Ecological Applications, 16(1), 2006, pp. 353–367
? 2006 by the Ecological Society of America
TRAJECTORIES OF ZOOPLANKTON RECOVERY IN THE LITTLE ROCK
LAKE WHOLE-LAKE ACIDIFICATION EXPERIMENT
THOMAS M. FROST,1,5JANET M. FISCHER,2,6JENNIFER L. KLUG,3SHELLEY E. ARNOTT,
4AND PAMELA K. MONTZ1
1Trout Lake Station, Center for Limnology, University of Wisconsin, 10810 County Highway N,
Boulder Junction, Wisconsin 54512 USA
2Department of Biology, Franklin and Marshall College, Lancaster, Pennsylvania 17604 USA
3Biology Department, Fairfield University, Fairfield, Connecticut 06824 USA
4Department of Biology, Queen’s University, Kingston, Ontario K7L 3N6 Canada
stressors such as acidification is an important challenge in ecology. Here we report on
zooplankton community recovery following the experimental acidification of Little Rock
Lake, Wisconsin, USA. One decade following cessation of acid additions to the northern
basin of Little Rock Lake (LRL), recovery of the zooplankton community was complete.
Approximately 40% of zooplankton species in the lake exhibited a recovery lag in which
biological recovery to reference basin levels was delayed by 1–6 yr after pH recovered to
the level at which the species originally responded. Delays in recovery such as those we
observed in LRL may be attributable to ‘‘biological resistance’’ wherein establishment of
viable populations of key acid-sensitive species following water quality improvements is
prevented by other components of the community that thrived during acidification. Indeed,
we observed that the recovery of species that thrived during acidification tended to precede
recovery of species that declined during acidification. In addition, correspondence analysis
indicated that the zooplankton community followed different pathways during acidification
and recovery, suggesting that there is substantial hysteresis in zooplankton recovery from
acidification. By providing an example of a relatively rapid recovery from short-term acid-
ification, zooplankton community recovery from experimental acidification in LRL gen-
erally reinforces the positive outlook for recovery reported for other acidified lakes.
Key words:acidification; biological resistance; pH stress; recovery; resilience; whole-lake ex-
Understanding the factors that affect biological recovery from environmental
Acidic deposition has been recognized as a major
environmental stress in aquatic ecosystems over the last
25 years (Stoddard et al. 1999, Driscoll et al. 2001).
Legislative actions to reduce rates of sulfur dioxide
emissions in North America and Europe were moti-
vated by concern about the ecological impacts of acidic
deposition, and consequently, sulfur dioxide emissions
were significantly reduced in the 1980s and 1990s
(Stoddard et al. 1999, Driscoll et al. 2001). Chemical
recovery has been reported for some North American
aquatic ecosystems that had been anthropogenically
acidified (Stoddard et al. 1999, Driscoll et al. 2003,
Keller et al. 2003). Improvements in water quality have
also been noted in other locations, including Scandi-
navia (Evans et al. 2001, Skjelkva ˚le et al. 2001, Forsius
Manuscript received 2 December 2004; revised 5 May 2005;
accepted 17 May 2005. Corresponding Editor: J. J. Elser.
5Published posthumously. This paper is dedicated to the
memory of Thomas M. Frost (1950–2000): scientist, mentor,
and friend. We remember our conversations with Tom about
Little Rock Lake’s ‘‘acid champs’’ and ‘‘acid chumps’’ with
6Corresponding author. E-mail: email@example.com
et al. 2003) and eastern Europe (Evans and Monteith
2001, Evans et al. 2001). However, it is important to
note that chemical recovery has not occurred in some
locations (e.g., the Adirondacks of North America,
Germany, and parts of southeastern Canada and the
United Kingdom) and is not expected in some impacted
systems unless further reductions in emissions are leg-
islated (Evans et al. 2001, Henriksen et al. 2002, Dris-
coll et al. 2003, Jeffries et al. 2003a, b, Keller et al.
Because biological recovery is a major goal of leg-
islative action, monitoring programs focused on aquatic
biota have been undertaken in a variety of locations
(Locke and Sprules 1994, Arnott et al. 2001, Walseng
et al. 2001, Keller et al. 2002, Nilssen and Waeervagen
2002, Findlay 2003, Holt and Yan 2003, Snucins 2003,
Vrba et al. 2003, Waeervagen and Nilssen 2003). These
high-quality long-term data sets are critical for ad-
dressing questions about the rate and trajectory of re-
covery (Parr et al. 2003). Several studies have sug-
gested that biological recovery may be delayed com-
pared to chemical recovery (Driscoll et al. 2001, Dixit
et al. 2002, Yan et al. 2003). Furthermore, the length
of the lag for biological recovery may vary substan-
THOMAS M. FROST ET AL.
Vol. 16, No. 1
tially among aquatic ecosystems. For example, Driscoll
et al. (2003) hypothesized that the lag between chem-
ical recovery and recovery of invertebrates in acidified
streams and lakes may range from three to 10 years.
