Crustacean zooplankton communities in lakes recovering from ...

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Crustacean zooplankton communities in lakes recovering from acidification W. Keller, N.D. Yan, K.M. Somers, and J.H. Heneberry

Abstract: Large reductions in sulphur emissions at the Sudbury, Ont., Canada, smelters in recent decades have resulted in decreased lake acidity, and biological improvements have followed. Lakes in the Sudbury area offer a very unique opportunity to develop our understanding of the processes regulating biological restructuring in aquatic ecosystems recovering from acidification. Here, we examine changes in crustacean zooplankton communities that have accompanied the chemical recovery of Whitepine and Sans Chambre lakes, near Sudbury, over the last two decades. In both these formerly acidic lakes, pH has increased to ~6.0, and some zooplankton community recovery has occurred. However, zooplankton communities have not completely recovered based on multivariate comparisons with the community composition of reference lakes. Although a number of acid-sensitive species have appeared, many did not persist, or did not achieve abundances typical of the reference lakes. This indicates that zooplankton community recovery will most likely depend on biotic and abiotic interactions within these lakes and not on factors affecting species dispersal. Both chemical and biological factors have large influences on biological recovery processes. Assessing biological recovery is very important since the restoration of healthy aquatic communities is a major objective of large-scale sulphur emission control programs. Résumé : Les réductions importantes des émissions de soufre dans les fonderies de Sudbury, Ont., Canada, au cours des dernières décennies ont entraîné une diminution de l’acidité des lacs et, par conséquent, une amélioration des conditions biologiques. Les lacs de la région de Sudbury fournissent ainsi une occasion unique de comprendre les processus de restructuration des écosystèmes aquatiques qui se remettent de l’acidification. Nous examinons ici les changements dans les communautés des crustacés du zooplancton qui ont suivi l’amélioration des conditions chimiques au cours des 20 dernières années dans les lacs Whitepine et Sans-Chambre, près de Sudbury. Dans ces deux lacs autrefois acidifiés, le pH a augmenté à ~6,0 et une certaine récupération de la communauté du zooplancton s’est produite. Cependant, des comparaisons multidimensionnelles avec des lacs témoins révèlent que les communautés zooplanctoniques ne sont pas totalement rétablies. Bien qu’un nombre d’espèces sensibles à l’acidité soient apparues, plusieurs n’y sont pas demeurées ou n’ont pas réussi à atteindre les densités habituelles des lacs témoins. Cela indique que le rétablissement de la communauté zooplanctonique dépendra très probablement d’interactions biotiques et abiotiques à l’intérieur de ces lacs, plutôt que de facteurs reliés à la dispersion des espèces. Tant les facteurs chimiques que biologiques agissent fortement sur les processus de récupération biologique. L’évaluation de la récupération biologique est très importante, car la restauration de la santé des communautés aquatiques est l’un des objectifs principaux des programmes de contrôle à grande échelle des émissions de soufre. [Traduit par la Rédaction]

Keller et al.

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Introduction Excessive acid deposition has acidified many thousands of lakes, with resulting damage to their biological communities (Schindler 1988). During the 1980s and 1990s, massive sulphur emission control programs were implemented in many areas including Canada, the United States, and Europe to combat the global problem of acid deposition. With the im-

plementation of emission control programs, it was expected that conditions in affected aquatic ecosystems would improve, and the focus of acid rain assessment programs began to change from documenting damage to investigating ecosystem recovery. Other than in the Sudbury, Ont., Canada, area, evidence of the chemical recovery of lakes is only beginning to emerge from regions where sulphur emissions and deposition have

Received 21 September 2001. Accepted 31 March 2002. Published on the NRC Research Press Web site at http://cjfas.nrc.ca on 24 May 2002. J16542 W. Keller1 and J.H. Heneberry. Ontario Ministry of the Environment, Cooperative Freshwater Ecology Unit, Laurentian University, Ramsey Lake Road, Sudbury, ON P3E 2C6, Canada. N.D. Yan. Biology Department, York University, 4700 Keele Street, Toronto, ON M3J 1P3, Canada. K.M. Somers. Ontario Ministry of the Environment, Dorset Environmental Science Centre, P.O. Box 39, Dorset, ON P0A 1E0, Canada. 1

Corresponding author (e-mail: [email protected]).

