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MARINE ECOLOGY PROGRESS SERIES
Mar Ecol Prog Ser
Vol. 242: 143–152, 2002 Published October 25
INTRODUCTION
Mass mortalities of marine organisms due to out-
breaks of disease appear to be increasingly common
throughout the world’s oceans (Harvell et al. 1999).
Along the coast of California, USA, the ecologically
© Inter-Research 2002 · www.int-res.com
*Corresponding author. Present address: Department of
Environmental Biology, The University of Adelaide, South
Australia 5005, Australia.
E-mail: todd.minchinton@adelaide.edu.au
Continued declines of black abalone along the
coast of California: are mass mortalities related
to El Niño events?
Peter T. Raimondi1, C. Melissa Wilson1, Richard F. Ambrose2, John M. Engle3,
Todd E. Minchinton1,*
1Department of Ecology and Evolutionary Biology, Long Marine Laboratory, 100 Shaffer Road, University of California,
Santa Cruz, California 95064, USA
2Environmental Science and Engineering Program, Department of Environmental Health Sciences, PO Box 951772,
University of California, Los Angeles, California 90095-1772, USA
3Marine Science Institute, University of California, Santa Barbara, California 93106, USA
ABSTRACT: The intertidal black abalone Haliotis cracherodii has experienced mass mortalities along
the coast of California, USA, since the mid-1980s. Mortality is due to infection by a pathogen that leads
to a fatal wasting disease called ‘withering syndrome’, where the foot of the abalone atrophies until it
can no longer adhere to the substratum. Massive die-offs due to withering syndrome were first noted
on the Channel Islands in 1986, and by 1992 withering syndrome was observed near Point Conception
on the mainland and was suspected to be spreading northward up the coast of California. The timing
of the initial mass mortalities following the strong 1982 to 1983 El Niño and an isolated outbreak of
withering syndrome in 1988 at Diablo Cove, north of Point Conception, following warm water dis-
charge from a power plant, led to the hypothesis that the onset of mass mortalities due to withering
syndrome may be triggered by elevated seawater temperatures. We surveyed black abalone popula-
tions at 7 sites along the mainland coast of California (including 3 where withering syndrome was al-
ready present) from 1992 to 2001, a period spanning 2 El Niño events, to determine whether (1) with-
ering syndrome and associated declines of black abalone were spreading northward up the coast; and
(2) these mass mortalities of black abalone could be related to elevated seawater temperatures during
El Niño events. Mass mortalities of black abalone due to withering syndrome were observed at the
5most southern sites (>90% decline in numbers in all size classes), but not at the 2 most northern sites,
and there was a clear pattern of decline from south to north over time. Massive die-offs of abalone
were not exclusively associated with times of elevated sea surface temperatures due to El Niño. Nev-
ertheless, rapid declines of abalone at 2 sites coincided with the strong 1997 to 1998 El Niño, and de-
clines during El Niño events were faster than those during non-El Niño years. Abalone at the 2 most
northern sites, where only slight declines occurred during the 1997 to 1998 El Niño, may not have been
infected by disease. It appears, therefore, that in the presence of the pathogen, warm water conditions
associated with El Niño may accelerate the development of withering syndrome and the rate of decline
of black abalone. Consequently, anthropogenic disturbances, such as discharges of heated water or
global warming, may increase the incidence of this fatal disease.
KEY WORDS: Withering syndrome · El Niño · Haliotis cracherodii · Human disturbance · Mass
mortalities · Marine diseases · Intertidal zone
Resale or republication not permitted without written consent of the publisher
Mar Ecol Prog Ser 242: 143–152, 2002
and once commercially important intertidal black
abalone Haliotis cracherodii has suffered massive local
die-offs (generally >90% losses) since the mid-1980s
(Davis et al. 1992, Steinbeck et al. 1992, Lafferty &
Kuris 1993, VanBlaricom et al. 1993, Altstatt et al.
1996). Mortality has been attributed to a chronic and
fatal condition called ‘withering syndrome’ (Tissot
1990, Haaker et al. 1992, Gardner et al. 1995, Fried-
man et al. 1997). The most prominent features of this
wasting disease in the field include reduced body
mass, weakness and a withered foot which prevents
the abalone from clinging to the substratum (Haaker et
al. 1992, Richards & Davis 1993).
Dying abalone with signs of withering syndrome
were first observed on several of the Channel Islands
off the coast of southern California in 1986 (Haaker et
al. 1992, see Fig. 1). By 1992, withering syndrome and
mass mortalities of black abalone had radiated
throughout the Channel Islands (Tissot 1990, Davis et
al. 1992, Richards & Davis 1993, VanBlaricom et al.