Here, we report on variation in the recovery trajectories
of zooplankton following the experimental acidifica-
tion of Little Rock Lake (LRL), Wisconsin, USA.
Freshwater zooplankton are well-suited to investi-
gation of biological recovery from acidification be-
cause they are relatively easy to monitor and have been
studied in a variety of geographic locations that are
recovering from acidification (Keller and Yan 1998).
Although recovery can proceed rapidly in some lakes,
most studies indicate that zooplankton recovery re-
quires about a decade (Keller and Yan 1998). A wide
variety of metrics have been used to evaluate zooplank-
ton recovery from acidification, including univariate
measures of indicator species abundances, aggregate
measures of zooplankton species richness and diver-
sity, and multivariate metrics of community compo-
sition (Yan et al. 1996). Several studies indicate that
multivariate measures of community composition are
sensitive indicators of recovery (Yan et al. 1996, Holt
and Yan 2003). For example, a multivariate index of
zooplankton species composition provides evidence of
recovery in nine acidic lakes in Killarney Park, Ontario,
Canada, where pH had risen above 6, whereas zoo-
plankton species richness did not change during the
same time period (Holt and Yan 2003). These studies
underscore the value of quantifying changes in species
composition, in addition to coarser metrics of com-
Detailed analyses of recovery of zooplankton species
composition following water quality improvements
have potential to reveal variation in recovery rates for
different components of the zooplankton community in
a given lake. For example, Arnott et al.’s (2001) anal-
ysis of recovery of plankton in Swan Lake, Ontario,
Canada, supports the hypothesis that recovery rates dif-
fer between taxonomic groups (e.g., rotifers vs. crus-
taceans). The rate of recovery to pre-acidified condi-
tions may also be influenced by the nature of the initial
response to acidification (e.g., whether the species de-
clined or thrived under acidified conditions). During
the first five years of recovery of Little Rock Lake from
experimental acid addition, several species that had
increased during acidification returned to pre-acidified
levels whereas the recovery of some species that de-
clined during acidification was delayed (Frost et al.
1998). Thus, patterns of biological recovery can be
complex and mechanisms driving these patterns remain
The goal of our study was to summarize patterns of
zooplankton recovery following a whole-lake acidifi-
cation experiment conducted in Little Rock Lake, Wis-
consin. Because the choice of metric may affect our
perception of recovery, we compared recovery trajec-
tories for highly aggregated community metrics (e.g.,
total zooplankton biomass) and population level met-
rics (e.g., biomass of individual species). We also fo-
cused on the role of biological factors that may affect
recovery. For example, we compared recovery trajec-
tories for species that were negatively affected by acid-
ification (‘‘acid chumps’’) and species that thrived un-
der acidic conditions (‘‘acid champs’’). Our study rep-
resents an interesting comparison to other recent stud-
ies examining zooplankton recovery from acid rain
(Arnott et al. 2001, Holt and Yan 2003). The design of
the Little Rock Lake experiment included pre-acidifi-
cation data and parallel monitoring of a closely
matched reference system. These features are typically
lacking in studies of anthropogenic acidification due to
historical and/or logistic reasons. Overall, we believe
that the ability to follow zooplankton community tra-
jectories in Little Rock Lake for 16 years, including a
full cycle of response and recovery (see Mittelbach et
al. 1995), provided a unique opportunity to gain in-
sights about ecological resilience to acidification.
In 1984, the two basins of Little Rock Lake, a bilobed
seepage lake located in northern Wisconsin, USA, were
separated using a vinyl curtain. Following a year of
baseline data collection, sulfuric acid was added to the
northern basin (hereafter, acidified basin). The pH of
the acidified basin was decreased sequentially to three
target pH levels each maintained for two years: 5.6
(1985–1986), 5.1 (1987–1988), and 4.7 (1989–1990).
The recovery phase began in 1991 when all acid ad-
ditions ceased and the acidified basin was allowed to
recover naturally. Data collection was completed in
2000. Throughout the entire period (1984–2000), the
southern basin (hereafter, reference basin) was unma-
nipulated and served as a reference system for the
changes that occurred in the acidified basin.
Details of the limnological sampling are summarized
here and described in detail elsewhere (Frost and Montz
1988, Brezonik et al. 1993, 2003). From 1984 to 2000,
water samples for chemical analysis were collected
from a central station in each basin once every two
weeks during the ice-free season and approximately
monthly during winter. Here we present only the pH
data, as changes in chemistry during acidification and
recovery have been described elsewhere (Brezonik et
al. 1993, 2003, Frost et al. 1999, Sampson and Brezonik
Samples for enumeration of zooplankton were col-
lected with a 33-L Schindler-Patalas trap (53-?m mesh)
at the frequency described above for chemical samples.
Samples were collected from fixed depths (0, 4, and 8
m in the acidified basin and 0, 4, and 6 m in the ref-
erence basin) and preserved with 4% sucrose-buffered
ZOOPLANKTON RECOVERY FROM ACIDIFICATION
formalin. With the exception of the surface sample, the
middle of the trap was positioned at the target depth.
