read the two articles and answer the questions below :What evidence is there that sea otters are a keystone species?Explain how the killer whale-sea otter-urchin food web is an example of top-down control. Explain the difference between Figure 2a and 2b from Estes and Palmisano (1974).What are the benefits of large-scale/long-term approaches in ecological research? Write out the citation for these journal articles using the format of the journal Ecology.Sea Otters: Their Role in Structuring Nearshore Communities
Author(s): James A. Estes and John F. Palmisano
Source: Science, New Series, Vol. 185, No. 4156 (Sep. 20, 1974), pp. 1058-1060
Published by: American Association for the Advancement of Science
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traders during the 18th century. Apparently, the once abundant sea otter
Abstract. A comparison of western Aleutian Islands with and without sea
population of the Near Islands was
otter populations shows that this species is important in determining littoral and
extirpated by overexploitation. Until
sublittoral community structure. Sea otters control herbivorous invertebrate poprecently, immigrantsfrom the densely
ulations. Removal of sea otters causes increased herbivory and ultimately results
populated Rat Islands have been unin the destruction of macrophyte associations. The observations suggest that sea able to reach the Near Islands, which
are located approximately 400 km
otter reestablishment indirectly affects island fauna associated with macrophyte
west-northwestand are separatedfrom
primary productivity.
the Rat Islands by wide, deep oceanic
Destruction of subtidal and inter- regions within the 60-m depth contour passes. Since 1959 there have been
tidal kelp and sea grass beds because (10). Adult, captive sea otters require scattered reports of sea otters in the
of overgrazing by dense populations 20 to 23 percent of their body weight Near Islands (10), although no major
of sea urchins has been observed over daily in food, and in the natural en- population reestablishmenthas yet oca wide geographicalrange (1, 2). Re- vironment forage species include ben- curred.
We have studied the nearshore mamoval of sea urchins by experimental thic invertebrates and fish (10, 13).
manipulations (2) and by accidental Considering the sea otters’ average rine communities of Amchitka Island
oil spills (3) has resulted in the rapid weight as about 23 kg (10), we con- in the Rat Island group and Shemya
development of marine vegetation. Be- servatively estimate that 35,000 kg Island in the Near Island group. Field
cause community structure differs in km-2 year-l of animal biomass is observations were made at Amchitka
the presence and absence of kelp beds consumed by foraging sea otters at at approximately bimonthly intervals
(4-6) and prey density in marine com- Amchitka Island. Thus, a high-density from October 1970 to August 1973
munities can be significantlyinfluenced sea otter population is an important and at Shemyafor 1 week each in Sepby predation (7), the structure of a member of the nearshoremarine com- tember 1971 and July 1972; observations were also made at Attu in the
marine community could be deter- munity.
Such high-density populations have Near Islands for 4 days in July 1972.
mined by the intensity of herbivore
We propose that the sea otter is the
existed in the Rat Island group for
predation (8).
primary cause of the differences obSpeculation regarding the interrela- about 20 30 years, after
served between the nearshore marine
tions of sea otters (Enhydra lutris) and
communitiesof the Rat Island and the
marine invertebrates has generated
Near Island groups. Sea urchins(Stroncontroversy in California. However,
Sea urchin density
gylocentrotussp.) (14) are an imporonly slight consideration has extended
of individualsper /4 m2)
tant sea otter food and are known to
beyond economic and esthetic argu100
20 40
be voracious algal grazers which can
ments by commercial abalone interests
consume and destroy large quantities
and groups concerned with the sea otof kelp. Our hypothesis is that a dense
ters’ welfare. The observations discussed in this report suggest that sea
populationof sea otters reduces the sea
urchins to a sparse population of small
otters have a profound effect on the
individuals by size-selective predation.
structure of marine communities.
resultantrelease from grazingpresa
sure permits a significant increase in
range from .the northern Japanese
the size of nearshoreand intertidalkelp
archipelago, through the Aleutian Is12
beds and associated communities.
lands, and along the coast
Benthic macrophytes in the Rat IsAmerica as far south as Morro Her- &
land group extend from the intertidal
moso, Baja California (9). At present, . 15
the sea otter occupies only remote por- a
region and cover most of the surface
of the rock substrate to depths of 20
tions of this original range in the Kuril,
to 25 m (Fig. 1). Major contributors
Commander, and Aleutian islands and
to these plant communities are Phaeof
There is an isolated population off the
ophyta (brown algae), Alaria fistulosa,
Laminarialongipes, L. groenlandica,L.
coast of central California, and recent
*– Vegetationcover (Amchitka)
yezoensis, L. dentigera, Agarum cribtransplants have reintroduced the sea
*–. Sea urchindensity (Amchitka)
rosum, Thalassiophyllumclathrus,Desotter into Oregon, Washington, and
*…. Sea urchindepsity (Shemya)
marestia sp., and various Rhodophyta
British Columbia. Continued expansion
(red algae). Sea urchins are generally
of the sea otters’ range may be ex80
conspicuous in shallow areas (0
to 20 m). However, relatively high
Vegetationcover (%)
The sea otter population of Amchitka Island, in the Rat Island group Fig. 1. Vegetation coverage and sea densities of sea urchins occur in micro(11) of the Aleutian archipelago, has urchin density plotted against depth. The habitats along more protected cracks
and Shemya and beneath holdfasts of macrophytic
been estimated to be 20 to 30 animals data for Amchitka Islandfrom
four and
Island represent averages
at depths of 10
per square
three study areas, respectively. Vegetation vegetation. Beginning
The feeding habitat of the sea otter is cover at Shemya Island is coincident with to 20 m, sea urchin densities increase
with depth and vegetation coverage delimited to the intertidal and sublittoral the ordinate.
Sea Otters:Their Role in StructuringNearshoreCommunities
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creases in areas of solid substrate (Fig.
