Biomass and production of amphipods in low alkalinity lakes affected by acid precipitation

Environmental Pollution,

PII:

SO269-7491(96)00063-Z

Vol. 94, No. 2, pp. 189-193, 1996 Copyright 0 1997Ekvier Science Ltd Printed in Great Britain. All rights reserved 0269-7491/96%15.00+0.00

ELSEVIER

BIOMASS AND PRODUCTION OF AMPHIPODS IN LOW ALKALINITY LAKES AFFECTED BY ACID PRECIPITATION

R. L. France* W.D.N.R.G. Limnetics, 417 Haney St, Winnipeg, Manitoba, Canada R3R OY5 (Received 8 December 1995; accepted 15 May 1996)

invertebrates (Uutala, 1981; Rooke & Mackie, 1984; Griffith et al., 1993). The purpose of the present study was to augment previously published data on the biomass and production of the amphipod Hyalella azteca (Saussure) (France, 1993a,b) with new information, in order to examine whether anthropogenic lake acidification has had a demonstrable effect on the secondary production of this littoral macroinvertebrate species. Survey data (Stephenson & Mackie, 1986; Peterson, 1987; Gibbons & Mackie, 1991; Grapentine & Rosenberg, 1992), laboratory toxicity experiments (de March, 1979; Stephenson & Mackie, 1986; France & Stokes, 1987a, 1987b; Mackie, 1989; Grapentine & Rosenberg, 1992; Pilgrim & Burt, 1993), in situ transplantations and manipulations (Grapentine & Rosenberg, 1992), documented extirpations (France & LaZerte, 1987; Grapentine & Rosenberg, 1992), population demographic studies (Stephenson & Makie, 1986), and simulation modeling (France & LaZerte, 1987) have all identified Hyalella azteca (henceforth Hyalella) as being very sensitive to low pH. This has subsequently led to the development of a protocol for the use of this species as a biomonitor of anthropogenic acidification (France, 1992a). The present paper examines whether previously observed differences in Hyalella abundance in relation to gradients in lake alkalinity (France, 1992a) were substantial enough to be reflected by corresponding differences in the productivity of these populations.

Abstract Population biomass and production of the amphipod Hyalella azteca (Saussure) were found to be related to alkalinity (ranging from 0.2 to 58.1 mg liter-‘) in 10 Canadian Shield lakes in south-central Ontario. Biomass and production of amphipods in the two lakes characterized by spring depressions of pH below 5.0 were found to be lower than those for populations inhabiting lakes that did not experience such acid pulses. The proportional biomass of amphipods in relation to the total littoral zoobenthos community was lower in lakes of low alkalinity than in circumneutral or hardwater lakes. Because production in these amphipod populations is known to depend closely on population abundance, the labour-intensive derivation of production rates yields relatively little information for biomonitoring that cannot be obtained from abundance data alone. 0 1997 Elsevier Science Ltd. All rights reserved.

INTRODUCTION Acid rain continues to be a major environmental problem, causing the depression of surface water pH over vast areas of Canada. For example, for lakes surveyed in 1980 and again in 1990, 28% were found to be more acidic, while a further 41% were found to have remained unchanged over this period (Gorrie, 1995). Of 11 surface waters sampled in the Haliburton-Muskoka region of south-central Ontario, five exhibited stable pH values and alkalinities and three indicated continuing acidification between 1983 and 1991 (Clair et al., 1995). The need to comprehend environmental stress in terms of alterations in ecosystem function or ‘integrity’ has been argued by Cairns (1977). Production, the generation of biomass per unit area with time, has been suggested as a measure of the consequences of ecosystem disturbance, because it incorporates both individual growth and population survivorship (Waters, 1977; Downing, 1985). To date, however, only a few studies have investigated the effects of anthropogenic acidification on the production of freshwater benthic

METHODS Amphipods were sampled from 10 lakes located in the Haliburton-Muskoka region of south-central Ontario, an area susceptible to, and currently receiving, acidic precipitation (Dillon et al., 1978, 1987; Jeffries et al., 1979; LaZerte & Dillon, 1984; Neary & Dillon, 1988). Details concerning the location and limnology of the study lakes, as well as various attributes of these Hyalella populations, are presented elsewhere (e.g. France, 1987a,b, 1992a,b; France & Stokes, 1988). In brief, Red Chalk is a double-basined lake with distinct inter-basin limnological (P. Dillon, Ont. Min. Environ., unpubl. data, 1987) and biological (France, 1987a, 1990;