Can. J. Fish. Aquat. Sci. 59: 726–735 (2002)

J:\cjfas\cjfas59\cjfas-04\F02-042.vp Tuesday, May 21, 2002 11:59:34 AM

DOI: 10.1139/F02-042

© 2002 NRC Canada


Keller et al.

been reduced (Stoddard et al. 1999). Evidence of biological recovery from lake acidification is even more limited. Lakescale manipulations (Keller et al. 1990a; Degerman et al. 1995; Sampson et al. 1995) indicate that biological improvements should follow the water quality improvements expected to result from sulphur emission reductions. However, evidence of the natural recovery of aquatic communities from acidification is rare. Some biological recovery, as well as striking chemical recovery, has been documented in lakes around Sudbury (Keller et al. 1992a, 1999) where emission reductions from area metal smelters were particularly large and began in the early 1970s. However, since recovery is at an early stage in many Sudbury area lakes, previous studies have not allowed detailed examination of long-term recovery patterns in lakes, which had reached pH levels that would not be expected to still severely limit acid-sensitive aquatic biota. A pH of about 6.0 appears to be necessary for the protection of many acid-sensitive taxa (Schindler 1988; Havens et al. 1993). With continuing chemical recovery in the Sudbury area, some lakes have now reached pH ~ 6.0. This chemical recovery permits evaluation of the natural biological recovery that has followed water quality improvements in lakes that have not had direct chemical manipulations. There can, of course, be different definitions of recovery. Here we accept that various outcomes may reasonably be expected from the biological recovery process (Keller and Yan 1998; Keller et al. 1999) and we consider recovery as the return to a typical, not necessarily a pre-stress, condition. Assessments of biological recovery are very important to the evaluation of acid rain controls, since the protection and restoration of aquatic communities is a major ultimate objective of emission reduction programs. Empirical documentation of the patterns of recovery in damaged lakes also offers important opportunities to increase our more general understanding of the processes regulating aquatic community structure and biodiversity. This paper examines long-term patterns in crustacean plankton communities in two Sudbury area lakes that have exhibited chemical recovery to pH ~ 6.0, in response to smelter emission reductions. To assess recovery in the crustacean zooplankton communities of these two lakes we have followed the approach of Yan et al. (1996), and compare temporal patterns in univariate and multivariate measures of community structure over a two-decade period to comparable spatial survey data for a set of 47 reference lakes, near Dorset, Ont., that have not shown any general temporal trends in pH during the study period. The range of variability in the zooplankton community data for the reference lakes provides our recovery targets.

Methods Study lakes The Sudbury lakes studied (Fig. 1), Whitepine (lat 47°17′N, long 80°50′W) and Sans Chambre (lat 46°43′N, long 81°07′W), are within the large area historically affected by the Sudbury smelter emissions. A summary of general physical and chemical characteristics of the lakes is provided in Table 1. As part of the widespread water quality improvements seen in this region (Keller et al. 1992b), these lakes

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have decreased in acidity following the implementation of large reductions (about 90% since the peak in the 1960s) in sulphur emissions from the Sudbury area metal smelters during the 1970s and 1990s. Both these lakes had average pH < 5.5 when monitoring commenced in 1980, a pH level at which substantial effects on sensitive zooplankton species are expected (Keller et al. 1990b; Havens et al. 1993). Both lakes now have average pH > 6.0 (Fig. 2). The Dorset reference lakes are located about 200 km southeast of Sudbury (Fig. 1) and are zoogeographically similar to the Sudbury lakes with respect to zooplankton (Sprules 1977). The lakes span a range of chemistry and morphometry, which encompasses the conditions in Whitepine and Sans Chambre lakes. General physical and chemical characteristics of the Dorset lakes are summarized in Table 1. Additional descriptions of the Dorset lakes are provided in Yan et al. (1996). Sampling and analysis Zooplankton were collected from both of the Sudbury lakes between 1980 and 1999. Whitepine Lake was sampled in all years, whereas some years (1982, 1984, 1986, 1987) were not included in the monitoring of Sans Chambre Lake. Samples were usually collected monthly during the ice-free season; however, sampling frequency was higher in some years in the early 1980s, and slightly reduced in some years in the mid-1990s (Tables 2 and 3). The 47 Dorset reference lakes were sampled monthly during the ice-free season for one year each (1983, 1984, 1987, or 1988). All zooplankton samples were collected as vertical tows through the water column with 12.5-cm-diameter, 80-µmmesh nets. Metered nets were used for the Dorset lakes and for the Sudbury lakes after 1981 to allow correction for filtration efficiency. Data for Sudbury lakes from 1980 and 1981 were adjusted for filtration efficiency by applying the mean efficiency for metered net collections in each lake during the 1980s. Single hauls from 1 m above bottom were taken in Sans Chambre Lake. In Whitepine Lake and each of the Dorset lakes, a series of hauls from three to seven fixed depths in the water column, at a single site, was taken and composited. Depths were chosen so that the composite sample was weighted to account for lake stratum volume. Samples were preserved with buffered sugar formalin to a final formalin concentration of 4%. Subsequently, a minimum of 250 crustacean zooplankton were identified and counted. Cladocera and mature Copepoda were identified to species and immature Copepoda were identified to suborder. To deal with changes in nomenclature over the course of the study we have combined counts of different species of Diaphanosoma to genus, have combined Daphnia dentifera with Daphnia mendotae, and have combined Daphnia pulicaria and Daphnia catawba with Daphnia pulex. Annual average species richness per collection and abundance were determined by averaging monthly data. Where more than one sample was available for a month, these values were averaged, to provide a monthly value, before generating annual averages. High numbers of animals (up to ~500 and ~700 animals per sample, in Whitepine and Sans Chambre, respectively) were counted in some samples in a few early years. Because richness is related to the number of © 2002 NRC Canada



