1

Ecological Impact of Introduced Trout on Native 

Aquatic Communities in Mountain Lakes

Phase III Final Report

by William J. Liss, Gary L. Larson, and Robert L. Hoffman, editors

U.S. Geological Survey

Forest and Rangeland Ecosystem Science Center

3200 SW Jefferson Way

Corvallis, OR 97331

Prepared for:

National Park Service

North Cascades National Park Service Complex

Sedro-Woolley, WA 

July 2002

This research funded by the U.S. Geological Survey through the Forest and Rangeland

Ecosystem Science Center
2

This report was peer-reviewed by four reviewers according to the USGS guidelines for

manuscript review. The information contained in this report is not available for citation

without permission from the authors. Further inquires concerning this manuscript should

be made to:

Gary L. Larson

USGS Forest and Rangeland Ecosystem Science Center

3200 SW Jefferson Way

Corvallis, OR 97331
3

Table of Contents

Chapter 1. Abundance and Behavior of Larval Long-toed Salamanders 

(Ambystoma gracile) in Naturally Fishless Lakes and Lakes

with Non-Reproducing Populations of Introduced Trout in the

Northern Cascade Mountains, Washington, USA. 4–35

Chapter 2. Changes in the Behavior of Ambystoma gracile Larvae After

the Removal of Fish from a Mountain Lake. 36–53

Chapter 3. Distributions and Abundances of Larval Salamanders (Ambystoma

macrodactylum) and Large Copepods (Diaptomus sp.) in Relation to 

Introduced Trout and Abiotic Factors in Mountain Lakes of North

Cascades National Park Service Complex. 54-105
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CHAPTER 1

Abundance and Behavior of Larval Long-toed Salamanders 

(Ambystoma macrodactylum) in Naturally Fishless Lakes and Lakes with NonReproducing Populations of Introduced Trout in the Northern Cascade Mountains,

Washington, USA.

Torrey J. Tyler1, William J. Liss1, Gary L. Larson2, Lisa M. Ganio3

1

Department of Fisheries and Wildlife, Oregon State University, Nash Hall 104,

Corvallis, Oregon 97331, USA.

2

USGS, Forest and Rangeland Ecosystem Science Center, 3200 SW Jefferson Way,

Corvallis, Oregon 97331, USA.

3

Department of Forest Science, Oregon State University, Richland Hall 201, Corvallis,

Oregon 97331, USA.
5

ABSTRACT

Fish introduction into mountain lakes to provided recreational opportunities could

potentially impact native biota, including amphibians, of these relatively pristine

ecosystems. We investigated the impact of non-reproducing populations of trout

(Oncorhynchus sp.) that were stocked at regular intervals and moderate densities on the

abundance and behavior of native long-toed salamander (Ambystoma macrodactylum)

larvae in lakes of the North Cascades National Park Service Complex, Washington, USA.

Fish densities were determined from stocking records and salamander densities were

estimated using snorkel methods. Eleven physical and chemical variables were also

measured for each lake sampled. Stepwise multiple regression indicated that salamander

density in fishless lakes was strongly positively related with total Kjeldahl-N (TKN)

concentration and weakly negatively related with pH. Salamander densities in lakes with

fish were not related to any of 11 physical and chemical variables investigated. Larval

salamander density was statistically lower in only one lake with a non-reproducing trout

population as compared to their densities in fishless lakes. The probability of

encountering salamander larvae closely associated with lake substrates that potentially

provided refuge was greater in lakes with fish than in fishless lakes, and greater for larger

sized larvae in both lakes with and without fish. The severity of trout impact on A.

macrodactylum larvae in mountain lakes would appear dependent upon the reproductive

status of trout in a lake and lake productivity, as indicated by TKN. Theory suggests that

large populations of salamanders may be less vulnerable to extinction from chance events

than small populations and they may serve as important sources of colonists. Since large

populations are predicted to occur in lakes with high TKN concentrations, a prudent and
6

precautionary management strategy would be to maximize protection of all NOCA lakes

with relatively high TKN. 
7

INTRODUCTION

Montane lakes in the western USA are popular locations for recreational angling

for stocked trout. Bahls (1992) conducted a survey of fisheries biologists and managers in

western states and found that about 65% of all montane and 95% of larger, deeper lakes

currently support fish. According to Bahls (1992), about 95% of these lakes could have

been naturally fishless.