1993). Along the mainland coast at this time, withering
syndrome and die-offs of black abalone were observed
at a single site, Diablo Cove in central California in
1988 (Steinbeck et al. 1992). Withering syndrome may
have also been present during this time along the
mainland coast south of Point Conception, but,
because populations of black abalone were so small
due to harvesting, the disease and associated mor-
talities may have gone undetected. In 1992, mass
mortalities were again observed along the mainland
coast, this time at a site near Point Conception, north of
the Channel Islands and south of Diablo Cove (Altstatt
et al. 1996). Subsequent monitoring by Altstatt et al.
(1996) over the next 4 yr revealed that declines of black
abalone were occurring at nearby sites to the north,
and they suggested that withering syndrome might be
progressing northward up the coast.
Explanations for the cause of withering syndrome
have largely focused on the presence of pathogens,
natural and anthropogenic environmental stresses,
and their interactions. An initial hypothesis was that
the disease was caused by thermal stress and starva-
tion due to elevated seawater temperatures and
reduced availability of food associated with El Niño
events (Tissot 1990, 1995, Davis et al. 1992, Richards
&Davis 1993). This hypothesis was put forth because
the disease and associated massive die-offs of black
abalone were initially observed at the Channel Islands
following the strong 1982 to 1983 El Niño and the
weaker 1986 to 1987 El Niño. This explanation ap-
peared to be supported when an isolated outbreak
of withering syndrome and massive die-offs of black
abalone were observed in 1988 at Diablo Cove on the
mainland coast of California, where the thermal dis-
charge of water from the Diablo Canyon Power Plant
raised seawater temperatures up to 11°C above ambi-
ent (Steinbeck et al. 1992). The presence of potential
pathogens and the geographic patterns of spread of
the syndrome and mortalities on the Channel Islands
and along the mainland coast of California provided
evidence for an infectious agent as the cause of disease
(Lafferty & Kuris 1993, Altstatt et al. 1996). Recently, an
intracellular bacterium, given the provisional status
of ‘Candidatus Xenohaliotis californiensis’, that infects
the epithelial cells of the gastrointestinal tract of black
abalone, has been identified as the causative agent of
withering syndrome (Friedman et al. 2000).
The pathogen and isolated cases of withering syn-
drome have now been observed in black abalone
along the central and extending toward the northern
coast of California, most notably at several sites where
mass mortalities have yet to occur (Altstatt et al. 1996,
Andree et al. 2000, authors’ pers. obs.). Abalone may
thus be infected with the bacterium before clinical
signs of withering syndrome are evident in the field
(Friedman et al. 1997, Andree et al. 2000) and the
appearance of isolated cases of withered abalone may
precede massive local die-offs. This lag between infec-
tion, the development of clinical withering syndrome
and the onset of mass mortalities may represent an
incubation period during which the bacteria grow to
critical levels within the local population. Stressful
environmental conditions, such as elevated water tem-
perature or reduced food supply, may increase the
susceptibility of abalone to disease, shorten the incu-
bation period, increase the incidence of withering syn-
drome and accelerate the onset of mass mortalities
of black abalone. Laboratory studies examining the
effects of thermal stress and lack of food on black
abalone have shown that neither appears to be the
direct cause of withering syndrome (Steinbeck et al.
1992, Friedman et al. 1997). Nevertheless, elevated
water temperatures appear to increase the rate of mor-
tality of black abalone (Steinbeck et al. 1992, Lafferty
& Kuris 1993, Tissot 1995, Friedman et al. 1997, see
also Moore et al. 2000 for studies with red abalone
Haliotis rufescens). Therefore, as is increasingly docu-
mented for other marine species (see Harvell et al.
1999), mass mortalities of black abalone due to wither-
ing syndrome may be triggered by prolonged periods
of above-average seawater temperatures, which are
characteristic of El Niño events.
Here, we present the results of surveys at 7 sites doc-
umenting the continued mass mortalities (and lack of
recovery) of populations of black abalone along the
mainland coast of California, USA, for nearly a decade
(1992 to 2001) spanning the El Niño events of 1991 to
1993 and 1997 to 1998 (Wolter & Timlin 1998). Our first
of 2 objectives was to determine whether withering
syndrome and associated declines of black abalone
144
Raimondi et al.: Effects of El Niño on withering syndrome in abalone
were progressing northward up the coast as predicted
by Altstatt et al. (1996). Our second objective was to
assess whether these mass mortalities of black abalone
could be related to elevated seawater temperatures
during El Niño, particularly the 1997 to 1998 event,
which was 1 of the 2 strongest of the last century
(Wolter & Timlin 1998). Surveys included 4 northern
sites where withering syndrome had not been ob-
served before the 1997 to 1998 El Niño event. We pre-
dicted that if El Niño triggered massive die-offs of
black abalone, then abalone at these sites should
decline simultaneously, as each site would experience
the same mass of warm water. Other spatial patterns of
decline would suggest the importance of alternative
factors. Because this study includes before and after
surveys of the abundance of black abalone at multiple
sites following one of the strongest El Niño events of
the last century, it provides the most rigorous test to
date of the hypothesis that elevated seawater tempera-
tures due to El Niño accelerate the decline of black
abalone.