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Can. J. Fish. Aquat. Sci. Vol. 59, 2002

Fig. 1. Locations of Whitepine and Sans Chambre lakes, near Sudbury, Ont., Canada, and the Dorset reference lakes.

Table 1. General characteristics of the Sudbury and Dorset study lakes. Dorset Distance from Sudbury (km) Area (ha) Mean depth (m) Max. depth (m) Secchi depth (m) pH Ca (mg·L–1) Total P (µg·L–1) DOC (mg·L–1)

Sudbury

pH > 6.0 (n = 22)

pH < 6.0 (n = 25)

Whitepine

Sans Chambre

~200 13.1–679.0 5.2–22.0 13.7–61.0 2.9–7.9 6.0–6.7 2.1–4.0 4–18 1.5–5.5

~200 7.2–195.0 1.8–12.4 5.8–36.5 1.3–9.3 5.3–5.9 1.2–2.8 4–22 1.5–8.7

89 66.9 5.9 22.0 6.4 6.3 1.8 5 2.5

30 14.5 5.6 15.0 4.5 6.2 1.7 8 2.9

Note: Sudbury chemistry data are ice-free period averages of monthly samples from 1999. Dorset chemistry data are ice-free period averages of monthly samples from one of 1983, 1984, 1987, or 1988. Max, maximum; DOC, dissolved organic carbon.

animals counted, richness for these lakes was standardized to a count of 250 animals, using relationships that had been established previously (Keller and Yan 1991). No correction was applied to the Dorset reference lakes because approximately 250 animals were counted in all samples. Following Yan et al. (1996) we employed correspondence analysis (CA) to generate our multivariate metrics of zooplankton community structure. Our input to the CA was average annual species abundance data transformed to log(x + 1) + 0.2. The factor of 0.2 was applied to further downweight the influence of uncommon species (K. Somers, unpublished data). The rarest species, including Acantholeberis curvirostris, Acroperus harpae, Eubosmina coregoni, Eucy-

clops speratus, and Aglaodiaptomus leptopus, were excluded from the analyses. Analyses were run separately for Whitepine Lake with the reference lakes, and for Sans Chambre Lake with the reference lakes.

Results Species occurrences and abundances During the 1980s and 1990s, 31 and 24 species of crustacean plankton were recorded in Whitepine and Sans Chambre lakes, respectively (Tables 2 and 3). Between 8 and 16, and 6 and 16 species were found in any one year in Whitepine and Sans Chambre lakes, respectively, but evalua© 2002 NRC Canada



Keller et al. Fig. 2. Average annual pH during the ice-free season (error bars indicate the range in values) for (a) Whitepine and (b) Sans Chambre lakes.

tion of total annual richness in the Sudbury lakes is complicated by variable sampling frequency (Tables 2 and 3) since sampling effort can greatly influence total richness estimates (Arnott et al. 1998). A number of species were detected in all, or almost all, study years. These included Cyclops bicuspidatus thomasi, Cyclops scutifer, D. pulex, Holopedium gibberum, Bosmina spp., and Leptodiaptomus minutus in Whitepine Lake (Table 2), and Bosmina spp., C. scutifer, H. gibberum, L. minutus, Orthocyclops modestus, and Mesocyclops edax in Sans Chambre Lake (Table 3). Species that were not detected at the beginning of our studies, but later appeared and persisted in the communities as common species included Epischura lacustris and Eubosmina longispina in Whitepine Lake (Table 2), and D. pulex, Tropocyclops extensus, Daphnia ambigua, and E. lacustris in Sans Chambre Lake (Table 3). Species that occurred throughout our period of record but showed alternating periods of presence or absence, often for several consecutive years, included Chydorus sphaericus, D. ambigua, D. mendotae, Diaphanosoma sp., M. edax, and T. extensus in Whitepine Lake, and D. mendotae, Skistodiaptomus oregonensis, and C. b. thomasi in Sans Chambre Lake (Table 3). Other species collected in these lakes were generally rare, occurring in 25% or less of the study years, and restricted to limited or sporadic occurrences (Tables 2 and 3). Overall differences (p < 0.05) in species abundances between the reference lakes and both Whitepine and Sans Chambre lakes included higher abundances of D. longiremis, S. oregonensis, Diaphanosoma sp., Neobosmina tubicen, D. retrocurva, D. dubia, and D. mendotae, and lower abundances of D. pulex and C. scutifer, in the reference lakes (oneway analysis of variance (ANOVA), Bonferroni multiple comparisons test). Species richness There were substantial between-year variations in average

