Ecotoxicology

, Volume 17, Issue 2, pp 117–131

Mercury and drought along the lower Carson River, Nevada: II. Snowy egret and black-crowned night-heron reproduction on Lahontan Reservoir, 1997–2006

Authors

  • Elwood F. Hill
    • Forest & Rangeland Ecosystem Science CenterU.S. Geological Survey
  • Robert A. Grove
    • Forest & Rangeland Ecosystem Science CenterU.S. Geological Survey
Article

DOI: 10.1007/s10646-007-0180-y

Cite this article as:
Hill, E.F., Henny, C.J. & Grove, R.A. Ecotoxicology (2008) 17: 117. doi:10.1007/s10646-007-0180-y

Abstract

Mercury concentrations in the floodplain of the Carson River Basin in northwestern Nevada are some of the highest ever reported in a natural system. Thus, a portion of the basin including Lahontan Reservoir was placed on the U.S. Environmental Protection Agency’s Natural Priorities List for research and cleanup. Preliminary studies indicated that reproduction in piscivorous birds may be at risk. Therefore, a 10-year study (1997–2006) was conducted to evaluate reproduction of snowy egrets (Egretta thula) and black-crowned night-herons (Nycticorax nycticorax) nesting on Gull Island in Lahontan Reservoir. Special attention was given to the annual flow of the Carson River, the resultant fluctuation of this irrigation reservoir, and the annual exposure of snowy egrets and night-herons to methylmercury (MeHg). The dynamic character of the river due to flooding and drought (drought effect) influenced snowy egret and night-heron reproduction more so than did MeHg contamination of eggs. During an extended drought (2000–2004) in the middle of the study, snowy egret nests containing eggs with concentrations of MeHg (measured as total mercury [THg] ∼ 100% MeHg) ≥0.80 μg THg/g, ww, all failed, but in 1997 and 2006 (wet years with general flooding), substantial numbers of young were produced (but fewer than at nests where eggs contained <0.80 μg/g). Thus, a variable reproductive threshold of tolerance to MeHg may be associated with habitat quality (food type and abundance). Clearly, drought was the most important factor affecting snowy egret annual productivity. In contrast to snowy egrets, night-herons generally had fewer nests meeting the 0.80 μg THg/g criterion, and those above the criterion were less sensitive to mercury than were snowy egrets. Furthermore, night-herons appeared more tolerant of drought conditions than snowy egrets because they nested earlier, selected more protected nesting sites, and had a more generalist diet that provided additional food options including terrestrial organisms, which also reduced exposure to MeHg. A putative biological effect threshold of 2.0 μg THg/g in whole blood for young of both species was evaluated, which was frequently exceeded, but with no evidence, while still in the colony, of an association with direct mortality. An evaluation of physiological associations with blood residues and post-fledging survival will be presented in future reports in this series.

Keywords

MercurySnowy egretReproductionBlack-crowned night-heronMiningDrought

Introduction

Approximately 6.8 × 106 kg of liquid mercury (Hg0) were released in mill tailings into the Carson River and its tributary canyons below Virginia City, Nevada during the Comstock Lode era of 1859–1890 (Smith 1943). Erosion has since washed a large portion of the contaminated tailings into the floodplains and wetlands of the Carson River Basin and the Lahontan Valley (a.k.a. Carson Sink), the terminus of the Carson River (Fig. 1; Van Denburgh 1973; Hoffman and Thomas 2000). However, since 1915 and completion of Lahontan Dam, the resultant 27-km long irrigation reservoir has served as a sink for most of the sediment-bound mercury washed downstream (Hoffman and Taylor 1998). Though the reservoir has spared the agricultural and wetlands of the Lahontan Valley from substantial mercury contamination for nearly a century, mercury concentrations in some of the streambanks and floodplain sediments in the Carson River Basin including Lahontan Reservoir are some of the highest ever reported in a natural system (Wayne et al. 1996).
https://static-content.springer.com/image/art%3A10.1007%2Fs10646-007-0180-y/MediaObjects/10646_2007_180_Fig1_HTML.gif
Fig. 1

Carson and Truckee River Basins in Nevada and California (USGS map modified from Lawrence 1998)

The persistence and degree of mercury contamination of the lower Carson River system (LCRS) has led to placement of a portion of the Carson River Basin including Lahontan Reservoir on the U.S. Environmental Protection Agency’s (EPA) National Priorities List (“Superfund”) for research and cleanup. Studies under this program showed high levels of mercury throughout key ecological components of the LCRS, and particularly in top trophic level piscivorous fish and birds (Ecology and Environment, Inc. 1998). The potential toxicity of these mercury concentrations to piscivorous birds was demonstrated in 1997–1998 through detection of cellular damage (i.e., histopathologic and physiologic) in the nervous, immune, hepatic, and renal systems of young snowy egrets (Egretta thula), black-crowned night-herons (Nycticorax nycticorax) (hereafter, night-herons), and double-crested cormorants (Phalacrocorax auritus) at about the time of fledgling (Henny et al. 2002). This study also suggested reproductive effects on snowy egrets when methylmercury (MeHg) residues in eggs (measured as total mercury [THg] ∼ 100% MeHg) exceeded 0.80 μg/g, wet weight (ww). In the same study, night-heron reproduction appeared normal for nests with egg residues of 0.80–1.8 μg THg/g.

The apparent species differences in sensitivity to mercury and uncertainties about natural influences on exposure in the LCRS indicated the need for additional research on the reproduction of fish-eating birds, especially the snowy egret (Henny et al. 2002). Of special interest, the initial nesting studies were conducted during the good water years of 1997 and 1998 (Fig. 2; Henny et al. 2002); whereas, the Carson River system is intermittently subject to extreme years of flooding and drought (Henny et al. 2007). THg concentrations in water above this reservoir were directly associated with Carson River annual water discharge. Furthermore, MeHg concentrations in water below the reservoir, although about 10-fold lower than above the reservoir (the reservoir is a sink for mercury), were directly related to annual concentrations of MeHg in both night-heron and snowy egret blood, in addition to MeHg in night-heron eggs. Thus, with annual changes in MeHg exposure and water levels (habitat conditions), it was not known how wading birds respond via nesting numbers and reproductive success. In addition, the determination of whether a “mercury effect” can be separated from a “habitat condition effect” became an important issue.
https://static-content.springer.com/image/art%3A10.1007%2Fs10646-007-0180-y/MediaObjects/10646_2007_180_Fig2_HTML.gif
Fig. 2

Annual water discharge for Carson River, 1996–2006 (solid line) and total snowy egret nests located on Gull Island in Lahontan Reservoir, 1999–2006 (dashed line). Equation for inset relationship (Y = 63.089 − 0.123X, adjusted r2 = 0.502, P = 0.0296)

This study was continued with snowy egrets and night-herons through 2006, for a total of 10 nesting seasons. Though reproduction and exposure to mercury were continuously evaluated for both species, the snowy egret was considered at greatest risk due to the species greater sensitivity to MeHg in eggs and its near total diet of aquatic invertebrates and fish. Also, this small egret probes sediments for invertebrates and incidental sediment ingestion may be an important additional route of exposure. In contrast, the night-heron is a more diversified feeder on fish and a wide array of aquatic and terrestrial invertebrates and vertebrates (Henny et al. 2002).