Concern about the potential impacts of stocked trout on native biota has been

increasing. Introduced trout appear capable of altering food webs in montane by reducing

abundance or eliminating larger, more visible vertebrate and invertebrate prey including

some species of frogs (e.g., Bradford, 1989; Bradford et al., 1993; Fellers and Drost,

1993; Blaustein et al., 1994; Knapp and Matthews, 2000), ambystomatid salamanders

(Taylor, 1983a; 1983b; Tyler et al, 1998a), and crustacean zooplankton (e.g.,

Starkweather, 1981; Stoddard, 1987; Donald et al., 1994; Liss et al., 1998), and by

altering nutrient dynamics in lakes (e.g., Leavitt et al., 1994).

In the Pacific Northwest, ambystomatid salamanders often are among the top

vertebrate predators in fishless montane lakes (Taylor, 1983a; Tyler et al., 1998a). Fish

can limit the distribution of ambystomatid salamanders (Thompson et al., 1980), and can

reduce survival and local population abundance (Petranka, 1983; Taylor, 1983a; 1983b;

Semlitsch, 1987; 1988; Sih et al., 1988; 1992; Tyler et al., 1998a; 1998b). Several studies

have demonstrated that fish can increase time that larvae spend in refuge (Sih et al., 1988;

1992; Jackson and Semlitsch, 1993), and restrict the range of substrates utilized by

salamanders (Semlitsch, 1987; Stangel and Semlitsch, 1987; Figiel and Semlitsch, 1990;
8

Tyler et al., 1998b), thereby limiting larval feeding opportunities and reducing growth

(Semlitsch, 1987; Figiel and Semlitsch, 1990; Tyler et al., 1998b).

 In North Cascades National Park Service Complex (NOCA) in northern

Washington, USA, lakes with trout can be grouped by the reproductive status of the trout

population (Tyler et al., 1998a; Liss et al., 1998). In lakes where fish can reproduce, trout

often reach high densities (average 524 fish/ha for fish larger than 177 mm total length as

determined by mark-recapture; range 25-724 fish/ha; Gresswell et al., 1997) and have a

complex age and size structure. In lakes where trout are incapable of reproducing, fish are

periodically stocked as fry or fingerlings at low to moderate densities with intervals

between successive stockings averaging about five years (average stocking density in 37

NOCA lakes = 179 fry/ha; range = 60-375 fry/ha; 1976 to 1993; unpublished; North

Cascades National Park Service Complex). 

Lakes in which trout do not reproduce and are periodically stocked are important

in fisheries management for several reasons. In NOCA, many anglers prefer to fish in

lakes with non-reproducing trout because trout densities are low and the fish can reach a

large size. Furthermore, these lakes may provide the best options for lake restoration if

deleterious effects on native biota are demonstrated because trout can be eliminated in a

few years without the use of chemical treatment simply through cessation of stocking. In

contrast, if fish impacts on native biota are not evident in lakes with non-reproducing

trout, managers could consider allowing continued stocking of these lakes.

Tyler et al (1998a) examined the impact of reproducing and non-reproducing trout

on larval Ambystoma macrodactylum in NOCA montane lakes. In fishless lakes they

found that larval density was positively related to total Kjeldahl nitrogen (TKN)
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concentration, an indicator of lake productivity (Lambou et al., 1983). Tyler et al. (1998)

found that in lakes with TKN >∼ 0.045 mg/L, larval densities in lakes with reproducing

fish were significantly lower than densities in fishless lakes. In contrast, larval densities

in lakes with non-reproducing fish were significantly lower than in fishless lakes only for

lakes with TKN >∼ 0.09 mg/L. For lakes with TKN concentrations below ~0.045 mg/l,

no differences in predicted larval densities between fishless lakes and lakes with either

reproducing or non-reproducing trout were found. However, in Tyler et al.’s (1998a)

study, the sample size of lakes with non-reproducing fish was small (n = 7) and the lakes

were not randomly selected. 

The current study was designed specifically to evaluate the impacts of nonreproducing trout on larval A. macrodactylum using a larger sample size of randomly

selected lakes than Tyler et al. (1998a). We tested the following hypotheses: 1) the

relative density of larval A. macrodactylum did not differ between fishless lakes and lakes

where trout cannot reproduce and are periodically stocked, and 2) the probability of

salamanders being hidden in lake substrate materials (e.g., talus, woody material, etc) did

not differ between fishless lakes and lakes with non-reproducing fish.

STUDY AREA

The North Cascades National Park Service Complex (NOCA) is located in the

Cascade Range of northern Washington, USA. There are approximately 150 lakes of

interest to fisheries managers in NOCA. The principle aquatic vertebrate predators in

NOCA montane lakes are stocked trout and larval ambystomatid salamanders. Although

most lakes within NOCA were naturally fishless during the last century, many NOCA

lakes were stocked with trout, primarily Oncorhynchus clarki and O. mykiss, to provide
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recreational angling opportunities. There are only two species of ambystomatid

salamanders (Ambystoma macrodactylum and Ambystoma gracile) present in NOCA

lakes, and they rarely co-occur (Liss et al., 1995; Tyler et al., 1998a).