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zooplankton community richness (Fig. 3); however, in both Sudbury lakes average species richness per collection increased (p < 0.05) over the study period based on regressions of richness against year (Whitepine, r = 0.55; Sans Chambre, r = 0.78). Average richness was also correlated (p < 0.05) with average annual pH (Whitepine, r = 0.42; Sans Chambre, r = 0.70), which was correlated (p < 0.05) with year (Whitepine, r = 0.83; Sans Chambre, r = 0.70). Comparison of the long-term patterns in the average richness of the Sudbury lakes with the average richness in the Dorset reference lakes with pH > 6.0 (Fig. 3) indicated that in the 1990s, richness values for both Sudbury lakes fell within the range of reference lake variability (mean ± 2 standard deviations = 7.8–12.3) in some years. By this metric, communities have shown recovery. Multivariate community structure The first two CA axes explained 39% of the transformed variation in species abundances when Whitepine Lake was included, and 43% of the transformed variation when Sans Chambre Lake was included (species scores for the axes are shown in Fig. 4a, 4b). In the Whitepine Lake CA, axis I (21% explained variation) was correlated (p < 0.05) with dissolved organic carbon (DOC; r = –0.50), total phosphorus (TP; r = –0.34), and calcium (Ca; r = –0.26), and axis II (18% explained variation) was correlated with pH (r = 0.60), aluminum (Al; r = –0.58), TP (r = –0.50), DOC (r = –0.38), and Ca (r = 0.26). In the ordination with Sans Chambre Lake, axis I (28% explained variation) was correlated (p < 0.05) with TP (r = 0.46), pH (r = –0.41), and Al (r = 0.36), and axis II (15% explained variation) was correlated with DOC (r = –0.63), Al (r = –0.43), pH (r = 0.42), TP (r = – 0.36), and Ca (r = 0.30). Temporally, Whitepine Lake shifted toward higher positive scores on CA axis II during the study period. Axis II scores increased significantly (r = 0.81, p < 0.05) over the study period based on a regression against sequential year of sampling. This trajectory indicates recovery, since higher positive scores on CA axis II are characteristic of the reference lakes with pH > 6.0 (Fig. 5a). However, Whitepine Lake scores never occupied the same region in ordination space on axis I as the reference lakes. Community structure, as defined by lake scores from CA, changed little in Sans Chambre Lake over the past two decades (Fig. 5b). Throughout this study period Sans Chambre Lake did not move in a consistent manner toward the region in the ordination occupied by the reference lakes. There were no significant correlations between axis I or axis II scores and sequential years based on linear regressions (p > 0.05).

Discussion Two decades of monitoring, during conditions of decreasing lake acidity, did reveal evidence of recovery in the crustacean zooplankton communities in Whitepine and Sans Chambre lakes. A number of “new” species became established, and persisted in the zooplankton communities of the lakes. The fact that some of these species, such as E. lacustris, are quite acid sensitive (Keller and Yan 1998) indicates that these biological changes are consistent with improved water quality conditions. Average species richness © 2002 NRC Canada



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Table 2. Percent occurrence of crustacean zooplankton in ice-free period samples from Whitepine Lake, 1980–1999.

Species Calanoid copepodid Cyclopoid copepodid Cyclops bicuspidatus thomasi Cyclops scutifer Daphnia pulex Holopedium gibberum Leptodiaptomus minutus Nauplius Bosmina spp. Epischura lacustris Bosmina (Eubosmina) longispina Mesocyclops edax Daphnia ambigua Daphnia mendotae Tropocyclops extensus Chydorus sphaericus Diaphanosoma sp. Alona sp. Bosmina (Neobosmina) tubicen Leptodora kindtii Alona affinis Alona guttata Bosmina (Eubosmina) coregoni Daphnia longiremis Eucyclops speratus Acantholeberis curvirostris Acroperus harpae Ceriodaphnia sp. Cyclops vernalis Daphnia retrocurva Eucyclops neomacruroides Latona setifera Sida crystallina Skistodiaptomus oregonensis