MATERIALS AND METHODS
Black abalone were monitored at 7 sites along the
mainland coast of California, USA, from 1992 to 2001
(and also at 5 other sites, but only since 1999, therefore
data are not presented) (Fig. 1). Four sites (Govern-
ment Point, Boathouse, Stairs and Purisima Point) were
established in 1992 to 1993. Data collected from these
sites from 1992 to 1995 have been previously reported
in Altstatt et al. (1996). The other 3 sites (Cayucos
Point, Piedras Blancas and Point Sierra Nevada) were
established in 1996 to 1997 and are located north of
Diablo Cove, where the isolated outbreak of withering
syndrome was observed in 1988. By the end of 1995,
black abalone at the 2 most southern sites, Govern-
ment Point and Boathouse, had already undergone
massive die-offs due to withering syndrome, and this
disease had also been detected at Stairs (Altstatt et al.
1996).
Sites were initially located within the intertidal zone
on rocky shores where black abalone were abundant.
Three permanent plots were established at each site.
The sizes and shapes of plots varied within and among
sites depending on the occurrence of black abalone
and local topography. Consequently, the total area
sampled varied among sites and ranged from 30 m2at
Stairs to 123 m2at Government Point. Sites were sam-
pled in the early spring (usually February to March)
and late autumn (usually October to November) of
each year, and an additional sample was taken at some
sites in May 1995. Occasionally, we could not sample
at a particular site because of logistical difficulties or
storms. One plot at Government Point could not be
reliably sampled, so data from this plot were excluded.
Two plots were destroyed during storms (1 at Stairs in
spring 1998 and 1 at Piedras Blancas in spring 2000).
Therefore, an additional plot with similar abundances
of abalone to the one that had been destroyed was
added at each of these sites, and the abundance of
black abalone was subsequently counted in these new
plots and the 2 original plots that had not been dam-
aged.
At each sampling time, the permanent plots were
thoroughly searched (using a flashlight in crevices) for
black abalone. Black abalone in each plot were
counted, and their maximal lengths were measured to
the nearest 5 mm for those <40 mm and to the nearest
10 mm for those >40 mm, without removing them from
the substratum. The lengths of occasional individuals
lodged deeply in crevices had to be estimated by eye.
Evidence of withering syndrome at a site was collected
by observing abalone for clinical signs of the disease
and noting recent accumulations of abalone shells,
which would rule out declines due to poaching. The
abundance of black abalone at each site was estimated
as the total number of individuals found in all 3 plots.
To determine whether the decline of black abalone
was dependent on their size, individuals were placed
into 4 categories based on their maximal shell lengths:
(1) <50 mm or juveniles (see Leighton & Boolootian
1963); (2) 50 to 90 mm or small adults; (3) 91 to 126 mm
or large adults; and (4) >126 mm or harvestable adults,
although recreational (individuals >126 mm) and com-
mercial (individuals >145 mm) harvesting of black
abalone was banned throughout California in 1993.
Linear regression analyses of abalone number (trans-
145
Fig. 1. Location of monitoring sites along the coast of central
California, USA
Mar Ecol Prog Ser 242: 143–152, 2002
formed to their natural logarithms) versus time for
juveniles, small adults, large plus harvestable adults,
and all size categories together were used to assess
increases or decreases in the population abundance at
each site.
Sea surface temperatures were obtained from satel-
lite data (West Coast Regional Node, CoastWatch,
National Oceanic and Atmospheric Administration or
NOAA; http://coastwatch.noaa.gov). Data presented
are monthly means and anomalies relative to monthly
means of sea surface temperatures from January 1992
to April 2001 for the 7 sites across the region extending
from Government Point in the south to Point Sierra
Nevada in the north. Although these data may not
accurately reflect the absolute seawater temperatures
experienced by black abalone in the intertidal zone
(which are likely to be more extreme), they parallel
data collected from coastal buoys in the region
(National Data Buoy Center, National Weather Ser-
vice, NOAA; http://ndbc.noaa.gov), and provide a good
relative measure of seawater temperatures over time.