This report evaluates annual nesting numbers and reproductive success of snowy egrets and night-herons at Gull Island in northeastern Lahontan Reservoir, the most mercury contaminated portion of the LCRS. Initially, per 1997–1998, our goal was to compare reproduction of the island colony at Lahontan Reservoir on the western perimeter of Lahontan Valley, a wetland colony on Carson Lake near the southern terminus of the Carson River, and a reference colony at Ryndon on the Humboldt River about 280 km to the northeast (Fig. 1). However, severe drought from 2000 through 2004 forced abandonment of the Carson Lake study area (Fig. 2). The essence of this report is on the period of 1999–2006 with appropriate reference to the initial 1997 and 1998 study (Henny et al. 2002).

Throughout the study of 10 consecutive reproductive cycles of snowy egrets and night-herons nesting on Gull Island in Lahontan Reservoir, the specific objectives of this paper were to: (1) evaluate the relationship between reproduction of the two species and mercury residues measured as THg in eggs using the “sample egg” technique (Blus 1984); (2) evaluate the relationship between reproduction of the two species in relation to the dynamic character of the Carson River’s annual flow and reservoir fluctuation (water conditions); and finally (3) evaluate the relative contribution of both mercury concentrations in eggs and habitat conditions on the reproduction of nesting populations, including size of the nesting populations.

Materials and methods

Study sites

Field surveys and sampling, per 1997–1998 (Henny et al. 2002), as reported herein were restricted to the mixed-species nesting colony on Gull and Evans Islands in the northeastern portion of Lahontan Reservoir, western Churchill Co., NV, and a similar nesting colony at our reference site about 16 km east of Elko, NV on the Humboldt River in central Elko Co., NV (Fig. 1).

Lahontan reservoir

Snowy egrets and night-herons nest primarily in the main stand of saltcedar (tamarisk; Tamarix sp.) on the eastern perimeter of Gull Island just above the high water mark when the reservoir is at capacity. During good water years, the saltcedar was nearly impenetrable and provided protection of eggs and nestlings from avian predators such as ring-billed and California gulls (Larus delawarensis and Larus californicus) that nest in large, dense colonies on the open ground. However, during drought years, the foliage in the main saltcedar stand was comparatively sparse with many snowy egret nests exposed to mid-day sun, high winds and possible avian predation. Smaller younger clusters of more heavily foliated saltcedar flourish along the southern and southwestern perimeter (lower elevation) of Gull Island and were favored for nesting by night-herons, but not by snowy egrets.

Evans Island, located about 0.4 km to the northeast is similar to Gull Island, but is much closer to the mainland (∼0.26 vs. 1.10 km). Much of the open ground on Evans Island was also used by nesting gulls. Night-herons nested in the perimeter saltcedar strands. Snowy egrets did not nest on Evans Island.

Neither Gull nor Evans Island were well vegetated around their perimeters due to extreme annual and temporal fluctuations in the water level of this irrigation reservoir, with water levels receding as the reproductive season progresses. Vegetated shallows around the islands that would normally harbor prey for wading birds were generally absent by the time the young snowy egrets and night-herons left their nests to forage. Therefore, both species, but especially the snowy egret that hatches about 2–4 weeks later than the night-heron, were dependent upon their parents for food while on the island.

Humboldt River-Ryndon

The mixed-species nesting colony on the Humboldt River was located in a dense stand of willows (Salix sp.) within the flood plain, but was separated from the river by a densely vegetated sandbar. The colony was comprised of great (Ardea alba), snowy and cattle egrets (Bubulcus ibis), and night-herons and was mostly located over water.

Egg sampling and nest success

Gull and Evans Islands were surveyed for nests of night-herons and snowy egrets from the time of the species’ spring arrival through the time the young began to leave their nest at about 2–3 weeks of age. All nests were marked and evaluated for progress at about weekly intervals. One randomly selected egg was removed from each of the first 10–15 clutches per species for estimate of clutch completion date, embryonic development and THg residues. The reference area was heavily sampled for THg residues during the first year (1997) of the study to define the control norm (Henny et al. 2002, 2007). Eggs were transported at ambient temperature to the laboratory and then refrigerated intact pending evaluation and preparation for shipment to the designated laboratory for THg analysis. Each egg was weighed, its volume determined (by water displacement), and was inspected for stage of development. Contents were transferred to a chemically clean jar, weighed, and then frozen in a standard freezer until shipped.

Bird sampling

Blood was collected from night-herons and snowy egrets at about 2–3 weeks of age to determine their level of mercury exposure at the time they leave the nest, but still depend on adults for food. The goal was to sample a minimum of 10 birds of each species per year at Lahontan Reservoir and the reference area. Our criteria for specimen selection for blood samples was that either bill length or body mass would exceed 5.5 cm or 600 g for night-herons and 4.0 cm or 250 g for egrets. The basic procedure was to capture the young on the nest or nearby, measure its bill length to estimate its age in days (Custer and Peterson 1991), check its weight, draw a blood sample and then return it to its nest. Blood samples (∼2 ml) were drawn by jugular venipuncture (23 ga needle) into a 4.5 ml lithium-heparinized bead Monovette® syringe. The sample was gently inverted several times for mixing with heparinized beads and immediately stored on wet ice for transport. The samples were then mixed on an electric rocker for 5 min and ∼0.5 ml was preserved in a 2.5-ml cryotube for storage in a standard freezer until analyzed.