1). Densities of sea urchins are highly
variable at these depths, but range up
to 680 m-2 (15). The majority of
these sea urchins have test diameters
of less than 32 mm (16). The increase
in sea urchin density with depth is
probablyrelated to decreasedpredation
by sea otters (and perhaps diving
birds). Feeding on small sea urchins
at these depths may be energetically
infeasible for predators.
Conversely, the Near Island group is
characterized by a distinct lack of
macrophytic vegetation below the
lower intertidal region. In many areas,
sea urchins almost completely carpet
the sublittoral immediately adjacent to
the littoral, but densities decrease as a
function of depth (Fig. 1). Differences
in size class distribution and biomass
between Near Island and Rat Island
sea urchin populations are shown in
Fig. 2. The larger size (age) classes
of sea urchins are missing from the
Rat Island group.
Despite the physical similarities and
geographical proximity of the Rat Islands and the Near Islands, there are
major floral and faunal differences between the marine communities of their
The Rat Islands have an almost complete mat of benthic marine brown
algae (kelp), predominantlyHedophyl-
are probably related to the presence
or absence of sea otters. The otters
Near Islands, H. sessile and L. longipes
effectively control sea urchin populaare heavily grazed by dense populations tions, and the absence of grazing presof sea urchins and chitons, and there sure allows vegetational communities
are extensive mussel beds and dense to flourish. Reducing the population of
populations of barnacles. Less than 1 sea otters makes it possible for the sea
percent of the attached kelp examined urchin population to increase, and this
at the Rat Islands was grazed (17).
leads to a significant reduction in the
At the Near Islands all kelp overhang- size of the kelp beds and associated
ing channels and tide pools was grazed, communities.
and more than 75 percent of the L.
More far-reaching consequences of
longipes plots and 50 percent of the H. these relations are suggested by comsessile plots sampled contained grazed paring food webs and faunal distribuplants (17). Barnacle and mussel den- tions between the island groups. Bensities, respectively, averaged 4.9 m-2 thic macrophytes are of considerable
and 3.8 m-2 at the Rat Islands and importance to nearshore productivity
1215 m-2 and 722 m-2 at the Near in temperate waters (21). Species
Islands (17). Sea urchin and chiton whose food webs originate from macdensities, respectively, averaged 8 m-2
rophytic algal productivity would cerand less than 1 m-2 at the Rat Islands
tainly be adversely affected by its reand 78 m-2 and 38 m-2 at the Near moval. We believe that some faunal
Islands (17).
differences between the Near Islands
Kelp beds at the Rat Islands shelter and Rat Islands are related to the
the shore from wave action to an ap- presence or absence of benthic macropreciable extent. Populations of sessile phytes as a nutritional base. Rock
intertidal invertebrates decline drasti- greenling (Hexagrammos lagocephalus),
cally at the Rat Islands since they can- harbor seals (Phoca vitulina), and
not compete successfully with kelp for bald eagles (Haliaeetus leucocephalus)
space and they are hampered by silt are abundant in the Rat Islands but
which accumulates because wave- are scarce or absent in the Near Isinduced turbulence has been reduced lands (19, 22). These species depend
largely on nearshore marine productivClimate, sea state, tidal ranges, and ity in the Aleutians (23). We propose
mean tidal levels are similar at both that reduced populations of these (and
lum sessile and L. longipes, covering
island groups (19, 20), and we com- perhaps other) species in the Near Isthese benches. Sessile, filter-feeding pared only coastlines of similar struc- lands may be related to reduced macinvertebrates-barnacles (Balanus glan- ture (with wide intertidal benches). rophyte productivity.
dula and B. cariosus) and mussels
We. conclude that the differences obOur results suggest that reestablish(Mytilus edulis)-and
motile, herbi- served between benthic communities ment of sea otters along the Pacific
vorous invertebrates-sea urchins and of the Near Islands and Rat Islands coast of North America will have prochitons (Katharina tunicata)-are
conspicuous, small, and scarce. At the
-300 a
OSea urchin number 300 ”
‘-Sea urchin biomass
.. ‘.,.
‘: .
:100 ?3
. ..
30 40 50 60 70
9b 10
Fig. 2. Sea urchinsize class distributionsand associatedbiomasscontributions.(a) Data collectedfrom AmchitkaIsland (highdensity sea otter populations).(b) Data collected from ShemyaIsland(sea ottersabsent).The dottedline representsthe largest
sea urchinsize classobservedat AmchitkaIsland.
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found ecological effects. That this is
currentlyhappeningis indicated by the
sea otter-abalone controversy in California. A decrease in sport and commercial abalone fisheries has been
reported following the influx of sea
otters into areas of previously unoccupied habitat (24). Surveysconducted
in 1967 by the California Department
of Fish and Game revealed that
throughout the sea otters’ range preferred sea otter forage items were reduced in number and restricted to
protected habitat as compared with
habitat outside the range (25). Also,
an increased diversity in sea otter
forage items has been reportedin areas
long inhabited by sea otters. This is
apparentlythe result of reduced availability of preferred sea otter forage
items (24).
The sea otter may also be important
in restoring kelp beds (and associated
species of animals) in southern California. Sea otters in California completely remove large sea urchins
(Strongylocentrotus franciscanus) from
areas by predation, permitting luxuriant development of the NereocystisPterygophora (brown algae) association (4). Recent increases in sea
urchin populations are correlated with
kelp bed reduction (5). Although kelp
bed reductions are obviously related to
phenomena more recent than the disappearanceof sea otters (26), the reestablishment of sea otters should
decrease invertebrate populations and
increase vegetational biomass.
The sea otter is an importantspecies
in determiningstructuresand dynamic
relations within nearshore communities, and so fits Paine’s (27) concept
of a keystone species. Many changes
have resulted from the near extinction
of the sea otters in these communities
during the 18th and 19th centuries. In
modern biological studies of nearshore
marine communities along the Pacific
coast of North America the species’
ecological importance has not been
considered in sufficient detail. We believe that the sea otter is an evolutionary componentessential to the integrity
and stability of the ecosystem.