To determine whether declines of black abalone
were exclusively associated with El Niño events, a
paired t-test was used to compare percent changes in
the abundance of adult abalone (≥50 mm) for 2 yr peri-
ods either during or not during an El Niño event for
each of the 5 sites where this was possible (1992 to
1994 versus 1994 to 1996 for Boathouse, 1992 to 1994
versus1995 to 1997 for Stairs, 1995 to 1997 versus 1997
to 1999 for Purisima Point, and 1997 to 1999 versus
1999 to 2001 for Piedras Blancas and Point Sierra
Nevada). To compare the rates of decline of adult
abalone during El Niño and non-El Niño years, we
plotted ‘survivorship’ curves for the local population
at each site by considering the peak abundance of
abalone to be equal to the average number of indi-
viduals at a given site in the 2 yr prior to the onset of
decline. The onset of abalone decline at a given site
was assessed retrospectively by considering changes
in abalone number and the appearance of withering
syndrome. The onset of decline was judged to be
between spring and autumn 1992 for Government
Point, autumn 1994 and spring 1995 for Boathouse,
spring and autumn 1995 for Stairs, and spring and
autumn 1998 for Purisima Point and Cayucos Point.
There was a decline between spring and autumn 1992
at Boathouse, but this did not appear to be related to
withering syndrome and is likely a sampling artifact.
Although evidence of withering syndrome was not
apparent at Piedras Blancas and Point Sierra Nevada,
we decided to plot data for these sites because minor
declines were observed between spring and autumn
1998. To determine whether the rates of decline of
adult abalone were greater during El Niño events than
in non-El Niño years, an independent t-test was used
to compare the time it took for the abundance of adult
abalone to decline to 10% of its peak value (indicating
a mass mortality) for 2 sites where declines occurred
during El Niño events (Government Point and Puri-
sima Point) and 2 sites where die-offs occurred in non-
El Niño years (Boathouse and Stairs).
RESULTS
Dramatic declines in the abundance of black abalone
were observed at the 5 southernmost sites, but not at
the 2 northernmost sites (Fig. 2). For all sizes of abalone
combined, there were significant negative slopes at
the 5 southernmost sites, no detectable change in slope
at Piedras Blancas and a positive slope at Point Sierra
Nevada (Table 1). Numbers at impacted sites were
reduced by >90%, whereas abundances at Piedras
Blancas declined only slightly and those at Point Sierra
Nevada increased. Abalone showed clinical signs of
withering syndrome at all sites where mass mortalities
occurred, and accumulations of fresh shells were
observed during and after the declines. At sites with
massive die-offs, significant declines occurred in all
size categories (Fig. 2, Table 1). The only 2 exceptions
were at sites where few individuals were present in a
given size category (large and harvestable adults at
Cayucos Point, juveniles at Government Point); how-
ever, the trends were the same. At both Piedras Blan-
cas and Point Sierra Nevada, there was a significant
increase in the number of juveniles over time but not in
the larger size categories (Fig. 2, Table 1).
The progression of the onset of mass mortalities pro-
ceeded from south to north, without exception, but the
rates of northward spread were variable among years
(Figs. 1 & 2). Large die-offs of abalone were first ob-
served at the southernmost site, Government Point,
from 1992 to 1993. Declines at Boathouse, the next
most northerly site, were more gradual and started in
1995 following years of relatively stable abundances.
After a period of recruitment in the mid-1990s, abalone
numbers at Stairs decreased in 3 steps during the
spring and summer of 1995, 1996 and 1997. During this
time, the abundance of abalone at Purisima Point, less
than 5 km north of Stairs, remained constant. After the
onset of the 1997 to 1998 El Niño, however, abalone
numbers at Purisima Point and Cayucos Point, a site
10s of km to the north and near Diablo Cove, declined
precipitously. In contrast, abundances of adult abalone
at the 2 most northerly sites, Piedras Blancas and Point
Sierra Nevada, decreased only slightly at this time.
Overall abalone abundance at these 2 northern sites
subsequently increased due to recruitment in the late
1990s. In contrast, new recruits or juveniles were
rarely observed at sites that had experienced mass
146
Raimondi et al.: Effects of El Niño on withering syndrome in abalone
mortalities and, consequently, the local populations of
abalone have not recovered.
Periods of elevated sea surface temperatures (posi-
tive sea surface temperature anomalies) were associ-
ated with El Niño events (Fig. 3). Sea surface tempera-
tures were lowest during non-El Niño periods from
1994 to 1996 (a relatively neutral period) and 1999 to
2001 (a La Niña period), intermediate during the rela-
tively moderate and prolonged El Niño of 1991 to 1993,
which began in late 1991 and extended into 1993, and
were highest during the strong El Niño of 1997 to 1998.