METHODS

Sixteen fishless lakes were randomly selected from a pool of 69 fishless lakes,

and 15 lakes with non-reproducing fish were randomly selected from a pool of 21 lakes.

The selection pools of 69 fishless lakes and 21 lakes with non-reproducing fish represent

lakes available for study after eliminating lakes with poor water clarity (i.e., glacial till),

lakes classified as alpine (an area dominated by exposed rock and ice; dominant

vegetation is clumped low in stature; generally high in elevation; Lomnicky, 1996), and

lakes with A. gracile present. Average stocking density in the 15 NOCA lakes with nonreproducing fish was 167 fry/ha (range = 63-312 fry/ha; 1976-1997; Table 1) and the

average interval between stockings was 5.2 years (range = 3-8 years; Table 1).

In 1998, 17 lakes (eight fishless and nine with non-reproducing fish) were

sampled. In 1999, 14 additional lakes (eight fishless and six with non-reproducing fish)

were sampled. Eight fishless lakes and seven lakes with non-reproducing fish were

sampled twice between mid-June and mid-September 1998. The rest of the 1998 lakes

were sampled once. In 1999, lakes became accessible in late July due to an unusually

heavy snow pack and consequently they were only sampled once. Fish presence or

absence in lakes was confirmed during each sampling visit by visual observations during

snorkeling and by setting gillnets for several hours. 

Larval salamanders were censused by snorkel surveys (Tyler et al., 1998a).

Snorkel methods tend to under-represent small, cryptic, and benthic individuals in density
11

estimates (Helfman, 1983). Therefore, larval salamander density estimates from snorkel

surveys are conservative. Tyler et al. (1998a) found no difference in larval A.

macrodactylum density estimates between surveys conducted at night and during the day.

Therefore, all snorkel surveys were performed during mid-afternoon.

Four 25 m segments of shoreline were randomly chosen along the perimeter of

each lake. The same shoreline segments were snorkeled on each sampling visit. During

salamander surveys of the shoreline segments, a snorkeler carefully searched through

substrate materials (talus, woody debris, fine organic matter, aquatic vegetation) within 

2 m of the shoreline and recorded the number of larvae observed (Tyler et al., 1998a).

During the surveys for larval salamanders, the snorkeler visually estimated the

total length (TL, mm) of individual salamanders with the aid of a hand-held ruler, and

recorded whether individual larvae were “hidden” or “not hidden.” A salamander was

classified as “hidden” if greater than half of its body was obstructed from the snorkeler’s

view (i.e., the salamander was behind or beneath substrates) prior to disturbance of

substrate materials (Tyler et al., 1998a).

Salamander species identification was made in the field based on larval

characteristics outlined in Corkran and Thoms (1996). When species identification could

not be ascertained in the field, representative larvae were captured and transported from

the field. Captured larvae were reared to metamorphosis in a laboratory to confirm

species identification.

Eleven abiotic variables were measured for each lake. A hand-held sonar gun was

used to determine maximum depth of each lake. Lake elevations were derived from 7.5

min USGS topographical maps, and lake surface areas were determined by digitization of
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lake shorelines outlined on these maps. During each sampling visit, water temperature

was recorded and water samples were collected from 1 m below the lake surface over the

lake’s deepest point. Water samples and temperature recordings were gathered over each

lake’s deepest point to standardize sampling between lakes. Temperature measurements

were taken during mid-afternoon with an Omega 871 thermo-couple. One L water

samples were collected with a 1.5 L van Dorn-style sampling bottle. Water samples were

frozen upon return from the field to facilitate transport. Frozen filtered (GF/C 1.2 um

glass fiber filter) and unfiltered water samples were transported to the Cooperative

Chemical Analytical Laboratory at Oregon State University, Corvallis, Oregon, for

analyses. Analyses of filtered water included total phosphorus, total Kjeldahl-N,

ammonium-N, and nitrate-/nitrite-N concentrations, whereas unfiltered water was

analyzed for alkalinity, pH, and conductivity.