Arizona Cooperative Wildlife Research
Unit, University of Arizona,
Tucson 85721
College of Fisheries,
University of Washington,
Seattle 98195
References and Notes
1.. N. S. Jones and J. M. Kain, Helgol. Wiss.
Meeresunters. 15, 460 (1967); J. H. Himmelman and D. H. Steele, Mar. Biol. 9, 315
(1971); D. K. Camp, S. P. Cobb, J. F.
VanBreedveld, BioScience 23, 37 (1973); P. K.
Dayton, R. J. Rosenthal, L. C. Mahan,
Antarct. J. U.S. 8 (No. 2), 34 (1973); J. C.
Ogden and R. A. Brown, Science 182, 715
2. R. T. Paine and R. L. Vadas, Limnol.
Oceanogr. 14, 710 (1969).
3. A. Nelson-Smith, in The Biological Effects
of Oil Pollution on Littoral Communities,
J. D. Carthy and D. R. Arthur, Eds. (Field
Studies Council, London, 1968), vol. 2, supplement.
4. J. H. McLean, Biol. Bull. 122, 95 (1962).
5. W. J. North, Kelp Habitat Improvement
Project, Annual Report for 1964-1965 (California Institute of Technology, Pasadena,
6. J. C. Quast, Calif. Dep. Fish. Game Fish
Bull. 139, 109 (1968).
7. R. T. Paine, Am. Nat. 100, 65 (1966); J. W.
Porter, ibid. 106, 487 (1972).
8. R. L. Vadas, thesis, University of Washington
9. A. Ogden, The California Sea Otter Trade
1784-1848 (Univ. of California Press, Berkeley,
1941); I. I. Barabash-Nikiforov, Kalan (Soviet
Ministrov RSFSR, 1947), published in English
as The Sea Otter, A. Birron and Z. S. Cole,
Transl. (Israel Program for Scientific Translations, Jerusalem, 1962).
10. K. W. Kenyon, The Sea Otter in the Eastern
Pacific Ocean (Government Printing Office,
Washington, D.C., 1969).
11. The Rat Islands are located at approximately
52?N, 178?E.
12. J. A. Estes and N. S. Smith, USAEC Res.
Dev. Rep. NVO 520-1 (1973).
13. P. Morrison, M. Rosenmann, J. A. Estes, in
14. There is some doubt about the species identification of the green sea urchin in this area
(that is, S. drobachiensis or S. polyacanthus).
15. L. Barr, BioScience 21, 614 (1971).
16. Test diameter refers to a measurement of
the external skeleton diameter, not including
17. Data were collected from randomly selected
1/4-m2 plots (Rat Islands, N
171; Near Islands, N
9) and from 1/16-m2 plots at intervals along transect lines (Rat Islands, N = 32;
Near Islands, N = 23) [5. F. Palmisano and
C. E. O’Clair, unpublished results; C. E.
O’Clair and K. K. Chew, BioScience 21, 661
results of experiments that confirm these
conclusions will be presented by J. F. Palmisano (in preparation).
19. J. A. Estes and J. F. Palmisano, personal
20. U.S. Department of Commerce, Coast and
Geodetic Survey, Tide Tables, West Coast,
North and South America, 1969 (Government
Printing Office, Washington, D.C., 1968).
21. L. R. Blinks, J. Mar. Res. 14, 363 (1955);
K. H. Mann, Mar. Biol 14, 199 (1972).
22. C. J. Lensink, thesis, Purdue University
(1962); K. W. Kenyon and J. G. King, “Aerial
survey of sea otters, other marine mammals
and birds, Alaska Peninsula and Aleutian
Islands, 19 April to 9 May 1965,” Bureau of
Sport Fisheries and Wildlife report, on file
at the Fish and Wildlife Service, Department
of Commerce, Washington, D.C. (1965).
23. T. H. Scheffer and C. C. Sperry, J. Mammal.
12, 214 (1931); V. B. Scheffer and J. W. Slipp,
Am. Midi. Nat. 32, 373 (1944); C. M. White,
W. B. Emison, F. S. L. Williamson, BioScience
21, 623 (1971).
24. P. W. Wild, paper presented at the Conference of the American Association of
Zoological Parks and Aquariums, Western
Region, San Diego, California, 21 February
25. E. E. Ebert, Underwater Nat. 5, 20 (1968).
26. Sport Fish. Inst. Bull. 238 (1972), p. 1.
27. R. T. Paine, Am. Nat. 103, 91 (1969).
28. Supported by AEC contracts AT(26-1)-520
and AT(26-1)-171 through subcontract from
Battelle Memorial Institute, Columbus, Ohio.
We are indebted to S. Brown, R. Glinski, P.
Lebednik, C. O’Clair, and N. Smith for field
assistance. We thank P. Dayton and R. Paine
for helpful comments in preparing the manuscript and J. Isakson for assistance with logistic problems. The U.S. Air Force and U.S.
Coast Guard provided access to their facilities
in the Near Islands.
21 January 1974; revised 16 April 1974
Puromycin: A Questionable Drug for Studying the
Mechanism of Thyroid Calorigenesis in vivo
Abstract. Puromycin fails to alter minimal oxygen consumption of rats treated
with thyroxine, provided the rectal temperatures of these rats are maintained at
37.80 to 38.1?C. The previously reported puromycin-induced decline in basal
metabolic rate of thyroxine-treated rats may have been due to the hypothermia
produced by this drug.
Thyroid hormone-induced alteration docrine and nonendocrinefactors studof the rate of protein synthesis is a fa- ied, the MOC appears to measure
miliar hypothesis proposed to explain
changes in thyroid state more specifithe elevated consumption rate of 02
cally than the BMR (6). Unlike vari-
observed after administration of thy- ous BMR methods, MOC is measured
roid hormones (1, 2). This hypothesis in sleeping or anesthetizedrats, at their
is based on the results of experiments thermoneutraltemperature(3, 6). Therthat measured basal metabolic rate moneutrality is defined as the highest
(BMR) before and after the use of in- test chambertemperaturethat maintains
hibitors of protein synthesis (such as a normal rectal temperature (37.8? to
puromycin) in vivo (1, 2).