Hypsometrically weighted mean abundances were cal-
culated for each basin. Zooplankton abundance was
converted to biomass using length–mass relationships
determined directly for Little Rock Lake species or
from the literature (Ruttner-Kolisko 1977, Pace and
Orcutt 1981, Culver et al. 1985, Yan and Mackie 1987).
Copepod nauplii were not identified to species but are
included in analyses of total zooplankton biomass, co-
pepod biomass, and the multivariate analyses of chang-
es in community composition. Additional details on
zooplankton analyses are provided in Frost and Montz
Samples for enumeration of large predatory zoo-
plankton (Chaoborus punctipennis, water mites, Ep-
ischura lacustris, and Leptodora kindtii) were collected
with a 50 cm diameter, 253-?m mesh conical plankton
net at a fixed sampling station after dark. Tows were
collected approximately once every two weeks during
the ice-free season from 0.5 m above the deepest point
of the basin to the surface, except in 1995 when sam-
ples were not collected. Samples were preserved with
Lugol’s iodine. We used unpublished dry masses of
Chaoborus punctipennis (Fischer 1994) to transform
abundance to biomass. Biomass estimates for water
mites, Epischura lacustris, and Leptodora kindtii were
calculated using published values (Meyer 1989, Law-
rence et al. 1987, and Hawkins and Evans 1979, re-
spectively). Additional details on predatory zooplank-
ton sampling are provided in Sierszen and Frost (1993).
We evaluated zooplankton community recovery from
acidification using a variety of metrics ranging from
population level (e.g., biomass of an individual zoo-
plankton species) to taxonomic groups (e.g., rotifer bio-
mass) to highly aggregated community level (e.g., total
zooplankton biomass). For each metric, we compared
the time series of annual mean values in the acidified
basin to the long-term mean and variability for the same
metric (i.e., annual means) in the reference basin. Fol-
lowing the approach of Arnott et al. (2001), we used
the 10th and 90th percentiles for each metric across all
years (1984–2000) to represent variability in the ref-
erence basin. We concluded that a species or group of
species in the acidified basin responded to acidification
if its annual mean biomass was above or below the
range of variability in the reference basin during the
acidification years. In a few cases in which a species
was slightly outside the range for only one year early
in the acidification and returned to within the range for
several years (e.g., Bosminids in 1986), we did not
classify this species as responding to acidification dur-
ing the first excursion from the reference basin range.
We concluded that a species or group of species had
recovered from acidification once its annual mean bio-
mass was consistently within the range of variability
defined by the 10th and 90th percentiles of the reference
basin data. In the cases of Daphnia parvula and Tro-
pocyclops extensus, we concluded that recovery oc-
curred in 1997 despite subsequent departures from the
10th and 90th percentiles of the reference basin data
because similar dynamics were noted in the reference
basin. We recognize that this is a subjective approach
guided by statistical principle and intuition, but suggest
that it is a good way to assess general patterns in com-
plex long-term data sets like ours. We also compared
the timing of chemical and biological recovery for each
taxon. Recovery lag was defined as the time delay be-
tween chemical recovery (based on return to the mean
annual pH value in the year before the species respond-
ed to acidification) and biomass recovery of each spe-
To compare trajectories of change in community
composition in the acidified basin to community com-
position in the reference basin, we used correspondence
analysis (CA). Correspondence analysis is an ordina-
tion method widely used by community ecologists to
examine differences in species composition across en-
vironmental gradients (Jackson 1993, Gotelli and El-
lison 2004). We log10(x ? 1)-transformed the biomass
data, excluded rare species (?5% of biomass of their
taxonomic group) from the analysis, and calculated CA
using SAS (SAS Institute 1996). Large predatory zoo-
plankton (Chaoborus punctipennis, water mites, Ep-
ischura lacustris, and Leptodora kindtii) were not in-
cluded in the analysis due to one year of missing data.
We examined correlations between CA axis scores and
pH, secchi depth, and chlorophyll to explore relation-
ships between environmental factors and changes in
zooplankton community composition. It is important
to note that these analyses were constrained by the data
available and all possible environmental drivers were
During the pre-manipulation year (1984), pH values
in the two basins of Little Rock Lake were very similar
(Fig. 1a). Sulfuric acid was added to the acidified basin
from 1985 to 1990, causing a stepwise decrease in pH.
Beginning in 1991, pH in the acidified basin was al-
lowed to recover. pH gradually rose until reaching pre-
manipulation levels in 1996 (Fig. 1). pH in the refer-
ence basin was variable over the 17-yr record but
showed no obvious directional trends (Fig. 1a). Com-
paring mean annual pH to the range of natural vari-
ability in pH in the reference basin provided a consis-
tent interpretation of recovery. Mean annual pH in the
acidified basin decreased below the range of variability
in the reference basin during the first year of acidifi-
cation (1985) and returned within the range of vari-
ability in the reference basin in 1996 (Fig. 1b).