All statistical comparisons and regression models were judged to be significant at

p<0.05. Stepwise multiple regressions were used to determine relationships between

abiotic factors and larval salamander densities for lakes in each fish category (fishless

and non-reproducing fish). The dependent variable for each regression was the natural

logarithm of average larval density in each lake. Independent variables were the average

values for each of the 11 abiotic variables. A Pearson’s correlation matrix was developed

to investigate relationships between chemical and physical variables used in the

regression analysis. A sequential Bonferroni adjustment was performed on the Pearson’s

correlation matrix to eliminate Type I error and maintain table-wide significance at α =

0.05 (Miller, 1981; Rice, 1989).
13

To test for differences in larval A. macrodactylum densities between fishless lakes

and lakes with non-reproducing fish, larval density predicted from the regression model

and the corresponding 95% confidence interval (CI) was determined for each fishless

lake. Average salamander density and corresponding 95 % CI was determined for lakes

with non-reproducing fish. Differences in larval densities between individual fishless

lakes and lakes with non-reproducing fish were judged to be significantly different if the

95% CIs did not overlap (Tyler et al., 1998a). 

Logistic regression analysis was performed to determine relationships between

numbers of hidden larvae, length of larvae, and fish category. Two size classes of larvae

were recorded and these were assumed to represent young-of-the-year A. macrodactylum

larvae (TL < 60 mm) and over wintering, pre-metamorphic larvae (TL ≥ 60 mm;

Nussbaum et al., 1983; Leonard et al., 1993). The logistic regression formula was used to

determine the probability of observing a salamander classified as “hidden”.

RESULTS

Stepwise linear regression analysis of fishless lakes identified a significant model

relating salamander density to mg/L total Kjeldahl nitrogen (TKN) and pH (p= 0.0001,

R2=77.2). Larval salamander density was positively related to total Kjeldahl nitrogen

concentration and negatively related to pH (Figure 1a and Figure 1b):

log(density) = 8.049 + 153.535 (TKN) – 2.23 (pH)

 (+7.045) (+24.058) (+0.998)

Simple regressions revealed that salamander density was more strongly related to TKN

(R2

 = 0.69) than to pH (R2 = 0.06). In the full multiple regression model, TKN explained

more of the total variation in larval density (partial R2 = 0.76) than did pH (partial R2  =
14

0.28). For fishless lakes, total Kjeldahl-N was correlated with total phosphorus

(p=0.0002) and pH was correlated with conductivity (p=0.0007) and alkalinity (p=0.001).

Stepwise linear regression analysis of lakes with non-reproducing trout did not identify a

significant model relating A. macrodactylum density to any of the 11 abiotic variables.

Since multiple regression analysis revealed no significant relationship between

larval density and the abiotic variables in lakes with non-reproducing fish, larval densities

in these lakes were averaged and the 95% CI for the group average was determined

(Table 2). To assess fish effects on larval salamander density, the 95% CI for salamander

density for lakes with non-reproducing fish was compared to the 95% CIs of individual

fishless lakes predicted from the regression model.

Observed salamander densities were generally higher in fishless lakes with 

TKN > ~0.06 mg/l than in lakes with non-reproducing fish, although only two lakes with

trout had TKN concentrations within this range (Figure 1a). Typically, salamander larvae

were absent or present at low density in lakes with TKN < 0.04 mg/l, regardless of

whether fish were present or absent. 

In only one fishless lake was predicted larval salamander density significantly

higher than in lakes with non-reproducing fish (MR2; Table 2). MR2 had the highest

TKN concentration of the fishless lakes surveyed (0.09 mg/l) and the highest observed

salamander densities of any surveyed lake. There was little overlap in CI’s for lakes with

TKN concentrations > 0.055 mg/L (Table 2). In lakes with TKN concentrations ≤ 0.05

mg/L there was substantial overlap in CI’s, except for FP9 and DD8 where average

salamander densities in lakes with non-reproducing fish was higher than the predicted

densities (Table 2).
15

Visually estimated total length (TL) of individual salamander larvae and fish

category were both significant factors in determining if larvae were “hidden” or “not

hidden” (logistic regression model; p<0.0001). The logistic regression model indicated

that the probability of encountering a “hidden” larva was greater for large larvae

(TL>60mm) than small larvae (TL<60mm) in both fish categories (Table 3). The model

also indicated that the probability of encountering a “hidden” larva was greater in lakes

with non-reproducing fish than in fishless lakes for both large and small larvae.

