (pers. than dig straight down for each individual clam. obs.), and if sea otters prefer larger clams, they The behavior of digging like a dog has also been may have preyed preferentially upon T. nuttallii. reported by Shimek (1977) for a sea otter taking However, clams remained abundant in small subtidal echiuroid worms and is apparently simi­ areas ofthe harbor in spite ofheavy predation by lar to the behavior of sea otters taking clams in sea otters. Densities under WharfNo. 2 averaged shallow subtidal and intertidal waters in Alaska about 17 clams/m2 ; and in this area they appear to (Calkins 1978). The holes reported by these au­ have a partial refuge from sea otters, which may thors were only halfthe size offreshly dugholes at havefound ittoo difficult to dig through the debris Monterey Harbor, however. The first author has ofchunks of asphalt and clumps ofbarnacle tests observed similar (1.5 m across and 0.5 m deep) embedded inthesediment. No such impedimentto holes dug by otters in the sand channels in 12 m of digging exists in areas A and B, where clams have water off kelp forests at Pacific Grove, Calif. In persisted in somewhat lower densities ofabout 14 areas such as PrinceWilliam Sound and Monterey and 91m2 , respectively. However, the species com­ Harbor, where otters forage heavily on clams, position ofclams was the same under WharfNo.2 their digging must cause a major disturbance of and in areas A and B, regardless ofpredation in­ the infaunal community. tensity. Sea otters have been termed "keystone pred­ By following tagged , Loughlin (1977) ators" (Estes and Palmisano 1974; Estes et aI. showed thatcertain seaotters made daily foraging 1978), because they regulate populations of trips to Monterey Harborfrom rafting locations as epibenthic invertebrates, perhaps through a pro­ far as 2 km away. In the present descriptions of cess of switching between prey species. At Mon­ their dive paths, sea otters feeding on items other tereyHarbor there is circumstantial evidence that than clams apparently located prey in a random sea otters have had a major impact on two other manner similar to Shimek's (1977) description of prey items. Surveys by the California Department an otter patting the surface of rocks and feeling of Fish and Game showed C. antennarius and C. the cracks. Observations of the bubble paths of productus were taken in abundance by fishermen otters taking clams in areas A and B oftheharbor, from the Monterey wharves prior to the return of however, indicatedthatthey usually did notspend sea otters, butthey wererarely taken at Monterey time searching for a suitable place to dig, nor did in 1972-74, while still caught in abundance at visual selection ofa patch ofclams appear to occur. piers north of the range of sea otters (California 2 4 Ifthe density ofclams in area A averaged 141m , Department ofFish and Game ). Observations on and ifan averagespotdug up by an otterwas 0.5 x the scuba dives reported here for 1976-77 confirm 1.5 m (0.75 m2) as observed in this report, then that cancer crabs are rare in the harbor. Mytilus random digging in area A would produce about 10 edulis and M. californianus formed dense clumps clams. This is greater than the average number of on wharf pilings prior to the return of sea otters six clams taken by otters on a series of dives. (Haderlie5), but aresmall and uncommon Perhaps the otters had learned the location of the there now (Haderlie and Donat 1978). Curiously, clam patches, and because sediment clouds nor­ large specimens ofB. nubilus arestill abundant on mally prevented visual cues as soon as the sub­ the pilings and were not taken in appreciable strate was disturbed, they simply dug haphazard­ numbers by sea otters, even though these barna­ ly within the patch. Indeed, Gentry and Peterson cles were taken frequently by otters at other loca­ (1967) compared the underwater visual acuity of tions in the Monterey area (pers. obs.). The factors sea otters with the sea lion, Zalophus califor­ which regulate preyselection by sea otters remain nianus, and harbor seal, Phoca vitulina, and pro­ poorly understood. posed that vision in otters may be better adapted for aerial situations of predator detection rather than for underwater prey location. 'California Department of Fish and Game. 1976. A pro­ posal for sea otter protection and research and request for the The strategy ofrepeatedly enlarging the hole to return of management to the State of California. Calif. Dep, capture clams is a good one, because it makes Fish Game, Oper. Res. Branch, Vol. 1: Text and summaries, 271 p. efficient use ofthe labor to start the hole on initial "E. C. Haderlie, Professor, Naval Postgraduate School, Mon­ dives. Anyone whohas dug in sand at the sea"n,~~e terey, CA 93940, pers. commun. May 1976. 