38.1?C) (3, 6). Oxygen consumption
Because of the importance of this was detected volumetrically with a
hypothesis, we tried to confirm the precision-bore glass tube (6); a servooriginal findings (2) by using a new system corrected for extraneous variaparameter-minimal oxygen consump- tions in ambient temperature and prestion (MOC) (3-6). Among the 70 en- sure (4). The MOC was expressed in
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Killer Whale Predation on Sea Otters Linking
Oceanic and Nearshore Ecosystems
J. A. Estes, et al.
Science 282, 473 (1998);
DOI: 10.1126/science.282.5388.473
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Killer Whale Predation on Sea
Otters Linking Oceanic and
Nearshore Ecosystems
J. A. Estes,* M. T. Tinker, T. M. Williams, D. F. Doak
After nearly a century of recovery from overhunting, sea otter populations are
in abrupt decline over large areas of western Alaska. Increased killer whale
predation is the likely cause of these declines. Elevated sea urchin density and
the consequent deforestation of kelp beds in the nearshore community demonstrate that the otter’s keystone role has been reduced or eliminated. This
chain of interactions was probably initiated by anthropogenic changes in the
offshore oceanic ecosystem.
Apex predators often initiate forces that cascade across successively lower trophic levels,
sometimes reaching the base of the food web
(1). Plant-herbivore interactions vary predictably with trophic complexity in such systems,
being weak or strong when the number of
trophic levels is odd or even, respectively (2).
Sea otters (Enhydra lutris) and kelp forests
provide a well-known example of this pattern
(3). After being protected from overhunting,
recovering otter populations transformed
nearshore reefs from two- to three-trophiclevel systems by limiting the distribution and
abundance of herbivorous sea urchins, thereby promoting kelp forest development (4).
Sea otters abounded across the North Pacific rim until unregulated exploitation in the maritime fur trade reduced the species to nearextinction by the early 20th century (5). Population regrowth began when protection was afforded under the International Fur Seal Treaty.
A geographically discordant recovery pattern
ensued because of the fragmented distribution
of surviving colonies, the discontinuous nature
of their habitat, and the otter’s limited dispersal
ability (5, 6 ). Consequently, by the 1970s otter
populations had recovered to near maximum
densities in some areas of their historic range,
were growing rapidly in others, and remained
absent from still others (7). The sea otter’s
predatory role in kelp forest ecosystems was
discovered by contrasting inhabited with uninhabited areas (8) and by observing changes
over time as the uninhabited areas were recolonized and their founding populations grew (4,
9). In addition to showing the influence of sea
J. A. Estes, Biological Resources Division, U.S. Geological Survey, A-316 Earth & Marine Sciences Building,
University of California, Santa Cruz, CA 95064, USA.
M. T. Tinker, Glenside Ecological Services, 79 High
Street, Victoria, British Columbia, V8Z 5C8, Canada.
T. M. Williams, Department of Biology, University of
California, Santa Cruz, CA 95064, USA. D. F. Doak,
Environmental Studies Board, University of California,
Santa Cruz, CA 95064, USA.
*To whom correspondence should be addressed. Email:
otters on North Pacific kelp forests, this approach has demonstrated a breadth of indirect
effects on coastal ecosystems (10). The sea
otter’s reputation as a keystone species (11) is
based on these interactions and processes.
Recently, sea otter populations have declined precipitously and unexpectedly over
large areas of western Alaska. We first detected
this decline through population surveys at Adak
Island in the central Aleutian archipelago,
which indicated that the otter population decreased ;25% per year through the 1990s,
resulting in nearly an order-of-magnitude overall reduction by 1997 (Fig. 1). Additional surveys of Little Kiska, Amchitka, and Kagalaska
Islands all show population declines of similar
timing and rate to that which occurred at Adak
(Fig. 1). Aerial surveys of the Aleutian archipelago conducted by the U.S. Fish and Wildlife
Service in 1965 and 1992 further indicate that
these declines are occurring throughout the region (12). The concurrent and widespread nature of these declines strongly suggests a causal
link with the oceanic environment.
Demographic explanations for the sea otter population declines are limited to reduced
fertility, increased mortality, or redistribution. Of these, reduced fertility and redistribution can be excluded. Studies of radiotagged sea otters at Amchitka Island in 1992–
94 and Adak Island in 1995–96 show that
birth rates of adult females and pup survival
rates from birth to weaning were similar to
those of stable populations. Redistribution is
equally unlikely because the declines were
synchronous over large areas—there have
been no population buildups on some islands
to account for the losses on others—and radio-tagged otters at Amchitka and Adak islands provided no indication of redistribution
during the declines (13). From this we conclude that the sea otter population declines
were caused by increased mortality.
Three lines of evidence point to increased
predation by killer whales (Orcinus orca) as the
reason for this mortality. First, although killer
whales and sea otters have been observed in
close proximity for decades, the first attack on a
sea otter was seen in 1991. Subsequently, nine
more attacks have been reported (14). We evaluated the likelihood that this cluster of recent
observations was due to chance alone by summing the number of person-days spent in the
Aleutian Islands by our research team before
and after 1990 (3405 person-days before; 4005
after), estimating the attack rate from the post1990 data (0.0015 attacks per day), and then
calculating the probability of no attacks being
seen before 1990 if the attack rate remained
constant over the 27-year period. By modeling
the expected number of observed attacks as a
Poisson process, the probability of zero attacks
being seen before 1990 is 0.006 (15).