Temperatures at the southernmost sites, Government
Point and Boathouse, were on average about 0.35°C
higher than those at Stairs and Purisima Point, which
were on average about 0.45°C higher than those at the
northernmost sites, Cayucos Point, Piedras Blancas
and Point Sierra Nevada. Average monthly sea surface
temperatures across all sites never exceeded 17°C in
non-El Niño years, but they remained above this level
for prolonged periods during El Niño events (Fig. 3).
During the 1991 to 1993 El Niño, temperatures at all
sites exceeded 17°C for several month in the late sum-
mer and autumn in 1992 and 1993, and they reached
18°C at the 2 southernmost sites. During the 1997
to 1998 El Niño, average temperatures attained 19°C
across all sites and more than 20°C at the southernmost
site. Importantly, temperatures remained above 18°C
for at least 4 mo during 1997 and did not drop below
14°C during the winter before peaking again in late
summer and early autumn 1998.
Adult abalone did not always decline during periods
of elevated sea surface temperatures due to El Niño.
For example, abalone numbers declined at Govern-
ment Point during the 1991 to 1993 El Niño, but they
147
Fig. 2. Haliothis cracherodii. Changes in number of black
abalone for each of 4 size classes (<50 mm or juveniles, 50 to 90
mm or small adults, 91 to 126 mm or large adults, and >126 mm
or harvestable adults) at 7 sites (arranged from south, Govern-
ment Point, to north, Point Sierra Nevada) from 1992 to 2001.
Note differences in scale of the y-axis. Sampling was done in
spring (S) and autumn (A) of each year, with an additional
sample in May (M) 1995; the asterisks indicate that sampling
was not done at that time. Shading indicates periods of elevated
seawater temperatures due to the El Niño events of 1991 to 1993
and 1997 to 1998. Data from Government Point, Boathouse,
Stairs and Purisima Point between spring 1992 and autumn
1995 have previously been reported in Altstatt et al. (1996)
Fig. 3. Changes in monthly means and anomalies relative to
monthly means of sea surface temperatures (SST, °C) from
January 1992 to April 2001. Shading indicates periods of ele-
vated seawater temperatures due to the El Niño events of
1991 to 1993 and 1997 to 1998
Mar Ecol Prog Ser 242: 143–152, 2002
increased at Stairs during this same interval (Fig. 2). In
addition, declines of black abalone were not exclu-
sively associated with periods of El Niño: percent
changes in the abundance of adult abalone did not dif-
fer significantly during El Niño events and non-El Niño
years (paired t-test: t= –0.33, p > 0.75, df = 4). Abalone
at Boathouse and Stairs declined during non-El Niño
years, whereas those at Government Point, Purisima
Point and Cayucos Point declined during El Niño
events (Fig. 2). The only consistent patterns were that
the abundance of adult abalone declined at all sites
during the 1997 to 1998 El Niño (although only slightly
at Piedras Blancas and Point Sierra Nevada), when
sea surface temperatures were highest, and did not
decline at any site during the 1999 to 2001 La Niña,
when sea surface temperatures were lowest (Figs. 2 & 3).
The rates of decline of adult abalone were also variable
among sites, but declines during El Niño events were
faster than those during non-El Niño years (Fig. 4).
Declines at Boathouse and Stairs, which occurred dur-
ing non-El Niño years in the mid-1990s, were slowest,
taking on average 27 mo for their abundances to be
reduced to below 25% of their peak levels (Fig. 4). The
rate of decline at Government Point during the 1991 to
1993 El Niño was intermediate, with levels dipping
25% below peak abundances in less than 19 mo, and
fastest at Purisima Point and Cayucos Point during the
1997 to 1998 El Niño, where abalone numbers were
reduced to about 25% of their peak abundances in less
than 12 mo (Fig. 4). Indeed, mass mortalities (i.e.
reductions to below 10% of peak abundance) occurred
significantly faster (independent t-test, t= 12.0, p < 0.01,
df = 2) during El Niño events (24 ± 1 mo, mean ± SE for
Government Point and Purisima Point) than during
non-El Niño years (41 ± 1 mo, mean ± SE for Boathouse
and Stairs).
DISCUSSION
Surveys reveal that mass mortalities of black aba-
lone due to withering syndrome are progressing north-
ward up the mainland coast of central California.
These results confirm the observations of Altstatt et al.