THOMAS M. FROST ET AL.
Vol. 16, No. 1
(REF) and treatment (TRT) basins of Little Rock Lake, Wisconsin, USA, from 1984 to 2000. Horizontal solid lines in (b)
indicate 10th and 90th percentiles in the reference basin for 1984–2000.
(a) Time series of pH values (samples were taken once every two weeks) and (b) annual mean pH in the reference
Response and recovery of aggregate groups
Despite a large decrease in pH, total zooplankton
biomass in the acidified basin stayed within the range
of variability in the reference basin until the final year
of acidification (Fig. 2a). Total zooplankton biomass
was lower in 1990 but recovered in 1991. During the
rest of the recovery period, total zooplankton biomass
was variable but generally stayed within the bounds of
the reference envelope (Fig. 2a). Although total rotifer
biomass increased during the later stages of acidifi-
cation, it did not increase above the reference basin
envelope until the second year of recovery (1992) and
returned to the range of reference basin variability in
1993 (Fig. 2b). Total cladoceran biomass responded to
acidification by increasing above the range of vari-
ability in the reference basin during the first year of
acidification (1985) and decreased to within the ref-
erence envelope early in the recovery period (1993)
(Fig. 2c). In contrast, total copepod biomass was rel-
atively insensitive to acidification (Fig. 2d). Total co-
pepod biomass stayed within the range of variability
in the reference basin until the final year of acidification
(1990) and recovered the following year (1991). Co-
pepods dominated the total zooplankton biomass
throughout the experiment (Fig. 2a, d).
Response and recovery in species composition
To assess changes in zooplankton species composi-
tion, we used correspondence analysis to compare the
community trajectory in the acidified basin to inter-
annual variation (i.e., the cloud of points) in the ref-
erence basin. When all species (except large predatory
zooplankton) were included in the analysis, dramatic
changes in the acidified basin zooplankton assemblage
were noted as early as 1986 when the community began
to move to the right along CA axis 1 (Fig. 3a, b). The
acidified basin community changed to a more acido-
philic composition during 1987–1991. However, a re-
covery trajectory began soon after acidification ended.
By 1994–1995, community composition in the acidi-
fied basin was similar to the reference basin. In 1996,
community composition had essentially returned to an
assemblage characteristic of the reference basin. Cor-
respondence analysis axis 1 was negatively correlated
with pH (n ? 34, r ? ?0.77, P ? 0.0001), whereas
CA axis 2 was negatively correlated with chlorophyll
(n ? 34, r ? ?0.40, P ? 0.02). It is interesting to note
that significant changes occurred in the reference basin
during the study period. The reference basin points with
the lowest scores on CA axis 2 correspond to 1996 and
1998–2000. The first two CA axes captured roughly
ZOOPLANKTON RECOVERY FROM ACIDIFICATION
(REF) and treatment (TRT) basins of Little Rock Lake. Horizontal solid lines indicate 10th and 90th percentiles in the
reference basin for 1984–2000.
Annual mean total biomass of (a) zooplankton, (b) rotifers, (c) cladocerans, and (d) copepods in the reference
57% of the variance (38.61 and 17.98 for axes 1 and
When only the rotifers were included in the CA, clear
changes in the acidified basin assemblage were noted
by 1987, the first year of the second stage of acidifi-
cation (Fig. 3c, d). Specifically, the acidified basin as-
semblage moved to the right on CA axis 1 towards a
composition characterized by Gastropus hyptopus,
Keratella taurocephala, and Synchaeta. Correspon-
dence analysis axis 1 was negatively correlated with
pH (n ? 34, r ? ?0.78, P ? 0.0001). During the
recovery period, rotifer community composition in the
acidified basin returned to the cloud of reference basin
points by 1994. The first two CA axes for the rotifer
community captured roughly 54% of the variance
(36.39 and 17.17 for axes 1 and 2, respectively).
The CA for cladocerans revealed substantial varia-
tion in the reference basin assemblage during the study
period across the first CA axis (Fig. 3e, f). It is im-
portant to note, however, that this pattern does not re-
flect simple directional change (e.g., from right to left)
in the reference basin assemblage. Instead, the trajec-
tory in the reference basin was more random. For ex-
ample, the five reference basin points with negative
scores on the first CA axis correspond to 1991, 1994,
and 1998–2000. Despite the variation in the reference
basin cladoceran assemblage, the acidified basin as-
semblage exhibited a clear response to acidification in
1986, reflecting a decrease in Daphnia dubia, Holo-
pedium gibberum, and Diaphanosoma and an increase
in Daphnia catawba. By 1991, however, the acidified
basin assemblage recovered to the broad region defined
by the reference basin points. CA axis 1 was positively
correlated with secchi depth (n ? 34, r ? ?0.41, P ?
0.02) and negatively correlated with chlorophyll (n ?
