Biotic Recovery from Acid Deposition 20 Years after the 1990 Clean

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Brooktrout Lake Case Study: Biotic Recovery from Acid Deposition 20 Years after the 1990 Clean Air Act Amendments James W. Sutherland† Division of Water, New York State Department of Environmental Conservation, 625 Broadway, Albany, New York 12233, United States

Frank W. Acker Patrick Center for Environmental Research, Academy of Natural Sciences of Drexel University, 1900 Benjamin Franklin Parkway, Philadelphia, Pennsylvania 19103, United States

Jay A. Bloomfield† Division of Water, New York State Department of Environmental Conservation, 625 Broadway, Albany, New York 12233, United States

Charles W. Boylen* Darrin Fresh Water Institute and Department of Biology, Rensselaer Polytechnic Institute, Troy, New York 12180, United States

Donald F. Charles Patrick Center for Environmental Research, Academy of Natural Sciences of Drexel University, 1900 Benjamin Franklin Parkway, Philadelphia, Pennsylvania 19103, United States

Robert A. Daniels† Cultural Education Center 3140, New York State Museum, Albany, New York 12230, United States

Lawrence W. Eichler Darrin Fresh Water Institute, Rensselaer Polytechnic Institute, 5060 Lakeshore Drive, Bolton Landing, New York 12814, United States

Jeremy L. Farrell Darrin Fresh Water Institute and Department of Biology, Rensselaer Polytechnic Institute, 5060 Lakeshore Drive, Bolton Landing, New York 12814, United States

Robert S. Feranec Cultural Education Center 3140, New York State Museum, Albany, New York 12230, United States

Matthew P. Hare Department of Natural Resources, Cornell University, Ithaca, New York 14853, United States

Sharon L. Kanfoush Department of Geology, Utica College, Utica, New York 13502, United States Received: July 30, 2014 Revised: January 16, 2015 Accepted: January 26, 2015

© XXXX American Chemical Society

A

DOI: 10.1021/es5036865 Environ. Sci. Technol. XXXX, XXX, XXX−XXX

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Environmental Science & Technology

Richard J. Preall Division of Fish and Wildlife, New York State Department of Environmental Conservation, P.O. Box 296, Ray Brook, New York 12977, United States

Scott O. Quinn† Division of Water, New York State Department of Environmental Conservation, 625 Broadway, Albany, New York 12233, United States

H. Chandler Rowell Division of Water, New York State Department of Environmental Conservation, 625 Broadway, Albany, New York 12233, United States

William F. Schoch Division of Fish and Wildlife, New York State Department of Environmental Conservation, P.O. Box 296, Ray Brook, New York 12977, United States

William H. Shaw† Science Division, Sullivan County Community College, Loch Sheldrake, New York 12759, United States

Clifford A. Siegfried† Cultural Education Center 3140, New York State Museum, Albany, New York 12230, United States

Timothy J. Sullivan E&S Environmental Chemistry, Inc., P.O. Box 609, Corvallis, Oregon 97339, United States

David A. Winkler Darrin Fresh Water Institute and Keck Water Research Laboratory, Rensselaer Polytechnic Institute, Troy, New York 12180, United States

Sandra A. Nierzwicki-Bauer* Darrin Fresh Water Institute and Department of Biology, Rensselaer Polytechnic Institute, 5060 Lakeshore Drive, Bolton Landing, New York 12814, United States S Supporting Information *

ABSTRACT: The Adirondack Mountain region is an extensive geographic area (26,305 km2) in upstate New York where acid deposition has negatively affected water resources for decades and caused the extirpation of local fish populations. The water quality decline and loss of an established brook trout (Salvelinus fontinalis [Mitchill]) population in Brooktrout Lake were reconstructed from historical information dating back to the late 1880s. Water quality and biotic recovery were documented in Brooktrout Lake in response to reductions of S deposition during the 1980s, 1990s, and 2000s and provided a unique scientific opportunity to re-introduce fish in 2005 and examine their critical role in the recovery of food webs affected by acid deposition. Using C and N isotope analysis of fish collagen and state hatchery feed as well as Bayesian assignment tests of microsatellite genotypes, we document in situ brook trout reproduction, which is the initial phase in the restoration of a preacidification food web structure in Brooktrout Lake. Combined with sulfur dioxide emissions reductions promulgated by the 1990 Clean Air Act Amendments, our results suggest that other acidaffected Adirondack waters could benefit from careful fish re-introduction protocols to initiate the ecosystem reconstruction of important components of food web dimensionality and functionality.