Species abbreviation Cal copep Cyc copep C b thom C scut D pulex H gibb L minu nauplius Bos spp E lacus E long M edax D ambig D men T ext C sphaer Diaph sp Alona sp N tub L kind A affin A gutt E core D long E sper A curv A harp Cerio sp C vern D retro E neom L seti S crys S oreg

1980 (7) 100 100 29 71 57 100 100 100 86 0 0 57 71 14 0 29 0 0 0 0 14 0 0 0 0 0 0 0 0 0 0 0 0 0

1981 (13) 85 100 31 77 85 62 100 100 77 0 0 54 62 8 8 8 0 0 0 23 15 0 0 0 0 0 0 0 0 0 0 0 0 0

1982 (13) 92 100 85 85 85 69 100 100 85 15 0 15 46 0 0 54 8 0 0 15 0 8 0 0 8 0 8 0 0 8 0 0 0 0

1983 (11) 91 100 91 82 91 100 91 100 100 27 0 64 0 9 27 82 0 0 0 9 0 18 0 0 0 0 0 0 0 0 0 0 9 0

1984 (5) 80 100 60 60 60 100 80 100 100 20 0 0 40 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

1985 (6) 83 100 83 67 83 100 100 100 67 50 0 0 0 0 33 17 0 0 0 0 0 0 0 0 0 0 0 17 0 0 0 0 0 0

1986 (6) 100 100 100 50 100 83 100 100 33 83 0 0 0 0 17 0 0 0 0 0 0 0 0 0 0 17 0 0 0 0 0 0 0 17

1987 (6) 100 100 83 67 67 83 100 100 83 67 17 0 17 0 17 0 0 17 17 17 0 0 0 0 0 0 0 0 0 0 0 0 0 0

1988 (5) 100 100 60 20 80 60 100 100 100 60 100 40 0 0 20 0 40 20 20 0 0 0 0 0 0 0 0 0 20 0 0 0 0 0

Note: Taxa are listed in order of decreasing overall occurrence in years. Daphnia dubia (species abbreviation D dubia) present in Dorset Reference

per collection in both lakes increased substantially to levels approaching, or in some years falling within, the range of variability observed in the reference lakes with pH > 6.0. Whether species richness will increase further remains to be seen. Despite the positive responses to reduced acidity that have occurred, zooplankton communities in the two Sudbury lakes have not truly “recovered” when recovery is defined as the lake positions with respect to our two CA axes. The trajectory of community change in Whitepine Lake, determined by CA, clearly indicates recovery; however, in both Whitepine and Sans Chambre lakes, community structure never completely resembled reference lake conditions. This interpretation of the multivariate patterns in species composition presumes that the range of variability in the reference lake data does provide suitable targets for recovery in our study lakes. The Dorset lakes provide the only comparably collected zooplankton reference data set that is available to help evaluate the responses of our Sudbury lakes. The reference lakes were, however, only sampled during the 1980s, whereas our Sudbury lake data also extend through the

1990s. Therefore, we cannot be completely certain that these reference data are fully representative of the 1990s, a decade with, for example, different weather patterns than the 1980s. Such uncertainty underscores the need for additional efforts to establish current biological reference data sets to aid in assessments of the status of aquatic ecosystems affected by acidification and other anthropogenic stressors. The reference and study areas are nonetheless zoogeographically similar, and lakes in both areas were sampled by comparable protocols. The reference lakes encompass the range of physico-chemical conditions in the Sudbury lakes, although the Sudbury lakes do tend to lie at the clear, small, low ionic strength end of the distribution of these characteristics in the reference lakes. The major overall difference between the Sudbury lakes and the Dorset lakes is in the comparative scarcity of a number of acid-sensitive zooplankton species in the Sudbury lakes, a difference that is attributable to the greater degree and duration of acidification damage around Sudbury. Collectively, this evidence indicates that the reference lakes are suitable for our comparisons. © 2002 NRC Canada



Keller et al.

1989 (6) 100 100 67 83 83 83 100 100 83 17 83 67 0 0 0 0 17 0 33 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

1990 (7) 100 100 71 57 71 100 100 100 29 43 86 0 57 14 14 29 57 0 14 0 0 0 0 0 0 0 0 0 0 0 0 14 0 0

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1991 (6) 100 100 67 83 100 100 100 100 33 100 100 33 33 0 0 0 83 0 17 33 0 0 0 0 0 0 0 0 0 0 0 0 0 0

1992 (7) 100 100 71 57 100 100 100 100 0 86 100 14 0 14 0 0 14 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

1993 (6) 100 100 67 50 100 100 100 100 50 100 100 33 17 17 0 17 17 0 0 0 0 0 17 0 0 0 0 0 0 0 0 0 0 0