Present address: Department of Biology, McGill University, 1205 Ave Dr Penfield, Montreal, Quebec, Canada H3A 1Bl. 189

190

R. L. France

France & Stokes, 1988) differences. Red Chalk Main, Red Chalk Bay, Blue Chalk, Harp and Little Clear lakes are circumneutral (pH 6.3-6.5, alkalinity 3.24.4 mg liter-‘). Dickie and Gullfeather lakes are slightly acidic (pH 5.8-6.0, alkalinity 0.4-1.5 mg liter-‘) which is probably a natural condition indicated by their higher colour (mean of 47 Hazen Units) compared to the other lakes (mean of 17 Hazen Units). The most acid lakes, Crosson and Heney, have average annual pH values of 5.5-5.7 (alkalinity 0.2-0.4 mg liter-‘) which, however, can decrease to below 5.0 during spring snowmelt (P. Dillon, Ont. Min. Environ., unpubl. data, 1987; Harvey, 1982), a phenomenon that is absent in the other lakes. Possibly as a result, both Crosson and Heney lakes have experienced numerous biological changes related to chronic anthropogenic acidification (Allison & Harvey, 1981; Harvey, 1982; Rooke & Mackie, 1984; Servos et al., 1985; Sun & Harvey, 1986; Trippel & Harvey, 1987; Shaw & Mackie, 1989; France, 1990, 1993~; France et al., 1991). Glen Lake is a hardwater system (pH 7.2, alkalinity 58.1 mg liter-‘) located within a dolomite drainage basin. Hyalella were collected with a hand-held corer (7.62 cm diameter) at water depths of 0.14.7 m from two to three regions of dense macrophyte (Ericaulon septangulare) growth, at a frequency of 613 times during the ice-free seasons of 1984 and 1985, as described in detail in France and Stokes (1988) and France (1990, 1992a, 1993a). The relationship between head length and dry weight (France, 1993a) was used to convert numbers to biomass, as in Mathias (1971). Production was calculated, as described in detail in France (1993a), by the size-frequency method, the most common procedure used for studies of Hyalella (Lindeman & Momot, 1983; Dehdashti & Blinn, 1991; Gibbons & Mackie, 1991; Edwards & Cowell, 1992; Wen, 1992). Biomass and production data for these amphipod ‘sub’-populations (i.e. sampling restricted to only those regions of macrophytic growth as described in France, 1990) were examined in two ways. Data for eight of these sub-populations are from France (1993a) and are expressed on a per m* basis. New data for Harp and Glen lakes have been similarly calculated and added for the present analysis. Because Hyalella density is strongly affected by macrophyte biomass (France & LaZerte, 1987; France & Stokes, 1988), data for the eight subpopulations were also expressed as per-g macrophyte biomass obtained from France (1993b). Again, new data for Harp and Glen lakes have been similarly calculated and added for the present analysis. Therefore, some of the present data have appeared previously, albiet not identified to the lake source, as in the present case. These earlier papers were concerned solely with comparisons of data from eight of the populations with those from other geographic regions (France, 1993a) or to understanding the inter-relationships among the variables that comprised production in eight of the populations (France, 1993b); potential influences of lake acidification were not mentioned in the original

papers. Here, the objective was to determine if the biomass and production of Hyalella displayed a gradient in relation to categories of lake acidification status (anthropogenically acidified, naturally acidified, circumneutral and hardwater) or to rankings of alkalinity such as found previously for abundance (France, 1992a), rather than to develop precise empirical predictions.

RESULTS

AND DISCUSSION

The mean annual biomass of Hyalella from macrophyte areas was found to be lowest in anthropogenically acidified Crosson Lake (0.4 g m-*) and highest in hardwater Glen Lake (1.4 g m-*) (Fig. 1, upper panel). Likewise, production ranged from 1.2 g m-* per year in Crosson Lake to 3.6 g m-* per year in Glen Lake (Fig. 1, lower panel). Hyalella abundance has previously been shown to be related to rankings of lake acidification status (France, 1992a). Similarly, rankings of area1 amphipod biomass and production were found here to be correlated (Kendall’s t=0.50 and 0.62, respectively) to rankings (Fig. 1) of lake alkalinity. Average macrophyte-normalized biomass and production of Hyalella

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Fig. 1. Relationship

of areal biomass and production of HyaShield lakes in south-central Ontario, ordered (from left to right) in terms of increasing alkalinity: (m) anthropogenically acidified lakes Heney and Crosson, (a) naturally acidic lakes Dickie and Gullfeather, (A) circumneutral lakes Blue Chalk, Red Chalk Main, Red Chalk Bay, Harp and Little Clear and (V) hard-

Iellu azteca from macrophyte beds in 10 Canadian

water Glen Lake. Data for lakes l-7 and 9, non-itemized for source, are from France (1993~). Data for lakes 2 and 8 are for 1985, whereas data for the other lakes are averages for 1984 and 1985.