Analytical chemistry

All samples were analyzed by laboratories under contract to the EPA. Mercury tissue analyses for years 1997 and 1998 were reported in Henny et al. (2002). Since eggs and blood contain essentially 100% MeHg (Henny et al. 2002), they were only analyzed for THg. Blood and egg samples were analyzed for THg at ToxScan Inc. (Watsonville, CA) using EPA methods 245.7 (1999, 2001, 2004, 2005) and 7471 (2000, 2002, 2003) of the EPA 6000/7000 series methods, with solids determination done using EPA method 160.3. Blood and eggs in 2006 were analyzed for THg at EPA Region 9 Laboratory (Richmond, CA) using EPA methods 245.1 and 7473/SOP535. All Hg concentrations are reported in μg/g (ww) except as noted. Egg residue concentrations were adjusted to fresh ww based on egg volume (Stickel et al. 1973). Quality assurance and quality control were acceptable at each of the analytical laboratories according to EPA guidelines. Samples of double-distilled deionized water used for final rinse of surgical instruments and to check syringes and needles were analyzed each year for mercury contamination. Minimum analytical reporting limits for THg in blood and eggs ranged from 0.02 to 0.10 μg/g, ww.

Statistical procedures

Mercury residue concentrations were log-transformed for summarization as geometric means and for statistical analyses. Due to unequal sample sizes, the General Linear Models Procedure (SAS Institute 1999) was used for analysis of variance (ANOVA). Tukey’s Studentized Range Test was used to separate means. Regression analysis was often used to define relationships associated with annual reproductive parameters and water (habitat) conditions. If the relationship was not significant (P > 0.05), a hatched line (instead of solid line) was used in the figures. A chi-squared (χ2) test was used to evaluate nesting success in relation to mercury concentrations in sample eggs. Statistical significance was set at α = 0.05, except for regression analyses mentioned above.

Results and discussion

The dynamic Carson River system

In 2000, the first year of what became an extended drought, many wetlands throughout the LCRS began drying out and forced alteration in nesting of both the snowy egrets and night-herons. After successful nesting in 1997–1999, neither species formed its usual nesting colonies in the wetlands of Carson Lake in 2000–2004. A similar response to drought was observed periodically with white-face ibis (Plegadis chihi) at Carson Lake between 1972 and 1988 (Henny and Herron 1989). Only general observations were made for nesting activity at Carson Lake from 2002 to 2006.

Nesting was consistently attempted during the 10-year study by snowy-egrets and night-herons in the mixed-species colony on Gull Island in Lahontan Reservoir (Fig. 1). The water level of the reservoir and timing of its drawdown for surface irrigation were critical factors in reproductive success. Both the water level and the drawdown of the reservoir are contingent upon the annual flow of the Carson River, and may change radically with consecutive years of drought often occurring (Fig. 2). During the course of this study, the first 3 years (1997–1999) were at the end of a wet cycle, the next 5 years (2000–2004) were considered an extended drought (with 2001 the driest year), and the last two years (2005–2006) were a return to wetter conditions.

Though nesting was initiated each year, the general drought conditions of 2000–2004 clearly affected foraging options and nurturing of young through time of fledgling, and Lahontan Reservoir was not again filled to capacity until 2006. During the drought years, the water level on 1 June was 1.4–2.5 m below 1997–1999 levels (Henny et al. 2007). This did not allow the littoral zone to develop around the reservoir to its usual springtime potential as a feeding ground for wading birds nesting on Gull Island. The drought also eliminated the availability of expansive feeding grounds in the upstream shallows of the reservoir from the mouth of the Carson River to Silver Springs Bay and many wetlands throughout the Lahontan Valley.

Bioavailability of mercury in the LCRS

The annual discharge of the Carson River was positively correlated with the translocation of THg from the Carson Basin downstream of the Comstock Mining Area into the Lahontan Reservoir and subsequently affected the bioavailability of MeHg (in water below reservoir) to snowy egrets and night-herons nesting on Gull Island (Henny et al. 2007). Bioavailability of MeHg in the birds was determined for both species by monitoring THg in their eggs (Table 1) and in the bloods of young (Table 2).
Table 1

Total mercury (THg) concentrations (geo. mean, μg/g, ww) in eggs of snowy egrets and black-crowned night-herons from Lahontan Reservoir, 1997–2006 (after Henny et al. 2007)

Year

Snowy egret

Night-heron

THg (eggs)

N

% ≥0.80 μg/ga

THg (eggs)

N

% ≥0.80 μg/gb

1997

0.23 Cc

8

12.5

0.69 ABc

17

46.6

1998

0.50 BC

10

20.0

0.48 ABC

10

10.0

1999

0.43 BC

15

13.3

0.49 ABC

15

6.7

2000

0.48 BC

15

13.3

0.47 ABC

15

13.3

2001

0.40 BC

15

13.3

0.33 BC

15

13.3

2002

0.78 B

10

60.0

0.26 C

10

0

2003

0.61 B

10

20.0

0.29 BC

10

0

2004

0.36 BC

10

0

0.34 BC

10

0

2005

0.51 BC

10

10.0

0.22 C

10

10.0

2006

1.93 A

10

90.0

1.01 A

10

50.0

Note: Egg concentrations analyzed as total mercury, but residue is ∼100% methylmercury

aReference area: ≥ 0.80 μg/g = 1/58 (1.7%)

bReference area: n ≥ 0.80 μg/g = 0/28 (0.0%)

cColumns sharing a letter are not significantly different

Table 2

Total mercury (THg) concentrations (geo. mean, μg/g, ww) in whole blood of young snowy egrets and black-crowned night-herons from the Lahontan Reservoir, 1997–2006 (after Henny et al. 2007)

Year

Snowy egret

Night-heron

THg (blood)

N

% ≥2.0 μg/ga

THg (Blood)

N

% ≥2.0 μg/gb

1997

3.57 ABc

5

100

2.61 ABc

11

64

1998

4.66 A

2

100

3.06 AB

4

75

1999

1.72 CD

11

55

1.38 BC

10

20

2000

0.79 E

15

13

0.78 C

3

0

2001

1.16 DE

4

0

2.31 ABC

3

67

2002

1.47 DE

11

27

1.07 BC

10

20

2003

3.39 ABC

31

100

2.26 BC

7

71

2004

1.89 BCD

43

47

1.61 BC

6

33

2005

5.52 A

10

100

1.36 BC

10

50

2006

5.24 A

10

90

7.38 A

10

100

Note: Blood concentrations analyzed as total mercury, but residue is ∼100% methylmercury

aReference area: n ≥ 2.0 μg/g = 0/67 (0.0 %)

bReference area: n ≥ 2.0 μg/g = 0/37 (0.0 %)

cColumns sharing a letter are not significantly different

Eggs were sampled during nesting prior to reservoir drawdown and while nearby wetlands and shallows around the reservoir usually contained water. Eggs laid later in the season in 1999 were compared to these early eggs to determine if timing (early vs. late clutches) influenced MeHg concentrations; no significant difference was detected (Henny et al. 2007). THg residues in eggs also provided a biological reference to temporal changes in reproductive risk. For this purpose we present the proportional number of eggs (= nests) containing ≥0.80 μg THg/g, ww. This level was used as an estimator based on our studies of snowy egrets (Henny et al. 2002) as well as studies of other species (Heinz 1979; Newton and Haas 1988). Despite apparent differences in tolerance, we also used the 0.80 criterion as our biological reference for night-herons. In our 1997 study, night-herons tolerated higher egg residues than 0.80 μg THg/g, ww, without apparent effect on reproduction (Henny et al. 2002).