1994 (6) 100 100 67 67 100 83 100 100 33 50 100 17 0 17 0 0 0 17 0 0 0 0 17 33 0 0 0 0 0 0 0 0 0 0

1995 (3) 100 100 67 67 100 67 100 100 67 33 100 0 0 33 0 33 0 0 0 0 0 0 0 33 0 0 0 0 0 0 33 0 0 0

1996 (3) 100 100 67 67 67 100 100 100 33 67 100 0 33 33 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

1997 (5) 100 100 60 60 100 100 100 100 60 60 100 60 40 0 40 0 0 20 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

1998 (5) 100 100 80 40 100 60 100 100 60 80 100 40 0 0 0 0 0 40 0 0 0 0 0 0 20 0 0 0 0 0 0 0 0 0

1999 (6) 100 100 67 50 100 100 100 100 83 50 83 67 17 0 50 0 33 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

% of years (20) 100 100 100 100 100 100 100 100 95 90 65 65 55 45 45 40 40 25 25 25 10 10 10 10 10 5 5 5 5 5 5 5 5 5

Lakes, but not in either of the Sudbury study lakes. Number in parentheses under year represents the total number of samples (n).

A number of factors may be involved in regulating biological recovery in these lakes. Both Whitepine and Sans Chambre lakes are headwaters, thus it might be expected that colonization opportunities from external sources could be limited. Invasion rates can be highly variable for different zooplankton species (Jenkins and Buikema 1998) and variability in factors such as invasion sequence and rate (Patrick 1967; Robinson and Edgemon 1988) may account for the variable temporal trajectories observed in lakes recovering from acidification. Most zooplankton colonization experiments and studies (e.g., Jenkins and Buikema 1998; Shurin 2000) have been comparatively short term (one year or less), and small scale with respect to surface area. They may not completely reflect the ultimate role of dispersal in determining community composition on the scale of decades in larger natural systems. Extended monitoring studies, as reported here, offer an important complement to experimental studies examining factors regulating aquatic communities, because they reveal the actual long-term, lake-scale patterns of community change. Long-term monitoring studies also have the advantage that

species have had a long temporal window for colonization, whether the vector of colonization is transport from sources external to the lake (Maguire 1963; Schlichting and Sides 1969) or from the sediment egg bank (De Stasio 1989; Hairston 1996). It is likely that most species in the species pool will be detected, even if they are rare, when sampling extends through decades. Examination of the two-decade record for Whitepine and Sans Chambre lakes revealed that a number of acid-sensitive (Keller at al. 1990b; Havens et al. 1993) species, including D. mendotae, D. retrocurva, and S. oregonensis, which were important in defining our CA axes, were present at times in both lakes, but never became common. This suggests that dispersal was not ultimately a major limitation to their establishment in the lake communities. The incomplete recovery, as indicated by multivariate analyses of the zooplankton community in Whitepine and Sans Chambre lakes, may reflect the limitations of time and unsuitable water quality. A pH of at least 6.0 appears to be necessary for the survival of many acid-sensitive zooplankton species (Keller at al. 1990b; Havens et al. 1993). A number of these species, which were relatively common in the © 2002 NRC Canada



0 0 0 0 0 0 0 0 0 0 0 0 0

A lept Daph sp Alona sp E long C glob C sphaer D retro P pedi N tub E core S crys

(4) 100 100 100 50 100 100 100 100 100 0 0 0 0 0

1980

D men S oreg

Species abbreviation Bos spp Cal copep Cyc copep C scut H gibb L minu M edax nauplius O mode D pulex T ext D ambig E lacus C b thom