INTRODUCTION Atmospheric sulfur deposition rates have decreased substantially over the past three decades across large portions of eastern North America and Europe,1,2 which is attributable to national and international environmental regulations and agreements

including the Clean Air Act (CAA) and its 1990 Amendments (CAAA) in the United States, the Eastern Canada Acid Rain Program, and the United Nations Economic Commission for Europe’s Convention on Long-Range Transboundary Air Pollution. In response, regional declines in surface water B

DOI: 10.1021/es5036865 Environ. Sci. Technol. XXXX, XXX, XXX−XXX

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Environmental Science & Technology

the lake;13−16 no other fish species were observed or netted in these surveys. Surveys in 1984 and 1985 captured no fish.17 The collective fisheries data suggest that brook trout disappeared from the lake between 1975 and 1984.

SO42− concentrations have occurred, and both acid-neutralizing capacity (ANC) and pH have increased to some extent in many lakes and streams.1−4 Data from northern Europe and eastern Canada are showing limited signs of biotic recovery.3−6 Water quality improvements have advanced to the extent that rates and trajectories of biological recovery, albeit on a limited basis, are being documented.7,8 About 1500 Adirondack lakes and ponds were surveyed during the 1980s.9 Of the waters above 600 m elevation, 54% had a pH below 5.5 and represented both naturally acidified brownwater and anthropogenically acidified clear-water lakes; 25% were fishless. Brooktrout Lake, in the southwestern region of Adirondack Park, is typical of thin-till, low dissolved organic carbon, Adirondack waters that have been culturally acidified10 and in which fish have been extirpated by acid deposition. Moreover, Brooktrout Lake represents a unique multigeneration case history within Adirondack Park in which we have documented the following events: (1) the long-term extirpation of a viable and healthy brook trout (Salvelinus fontinalis [Mitchill]) fishery in response to the impact of acid deposition on water quality; (2) improvements in water quality and ecosystem biota in response to reduced sulfur dioxide emissions promulgated by the 1990 CAA Amendments; (3) the re-establishment in the lake of a population of brook trout; and (4) self-sustaining in situ reproduction in the brook trout population, which is the initial phase in the restoration of a preacidification food web structure and functionality. The decline and extirpation of brook trout from Brooktrout Lake were documented from an extensive search of New York State Department of Environmental Conservation (NYSDEC) historical fishery records. These records and additional information obtained from other sources also provided the documentation of water quality decline in the lake throughout the 1900s. In 1894, Wallace11 described Brooktrout Lake as one of dozens or more waters in the region where “crystal depths swarm with speckled-trout of superior weight and quality”. Subsequent water chemistry changes and the decline and eventual elimination of brook trout during the 1900s in response to acid deposition were documented from historical information (Table 1). Fishery data from a May 1936 angling report stated a



METHODS Brooktrout Lake Description. Brooktrout Lake is located in the southwestern region of the Adirondack Park in Hamilton County, within the Oswegatchie/Black drainage basin, at an elevation of 722 m (AMSL) with the lake outflow situated at latitude 43°36′00″ and longitude 74°39′45″. The lake is a clear-water, moderate-sized (30 ha, 24.5 m depth), headwater system, with a steep-sloped, densely forested (95% conifers, 5% deciduous) watershed (176.9 ha) having no permanent inflowing tributaries. The mean annual precipitation, snowfall, and runoff for the watershed were estimated at 90.9, 29.7, and 77.5 cm of water, respectively.18 Field and Laboratory Methods. Brooktrout Lake was monitored intermittently in the 1980s by the NYSDEC. From 1994 to 2006, the lake was monitored twice each midsummer by the Adirondack Effects Assessment Program (AEAP), which was designed to evaluate long-term effects of the 1990 Clean Air Act Amendments on the biota of acid-affected lakes.19 From 2006 to 2012, the lake was sampled at least three times yearly from late June through early September. Collections at Brooktrout Lake included samples for water chemistry, depth profiles of temperature, dissolved oxygen (concentration/saturation), light and samples for phytoplankton, zooplankton, benthos, macrophytes, and fish (Supporting Information Table S1). Water samples were collected at the same time as sampling for phytoplankton and zooplankton to provide contemporaneous water chemistry data. Site visits occurred during midsummer thermal stratification, and samples were collected at the site of maximum depth. Sampling for benthos, macrophytes, and fish was more time-consuming and, therefore, conducted at different times. Analytical chemistry procedures followed standard methods (Table S2. Regional values for SO42− in wet deposition were obtained from the National Atmospheric Deposition Program (NADP) Web site20 for Bennett Bridge (NY52), which has a long-term record dating back to 1980. Phytoplankton. Phytoplankton samples were collected from the photic zone (surface to 1% light intensity) using an integrated hose technique. Samples were stored in amber 250 mL polyethylene bottles in a 3% gluteraldehyde/formaldehyde solution. For species identification and enumeration, samples were concentrated by centrifugation (20 min at 1000g) and Utermöhl sedimentation chambers (10 mL), examination with an inverted compound microscope, identification to lowest possible taxon (at up to 1500× magnification), and enumeration of random fields. Five hundred natural units (colonies or individual cells) were identified and enumerated (at 645×) from each sample; large forms were identified and enumerated at low power (150×). Standard taxonomic references were used as described by Charles et al.21 Zooplankton. Replicate zooplankton samples were collected using a constant flow pump, 64 μm mesh net, integrated to the depth of the photic zone or 15 m. Samples were rinsed into 250 mL PE bottles, narcotized with CO2, and preserved with formalin. At least 100 L of water was pumped for each zooplankton sample from the center of the lake. Identifications were made to species whenever possible using standard taxonomic keys.19