34, r ? ?0.35, P ? 0.04), whereas CA axis 2 was
negatively correlated with pH (n ? 34, r ? ?0.49, P
? 0.003). The first two CA axes for the cladoceran
community captured roughly 86% of the variance
(58.09 and 28.23 for axes 1 and 2, respectively).
Similar to cladocerans, the CA for copepods reveals
substantial variation in the reference basin assemblage
that complicates the interpretation of response and re-
covery in the acidified basin assemblage (Fig. 3g, h).
THOMAS M. FROST ET AL.
Vol. 16, No. 1
rotifers, cladocerans, and copepods. Panels in the left columns (a, c, e, g) present the trajectory of years in the reference
(REF) and acidified (TRT) basins. Panels on the right (b, d, f, h) show the taxa scores from the ordination of species. Taxa
abbreviations are spelled out in Table 1.
Scatterplots of the first two axes of the correpondence analysis (CA) for the entire zooplankton community,
Reference basin points that fall outside of the main
cloud of points correspond to 1995, 1996, and 1998–
2000. Nonetheless, we interpret the departure of the
acidified basin assemblage along the first CA axis from
the reference basin cloud beginning in 1988 as a re-
sponse to acidification. Correspondence analysis axis
1 was negatively correlated with pH (n ? 34, r ?
?0.62, P ? 0.0001). Movement to the right along CA
axis 1 represents an increase in Tropocyclops extensus
and a decrease in all other copepod species. A recovery
trajectory is evident beginning in 1991 and complete
by 1997. The first two CA axes for the copepod com-
munity captured roughly 85% of the variance (63.50
and 21.46 for axes 1 and 2, respectively).
Response and recovery of individual taxa
Almost all rotifer and crustacean taxa in the acidified
basin decreased or increased outside the range of bio-
mass recorded in the reference basin during the acidi-
fication period or during the first two years of the re-
covery period when pH was still low (Table 1, Figs. 4–
6). All three of the species that did not respond during
acidification or early recovery were rotifers (Table 1).
Only two species, Asplanchna and Daphnia catawba,
responded to the first phase of acidification. Asplan-
chna decreased in the acidified basin, whereas Daphnia
catawba increased. Six species responded to the second
phase of acidification, including four species that de-
creased and two species that increased. During the third
phase of the acidification, five species decreased and
five species increased. One species (Keratella crassa)
decreased during the last phase of the acidification but
increased dramatically during recovery. Of the 19 ro-
tifer and crustacean taxa that responded during the
acidification period, 84% had recovered by 1996 when
pH in the acidified basin returned to pre-acidification
levels. Interestingly, two taxa that had not responded
during the acidification phase of the experiment (bos-
minids and Gastropus hyptopus) increased sharply dur-
ing the early phases of recovery (1991–1992) and then
quickly returned to the range of the reference basin for
the duration of the recovery period (Figs. 4, 5).
ZOOPLANKTON RECOVERY FROM ACIDIFICATION
FIG. 3. Continued.
The two dominant invertebrate predators in Little
Rock Lake responded differently to acidification (Fig.
7). Water mites were adversely affected by acidifica-
tion, exhibiting very low abundances during 1989–
1993 (Fig. 7a). We interpret the higher abundances of
water mites in 1994 and later years as evidence of
recovery. In contrast, the phantom midge, Chaoborus
punctipennis, increased with acidification and first de-
parted from the reference basin envelope in 1988 (Fig.
7b). At this time, we noted a decline in total zooplank-
ton biomass (Fig. 2a). However, biomass of Chaoborus
decreased to values within the range of variability ob-
served in the reference basin by 1992 (Fig. 7b). Both
taxa had high variability in the reference basin through-
out the study period.
During the acidification period, nine species were
favored by acidification and increased in abundance
(‘‘acid champs’’) and 11 species declined (‘‘acid
chumps’’) (Table 1). This count does not include two
species that increased during the recovery phase. In
addition, one species (Keratella crassa) decreased in
abundance during acidification but increased dramati-
cally during recovery. Due to the complexity of this
response, we were unable to classify Keratella crassa
as an acid champ or acid chump. In the early part of
the recovery phase, acid champs tended to recover
more rapidly than acid chumps (Fig. 8a). Recovery of
both acid champs and acid chumps was complete by
1997. In general, species recovered at a pH that was
higher than the pH to which they responded during the
acidification period (Fig. 8b). Only three species re-
covered at pH levels that were lower than the level at
which they responded.
Of the 20 species that responded during the acidi-
fication period, eight (40%) had a lag in recovery (Table
1). In these cases, there was a time delay between chem-
ical recovery (defined for each species based on pH
levels in the year before the species responded to acid-
ification) and biological recovery. In this group of spe-
cies with lagged recovery, four were acid champs and
four were acid chumps. Recovery lags varied from 1
to 6 yr. Mean lag time varied across taxonomic groups.
Mean lag times for rotifers, cladocerans, and copepods
were 0.78, 1, and 3.25 yr, respectively. The two in-
vertebrate predators, mites and Chaoborus punctipen-
nis, exhibited lags of 2 and 0 yr, respectively.