148
Table 1. Haliothis cracherodii. Results of linear regression analyses (model: ln[number + 1] = slope[time] + intercept) of changes
in numbers of black abalone in each of 4 size categories at 7 sites over time (time is measured in mo [Month 1], from January 1992
to March 2001 [Month 111]). t: t-statistic
Size category and site Intercept Slope r2tpn
All abalone
Government Point 2.88 –0.026 0.56 –4.4 <0.001 17
Boathouse 6.72 –0.035 0.86 –11.00<0.001 20
Stairs 6.91 –0.036 0.77 –7.7 <0.001 20
Purisima Point 7.57 –0.032 0.68 –5.5 <0.001 16
Cayucos Point 4.48 – 0.028 0.49 –2.8 c0.024 10
Piedras Blancas 5.24 –0.000 0.00 –0.1 <0.920 8
Point Sierra Nevada 4.29 –0.008 0.60 –3.7 <0.005 11
Large and harvestable adults (> 90 mm)
Government Point 2.45 –0.021 0.54 –4.2 <0.001 17
Boathouse 5.76 –0.035 0.82 –9.1 <0.001 20
Stairs 4.79 –0.025 0.55 –4.7 <0.001 20
Purisima Point 7.10 –0.036 0.74 –6.3 <0.001 16
Cayucos Point 2.24 – 0.012 0.13 –2.3 <0.306 10
Piedras Blancas 4.69 –0.004 0.04 –0.5 <0.639 8
Point Sierra Nevada 3.39 –0.006 0.18 –1.4 <0.200 11
Small adults (50 to 90 mm)
Government Point 1.84 –0.023 0.41 –3.2 <0.006 17
Boathouse 6.15 –0.036 0.89 –12.00<0.001 20
Stairs 6.69 –0.039 0.82 –9.1 <0.001 20
Purisima Point 6.48 –0.027 0.57 –4.3 <0.001 16
Cayucos Point 3.99 – 0.028 0.40 –2.3 <0.050 10
Piedras Blancas 4.74 –0.002 0.16 –1.1 <0.322 8
Point Sierra Nevada 4.02 –0.004 0.12 –1.1 <0.298 11
Juveniles (<50 mm)
Government Point 0.14 –0.002 0.13 –1.5 <0.162 17
Boathouse 3.40 –0.020 0.38 –3.3 <0.004 20
Stairs 4.25 –0.032 0.52 –4.4 <0.003 20
Purisima Point 4.27 –0.032 0.43 –3.2 <0.006 16
Cayucos Point 2.64 – 0.026 0.66 –3.9 <0.005 10
Piedras Blancas –0.540–0.033 0.58 –2.9 <0.029 8
Point Sierra Nevada –0.310–0.037 0.54 –3.2 <0.010 11
Raimondi et al.: Effects of El Niño on withering syndrome in abalone
(1996) that mortalities of black abalone were spread-
ing northward from Point Conception. Populations of
black abalone at Government Point, Boathouse and
Stairs, which had declined or were in decline by 1995
(Altstatt et al. 1996), continued to decline and have not
recovered. By 1998, abalone at 2 more northerly sites,
Purisima Point and Cayucos Point, were hit by massive
die-offs. Although these spatial patterns of decline
suggest that the disease is gradually moving north-
ward, the timing of the onset of declines was highly
variable. For example, progression of the mass mor-
talities between Boathouse and Stairs, which are sepa-
rated by more than 20 km, took about 1 yr (Altstatt et
al. 1996), whereas it took about 2 yr for mass mortali-
ties to be observed at Purisima Point, which is less than
5 km north of Stairs. Moreover, declines at Cayucos
Point, which is more than 50 km north of Stairs, were
coincidental with those at Purisima Point. These tem-
poral patterns of decline suggest that the incidence of
disease and the onset of mass mortalities may not be
simply due to the gradual northward progression of the
pathogen causing withering syndrome (Altstatt et al.
1996). Withering syndrome was observed at Govern-
ment Point and near Cayucos Point years before the
mass mortalities (Altstatt et al. 1996), and recent sur-
veys have shown that isolated cases of withering syn-
drome are present in black abalone at sites as far north
as the San Francisco area (Altstatt et al. 1996, Andree
et al. 2000, authors’ pers. obs.). It is possible that red
abalone Haliotis rufescens, which also exhibit clinical
signs of withering syndrome (Moore et al. 2000), from
commercial farms along the mainland coast of central
California, may transmit the disease to intertidal popu-
lations of black abalone, but whether this occurs is
unknown. Consequently, determining the pattern of
spread of the causative agent may be confounded by
anthropogenic influences. There does appear, how-
ever, to be a lag between the incidence of withering
syndrome in a local population of black abalone and its
subsequent demise due to the disease. The patterns of
mass mortality of black abalone still appear to follow
this south-to-north progression, suggesting that sea-
water temperature or some other factor related to lati-
tude may trigger the onset of declines.
Whether elevated sea surface temperatures due to El
Niño events are responsible for the onset of mass mor-
talities of black abalone remains equivocal. Numbers
declined at Government Point during the moderate
and prolonged 1991 to 1993 El Niño, but they in-
creased at Stairs. Moreover, mortalities were not
exclusively associated with El Niño years, as massive
die-offs of black abalone were observed at Boathouse
and Stairs in non-El Niño years during the mid-1990s.