Table 1. Fisheries Information Compiled for Brooktrout Lake since the Late 1800s, Documenting the Decline and Extirpation of the Resident Brook Trout Population date

source (ref)

1894 Wallace11

1936 Morgan12 1950 Pfeiffer13 1964 Brewer14 1969 Lantiegne and Wich15 1975 Morehouse16 1984 ALSC17 1985 ALSC17

fishery information described Brooktrout Lake as one of dozens or more waters in the region where “crystal depths swarm with speckled-trout of superior weight and quality” “good” brook trout catch excellent brook trout catch (= 60); population self-sustaining; good arthropod diet similar netting effort to Pfeiffer, but smaller catch (= 32); population self-sustaining only 6 fish netted; population appears selfsustaining only 2 fish netted; no evidence of reproductive success no fish netted no fish netted

“good catch” of brook trout averaging about 0.45 kg.12 Major surveys conducted in the 1950s, 1960s, and 1970s documented the decline of brook trout density and reproductive potential in C

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Table 2. Historical Water Quality Information Compiled for Brooktrout Lake Documenting the Decline of Chemical, Physical, and Biological Conditions from Acid Deposition date

source (ref)

study type

chemical

1920s Uutala, 1987

30

sediment core inferred acidity increase

1940s Uutala, 1987

30

sediment core inferred acidity increase

1950 Pfeiffer, 195013 1950s Rowell, unpublished 1960 Smol, unpublished

physical

chironomid stratigraphy; decline in Microspectra and Heterotrissocladius changi after 1920 chironomid stratigraphy; increase in Zalutschia cf. briani and Tanytarsus after 1940

water column first field pH (colorimetric) 6.0 sediment core inferred acidity increase sediment core inferred acidity increase

Secchi = 11.8 m

Secchi = 11.0 m

1975

Morehouse, 197516

water column

1975 1984

Wood, 197833 ALSC, 198517

water column water column

1984

Sutherland, 198918

water column

1987

Sutherland, unpublished water column

1988

Sutherland, unpublished water column

biological

diatom stratigraphy; appearance of Fragilariforma acidobiontica chrysophyte stratigraphy; decline in Mallomonas “small”, M. acaroids, and M. punctifera; increase in M. hamata; decline in Synura spinosa; increase in S. echinulata and S. petersenii

midsummer surface pH 4.99; SO42− concn = 118.1 μequiv L−1 midsummer surface pH 4.92 midsummer av surface pH 5.10; SO42−concn = 114.3 μequiv L−1 midsummer surface pH 4.83; SO42− concn = 124.0 μequiv L−1; high dissolved oxygen concentration

Secchi = 15+ m Secchi = 7.5 m

chl a 2.12 μg L−1 9 phyto spp. 3 rotifer spp; 3 crustacean spp. av Secchi = 10.7 m av chl a = 0.54 μg L−1 av rotifer spp. = 2 av crustacean spp. = 2 Secchi = 8.5 m

midsummer av surface pH 5.16; av SO42− concn = 116.0 μequiv L−1; high dissolved oxygen concentration midsummer surface pH 5.16; Secchi = 9.0 m SO42− concn = 134.0 μequiv L−1; high dissolved oxygen concentration