THOMAS M. FROST ET AL.
Vol. 16, No. 1
Graphs are grouped by the nature of the response to acidification, with decreasing species first, increasing species second,
and species with more complex responses or no response last. Horizontal solid lines indicate 10th and 90th percentiles in
the reference basin for 1984–2000.
Annual mean biomass of rotifer species in the reference (REF) and treatment (TRT) basins of Little Rock Lake.
One decade following cessation of acid additions in
Little Rock Lake, recovery of the zooplankton com-
munity was essentially complete. As others have re-
ported for other lakes, biological recovery in LRL gen-
erally lagged behind chemical recovery (Arnott et al.
2001, Jeffries et al. 2003b, Skjelkva ˚le et al. 2003). In
LRL, recovery of chemical parameters including major
ions (Sampson 1999), minor metals (Brezonik et al.
2003), and nutrients (Sampson and Brezonik 2003)
generally paralleled changes in pH. In contrast, ap-
proximately 40% of zooplankton species exhibited a
recovery lag (Table 1). In these cases, the pH had re-
turned to a level higher than the pH level at which the
original response to acidification had occurred, but bi-
ological recovery was delayed. Compared to most spe-
cies with relatively short recovery lags, the ?4-yr de-
lays in recovery of Leptodiaptomus minutus, Tropo-
cyclops extensus, and Daphnia parvula were especially
long. Nonetheless, even these recovery lags were rel-
atively short in comparison to the longer lags observed
in anthropogenically acidified lakes where recovery
can be delayed for decades (Yan et al. 1996, Arnott et
al. 2001). The relatively short recovery lags in LRL
may be related to the experimental acidification pro-
cedure wherein pH was maintained at 4.7 for only 2
ZOOPLANKTON RECOVERY FROM ACIDIFICATION
FIG. 4. Continued.
yr. Although some species decreased dramatically in
LRL when conditions were most acidic, abundances
were typically above the detection limit. It is logical
that recovery from low abundance may proceed more
rapidly than recovery from complete extirpation events
such as those reported for anthropogenically acidified
lakes. Vinebrook et al. (2003) report a similar result
for epilithic algal assemblages in boreal lakes. Specif-
ically, recovery of algal assemblages from a relatively
short experimental acidification was more rapid than
recovery from regional atmospheric acidification.
Determination of biological recovery depends to a
large extent on the specific metric of community re-
sponse chosen by the investigator in a particular study.
In general, we observed that highly aggregated com-
munity metrics (e.g., total zooplankton biomass) were
less sensitive indicators of response and recovery from
acidification than metrics that incorporated the identity
of individual species (e.g., multivariate community
analyses and biomass of individual species). For total
zooplankton, rotifers, and copepods, aggregate biomass
in the acidified basin deviated from the reference basin
range for only 1–2 yr whereas the multivariate analyses
for these groups suggested that the acidified basin com-
munities departed from the range of variability in the
reference basin for 7–9 yr. This pattern was not ob-
served for cladocerans, however, in which aggregate
biomass was more sensitive than community compo-
THOMAS M. FROST ET AL.
Vol. 16, No. 1
basins of Little Rock Lake. Graphs are grouped by the nature of the response to acidification, with decreasing species first
and increasing species second. Horizontal solid lines indicate 10th and 90th percentiles in the reference basin for 1984–
Annual mean biomass of (a–e) cladoceran species and (f) bosminids in the reference (REF) and treatment (TRT)
sition. Cladoceran biomass in the acidified basin was
out of the reference basin range for 8 yr whereas the
CA for community composition indicated significant
species shifts in the acidified basin for only 5 yr (Figs.
2 and 3). Overall, we agree with Yan et al. (1996) that
multivariate metrics that represent species abundances
are most appropriate for analysis of recovery from per-
turbation. Important shifts in species composition can
be masked in more aggregate variables like total zoo-
plankton biomass due to processes such as compen-
satory dynamics (Frost et al. 1995, Fischer et al. 2001).
Furthermore, many definitions of biological recovery
emphasize the return of particular indicator species to
the ecosystem (Gunn and Sandøy 2003).
Previous studies suggest that the rate of recovery
can also vary substantially among taxonomic groups.
For example, in Swan Lake, Ontario, recovery of the
rotifer community proceeded quickly compared to
crustacean recovery (Arnott et al. 2001). Examination
of the CA for rotifers, cladocerans, and copepods re-
veals a different pattern in LRL. Cladoceran commu-
nity composition appeared to have recovered in 1991
shortly after acid addition ended, whereas rotifer re-
covery was delayed until 1994. Of the three taxonomic
groups, copepod recovery proceeded most slowly and
was delayed until 1997. Slow recovery of copepods
was also reflected in the notably long mean recovery
lags (3.25 yr) compared to rotifers and cladocerans
(0.78 and 1 yr, respectively). Differences in rates of
recovery among taxonomic groups were probably not
attributable to a lack of colonists as all of these groups
produce resting stages that provide a source of internal
colonists from the lake sediments (Hairston 1996). Fur-
thermore, the relatively short duration of the most acid-
ic conditions in LRL was probably not long enough to
result in depletion of the egg bank. It is possible that
ZOOPLANKTON RECOVERY FROM ACIDIFICATION
Graphs are grouped by the nature of the response to acidification with decreasing species first and increasing species second.