During the strong 1997 to 1998 El Niño, we predicted
that if increased seawater temperatures triggered mas-
sive die-offs of black abalone, then abalone numbers at
all sites that had not yet experienced mass mortalities
should decline simultaneously, because each of these
sites would be influenced by the same mass of warm
water. The abundance of adult abalone did indeed
decline at all sites, but mass mortalities occurred only
at the 2 southernmost sites, Purisima Point and Cayu-
cos Point, and numbers at the 2 more northern sites,
Piedras Blancas and Point Sierra Nevada, decreased
only slightly. This difference might be because the
pathogen causing withering syndrome may have been
present at Purisima Point and Cayucos Point, but
absent from Piedras Blancas and Point Sierra Nevada.
Withering syndrome was observed at a site near Cayu-
cos Point in 1995, and Purisima Point is near Stairs,
which had already undergone massive die-offs due to
149
Fig. 4. Haliothis cracherodii. Declines in the numbers of adult
(≥50 mm) black abalone since the onset of the decline during
the 1991 to 1993 El Niño event (Government Point), non-El
Niño years (Boathouse, Stairs) and the 1997 to 1998 El Niño
event (Cayucos Point, Purisima Point, Point Sierra Nevada
and Piedras Blancas). Note that abundances at Point Sierra
Nevada 2 yr after the onset of decline were plotted as 100%
even though they exceeded the initial peak abundance
Mar Ecol Prog Ser 242: 143–152, 2002
withering syndrome. In contrast, there was no evi-
dence of diseased abalone at the 2 northernmost sites.
Therefore, elevated sea surface temperatures due to El
Niño may have triggered mass mortalities at the 2
southern sites because the pathogen was already pre-
sent or near threshold numbers in the local popula-
tions.
Although mass mortalities of black abalone do not
appear to depend on increased seawater temperatures
associated with El Niño, local populations of abalone
declined faster during El Niño events than during non-
El Niño periods, particularly the strong 1997 to 1998
El Niño. Sea surface temperatures during the 1997 to
1998 El Niño exceeded 18°C for 4 mo (also observed at
the southern sites during the 1991 to 1993 El Niño),
and temperatures may have been higher in the inter-
tidal region where black abalone live. Laboratory ex-
periments have shown that apparently healthy black
abalone exhibit substantially increased mortality when
subjected to temperatures of 18°C for 6 mo compared
to ambient seawater temperatures of 10 to 14°C (Stein-
beck et al. 1992). Additionally, elevated seawater tem-
peratures promoted the development of withering
syndrome in black abalone already exhibiting clinical
signs of the disease (Friedman et al. 1997, see also
Moore et al. 2000 for comparable results with Haliotis
rufescens). Further, Moore et al. (2000) reported that
commercial abalone farmers observe an increased
incidence of withering syndrome in red abalone H.
rufescens when seawater temperatures reach 18°C,
and during the 1997 to 1998 El Niño they reported
unusually high numbers of individuals with signs of
withering syndrome. In contrast, sea surface tempera-
tures hardly rose above 16°C during non-El Niño
years. Consequently, prolonged thermal stress in
combination with the presence of the pathogen may
promote the development of withering syndrome and
accelerate the massive die-offs of black abalone
(Lafferty & Kuris 1993).
The mechanisms by which black abalone acquire
withering syndrome and transmit the disease, and how
individual cases lead to widespread mortality of a local
population, are still uncertain and likely complex. The
pathogen causing withering syndrome may incubate
for many months before clinical signs are evident in
the field (Friedman et al. 1997, Andree et al. 2000),
making it difficult to assign causation. At the local
scale of a site, the prevalence and rate of transmission
of the disease, which may be directly communicable
among individuals (Gardner et al. 1995, Friedman et
al. 1997), likely increases as the pathogen reproduces
within infected individuals. Mass mortalities at a site
may then occur once the levels of bacteria reach a crit-
ical threshold within the local population. Stressors
such as elevated water temperatures during El Niño
may increase the prevalence of the pathogen, the sus-
ceptibility of abalone to infection, and the rate at which
bacteria reproduce within and are transmitted among
individuals at a site (Harvell et al. 1999). This study has
not, however, shown a causative link between ele-
vated seawater temperatures during El Niño and the
rate of decline of abalone. Mortality may indeed pro-
ceed indirectly through other stresses (e.g. starvation),
which may or may not be related to El Niño (Tissot
1990, 1995, Davis et al. 1992, Richards & Davis 1993). It
has been suggested that the removal of natural preda-
tors (e.g. sea otters) and a ban on the harvesting of
black abalone may have dramatically increased the
local densities of abalone, thus increasing intraspecific
competition and the opportunity for transmission of the
disease (Davis et al. 1992). Such stresses, coupled with
potential reductions in the availability of food and
increased seawater temperatures during El Niño, may
ultimately lead to the decline of local populations of
black abalone (Davis et al. 1992). Indeed, elevated sea-
water temperatures, such as those associated with El
Niño events, have been implicated in the demise of
several commercially and ecologically important spe-
cies of marine benthic invertebrates (e.g. Engle 1994,
Scheibling & Hennigar 1997, Eckert et al. 2000). Other
natural and anthropogenic stresses, particularly those
that elevate water temperatures (e.g. thermal dis-
charges, global warming), would also be expected to
accelerate the spread of withering syndrome and mass
mortalities throughout populations of black abalone
along the coast of California (Tissot 1995). With the
increase in the frequency and duration of El Niño
events in recent decades (Trenberth & Hoar 1996,
Fedorov & Philander 2000) and the escalation of
anthropogenic disturbance along the world’s coast-
lines, disease is expected to play an increasingly
important role in structuring ecological communities at
local and global scales (Harvell et al. 1999).