Biomass and production of amphipods

showed a gradient in response to ranked groupings of lake alkalinity (Fig. 2). Estimates of both macrophytenormalized biomass and of production for Hyalella in the anthropogenically acidified lakes (Crosson and Heney) were found to be significantly different @ < 0.001, t-test) compared to those for the hardwater lake (Glen). With respect to the total littoral zoobenthos

m 0 m

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Fig. 2. Comparison of macrophyte-normalized biomass and production of HyaIellu azteca in 1985 and 1984 (when available, see Fig. 1) for anthropogenically acidified (n = 3), naturally acidic (n = 4), circumneutral (n = 9) and hardwater (n = 2) lake-years. Error bars represent f 2 SE about mean estimates to compensate for pseudo-replication of different years for individual lakes. Biannual averaged data for eight of these lakes. non-itemized for source, are from France (1993b).

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biomass (+SD) of communities of the study lakes. Sample sizes and lake groupings are the same as those in Figs 1 and 2. Biomass data for other zoobenthos organisms are from France (1990).

191

community (France, 1990), there was a gradient in the proportional biomass of Hyalella in relation to the lake alkalinity groupings (Fig. 3). Therefore, amphipods behave similarly to gastropods and turbellarians and opposite to odonates and hydracarinids in these lakes (France, 1990) in terms of their response to differences in alkalinity. The present results for amphipods support the earlier research of Rooke and Mackie (1984) on molluscs in suggesting that the population productivity of acid-sensitive benthic macroinvertebrates may be reduced in the littoral zones of low-alkalinity Ontario lakes exposed to anthropogenic acidification. Waters (1977) considered such measurements of secondary production to be reflective of ecosystem ‘health’, implying, therefore, in the present case, that both Heney and Crosson lakes can be referred to as being ‘unhealthy’, a result consistent with research on other macroinvertebrates and fishes in these systems. Benke (1984) believed that secondary production ‘can provide considerable insight into understanding the ecosystem-level consequences of various stresses’. Due to the variable nature of the responses of the components that comprise production rates, it is doubtful, however, that such measures will provide considerable insight into the mechanisms of stress on an individual population level basis (France, 19936). In the present example, the decreased rates of amphipod production in the anthropogenically acidified lakes are more closely associated with alterations in Hyalella density than with growth rates (France, 1993b). Therefore, because the present dynamic production rates so closely match those of previous measures of static densities (France, 1992a), the author remains unconvinced that the labour-intensive generation of such production estimates provides any further insight into either the mechanistic causes or to the predictive consequences of acidification damage that cannot be gleaned from a careful analysis of the abundance data alone. This is not to say, however, that production rates are in themselves valueless, especially if the research is directed, as Benke (1984) implied, toward more process-oriented questions such as material cycling between trophic categories (e.g. Milstead & Threlkeld, 1986) or to tracing contaminant flow (e.g. Stephenson & Mackie, 1989). However, in the context of simply describing reductions in ecosystem ‘health’ (sensu Waters, 1977), because of logistic difficulties in generating production rates and the resulting rarity of any cross-system comparisons of these measures (France, 1989), studies such as the present one and those of Rooke and Mackie (1984) and Griffith et al. (1993) are probably of a more academic interest, rather than a pragmatic or biomonitoring utility.

ACKNOWLEDGEMENTS

Logistical assistance from, and profitable discussions with P. Welbourn, T. Howell, N. Yan, R. Hall, D. Jackson, G. Krantzberg, N. Collins, P. Dillon, R. Reid, B. LaZerte, L. Harding, P. Ashcroft-Moore and other

192 members

R. L. France of the University

of Toronto-Dorset

community are greatly appreciated. for reviewing the manuscript.

A. Locke

research is thanked

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