Horizontal solid lines indicate 10th and 90th percentiles in the reference basin for 1984–2000.
Annual mean biomass of copepod species in the reference (REF) and treatment (TRT) basins of Little Rock Lake.
the long lag in recovery for copepods in LRL may have
been related to their relatively long generation times,
which are generally on the order of 2–3 wk or more in
north temperate lakes (Williamson and Reid 2001).
These long generation times may slow the rate of pop-
ulation responses to changes in environmental condi-
tions for some species. For example, beginning in 1991,
we observed a slow increase in biomass of Mesocyclops
edax but this species did not fully recover to reference
basin levels until the following year.
Others have proposed that delays in recovery such
as those we observed in LRL may be attributable to
‘‘biological resistance’’ wherein establishment of via-
ble populations of key acid-sensitive species following
water quality improvements is prevented by other com-
ponents of the community that thrived during acidifi-
cation (Yan et al. 2003). For example, dense popula-
tions of invertebrate predators such as Chaoborus in
fishless acidic lakes may impede recovery of some
crustaceans (Holt and Yan 2003, Yan et al. 2003). It is
unlikely that this invertebrate predator played a major
role in LRL because Chaoborus abundance had de-
clined to reference basin levels by 1992. However, our
analysis of the timing of recovery of acid chumps and
acid champs does support the biological resistance hy-
pothesis. We observed that the recovery rate for acid
champs was faster than acid chumps (Fig. 8). Indeed,
greater than 65% of all species in the acid champ cat-
egory had declined to reference basin levels by 1993,
whereas only about 35% of species in the acid chump
group had recovered by this time. Recovery of more
than 75% of acid champs was observed in 1996, and
full recovery of acid champs and chumps followed in
1997. This pattern may reflect biological resistance
wherein some key strong interactors in the acid champ
category limited population growth of acid chumps
through interactions such as competition or predation.
The multivariate analyses of community responses
provided a second line of evidence suggesting that bi-
ological resistance may play an important role in zoo-
plankton recovery from acidification. The recoverypat-
tern in the CA plots indicates that there was substantial
THOMAS M. FROST ET AL.
Vol. 16, No. 1
(TRT) basins of Little Rock Lake. Horizontal solid lines indicate 10th and 90th percentiles in the reference basin for 1984–
2000. Large predatory invertebrates were not sampled in 1995.
Annual mean biomass of (a) water mites and (b) Chaoborus punctipennis in the reference (REF) and treatment
hysteresis in the recovery trajectory of zooplankton in
LRL. Hysteresis is a term borrowed from physics in-
dicating that a system does not simply retrace its path
as driving variables change (Gutschick and BassiriRad
2003, Scheffer et al. 2004) and has been reported pre-
viously for algal responses to acidification (Vinebrooke
et al. 2003). We observed hysteresis in zooplankton
recovery from acidification in LRL because the com-
munity did not follow the same path during acidifi-
cation and recovery (Fig. 3). This pattern was espe-
cially notable in the CAs for all species, rotifers, and
copepods indicating that community composition trav-
eled through novel configurations during recovery. We
believe that this pattern may be indicative of biological
resistance to recovery. For example, although species
such as Daphnia parvula and Keratella crassa were
not dominant species prior to or during acidification,
they became prevalent during recovery. Recovery of
some acid chumps (e.g., Daphnia dubia and Keratella
cochlearis) may have been delayed by interactions with
these potential competitors.
The biological resistance hypothesis suggests that
processes governing community dynamics during re-
covery differ from processes that drive responses to
acidification. For example, previous analyses of species
interactions in LRL during acidification suggest that
acid chumps are acid-sensitive, superior competitors
that can suppress acid champs as long as pH is high
(Fischer et al. 2001). Accordingly, one would expect
that acid chumps would increase quickly following
chemical recovery and subsequently cause a decline in
acid champs. However, acid champs appeared to de-
cline before acid chumps increased (Fig. 8a). It is pos-
sible that the early recovery of one or two key species
in the acid chump category (e.g., Asplanchna or Me-
socyclops edax) could cause dramatic declines in sev-
eral acid champs that interact with these predators. It
is also possible that small increases in acid chumps that
fall short of complete recovery as we have defined it
may nonetheless be sufficient to initiate decreases in
some acid champs. Alternatively, our observation that
declines in acid champs generally preceded increases
in acid chumps may reflect shifts in competitive hi-
erarchies during pH recovery as environmental con-
ditions and relative abundances of chumps and champs
change. For example, the outcome of competition may
depend on the level of stress for acid chumps while pH
is increasing. Unfortunately, it is impossible to identify
mechanisms driving recovery dynamics without addi-
tional experiments that test the role of each recovering
Overall, zooplankton community recovery from ex-
perimental acidification in LRL generally reinforcesthe
positive outlook for recovery reported for other acid-
ified lakes (Arnott et al. 2001, Holt and Yan 2003).