Statistical Methods. Although Brooktrout Lake was sampled on multiple occasions since 1984, only the midsummer (July, August) values for chemistry, productivity analytes, and biota were analyzed and described here. The midsummer period of thermal stratification in Brooktrout Lake represents the lowest seasonal variance within the ecosystem, and data from this period can be used to assess interannual variability and to detect trends. In addition to field data collected by the authors associated with this project, data collected by the Adirondack Lakes Survey Corporation (ALSC) on 52 Adirondack lakes, including Brooktrout Lake, also were evaluated.22 Individual values collected during the 29 year period were compared with linear trend analysis using the least-squares method, and the means for the 1980s and 2010−2012 data were tested for significant differences using an unpaired t test. Fish Stocking. During late October 2005, 19 adult Horn Lake heritage strain brook trout (length range = 220−445 mm) netted, then marked, from nearby Tamarack Pond were introduced into Brooktrout Lake; at least two fish were identified as females. In early November 2006, 2000 marked Horn Lake heritage strain brook trout fingerlings (102−152 mm), raised in a regional hatchery were also released into Brooktrout Lake. Helicopter stocking was the only means of introducing fish to Brooktrout Lake because it is located in a remote wilderness area and the outlet stream characteristics (steep elevation change, hydraulic barriers such as waterfalls) preclude upstream migration. Changes in water quality and all levels of water column biota (phytoplankton, rotifers, and crustacean zooplankton) were monitored on a monthly basis (May−October 2005− 2012) following the introduction of fish to the lake. Additional stockings of 900 and 1100 marked Horn Lake heritage strain fingerlings occurred during 2006 and 2007, respectively. Fish Sampling. Fish were sampled to assess their condition and to determine if spawning occurred. Between 2007 and 2012 fish were collected with Adirondack trap nets set perpendicular to shore with opening set 1−1.5 m deep. The lead on these traps was 23 m, wings were 3 m, and frame area opening was 1.5 m2;

chl a < 0.1 μg L−1; phytos are 100% pyrrhophytes

chl a = 0.49 μg L−1 rotifer spp. = 5 crustacean spp. = 3

however, the distance from shore of the set was determined by the depth of the opening and not the length of the lead.23 Traps were the preferred method of capturing fish because their use minimized the amount of stress on captured fish; gill net captures invariably resulted in the sacrifice of the fish. The nets were set in spring and/or autumn when air and water temperatures were lower and the lake unstratified, again to minimize stress on captured fish.24 Small mesh gill nets were set perpendicular to shore in late spring from 2010 to 2012, specifically to capture young fish. The nets were 7.5 m long and 1.5 m deep, and mesh was 13 mm bar and set to a depth of 5 m. Nets were pulled at 24 h. After capture, fish were measured to nearest mm standard length (SL) and checked for clipped fins, the method of marking used on hatchery fish stocked in the lake. Unmarked fish were sacrificed in 2010 to conduct isotope and genetic analysis; in subsequent years, all fish were released. The use of trap nets and gill nets yielded captures of fish of different size classes. In spring, shorelines were examined for spawning activity and the development of redds. In April and June 2012 fish observed in the littoral zone of the lake with parr marks were photographed. Fish Collagen Determinations. Fish collagen (the main structural protein of connective tissues) from wild caught, mixed history, and hatchery fish and samples of state hatchery food were analyzed using carbon and nitrogen isotope analysis to distinguish the source of diet.25 To obtain bone collagen stable isotope values, we followed the general methodology described in a prior study.26 Briefly, dermestid-cleaned vertebrae were washed in distilled water to remove any adhered materials. The vertebrae then were placed into 0.5 N HCl at room temperature to remove the mineral portion of the bone, generally about 24 h. Samples were rinsed with distilled water and then decanted, after the mineral portion of the bone was fully dissolved. To remove any lipids, these samples were placed in a mixture of chloroform, methanol, and water (ratio of 2:1:0.8 by volume) as described in the literature.27 Once the lipids were removed, the samples were washed, gelatinized, and freeze-dried. Collagen samples then were loaded into tin cups and analyzed using a Carlo Erba D

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Table 3. Midsummer Values and Net Change of Acidification and Productivity Analytes in the Epilimnion of Brooktrout Lake from the 1980s through 2010−2012a analyte

(a) 1980s mean (±SD)

(b) 2010−2012 mean (±SD)

(b) − (a) net change (Δ)

significance level (p)

[H+] (μequiv L−1) ANC (μequiv L−1) SO42− (μequiv L−1) NO3− (μequiv L−1) total P (μg L−1) DOC (mg L−1) Ca (μequiv L−1) Secchi (m) chl a (μg L−1) reactive silica (mg L−1) total Al (μM L−1) labile monomeric Al (μM L−1) [IMA]

8.15 (2.54) −1.90 (10.31) 118.18 (9.16) 17.06 (7.36) 3.29 (1.80) 0.71 (0.49) 68.22 (7.56) 8.89 (1.97) 0.85 (0.68) 3.31 (0.21) 19.11 (7.13) 12.17 (2.93)

1.30 (0.26) 11.73 (3.77) 52.09 (3.88) 7.52 (2.43) 4.00 (2.09) 2.40 (0.46) 41.65 (12.46) 5.92 (0.66) 1.86 (1.04) 2.39 (0.28) 7.52 (3.10) 1.02 (0.77)

−6.85 +13.63 −66.09 −9.54 +0.71 +1.69 −26.57 −2.97 +1.01 −0.92 −11.59 −11.15