8

0

0 0 0 0 0

0 0 0 0

0

0

0 0 0 17 0

0 0 0 0

0 0

(6) 83 100 100 100 83 100 100 100 17 100 50 0 0 0

(13) 85 100 100 62 100 100 62 100 54 0 0 0 0 8 0 0

1983

1981

0

0

0 0 0 17 0

0 0 0 0

0 0

(6) 100 100 100 83 100 83 67 100 0 100 33 0 0 17

1985

0

0

0 0 17 0 0

0 17 0 0

0 0

(6) 50 100 100 50 83 100 67 100 83 100 17 100 17 17

1988

0

0

0 0 0 0 0

0 17 17 0

0 0

(6) 83 100 100 83 83 100 50 100 33 100 33 67 17 0

1989

0

0

0 0 0 0 0

0 17 0 33

0 17

(6) 67 100 100 50 100 100 33 100 83 100 50 83 17 33

1990

0

0

0 0 0 0 0

0 0 0 0

14 14

(7) 71 100 100 43 100 100 71 100 71 100 86 43 43 29

1991

0

0

0 11 11 0 0

0 0 0 0

11 11

(9) 89 100 100 44 100 100 44 100 44 100 33 11 44 11

1992

0

0

0 0 0 0 0

0 22 0 0

0 0

(9) 89 100 100 56 1 00 100 89 100 56 100 22 78 11 11

1993

0

0

33 17 0 0 0

0 0 0 17

17 17

(6) 100 100 100 67 83 100 67 100 83 83 50 83 17 17

1994

0

14

29 0 0 0 0

0 0 0 0

14 0

(7) 43 100 100 86 1 00 100 86 100 100 71 71 43 29 0

1995

0

0

0 0 0 0 0

50 0 0 0

0 0

(4) 25 100 100 50 100 100 50 100 25 100 50 0 25 0

1996

0

0

0 0 0 0 20

100 0 0 0

20 20

(5) 100 100 100 40 1 00 100 60 100 80 80 80 40 40 0

1997

0

0

0 0 0 0 0

60 0 20 0

0 0

(5) 80 100 100 40 100 100 60 100 100 100 40 40 20 0

1998

0

0

0 0 0 0 0

50 0 17 0

33 0

(6) 83 100 100 50 100 100 67 100 83 100 83 100 0 17

1999

6

6

13 13 13 13 6

25 25 19 13

38 31

(16) 100 100 100 100 100 100 100 100 94 88 88 69 69 56

% of Years

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Note: Taxa are listed in order of decreasing overall occurrence in years. Daphnia dubia (species abbreviation D dubia) present in Dorset Reference Lakes, but not in either of the Sudbury study lakes. Number in parentheses represents the total number of samples (n).

Species Bosmina spp. Calanoid copepodid Cyclopoid copepodid Cyclops scutifer Holopedium gibberum Leptodiaptomus minutus Mesocyclops edax Nauplius Orthocyclops modestus Daphnia pulex Tropocyclops extensus Daphnia ambigua Epischura lacustris Cyclops bicuspidatus thomasi Daphnia mendotae Skistodiaptomus oregonensis Aglaodiaptomus leptopus Daphnia sp. Alona sp. Bosmina (Eubosmina) longispina Chydorus globosus Chydorus sphaericus Daphnia retrocurva Polyphemus pediculus Bosmina (Neobosmina) tubicen Bosmina (Eubosmina) coregoni Sida crystallina

Table 3. Percent occurrence of crustacean zooplankton in ice-free period samples from Sans Chambre Lake, 1980–1999.



© 2002 NRC Canada


Keller et al. Fig. 3. Average annual ice-free period richness per collection, for crustacean zooplankton in Whitepine (䊊) and Sans Chambre (䉱) lakes, 1980–1999, in comparison to the Dorset reference lakes with pH > 6.0.

reference lakes and were important in defining community structure in the CA ordinations, are still rare in the Sudbury study lakes. Recovery of the crustacean zooplankton community was observed within a decade after the liming of Nelson Lake, near Sudbury (Yan et al. 1996), and zooplankton communities appear to have recovered in other Sudbury area lakes that have had pH > 6.0 for over a decade (Holt and Yan 2003). However, average pH > 6.0 has only been achieved very recently in Whitepine and Sans Chambre lakes, and pH minima are still slightly under 6.0. Despite two decades of monitoring, it appears that additional time, given conditions of suitable habitat quality, may be required for complete recovery of these communities. Other factors also appear to be involved in regulating the recovery process in these lakes. The observation that community structure did show some evidence of recovery in Whitepine Lake, but showed very little change in Sans Chambre Lake, even though the extent of pH changes was generally similar, suggests that different mechanisms of control may currently dominate in these lakes. Biological as well as chemical factors may be important influences on the recovery of zooplankton communities (Keller and Yan 1998), and in some very important respects, Whitepine and Sans Chambre lakes differ in their biological characteristics. Whitepine Lake has always had abundant fish during our study period, although the community composition has changed dramatically, from dominance by yellow perch (Perca flavescens) to lake trout (Salvelinus namaycush) (Gunn and Mills 1998). This change in the fish community may have favoured the recovery of zooplankton species through the relaxation of fish planktivory (Keller and Yan 1998). Not surprisingly, given the abundant fish and relatively nutrient poor status, abundances of the predatory invertebrate, Chaoborus, are very low in Whitepine Lake (late summer abundances of 1–11 animals·m–3 based on sampling in 1982–1984 and 1988; W. Keller, unpublished data) and are unlikely to have affected zooplankton species abundances through predation.