Second, we evaluated the impact of killer
whales on sea otter populations at Adak Island
by contrasting otter population trends and survival rates between Clam Lagoon, an area
uniquely inaccessible to killer whales, and adjacent Kuluk Bay, an open coastal environment
(Fig. 2). Sea otter numbers were stable from
1993 through 1997 in Clam Lagoon, whereas in
Kuluk Bay they declined by 76%. In 1995, we
marked 17 otters in Clam Lagoon and another
37 in Kuluk Bay with flipper tags and surgically
implanted radio transmitters in order to compare their behavior and demography. There was
virtually no movement of the marked animals
between these areas. However, through year 1
of the study, the disappearance rate of sea otters
in Kuluk Bay (65%) was greater than five times
that of Clam Lagoon (12%), a trend that continued through year 2.
Finally, we estimated how many otters must
have been eaten by killer whales to drive the
decline rates, and then compared the actual
number of observed attacks with the expected
number of observed attacks based on this estimate. This analysis was done for the area between Kiska and Seguam Islands. Before the
onset of the decline, an estimated 52,656 otters
inhabited this area (16 ). Life table statistics
(age-specific birth and death rates) were estimated from data collected during earlier field
studies to construct a Leslie matrix for a stationary population. We then added an age-constant death rate (17) from killer whale predation
sufficient to reduce the population by 78% over
6 years—the observed rate and magnitude of
decline at Adak. The simulation was run by
holding the number of individuals that died
from killer whale predation constant over time,
which produced a loss estimate of 6788 otters
per year. The expected number of observed
attacks produced by this approach is 5.05 for
this 6-year period (18). This compares favorably with the 6 attacks that were seen.
Disease, toxins, and starvation, which are
three other causes of elevated mortality in
wildlife populations, can be dismissed as
causes of the population declines. Any one of
these should have produced substantial numbers of beach-cast carcasses, whereas very SCIENCE VOL 282 16 OCTOBER 1998
Downloaded from on September 7, 2007
few were found. Marked increases in sea
urchin biomass during the population decline
at Adak (Fig. 1) are further evidence against
starvation, because sea urchins are the principal prey of sea otters in the Aleutian Islands
(19). Although we looked specifically for
Fig. 1. (A) Changes in sea otter abundance over time at several islands in the Aleutian archipelago
and concurrent changes in (B) sea urchin biomass, (C) grazing intensity, and (D) kelp density
measured from kelp forests at Adak Island. Error bars in (B) and (C) indicate 1 SE. The proposed
mechanisms of change are portrayed in the marginal cartoons—the one on the left shows how the
kelp forest ecosystem was organized before the sea otter’s decline and the one on the right shows
how this ecosystem changed with the addition of killer whales as an apex predator. Heavy arrows
represent strong trophic interactions; light arrows represent weak interactions.
signs of disease, none were found (20). Elevated contaminant concentrations have been
reported in the Aleutian Islands (21), but
subsequent analyses from 39 sites across the
Aleutian archipelago have shown that these
are restricted to a few small areas (22), which
is inconsistent with the widespread declines
in otter numbers.
The collective evidence thus leads us to
conclude that increased killer whale predation has caused the otter declines. Although
the population size and status of killer whales
in the Aleutian Islands are unknown, these
animals are commonly seen. From the energetic requirements of free-ranging killer
whales and the caloric value of sea otters, we
estimate that a single killer whale would consume 1825 otters per year and thus that the
otter population decline could have been
caused by as few as 3.7 whales (23).
Strikingly rapid changes in the kelp forest
ecosystem have accompanied the sea otter
population declines (Fig. 1). In 1987, when
otters at Adak Island were near equilibrium
density, the kelp forests were surveyed at 28
randomly selected sites (4). Otters were still
numerous at Adak in 1991, when five of these
sites were randomly chosen for the measurement of plant tissue loss to herbivory (24).
Using similar procedures at the same sites in
1997, we resurveyed the kelp forest and repeated the measurements of plant tissue loss
to herbivory. Over the 10-year interim, sea
urchin size and density increased to produce an eight-fold increase in biomass,
while kelp density declined by more than a
factor of 12 (Fig. 1). The average rate of
kelp tissue loss to herbivory increased from
1.1% per day in 1991 to 47.5% per day in
1997 (Fig.1). Observations made in August
of 1997 revealed similar changes at Kiska,
Amchitka, and Kagalaska Islands.
Killer whales and sea otters have co-inhabited the west-central Aleutian archipelago for
much of the past half century, and probably for
millennia before. Thus, it is necessary to exFig. 2. Population trends and survival rates of
sea otters in Clam Lagoon (solid squares) and
adjacent Kuluk Bay (open circles), Adak Island,
Alaska. (A) The rate of population change r,
calculated as the slope of the linear best fit to
the natural log of the number of otters counted
versus year, for Kuluk Bay between 1993 and
1997 was – 0.345 (SE 5 0.058), which is significantly different from 0 (R2 5 0.946, P 5
0.027). In Clam Lagoon, the rate of change over
this same period was 0.006 (SE 5 0.034), which
is not significantly different from 0 [R2 5 0.011,
P 5 0.867; statistical power to detect r $ 0.1 5
0.9]. The measured rates in Kuluk Bay and Clam
Lagoon differed significantly (x2 5 27.26, 1 df,
P , 0.001). (B) Survival rates of marked sea
otters differed significantly between Clam Lagoon (0.88 year–1) and Kuluk Bay (0.35 year–1;
x2 5 13.52, 1 df, P , 0.001).