Blood from young was sampled ∼6 weeks after eggs were laid. Mercury in whole blood of young is an indicator of contamination at foraging sites used by adults within a few days prior to the blood sample. Young were bled when 13–27 days old; THg residues in blood were not affected by age over this span (Henny et al. 2007). Eggs were laid and collected while most wetlands were flooded; whereas, blood was sampled later while many wetlands were drying out, especially during drought such as 2000–2004. Blood THg also provided a biological reference point. We chose to use blood residue of 2.0 μg THg/g, which is an arbitrary half-value of the 4.0 μg THg/g considered “extra high” risk for the adult common loon (Gavia immer; Evers et al. 2004). The criteria of 2.0 μg THg/g in blood seemed reasonable because young snowy egrets and night-herons were more sensitive than adults to mercury toxicity (Henny et al. 2002).

Mercury in snowy egret eggs

THg concentrations in snowy egret eggs were not related to MeHg in water below the reservoir or to annual water discharge down the Carson River (as indirectly measured by acre feet of water in the reservoir; Henny et al. 2007). Over the 10-year study, THg residues in snowy egret eggs were not statistically different from 1998 to 2005 (Table 1). During this span, including five successive years of general drought throughout the LCRS (2000–2004), there was no apparent trend in egg THg associated with the irregular annual water discharge for the Carson River (Table 1; Fig. 2, see Henny et al. 2007, Table 5). In contrast, the Carson River flooded in 1997 and 2006 and produced the lowest and highest egg residues (geo. mean, 0.23 and 1.93 μg THg/g, ww), although 1997 had the lowest geometric mean, that year differed (statistically) only from 2002, 2003 and 2006 (Table 1).

We concluded that when the flow of the Carson River remains within its main channel, regardless of whether it is a good or poor water year, snowy egrets (feeding almost exclusively on aquatic organisms) received a comparatively constant exposure to mercury when foraging in primary wetlands during spring runoff. For example, the geometric means for THg in snowy egret eggs between 1998 and 2005 varied from 0.36 (2004) to 0.78 μg THg/g, ww (2002) (Table 1). The median geometric mean during this 8-year period was 0.49 μg THg/g, ww.

However, during flood years such as 1997, a “100-year” event, and 2006, much new particle-bound mercury from eroded tailings is deposited throughout the LCRS, and especially into Lahontan Reservoir and surrounding wetlands. Though we have no empirical evidence to explain the 8.4-fold different in the geometric means for THg in snowy egret eggs between 1997 and 2006, we suspect that it was the product of wetland conditions preceding the flood events. The wetlands and shallows around Lahontan Reservoir were saturated for several years prior to the 1997 flood. Thus, per 1998–2005, the birds likely foraged in well-established wetlands containing comparatively stable concentrations of MeHg, which in turn was diluted by the flood event. Even though much particle-bound mercury was washed downstream, it precipitated rapidly from the water column and was generally unavailable in preferred forage of the snowy egrets.

In contrast to 1997, the 2006 flood was preceded by five low water years (2000–2004), during which much wetting and drying of wetlands occurred each year. This process facilitates methylation of inorganic mercury deposited in sediments during years of runoff and enhances its bioavailability. We therefore suggest that in 2006, following significant wetland recovery in 2005 (a high water year), aquatic organisms flourished, and accumulated increased MeHg, which was transferred to snowy egrets as evidenced by 90% of the nests containing eggs exceeding 0.80 μg THg/g (Table 1). This 90% occurrence is remarkable when compared to other years when only 2002 (60%), a drought year, exceeded 20% of nests with ≥0.80 μg THg/g; the 10-year median rate of snowy egret eggs above the 0.80 criterion was 13% (Table 1).

Mercury in night-heron eggs

Different than for snowy egret, annual THg concentrations in night-heron eggs were directly related to MeHg in water below the reservoir and annual water discharge down the Carson River (Henny et al. 2007). Between 1997 and 2006, 122 night-heron nests were sampled at Lahontan Reservoir for egg THg. Geometric means varied from 0.22 to 1.01 μg THg/g, ww; a difference of 4.6-fold (Table 1); however, only the lowest 2 years (2005, 2002) differed significantly from the highest 2 years (1997, 2006). The median percentage of night-heron eggs exceeding 0.80 μg THg/g was 10% (compared to 13% for snowy egret) with 47 and 50% incidence during the extreme two flood years of 1997 and 2006. In all other years, including the drought (2000–2004), incidence of nests exceeding the 0.80 threshold varied from zero (3 years) to 13%; none of the 28 night-heron eggs from the reference site exceeded 0.80 μg THg/g. A comparison of the five drought years (2000–2004) vs. the five wetter years (1997–1999, 2005–2006) indicated that eggs of both night-herons and snowy egrets contained lower THg concentrations (arithmetic means) in drought years (0.34 and 0.53 μg/g) than in wetter years (0.58 and 0.72 μg/g) as well as less annual variability in drought years (CV = 23.7 and 32.5%) than in wetter years (CV = 50.9 and 95.3%).

Mercury in blood

Annual THg concentrations in blood of both snowy egrets and night-herons were directly related to annual MeHg concentrations in water below the reservoir, which was also directly related to annual water discharge down the river (Henny et al. 2007). The pattern of temporal changes in blood THg concentrations was similar for young snowy egrets and night-herons on Lahontan Reservoir (Table 2). Over the 10-year study, 88 of 142 (62.0%) snowy egret blood samples contained ≥2.0 μg THg/g in whole blood. The percentage of snowy egret blood samples per year with ≥2.0 μg THg/g varied from zero (n = 1) to 100% (n = 4); none of the snowy egrets sampled at the reference site met the 2.0 μg criterion. During the same period, 38 of 74 (51.4%) night-heron bloods contained ≥2.0 μg THg/g. The percentage of night-heron bloods with ≥2.0 μg THg/g also varied from zero (n = 1) to 100% (n = 1); none of the night-heron blood sampled at the reference site met the 2.0 μg criterion.