162 Acknowledgments EFFECT OF ZINC ON FIN REGENERATION IN THE MUMMICHOG, FUNDULUS HETER0CLITUS, John S. Pearse, Ronald Jameson, and an AND ITS INTERACTION WITH anonymous reviewer provided advice and critical METHYLMERCURY discussion for this study. Christopher Harrold gave technical and diving help. We thank thestaff Methylmercury has been found to retard fin re­ at Hopkins Marine Station ofStanford University generation in the marsh killifish, Fundulus for their assistance. This work was partially confluentus, and striped mullet, Mugil cephalus funded by the U.S. Fish and Wildlife Service. (Weis and Weis 1978). In F. confluentus the re­ tarding effect of methylmercury was masked in Literature Cited water of reduced salinity (9%0). Cadmium, which also retarded fin regeneration in killifish (Weis CALKINS, D. G. 1978. Feeding behavior and major prey species of the sea and Weis 1976), interacted antagonistically with otter,Enhydra lutris, in Montague Strait, Prince William methylmercury so that fish exposed simultane­ Sound, Alaska. Fish. Bull., U.S.76:125-131. ously to the two metals exhibited growth rates ESTES, J. A., AND J. F. PALMISANO. comparable to controls (Weis and Weis 1978). 1974. Sea otters: their role in structuring nearshore com­ munities. Science (Wash., D.C.) 185:1058-1060. This paper reports on the effects of zinc on re­ ESTES, J. A., N. S. SMITH, AND J. F. PALMISANO. generation in the mummichog, F. heteroclitus, 1978. Sea otter predation and community organization in and the effects ofcombinations of methylmercury the western Aleutian Islands, Alaska. Ecology 59:822­ and zinc on this process. 833. FARO,J.B. 1969. A survey ofsubtidal sea otterhabitatoff PointPinos, Methods California. M.A. Thesis, Humboldt State Univ., Arcata, Calif., 278 p. Fish were collected by seining in the vicinity of GENTRY, R. L., AND R. S. PETERSON. Montauk, N.Y. The lower portion of each caudal 1967. Underwater vision ofthe sea otter. Nature (Lond.) 216:435-436. fin was amputated with a scalpel, and approxi­ HADERLIE, E. C., AND W. DONAT III. mately 15 fish were placed in each ofseveral all­ 1978. Wharf piling fauna and flora in Monterey Harbor, glass aquaria with 10 I of300/00 salinity water. The California. Veliger 21:45-69. temperature was 20°_22° C and the photoperiod HOUK, J. L., AND J. J. GEIBEL. was 14 h light/10 h darkness. Fish were fed com­ 1974. Observation of underwater tool use by the sea otter, Enhydra lutris LinnaeuB. Calif. Fish Game 60:207-208. merical fish food and live grass shrimp,Palaemo­ LOUGHLIN, T. R. netes pugio. Tanks were dosed with methylmer­ 1977. Activity patterns, habitat partitioning, and groom­ curic chloride (I.C.N. Pharmaceuticals, Plainview, ing behavior of the sea otter, Enhydra lutris, in Califor­ N.Y.l) from a 0.1 mg/ml stock solution in nia. Ph.D. Thesis, Univ. California, Los Ang., 110 p. MCCLENEGHAN, K., AND J. A. AMES. 0.2% NaHCOa to yield a final calculated concen­ 1976. A unique method of prey capture by a sea otter, tration of 0.050 or 0.025 ppm depending on the Enhydra lutris. J. Mammal. 57:410·412. experiment, and/or with ZnCl2 (Reagent Grade, RADINSKY, L. B Fisher Scientific) from a 1.0 mg/ml stock solution 1968. Evolution ofsomatic sensory specialization in otter to yield calculated concentrations of 1.0, 3.0, or brains. J. Compo Neurology 134:495-505. SHIMEK, S. J. 10.0 ppm. Aquaria were washed, refilled, and re­ 1977. The underwater foraging habits of the sea otter, dosed after 2, 4, 7, 9, and 11 days. Regenerating Enhydra lutris. Calif. Fish Game 63:120-122. fins were measured with a calibrated ocular mi· STEPHENSON, M. D. crometer in a stereomicroscope at 7,9, 11, and 14 1977. Sea otter predation on Pismo clams in Monterey Bay. Calif. Fish Game 63:117-120. days. Experiments were terminated at 2 wk be­ cause after that time it became difficult to ascer­ ANSON H. HINES tain the point at which the amputation had been Chesapeake Bay Center for Environmental Studies made. The amputation plane can be seen clearly Smithsonian Institution in Figure 1, a control fin 1 wk after amputation. P.O. Box 28, Edgewater, MD 21037 Three experiments were performed. Experi­ THOMAS R. LOUGHLIN ment I involved exposure of fish 3.5·4.2 em stan· Office ofMarine Mammals and Endangered Species National Marine Fisheries Service, NOAA 'Reference to trade names does not imply endorsement by the Washington, D C 20235 National Marine Fisheries Service, NOAA.

FISHERY BULLETIN: VOL. 78, NO.1, 1980. 163