Downloaded from on September 7, 2007
plain why the behavior of killer whales toward
sea otters has recently changed. The most likely
explanation is a shift in the prey resource base
for killer whales. Some killer whale groups or
individuals feed on marine mammals (25), including Steller sea lions and harbor seals, and
populations of both these species recently have
collapsed across the western North Pacific. Sea
lion populations began to decline in the late
1970s, and their numbers had reached minimum levels in the Aleutian islands by the late
1980s (26 ), a time that coincides with the onset
of otter declines. Although the exact cause of
the pinniped decline is uncertain (27), it probably relates to reduced abundance and altered
species composition of their prey (28). Recent
population declines of piscivorous marine birds
are consistent with this explanation (29). Why
forage fish stocks have shifted is not well understood, although the change was likely
caused by some combination of effects from the
region’s burgeoning fisheries, increased ocean
temperature, and depletion of baleen whales
Regardless of the ultimate cause, sea otter
population declines and the consequent collapse
of kelp forest ecosystems almost certainly have
been driven by events in the offshore oceanic
realm. Our proposed explanation involves a
chain of ecological interactions, beginning with
reduced or altered forage fish stocks in the
oceanic environment, which in turn sent pinniped populations into decline. Pinniped numbers eventually became so reduced that some of
the killer whales who once fed on them expanded their diet to include sea otters. This shift in
killer whale foraging behavior created a linkage
between oceanic and coastal ecosystems and in
so doing transformed coastal kelp forests from
three- to four-trophic-level systems, thereby releasing sea urchins from the limiting influence
of sea otter predation. Unregulated urchin populations increased rapidly and overgrazed the
kelp forests, thus setting into motion a host of
effects in the coastal ecosystem.
Parts of this scenario are well documented,
others are more speculative, and still others
have yet to be evaluated. Nonetheless, the data
are sufficient to make several points of broader
ecological significance. First, our findings afford evidence of the often underappreciated
importance that uncommon and transient species can have in controlling community structure, demonstrating further that such species
can link interactions across ecosystems. Although intersystem linkages are becoming increasingly well known (31), this example is
unusual because the linkage is formed through
the activities of a top-level carnivore. Additionally, our results are relevant to understanding
food web dynamics, because they demonstrate
that adding another apex predator to a system
under top-down control has predictable effects
on plant populations at the base of the food
chain. Finally, results from this long-term study
have implications for both the approach to and
scale of other ecological field studies. The
events reported here could not have been chronicled or even detected in a short-term study,
were unanticipated, and thus seem poorly suited
for analysis by a priori hypothesis testing.
These points emphasize the potential significance of large-scale ecological events and the
consequent need for large-scale approaches in
ecological research.
References and Notes
1. S. R. Carpenter and J. F. Kitchell, The Trophic Cascades
in Lakes (Cambridge Univ. Press, Cambridge, 1993).
2. N. G. Hairston et al., Am. Nat. 94, 421 (1960); S. D.
Fretwell, Oikos 50, 291 (1987); M. E. Power, Science
250, 811 (1990).
3. P. D. Steinberg et al., Proc. Natl. Acad. Sci. U.S.A. 92,
8145 (1995).
4. J. A. Estes and D. O. Duggins, Ecol. Monogr. 65, 75
5. K. W. Kenyon, North American Fauna 68, 1 (1969).
6. M. L. Riedman and J. A. Estes, Biol. Rep. U.S. Fish
Wildl. Serv. 90 (14), 1 (1990).
7. L. M. Rotterman and T. Simon-Jackson, in Selected
Marine Mammals of Alaska, J. W. Lentfer, Ed. (PB8817462, National Technical Information Service,
Springfield, VA, 1988), pp. 237–275.
8. J. A. Estes and J. F. Palmisano, Science 185, 1058
9. G. R. Van Blaricom and J. A. Estes, Eds., The Community Ecology of Sea Otters (Ecological Studies No. 65,
Springer-Verlag, NY, 1988).
10. D. O. Duggins et al., Science 245, 170 (1989); P. K.
Dayton, Fish. Bull. 73, 230 (1975); D. O. Duggins,
Ecology 61, 447 (1980); D. C. Reed and M. S. Foster,
ibid. 65, 937 (1984); J. A. Estes, in Aquatic Predators
and Their Prey, S. P. R. Greenstreet and M. L. Tasker,
Eds. (Fishing News Books, Oxford, 1996), pp. 65–72.
11. M. E. Power et al., Bioscience 46, 609 (1996).
12. By 1965, otter populations had recovered to preexploitation levels at most of the Aleutian islands,
from Kiska in the west to Adak in the east (5). Of the
21 islands in this region that were surveyed in both
1965 and 1992, sea otter counts decreased at all but
one, for an average reduction of 58%. The 1965 data
are from (5); the 1992 data are from T. J. Evans et al.,
Technical Report MMM 97-5 (U.S. Fish and Wildlife
Service, Anchorage, AK, 1997).
13. Among resightings of radio-tagged otters at Adak
(1635 resightings of 52 otters) and Amchitka (3711
resightings of 98 otters), the maximum distances
moved were 4.31 and 6.95 km, respectively. From
1992 to 1997, most of the marked animals that were
lost from these populations disappeared suddenly
and without a trace, after being seen regularly in
predictable locations through months of study.
14. B. B. Hatfield et al., Mar. Mamm. Sci., in press.
15. This probability was calculated from the Poisson
probability density function f(x) 5 e–mmx/x!, for m 5
5.1 (the expected number of attacks seen) and x 5 0
(the number of attacks actually seen).
16. This number was obtained from counts made during a
1965 aerial survey (5) and adjusted upward by a factor
of 5.62 to account for the proportion of animals that
were not seen. The adjustment factor was calculated
from a 1972 estimate of sea otter abundance at Amchitka Island [estimate, 6432; from J. A. Estes, in The
Environment of Amchitka Island, M. L. Merritt and R. G.
Fuller, Eds. (TID-26712, U.S. Energy Research and Development Administration, Springfield, VA, 1977), pp.
511–526] divided by the number of otters counted at
Amchitka in the 1965 aerial survey (1144).
17. The age-constant death rate was inferred from the
age-constant rates of otter disappearance seen in our
field studies of marked sea otters at Adak Island.