733 Fig. 4. (a) Crustacean zooplankton species scores on correspondence analysis (CA) axes for the ordination with Whitepine Lake and the reference lakes. Species abbreviations are identified in Table 2. (b) Crustacean zooplankton species scores on CA axes for the ordination with Sans Chambre Lake and the reference lakes. Species abbreviations are identified in Table 3.

In contrast, Sans Chambre Lake was essentially fishless at the beginning of our studies, containing only a few individuals of brown bullhead (Ictalurus nebulosus) and central mudminnow (Umbra limi). The lake was successfully stocked with smallmouth bass (Micropterus dolomieu) in the early 1980s, but predation by smallmouth bass does not appear to exert a strong direct effect on pelagic invertebrates including crustacean zooplankton and Chaoborus. Chaoborus abundance in Sans Chambre Lake is high, with late summer abundances of 107 animals·m–3 and 124 animals·m–3 in 2000 and 2001, respectively (W. Keller, unpublished data). Chaoborus predation can exert a large effect on crustacean zooplankton at Chaoborus abundances of more than 30–50 animals·m–3 (Nyberg 1984; Yan et al. 1991). Chaoborus predation can decimate and even eliminate some zooplankton species, including comparatively small Daphnia species such as D. mendotae and D. retrocurva (Vanni 1988), which are rare in Sans Chambre © 2002 NRC Canada



734 Fig. 5. (a) Lake scores on correspondence analysis (CA) axes for the ordination with Whitepine Lake and the reference lakes. (b) Lake scores on CA axes for the ordination with Sans Chambre Lake and the reference lakes.


be needed before the zooplankton community can respond to reduced acidity. The recovery of damaged aquatic ecosystems after the removal of stress is a very complex, poorly understood process (Cairns 1990; Power 1999). In general, the factors affecting biological recovery fall into two categories: (i) chemical, physical, and biological factors related to habitat quality, and (ii) factors related to the dispersal of organisms. Understanding the relative roles of processes operating within lakes versus processes related to dispersal is essential to the development of our knowledge of aquatic ecosystem recovery, and is also fundamental to addressing broader ecological questions about the factors regulating biodiversity in aquatic systems. Whether these different processes are termed local versus regional (e.g., Lukaszewski et al. 1999; Shurin et al. 2000) or internal versus external (e.g., Keller and Yan 1998), a key question is if community structure is primarily regulated by factors affecting the dispersal of species, or by factors affecting the survival and persistence of species. The re-establishment of some zooplankton species including hypolimnetic forms and the “glacial opportunists” is expected to be limited by dispersal abilities (Schindler 1987; Keller and Yan 1998) and the regional species pool will have an overriding effect on local species assemblages. However, increasing experimental evidence is emerging that demonstrates the importance of “local” processes in determining zooplankton community structure (Arnott and Vanni 1993; Lukaszewski et al. 1999; Shurin 2000). Different mechanisms appear to be the primary current controls on zooplankton community recovery in Whitepine (duration of suitable habitat conditions) and Sans Chambre (biological resistance) lakes. However, both these examples provide empirical evidence for the importance of within-lake factors as controls on biological recovery. Our results suggest that the successful establishment of most common zooplankton species in these lakes as they recover from acidification will mainly depend on biotic and abiotic interactions, not on factors affecting species dispersal.

Acknowledgements Lake. The current characteristics of the Sans Chambre Lake zooplankton community, including scarcity of small Daphnia, absence of Diaphanosoma birgei, dominance by D. pulex, and the frequent occurrence of A. leptopus and O. modestus, are consistent with communities in fishless lakes exhibiting high Chaoborus predation (Vanni 1988; Arnott and Vanni 1993; Keller and Conlon 1994). Thus, biological resistance (Nyberg 1984; Keller and Yan 1998) through intensive invertebrate predation is probably limiting the recovery of zooplankton in Sans Chambre Lake. Chaoborus abundance varies widely in the reference lakes (Persaud and Yan 2001) but none of the near-neutral reference lakes are fishless. Based on its size of 14.5 ha, Sans Chambre Lake was probably also not fishless prior to acidification (Matuszek et al. 1990), and therefore our recovery targets based on reference data would be valid for that lake. Substantial recovery of zooplankton communities in this lake may require not just suitable water quality, but biological intervention through stocking of planktivorous fish. It is likely that a reduction in invertebrate predation pressure will

This paper is a contribution from the Aquatic Restoration Group of the Cooperative Freshwater Ecology Unit, a partnership between Laurentian University, the Ontario Ministry of the Environment, the Ontario Ministry of Natural Resources, Inco Limited, Falconbridge Limited, and Environment Canada. We thank Shelley Arnott and the Journal referees for helpful comments on the manuscript, and Peggy Gale and Jim Carbone for their many years of help collecting zooplankton samples.

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