Black abalone play an important ecological role in
coastal communities and once formed an important
commercial and recreational fishery (Davis et al. 1992).
The prognosis for rapid, natural recovery of black
abalone populations along the southern and central
coasts of California is not good, and in 1999 Haliotis
cracherodii was listed as a candidate species for pro-
tection under the USA Endangered Species Act. With-
ering syndrome has already been observed in black
abalone at other sites along the central coast and
extending toward northern California (authors’ pers.
obs.) and, therefore, mass mortalities in these regions
are likely. The disease affects all size classes of indi-
viduals. Few healthy abalone remain at sites where
massive die-offs have occurred, and there has been
little successful recruitment subsequent to the declines
(Richards & Davis 1993, VanBlaricom et al. 1993, Tissot
150
Raimondi et al.: Effects of El Niño on withering syndrome in abalone
1995; see also Miller & Lawrenz-Miller 1993). The lack
of recruits may reflect unsuccessful spawning due to
low densities of adults (Breen & Adkins 1980), limited
larval dispersal (Prince et al. 1988, Hamm & Burton
2000), alteration of suitable habitat for recruitment as
space previously occupied by adult abalone is colo-
nized by other species (Miller & Lawrenz-Miller 1993,
Lafferty & Kuris 1993, Altstatt et al. 1996) or the con-
tinued but undetected presence of disease at these
sites. Similar to other species of abalone (Prince et
al. 1987, 1988, McShane 1992), recruitment of black
abalone appears to be patchy and extremely localized.
Indeed, pulses of recruitment at sites with relatively
stable populations (e.g. Stairs in the mid-1990s and
Point Sierra Nevada in the late 1990s) were not
observed at sites only 10s of km to the south, where
populations had undergone mass mortalities (e.g. Gov-
ernment Point in the mid-1990s and Purisima Point in
the late 1990s). Given these patterns of recruitment
and the northward progression of mass mortalities, it
appears that the replenishment of black abalone popu-
lations from natural recruitment will take decades, if
it occurs at all. Consequently, intervention, such as
laboratory culture, outplanting and establishment of
protected areas for reproductive adults (see Wallace
1998), may eventually be needed to prevent extinction
of black abalone.
Acknowledgements. We thank Jessie Altstatt, the MMS
MINT Team, and numerous assistants and volunteers for help
in the field. We are grateful to many people for granting
access to the study sites. These include Tim King and the
Bixby Ranch Corporation and Brad Lendberg and the Cojo-
Jalama Ranch (Government Point), the Vandenberg Air Force
Base, especially Nancy Read and the staff at the Recreation
Center (Boathouse, Stairs, and Purisima Point), the United
States Geological Survey (USGS) (Piedras Blancas) and the
Hearst Corporation (Point Sierra Nevada). This work was
funded by a Natural Sciences and Engineering Research
Council (NSERC) of Canada Postdoctoral Fellowship to
T.E.M. and awards to P.T.R. from the US Department of
Interior (Minerals Management Service), the UC Toxic
Substances Research and Teaching Program, the National
Science Foundation, and the Packard Foundation. This is
contribution number 89 from PISCO, the Partnership for
Interdisciplinary Studies of Coastal Oceans: A Long Term
Ecological Consortium funded by the David and Lucile
Packard Foundation.
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Editorial responsibility: Lisa Levin (Contributing Editor),
La Jolla, California, USA
Submitted: July 27, 2001; Accepted: April 5, 2002
Proofs received from author(s): October 8, 2002