18. The expected number of observed attacks was calculated as N(t/T )(a/A), where N 5 40,728 otters, which is
the estimated number eaten by killer whales between
1991 and 1997; t 5 21,677 hours, which is the number
of person-hours of field time spent by our research
team during this period; T 5 52,560 hours (that is, 6
years); a 5 1 km, which is the observer’s sighting
window [that is, two times the maximum distance from
observers that attacks have been seen (14)]; and A 5
3327 km, which is the area’s coastal length.
J. A. Estes et al., in Worldwide Furbearer Conference
Proceedings, J. A. Chapman and D. Pursley, Eds. (Univ.
of Maryland Press, Frostburg, MD, 1981), pp. 606 –
Gross observation and hematological analyses of
66 sea otters captured at Adak, Amchitka, Kiska,
and Kanaga Islands during the summer of 1997
failed to provide any known sign of disease. All of
these animals appeared to be in excellent health
(D. Jessup, Senior Wildlife Veterinarian, California
Department of Fish and Game, Santa Cruz, CA,
personal communication).
J. A. Estes et al., Mar. Poll. Bull. 34, 486 (1997).
S. Reese, thesis, University of California, Santa Cruz
We have estimated that 40,000 sea otters would have
to have been eaten to drive the observed decline. The
minimal number of killer whales necessary to consume
this number of otters was determined by measuring the
caloric value of sea otters; estimating the field metabolic rate of killer whales, discounted for assimilation
efficiency; and then equating these values to estimate
the number of sea otters needed to fuel a wild killer
whale. The caloric content of adult sea otters, determined by adiabatic bomb calorimetry of homogenized
carcasses, averaged 1.81 6 0.04 kcal gm–1 of wet
weight. Field metabolic rate (FMR) was 7934 watts ( W)
for female and 11,800 W for male killer whales (51 to
59 kcal kg–1 of killer whale per day). Values for FMR
were based on field metabolic rates of odontocetes
(D. P. Costa and T. M. Williams, unpublished data) and
their basal metabolism [B. Kriete, thesis, Univ. of British
Columbia (1995)]. Our estimate of killer whale FMR
compares with the 30 to 62 kcal kg–1 day–1 reported by
L. G. Barrett-Lennard et al. [Report for the North Pacific
Universities Marine Mammal Consortium (Univ. of
British Columbia, Vancouver, BC, Canada, 1994)],
R. W. Baird [thesis, Simon Frasier University, Vancouver, BC, Canada, (1994)], and B. Kriete [thesis,
Univ. of British Columbia, Vancouver, BC, Canada,
(1995)]. The caloric value of sea otters compares
with a range of 0.78 to 3.55 kcal gm–1 of wet
weight for fish and other marine mammals that
make up the killer whale diet. An adult male sea
otter weighing 34 kg provides 61,540 kcal (34,000
gm 3 1.81 kcal gm–1 of wet weight); a 23-kg adult
female otter provides 41,630 kcal. From this, we
calculated that an adult female killer whale feeding
exclusively on sea otters would need three male or
five female sea otters per day, and an adult male
would require five male or seven female otters per
day. The average consumption rate (five otters per
whale per day) was divided into the sea otter loss
estimate to determine how many killer whales
would be needed to account for the losses. Based
on this approach, 3.7 killer whales feeding exclusively on sea otters would be sufficient to drive the
population decline.
These measurements of plant tissue loss were obtained by placing preweighed pieces of tissues
from blades of the four most common kelp species—Alaria fistulosa, Laminaria groenlandica, Agarum cribrosum, and Thalassiophyllum clathrus— on
the seafloor and recording their change in mass
over 24 hours relative to that of adjacent caged
controls. Five replicates were done for each species
at each site.
J. R. Heimlich-Boran, Can. J. Zool. 66, 565 (1988);
J. K. B. Ford et al., Killer Whales: The Natural
History and Genealogy of Orcinus orca in British
Columbia and Washington State (Univ. of British
Columbia Press, Vancouver, BC, 1994).
A. E. York et al., in Metapopulations and Wildlife
Conservation, D. R. McCullough, Ed. (Island Press,
Washington, DC, 1996), pp. 259 –292.
M. A. Pascual and M. D. Adkison, Ecol. Appl. 4, 393
R. L. Merrick et al., Can. J. Fish. Aquat. Sci. 54, 1342 SCIENCE VOL 282 16 OCTOBER 1998
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31. G. A. Polis and D. R. Strong, Am. Nat. 147, 813
(1996); G. A. Polis et al., Annu. Rev. Ecol. Syst. 28,
289 (1997).
32. Supported by grants from NSF and the Office of
Naval Research, and by a contract from the U.S.
Navy. The Alaska Maritime National Wildlife Refuge provided logistic support for work in the Aleu-
Induction of Antigen-Specific
Cytotoxic T Lymphocytes in
Humans by a Malaria DNA
Ruobing Wang,* Denise L. Doolan,* Thong P. Le,†
Richard C. Hedstrom, Kevin M. Coonan, Yupin Charoenvit,
Trevor R. Jones, Peter Hobart, Michal Margalith, Jennifer Ng,
Walter R. Weiss, Martha Sedegah, Charles de Taisne,
Jon A. Norman, Stephen L. Hoffman‡
CD81 cytotoxic T lymphocytes (CTLs) are critical for protection against intracellular pathogens but often have been difficult to induce by subunit vaccines in
animals. DNA vaccines elicit protective CD81 T cell responses. Malaria-naı̈ve volunteers who were vaccinated with plasmid DNA encoding a malaria protein developed antigen-specific, genetically restricted, CD81 T cell–dependent CTLs. Responses were directed against all 10 peptides tested and were restricted by six
human lymphocyte antigen (HLA) class I alleles. This first demonstration in healthy
naı̈ve humans of the induction of CD81 CTLs by DNA vaccines, including CTLs that
were restricted by multiple HLA alleles in the same individual, provides a foundation
for further human testing of this potentially revolutionary vaccine technology.