As with the egg samples, the annual blood residue data were split into the same five drought years and five wetter years at Lahontan Reservoir. The blood of both night-herons and snowy egrets generally contained lower THg concentrations (arithmetic means) in drought years (1.61 and 1.74 μg/g) than in wetter years (3.16 and 4.14 μg/g), but both species showed considerable annual THg variability during both the drought years (CV = 42.9 and 58.0%) and the wet years (CV = 78.5 and 37.2%).

Foraging and drought

Earlier discovered relationships for both species between annual THg concentrations in blood and eggs and the annual water discharge down the river indicated that MeHg availability was generally lower in drought years than in flood years (Henny et al. 2007). However, mercury residues in eggs and bloods of snowy egrets and night-herons may provide inferences into further differences between the two species in their selection of foraging grounds and diets during drought and flood years. Our initial impression was that during drought, night-herons (with a more generalist diet) may increase their proportional consumption of terrestrial vertebrates and thereby, compared to snowy egrets, reduce their exposure to mercury. We expected the annual mercury exposure of snowy egrets to approximate the annual difference (50.4%) in MeHg in water below the reservoir during drought years (arithmetic mean 0.223 ng/L) and wetter years (0.450 ng/L) due to their virtual dependence on aquatic organisms and being forced into the bottom lands of the Carson River as LCRS wetlands dried out. The river is the conduit for new mercury input from eroded mill tailings each spring; and, as mentioned, translocated mercury (in lower concentrations) during low water years is generally contained in the river channel.

THg residues in night-heron eggs and bloods decreased in drought years. When 1997–1999 and 2005–2006 were pooled for comparison to the drought years of 2000–2004; egg and blood THg concentrations decreased by averages of 41.5 and 49.1% (Tables 1 and 2). This similarity in decreases of THg in eggs and bloods suggests that foraging patterns and diet of night-herons were generally consistent throughout the entire nesting season (no “major” shift to terrestrial vertebrates with lower MeHg concentrations (see Henny et al. 2002)) despite the drawing down of the Lahontan Reservoir for irrigation and temporal drying out of nearby wetlands. Egg THg residues represent dietary exposure of night-herons during late April through mid-May while blood THg residues represent exposure during early to mid-June.

Concentrations of THg in eggs and bloods of snowy egrets decreased during drought years by respective averages of 26.9 and 58.0% (Tables 1 and 2). These differences, especially compared to an expected 50.4% change based upon MeHg in water below the reservoir, suggest that snowy egrets foraged in different habitats during pre-egg laying and post-hatch periods in drought and wetter years. In May, snowy egrets in wetter years foraged in temporary wetlands throughout the LCRS but during drought years, they soon became dependent on the riverine shallows of the Carson River upstream of Lahontan Reservoir toward the Comstock mining area (unpubl. aerial survey; this study). We believe the reason for the large decrease in blood THg residues during drought years is that comparatively little THg is methylated to MeHg upstream of the reservoir and along the main river (away from wetlands (see Gustin et al. 2006)) where snowy egrets were feeding.

Nesting and reproduction

Timing of nesting

Migrating night-herons and snowy egrets return to the LCRS from their wintering grounds each spring, but clutch completion dates varied considerably from year to year (Table 3). Night-herons generally laid eggs earlier than snowy egrets, but in two of the most severe drought years (2001–2002), night-heron clutch completion was delayed and similar to dates for snowy egrets. Clutch completion dates for the earlier nesting night-heron seemed to fluctuate more than snowy egret dates during the 10-year period with 2 years considered “early” and 2 years considered “late” (Table 3). A further evaluation showed that night-herons completed clutches earlier in years with a higher annual Carson River water discharge (Fig. 3a). In contrast, the generally later nesting snowy egrets showed no relationship between annual water discharge and clutch completion dates (Fig. 3b).
Table 3

Estimated clutch completion dates (Julian day) for first 10 clutches located each year of black-crowned night-herons and snowy egrets at Lahontan Reservoir, 1997–2006

Year

Night-heron

Snowy egret

Mean ± 2 SE, N

Seasona

Mean ± 2 SE, N

Seasona

1997

125.50 ± 4.97, 10

Average

134.00 ± 3.02, 8

Average

1998

113.90 ± 5.60, 10

Early

130.78 ± 3.65, 9

Early

1999

128.50 ± 4.74, 10

Average

144.90 ± 2.36, 10

Average

2000

126.11 ± 6.54, 9

Average

143.30 ± 4.56, 10

Average

2001

141.10 ± 4.81, 10

Late

140.50 ± 1.61, 10

Average

2002

136.40 ± 5.99, 10

Average

135.10 ± 1.92, 10

Average

2003

140.40 ± 4.60, 10

Late

147.20 ± 2.27, 10

Average

2004

129.70 ± 4.55, 10

Average

134.40 ± 2.63, 10

Average

2005

119.90 ± 1.99, 10

Early

148.40 ± 2.57, 10

Late

2006

123.70 ± 1.37, 10

Average

150.00 ± 2.31, 10

Late

10-year means

128.52 ± 5.53, 10

140.86 ± 4.35, 10

Note: Julian Day is the day in the year with January 1 = Julian Day 1, e.g., Julian Day 128 = May 8, and 140 = May 20 (except in leap years 2000 and 2004)

aSeason “early” or “late” when mean clutch completion date (±2 SE, i.e., 95% confidence limit) does not overlap the 10-year mean

https://static-content.springer.com/image/art%3A10.1007%2Fs10646-007-0180-y/MediaObjects/10646_2007_180_Fig3_HTML.gif
Fig. 3

Relationship between annual water discharge from the Carson River and annual clutch completion dates (Julian Day) for black-crowned night-herons (a) and snowy egrets (b) nesting at Lahontan Reservoir, 1997–2006. Dashed regression line, not significant