The LRL example differs from these previous studies
of anthropogenically acidified lakes in several impor-
tant ways. Increases in metals with acidification are a
common feature in anthropogenically acidified lakes
(LaZerte 1986) but were less dramatic in LRL (Bre-
zonik et al. 2003). Lower concentrations of metals in
LRL might have contributed to its rapid recovery from
matched reference systems have often been lacking for
logistical and/or historical reasons in other studies. In
LRL, we had the luxury of one year of pre-acidification
data and parallel monitoring of the reference and acid-
ified basins. We were somewhat surprised by the var-
ZOOPLANKTON RECOVERY FROM ACIDIFICATION
Lake, Wisconsin, USA, first left the region, defined by 10th and 90th percentiles of the reference basin, as well as the pH
and year when the response variable recovered.
For each response variable, the pH and year when the response variable in the acidified basin of Little Rock
Response RecoveryRecovery lag
Keratella cochlearis (Keraco)
Trichocerca cylindrical (Tric)
Gastropus stylifer (Gasts)
Keratella taurocephala (Kerat)
Polyarthra remata (Polyr)
Polyarthra vulgaris (Polyv)
Gastropus hyptopus (Gasth)
Keratella crassa (Keracr)
Kellicottia longispina (Kell)
Keratella hiemalis (Kerah)
Daphnia dubia (Daphd)
Holopedium gibberum (Holo)
Diaphanosoma birgei (Diap)
Daphnia catawba (Daphc)
Daphnia parvula (Daphp)
Diacyclops thomasi (Diac)
Leptodiaptomus minutus (Lept)
Mesocyclops edax (Meso)
Tropocyclops extensus (Trop)
Large predatory invertebrates
Notes: A subjective approach guided by statistical principle and intuition was used to judge recovery. Specifically, we
concluded that a species had recovered from acidification once its annual mean biomass was consistently within the range
of variability defined by the 10th and 90th percentiles of the reference basin data (see Methods: Data analysis for additional
details). Species that never left the reference region are labeled NR. Lag was defined as the time delay between chemical
recovery (based on return to the mean annual pH value in the year before the species responded to acidification) and biomass
recovery of each taxon. Species that did not respond during the acidification phase (1985–1990) are denoted NA. Direction
of change refers to whether the taxa increased (I) or decreased (D). Irindicates that the taxon increased early in the recovery
period. Codes in parentheses after species names are used to denote species in Fig. 3.
† Note that Daphnia catawba increased above the 90th percentile for the reference basin in 1997–2000.
iability of the reference basin during our study period.
In many ways, the reference basin was a moving target
and some changes in community composition in the
reference basin were nearly as dramatic as the species
shifts in the treatment basin (see Fig. 3e). The vari-
ability in the reference system broadened the recovery
target in LRL and provides a reminder that recovery
cannot always be defined as an exact reconstruction of
While the recovery of zooplankton in LRL and other
lakes paints a hopeful picture for recovery from acid-
ification, it is important to point out that recovery has
been delayed for decades or indefinitely in other sys-
tems (Yan et al. 1996, Arnott et al. 2001). Other authors
have attributed differences in recovery rates to duration
and severity of acidification and suggest that systems
subjected to severe damage for extended time periods
may have limited capacity for recovery (Yan et al.
1996). We believe that the recovery of zooplankton in
LRL underscores this point by providing an example
of rapid recovery from a relatively mild and short acid-
ification experiment. Overall, there appears to be a fa-
vorable outlook for ecological recovery from pertur-
bations such as acidification when remediation policies
THOMAS M. FROST ET AL.
Vol. 16, No. 1
covered in each year of the recovery phase. (b) Relationship
between the pH at which a species responded during the acid-
ification period and the pH at which it recovered. Pointsabove
the 1:1 line indicate species that recovered at higher pH than
they responded to during the acidification phase. We used a
subjective approach guided by statistical principle and intu-
ition to judge recovery. Specifically, we concluded that a
species had recovered from acidification once its annual mean
biomass was consistently within the range of variability de-
fined by the 10th and 90th percentiles of the reference basin
data (see Methods: Data analysis for additional details on our
approach). ‘‘Acid champs’’ are species that were favored by
acidification and increased, whereas species in the ‘‘acid
chumps’’ category declined during the acidification phase of
(a) Cumulative percentage of species that had re-
are implemented in a timely fashion; however, delays
in implementing policy changes may exceed the ca-
pacity for ecosystem resilience.
The Little Rock Experimental Acidification Project has
been supported by funding from the National Science Foun-
dation, the U.S. Environmental Protection Agency, the U.S.
Geological Survey, and the state of Wisconsin. It has also
received logistic assistance from the North Temperate Lakes
Long Term Ecological Research Program. Comments from
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