During 1990–1994, the administration of “naked” plasmid DNA encoding a specific protein
antigen was shown to induce expression of the
protein in mouse myocytes (1), to elicit antibodies against the protein (2), and to manifest
protection against influenza (3) and malaria (4)
that was dependent on CD81 T cell responses
against the expressed protein. Hundreds of publications have now reported the efficacy of
R. Wang, Malaria Program, Naval Medical Research
Institute, Bethesda, MD 20889 –5607, USA, and Henry
M. Jackson Foundation, Rockville, MD 20852,
USA. D. L. Doolan, Malaria Program, Naval Medical
Research Institute, Bethesda, MD 20889 –5607, USA,
and Pan American Health Organization, Regional Office of the World Health Organization, Washington,
DC 20037, USA. T. P. Le, R. C. Hedstrom, Y. Charoenvit, T. R. Jones, W. R. Weiss, M. Sedegah, S. L. Hoffman,
Malaria Program, Naval Medical Research Institute,
Bethesda, MD 20889 –5607, USA. K. M. Coonan, Medical Division, U.S. Army Medical Research Institute of
Infectious Diseases, Fort Detrick, MD 21701, USA. P.
Hobart, M. Margalith, J. A. Norman, Vical, San Diego,
CA 92121, USA. J. Ng, C. W. Bill Young Department of
Defense Bone Marrow Donor Program, Naval Medical
Research Institute, Bethesda, MD 20889–5607, USA. C.
de Taisne, Pasteur-Merieux Connaught-France, 69007
Lyon, France.
*These authors contributed equally to this work.
†Present address: Clinical Research, Pasteur-Merieux
Connaught-USA, Swiftwater, PA 18370, USA.
‡To whom correspondence should be addressed. Email:
DNA vaccines in small and large animal models of infectious diseases, cancer, and autoimmune diseases (5).
DNA vaccines elicit antibodies and CD41 T
cell responses in animals, but their major advantage at the immunological level has been their
capacity to induce antigen-specific CD81 T cell
responses, including CTLs, which is a major
mechanism of protection against intracellular
pathogens. Important to our method of developing a malaria vaccine is the induction of CD81
T cell responses against Plasmodium falciparum
–infected hepatocytes (6). The lysis of cells in a
standard chromium release assay was used as a
surrogate for antihepatocyte responses, because
it has been established that CD81 CTLs, which
recognize peptide-pulsed target cells, also recognize and eliminate parasite-infected hepatocytes (6). On the basis of our work with rodents
(4, 7) and our work and that of others with
rhesus monkeys (8, 9), we have developed a
plan for manufacturing and testing the efficacy
of a multigene P. falciparum liver-stage DNA
vaccine in humans (10). This has been contingent on establishing that DNA vaccination of
humans is safe and induces antigen-specific,
genetically restricted, CD81 T cell–dependent
CTLs. Recently, the presence of CTL responses
in human immunodeficiency virus (HIV)–infected individuals after vaccination with plas-
tian Islands. We thank C. Dominick, B. Konar, J.
Meehan, K. Miles, and J. Stewart for field assistance
and K. Clifton, D. Croll, E. Danner, L. Fox, B. Lyon, R.
Ostfeld, M. Power, and A. Springer for comments
on the manuscript.
27 May 1998; accepted 20 July 1998
mid DNA encoding the nef, rev, or tat genes or
the env and rev genes of HIV was reported (11).
Interpreting these results is difficult because of
the concurrent HIV infection, which has been
demonstrated to prime individuals for a CTL
response that is independent of immunization.
Accordingly, 20 healthy, malaria-naı̈ve
adults were recruited and randomized into four
dosage groups of five individuals. Three injections of 20, 100, 500, or 2500 mg of plasmid
DNA encoding the P. falciparum circumsporozoite protein (PfCSP) (12) were administered at
4-week intervals in alternate deltoids (13). The
details of recruitment, safety, and tolerability
were reported elsewhere (14). To assess CTL
responses, we collected peripheral blood mononuclear cells (PBMCs) from each volunteer before vaccination, 2 weeks after the second immunization, and 2 and 6 weeks after the third
immunization. These cells were either assayed
while fresh for recall antigen-specific CTL responses (15) or were frozen (16) for subsequent
study. In parallel, CTL assays were carried out
with PBMCs from nonimmunized control volunteers. Cytolytic activity was assessed after
both primary and secondary in vitro restimulation against HLA-matched and HLA-mismatched PfCSP-specific and control targets.
The percent lysis and the percent specific lysis
were determined as described (15). The most
sensitive and specific method (17) for demonstrating the presence of CTLs was with effector
cells that were expanded in vitro by exposure to
cells infected with canary pox (ALVAC) expressing the PfCSP (18) and with target cells
that were sensitized with PfCSP-derived synthetic peptides (19). There was no apparent difference between the primary and secondary assays (20) or between the fresh and frozen specimens (21).
For logistical reasons, fresh PBMCs were
studied only before vaccination and after the
second immunization in the 20- and 100-mgdosage groups but were studied before vaccination and after all immunizations in the 500- and
2500-mg-dosage groups, with the exception of
one individual (13). For 14 individuals, adequate amounts of frozen PBMCs were available
for further analysis. A typical pattern of CTL
responses is presented in Fig. 1A. These responses were peptide-specific and genetically
restricted because there was little or no recognition of autologous targets that were incubated
with the control peptide or of HLA class I–mismatched targets that were incubated with the
specific peptide. This activity was shown to be
CD81 T cell– dependent by restimulating
Downloaded from on September 7, 2007
(1997); R. L. Merrick and D. G. Calkins, U.S. Department of Commerce, NOAA Tech. Rep. NMFS 126, 153
29. A. Springer, Alaska Sea Grant Report 93-01, 14 (Univ.
of Alaska, Fairbanks, AK, 1993).
30. National Research Council, The Bering Sea Ecosystem
(National Academy Press, Washington, DC, 1996).

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