Timing of migration and nesting is an interactive product of physiologic and ambient factors. In the LCRS where night-heron nesting was generally delayed during drought (Table 3), total egg volume (clutch size × egg volume) per clutch paralleled water conditions (cf. Figs. 2 and 4a). That is, egg volume, which equals energy for embryonic development, was decreased during drought and translated into reduced hatchability, especially in the most severe drought years of 2000–2002 (Table 4). In contrast, total egg volume for snowy egrets, which tended to nest later and on a more consistent annual schedule than night-herons, appeared less clearly related to drought (cf. Figs. 2 and 5a), but of equal interest, total egg volume for night-herons was negatively correlated with clutch completion date (Fig. 4b), while total egg volume for snowy egrets was positively correlated with clutch completion date (Fig. 5b).
https://static-content.springer.com/image/art%3A10.1007%2Fs10646-007-0180-y/MediaObjects/10646_2007_180_Fig4_HTML.gif
Fig. 4

Comparisons at Lahontan Reservoir between black-crowned night-heron total egg volume (mean clutch size × egg volume) and nesting year (a) and between total egg volume and clutch completion date (b)

Table 4

Snowy egret and black-crowned night-heron reproduction at Lahontan Reservoir, 1997–2006

Year

Total nests

Complete clutchesa

Nests to endpointd

Young/Nest

Successful nestse

 

Nb

Clutch size

Hatchabilityc

   

Snowy egret

1997

ND

(4)

(4.00)

ND

(7)

(0.57)

(2) (28.6%)

1998

ND

13

3.31

ND

ND

ND

ND

1999

41

33

3.61

56.9%

ND

ND

ND

2000

60

46

3.28

57.4%

42

0.76

18 (42.9%)

2001

66

56

3.46

8.2%

43

0.14

3 (7.0%)

2002

53

46

3.37

42.2%

49

0.24

7 (14.3%)

2003f

50

42

4.05

48.9%

34

0.45

8 (23.5%)

2004g

42

38

3.95

78.9%

17

1.94

13 (76.5%)

2005

40

39

4.05

72.3%

34

2.44

28 (82.4%)

2006

29

28

4.32

71.5%

23

2.70

19 (82.6%)

Night-heron

1997

ND

15

3.80

60.8%

17

1.53

12 (70.6%)

1998

ND

14

3.29

66.7%

ND

ND

ND

1999

38

30

3.27

70.3%

14

1.29

10 (71.4%)

2000

ND

9

3.11

29.2%

16

0.32

3 (18.8%)

2001

ND

21

2.86

32.4%

20

0.45

6 (30.0%)

2002

ND

21

3.05

51.0%

24

1.00

15 (62.5%)

2003h

40

31

3.06

62.2%

30

1.00

15 (50.0%)

2004i

39

34

3.09

64.7%

25

1.36

17 (68.0%)

2005

43

37

3.43

73.7%

35

1.91

30 (85.7%)

2006

28

24

3.83

84.0%

24

2.92

21 (87.5%)

Note: ND = No data; limited snowy egret data from 1997 ( ) not used in overall evaluation

aComplete clutch is based on evidence of incubation

bNot to be used to reflect year-to-year population numbers

cAverage percent hatch when all clutches weighted equally

dIncludes nests observed through failure or 2 weeks post-hatch

eSuccessful nests have at least 1 young at 14 days of age

fClutch size at reference area 3.63 (N = 27)

gClutch size at reference area 3.71 (N = 28)

hClutch size at reference area 3.00 (N = 15)

iClutch size at reference area 3.35 (N = 17)

https://static-content.springer.com/image/art%3A10.1007%2Fs10646-007-0180-y/MediaObjects/10646_2007_180_Fig5_HTML.gif
Fig. 5

Comparisons at Lahontan Reservoir between snowy egret total egg volume (mean clutch size × egg volume) and nesting year (a) and between total egg volume and clutch completion date (b). Note: 1997 excluded from analyses because clutch size based upon only four clutches

Reproduction

Monitoring avian reproduction is based on nesting attempts (i.e., complete egg clutches under incubation), the rate of hatching, and ultimately, the number of young per nesting attempt (Table 4). During this study, compatible data were derived for night-herons and snowy egrets for a continuum of wet and dry years, but are exclusive to nesting in the island rookery in Lahontan Reservoir and are not intended to infer reproductive success for these species throughout the wetlands of Lahontan Valley.

Though island and marsh nesting night-herons and snowy egrets likely share feeding grounds to some degree in the LCRS, factors affecting nesting success in the two habitats are very different. For the island colony, both species use established and well protected nest sites with the main challenge being delivery of adequate nutrition to ensure successful departure of young from the island. Gull Island does not have land predators. In contrast, new colonies were formed each year in the marshes of Stillwater National Wildlife Refuge (NWR) and Carson Lake, but in some drought years (e.g., 2001, 2002) nesting was abandoned entirely during incubation or while young were still in the nest. Compared to snowy egrets who continued to nest in the main Gull Island rookery during drought despite progressive deterioration of the expansive saltcedar grove, night-herons shifted their nesting to alternative sites in small clusters of young saltcedar around the perimeter of Gull Island and to nearby Evans Island. Thus, the number of night-heron nests located and the number of complete clutches reported for the first three years of drought (2000–2002) are biased low since only the main rookery was surveyed during that period (Table 4).

While snowy egrets and possibly night-herons nesting in Lahontan Reservoir increased in numbers during drought years (Fig. 2; Table 4), both species were confronted with foraging difficulties. During the drought, the reservoir was not filled to optimal springtime levels and then was drawn down early to accommodate irrigation commitments (Henny et al. 2007). In response, the littoral zone around the reservoir, and especially the expansive shallows near the upstream end, did not develop normally during drought and a convenient and productive food source was eliminated. Also, during the period of low flow of the Carson River (2000–2004; Fig. 2), many wetlands throughout the Lahontan Valley dried out. Thus, procurement of food was undoubtedly more difficult during drought years, and was especially problematic for the later nesting snowy egrets, which are more dependent on an aquatic diet than are night-herons.

Snowy egret

Snowy egrets nested on Gull Island in Lahontan Reservoir in numbers inversely related to the recent water cycle (Fig. 2), and, by inference, availability of wetlands in the LCRS. This cycle covered 12 years and three phases: (1) 1995–1999—above normal precipitation in the Carson River drainage generally maintained LCRS wetlands; (2) 2000–2002—regional drought and drying out of LCRS wetlands; and (3) 2003–2006—progressive recovery of LCRS wetlands with 2005–2006 breaking the 5-year drought. The year 2005 was sufficiently wet to begin recharging many wetlands that dried out in 2001, one of the driest years on record for the Carson River drainage.

As the wetlands throughout the LCRS rapidly dried out each spring during the drought, preferred foraging grounds were lost and snowy egret nesting generally failed (L.A. Neel, Nevada Department of Wildlife; W.H. Henry, U.S. Fish and Wildlife Service, personal communication). Lahontan Reservoir was the exception in 2000 when 43% of the nests on Gull Island successfully produced about 35 fledglings, but as wetlands further deteriorated in 2001 and 2002, nesting success was negligible at 7 and 14%; a net of 6 and 12 fledglings (Table 4). With slightly more water discharged from the Carson River in 2003, and the wetlands beginning to recover, nesting success improved to 24%, but with only 15 fledglings produced. As conditions gradually improved throughout the LCRS in 2004–2006, nesting on Gull Island decreased to an estimated 35–45 nests (apparently some snowy egrets moved back to marshes) compared to more than 65 in 2001, but nesting success was 77–83% and produced 1.94–2.70 fledglings per nest (Table 4). At this rate of production, at least 74, 85 and 76 snowy egrets fledged on Gull Island in 2004, 2005, and 2006, respectively.

It is important to recall that young 2–3 weeks of age are able to leave the nest, but remain dependent on adults for food. They also remain at the colony for several more weeks learning to forage and to fly. However, Gull Island is virtually devoid of feeding shallows during drought years when the reservoir was not filled during springtime and was drawn down early for irrigation. Therefore, the transition to independence for young at Gull Island is entirely dependant on parental delivery of adequate nutrition. The timing of snowy egret dispersal from Gull Island and survival to first migration was studied by radio telemetry in 2001–2004 and is the subject of Part III in this series.

Snowy egret nesting essentially failed on Gull Island during the peak drought years of 2001 and 2002 (Table 4). However, the proportional contribution of the drought to nesting failure was not known. Thus, the annual water discharge of the Carson River (= reservoir dynamic, general wetland health, and availability of feeding grounds) was regressed against timing of nesting (Fig. 3), clutch size, hatchability, and young per nest (Fig. 6). None of these variables yielded a statistically significant correlation, though the ultimate criterion of young produced per nesting attempt was more strongly related to annual water discharge (P = 0.058; Fig. 6c).
https://static-content.springer.com/image/art%3A10.1007%2Fs10646-007-0180-y/MediaObjects/10646_2007_180_Fig6_HTML.gif
Fig. 6

Relationships between annual water discharge from the Carson River and snowy egret clutch size (a), hatching success (b) and number of young per nesting attempt (c). Dashed regression line, not significant

Black-crowned night-heron

The earlier nesting night-herons on Gull Island responded directly to the regional water cycle of wet conditions (1997–1999), drought (2000–2004), and recovery (2005–2006) (Table 4; Figs. 2, 3, and 7). As discussed previously, night-heron clutches were completed earlier in years of high annual water discharge in the Carson River (Fig. 3a), and clutch sizes were larger (Fig. 7a). These wetter water years enhanced the development of productive feeding grounds around the reservoir and maintained wetlands throughout the Lahontan Valley. In response to these favorable conditions, increases were also noted in the percentage of eggs hatching (P = 0.091) and the number of young per nesting attempt (P = 0.072) (Table 4; Fig. 7b, c).
https://static-content.springer.com/image/art%3A10.1007%2Fs10646-007-0180-y/MediaObjects/10646_2007_180_Fig7_HTML.gif
Fig. 7

Relationships between annual water discharge from the Carson River and black-crowned night-heron clutch size (a), hatching success (b) and young per nesting attempt (c). Dashed regression line, not significant

Drought years, and especially early stages of drought in 2000 and 2001, adversely affected night-heron reproduction (Table 4). Whether the total reproductive effect was properly represented in the data is uncertain because a portion of the night-heron colony moved a short distance (but remained on the islands) with the onset of the drought and only those remaining in the main saltcedar rookery were surveyed from 2000 through 2002. We assume that night-heron production at the alternative nest sites on the islands was at least equal to those continuing to nest in the main rookery because the alternative sites were better concealed and both groups likely shared foraging grounds. Thus, the data for night-herons presented in Table 4 seems reasonable and representative, with the more generalist-feeding night-herons faring somewhat better than snowy egrets during the extended drought.

Reproductive toxicology

In addition to monitoring for the biological presence of mercury in natural systems, eggs and bloods of birds have been used as indicators of reproductive risk to wild populations (e.g., Wolfe et al. 1998; Weiner et al. 2002; Eisler 2006; Scheuhammer et al. 2007). During the period 1997–2006, 113 snowy egret eggs were sampled for THg analysis at the Lahontan Reservoir colony on Gull Island (Table 1). The percentage of eggs sampled with ≥0.80 μg THg/g is also presented because literature and an earlier investigation, which included snowy egret data from Carson Lake, NV in 1997 (Henny et al. 2002), suggested that THg ≥0.80 μg/g in eggs of snowy egrets may have adversely affected their reproductive success, but not night-herons. Over the 10 years reported herein, 27 snowy egret eggs (23.9%) from Lahontan Reservoir contained THg concentrations ≥0.80 μg/g. At the reference area along the Humboldt River, only 1 of 58 (1.7%) snowy egret eggs exceeded ≥0.80 μg/g. During the drought years, the ≥0.80 threshold for snowy egret eggs showed consistent results (Table 5). The 10 nests in Group B (2000, 2002, 2003, 2005) produced no young when THg was ≥0.80, while the other 30 nests in Group B with <0.80 produced 53 young or 1.77 young/nesting attempt (χ2 = 14.85, l d.f., P = 0.0001). The data in Group D (2001 and 2004) could not be used in the test because either no young were produced at all (2001) in the sampled series, or no eggs were obtained in the ≥0.80 μg/g category (2004). The data in Group C (2006), which was a wet year, yielded an important change in the reproductive response—eight of nine nests contained eggs with ≥0.80 μg/g and 2.89 young/nesting attempt were fledged, the only nest with <0.80 μg/g yielded 4.00 young. Of special interest is Group A from another wet year (1997), which also produced some young when eggs contained ≥0.80 μg/g. This study indicated that embryonic and hatchability tolerance of MeHg is well above 0.80 μg/g in eggs under certain conditions. We believe that when forage is in abundance and parental attentiveness is optimized, all facets of avian reproduction are optimized. Thus, the use of a singular residue criterion for diagnosis is not realistic.
Table 5

Mean number of young snowy egrets produced from each nesting attempt with final outcome determined in relation to total mercury (THg) in sampled egg from each nest

  

Mean no. young/nest

Year

<0.80 μg THg/g (N)

≥0.80 μg THg/g (N)

Group Aa

1997

1.09 (11)

0.67 (12)

Group Bb

2000

0.91 (11)

0.00 (2)

2002

1.50 (4)

0.00 (5)

2003

1.40 (5)

0.00 (2)

2005

1.91 (10)

0.00 (1)

Group Cc

2006

4.00 (1)

2.89 (9)

Group Dd

2001

0.00 (11)

0.00 (2)

2004

2.00 (10)

No eggs

aFrom Henny et al. (2002) and a flood year

bGenerally dryer years, no young produced at nests with egg concentrations ≥0.80 μg THg/g, but young produced when <0.80 μg THg/g

cWet year with general flooding

dEither a dry year with no young produced at all from sample nests, or a year with no eggs containing ≥0.80 μg THg/g

The behavior of adults, which contained extremely high liver and kidney THg concentrations in 1998 (Henny et al. 2002), and their ability to feed young is a critical factor in reproductive success. The available food supply is generally limited during drought. Because reproductive physiology and sexual behavior are so sensitive to the supply of metabolic fuels, when food intake is limited or an inordinate proportion of dietary energy is invested in physical activity or maintenance of homeostasis in an unfavorable environment, reproduction may be suspended in favor of metabolic processes that ensure individual survival (Wade et al. 1996). Neurological effects on adults related to higher MeHg concentrations, as reflected in higher THg concentrations in eggs laid, may be expected to be more pronounced in years with the additional stress of drought. We cannot pinpoint the concentration where the reproductive system broke down because inadequate numbers of nests with an egg collected in each THg category (<0.80 vs. ≥0.80 μg/g) were monitored during the drought and wetter years. The ≥0.80 μg/g concentration seems useful in drought years when adults were more stressed (no production), but in wetter years (1997 and 2006) young were often produced to ∼2–3 weeks of age at nests with those concentrations. Percentages are not provided because sample sizes were small; however, the concept of a variable toxicity threshold for young produced to ∼2–3 weeks of age associated with habitat condition (food supply) appears real. Stress on adult snowy egrets associated with the drought years seems readily apparent from the greatly reduced productivity in those years (even at nests with eggs <0.80 μg THg/g), and especially in 2001 when almost all nests were abandoned by adults shortly after egg laying. Similarly, Hoffman et al. (1992) reported more severe toxicological effects when dietary protein was diminished in a laboratory study with mallard (Anas platyrhynchos) ducklings.

Another way of evaluating snowy egret production during the drought of the middle years (2000–2004) of this study is as follows. Assuming that all nests with ≥0.80 μg THg/g failed because of THg (see Table 5), the maximum contribution of THg to nest failure (% THg loss in parentheses) is shown after the overall percentage failure for each year (Table 4): 2000—57.1% (13.3%); 2001—93.0% (13.3%); 2002—85.7% (60.0%); 2003—76.5% (20.0%); and 2004—23.5% (0%). Thus, the 5-year average failure rate during drought was 67.2%, with an estimated 21.3% failing due to THg concentration in eggs. In the wetter years of 2005 and 2006, only 17.6 and 17.4% failed (Table 4). Thus, THg in the eggs ≥0.80 μg THg/g (10% in 2005 and 90% in 2006) was likely not responsible for much nest failure during the wetter years. Drought was certainly devastating to snowy egret annual productivity, and exacerbated the effects of mercury.

As mentioned, we also used the 0.80 μg/THg/g ww criterion for eggs of night-herons as a reference point, but not as a toxic threshold. In general, mercury residues in eggs were slightly lower for night-herons than for snowy egrets (Table 1). However, night-heron nesting success on Gull Island was consistently better than the snowy egret (Table 4). Night-heron success was attributed to their tending to arrive at Gull Island earlier than the snowy egret, selection of more favorable nesting sites, and their more diverse feeding habits, which included terrestrial foraging. We did not detect any evidence of reproductive toxicity to night-herons (less sensitive to mercury) that could be separated from ambient effects of drought.

Our use of whole blood mercury (2.0 μg THg/g) as a criterion of significant exposure for purposes of monitoring and potential toxicity was an effective non-destructive technique for measuring mercury in a natural system. Though 50% or more of the snowy egrets and night-herons exceeded the criterion in 6 of 10 years (Table 2), we detected no evidence of mortality to young, while in the colony, associated with high blood THg concentrations. A detailed evaluation of physiological associations with blood residues and post-fledging survival via telemetry will be presented in future reports in this series.

Conclusions

The wetlands of the LCRS, and especially Lahontan Reservoir, are generally contaminated with high concentrations of mercury from historic mining effluent. This 10-year (1997–2006) study of snowy egret and night-heron reproduction revealed putative biological effect levels of mercury above 0.80 μg THg/g, ww, in eggs throughout the study period. The overall proportion of snowy egret and night-heron eggs exceeding this criterion was 23.9 and 16.4%. Clear evidence of such levels affecting reproduction was confounded by 5 years of drought (2000–2004) in the middle of the study. During this period of drought, all measured facets of reproductive success in both species were depressed regardless of THg concentrations. No evidence of reduced reproductive success associated with eggs exceeding 0.80 μg THg/g was detected for night-herons. For snowy egrets, nests with eggs exceeding 0.80 μg THg/g all failed during drought years, but during wetter years when food was abundant, nests with residues above 0.80 μg THg/g were often successful. Therefore, it appears that this criterion is more related to extrinsic factors of nutrition (antioxidants, vitamins, etc.) and parental nurturing of eggs and young rather than intrinsic factors of THg toxicity to the developing embryo. This long-term study indicates a continued need for interaction studies with environmental factors and resulting bird condition to further develop mercury residue criteria for reproductive toxicity.

Acknowledgments

We thank K. Penner and J. Sizemore, Nevada State Parks for assisting in field aspects of the study at Lahontan Reservoir. P. Bradley and associates, Nevada Department of Wildlife, Elko, assisted with field data collection at the reference site. W. Praskins (San Francisco, CA) and S. Taylor (Research Triangle Park, NC) coordinated the study for EPA, which partially funded this study. The use of trade, product, or firm names in this publication is for descriptive purposes only and does not imply endorsement by the U.S. Government.

Copyright information

© Springer Science+Business Media, LLC 2007