DISCUSSION 

The abundance of larval A. macrodactylum varies considerably among fishless

lakes in NOCA, suggesting that abiotic factors played an important role in determining

larval distribution and density. Of the 11 abiotic variables we measured, only TKN

concentration and to a lesser extent pH, were significantly related to larval density in

fishless lakes. The positive relationship between larval densities and TKN could have

been indicative of a lake productivity gradient. Total Kjeldahl-N is a measure of

ammonia plus all organically derived nitrogen (Lambou et al., 1983). Algae and bacteria

do not readily utilize organic nitrogen, thus TKN does not have an active role in lake

energetics (Goldman and Horne, 1983). However, TKN, when correlated with

phosphorus as it is in NOCA lakes, has been identified as a good predictor of lake

productivity as measured by chlorophyll concentration (Lambou et al., 1983) or by total

plankton biomass (Paloheimo and Fulthorpe, 1987). The link between TKN and larval

salamander densities appears to be through food web associations. Through examination

of salamander stomach contents, Tyler et al. (1998a) found that larval A. macrodactylum
16

utilized cladoceran zooplankton as a major food resource in NOCA lakes. Cladoceran

density was positively correlated with TKN concentrations (Tyler et al., 1998a). 

A simple explanation of the negative relationship between larval density and pH

is not evident. The range of pH values in sampled lakes was narrow and centered around

neutral (6.25 – 7.825). Only three fishless lakes had pH > 7.5 (Table 2). In two of these

lakes, no salamanders were observed, possibly influencing the significance of pH in the

final model. Both TKN and pH have been shown to be indicators of the trophic state in

lakes (Lambou et al., 1983; Paleheimo and Fulthorpe, 1987), however, TKN and pH

relate to larval A. macrodactylum densities in opposing manners in our study. In any

event, as indicated by comparison of partial R2’s, TKN explained a much greater

proportion of the variation in larval density than pH. 

Based on the present study and Tyler et al. (1998a), two factors appear to play a

major role in mediating trout predation on larval A. macrodactylum in NOCA lakes: TKN

concentration and the reproductive status of the trout population. The reproductive status

of fish in NOCA lakes likely serves as an indicator of the density, and size and age

structure of trout. In NOCA, fish densities tend to be higher and age and size structures

more diverse in lakes with reproducing trout than in lakes with non-reproducing trout

(Gresswell et al, 1997). 

Populations of A. macrodactylum that inhabit lakes with relatively high TKN

concentrations appear to be the most vulnerable to stocked trout in NOCA. Tyler et al.

(1998a) found significant differences in larval abundance between fishless lakes and

lakes with reproducing trout for TKN concentrations > ~ 0.045 mg/L. In contrast, both

the present study and Tyler et al. (1998a) detected significant differences in predicted
17

larval A. macrodactylum densities between fishless lakes and lakes with non-reproducing

fish only when fishless lakes had TKN ≥ 0.09 mg/l. Although there were no significant

differences in predicted salamander densities between lakes with non-reproducing fish

and fishless lakes with 0.055 mg/l >TKN ≤ 0.09 mg/l, there was little overlap in the 95%

CI’s for lakes within this TKN range. However, only two populations with nonreproducing fish were sampled within this range.

A notable feature of high elevation salamander populations in NOCA is that larval

densities vary considerably among fishless lakes (0-65 individuals/100 m of shoreline in

the present study) and that the variation appears to be best explained by TKN. In the

fishless condition, lakes with high TKN likely would support relatively high densities of

larval salamanders. Large, relatively stable populations may be less vulnerable to

extinction from stochastic events than small, highly variable populations (e.g., Shaffer,

1987; Goodman, 1987a). Large populations could serve as important sources of colonists

(sensu Pulliam, 1988; Harrison, 1994) that could reestablish extinct local populations or

“rescue” (Stacey et al., 1996) smaller populations that are declining toward extinction.

Funk et al. (1999) present evidence suggesting that A. macrodactylum was able to

colonize lakes within 20 years following extinction of trout populations in the lakes. In

addition, the degree of isolation (or distance) of sources of dispersers from vacant

habitats could also be of great importance in influencing recolonization of these habitats

(Sjogren-Gulve and Ray, 1997; Funk et al., 1999). A prudent and precautionary

management strategy would be to maximize protection of all NOCA lakes with relatively

high TKN concentrations (> ~ 0.05 mg/l), regardless of the reproductive status of the fish

population.
18

In the present study and in Tyler et al. (1998), larval densities were not found to

be significantly different between lakes with fish and fishless lakes for relatively low

concentrations of TKN (< ~0.05 mg/l). Larval densities in these lakes were low,

presumably because of low TKN, regardless of whether fish were present. Although trout

do not appear to significantly affect larval densities in these lakes, smaller populations

may have importance to conservation of the species. Small populations could increase the

size and persistence of a metapopulation (Goodman, 1987b; Howe et al., 1991) and

enhance the genetic diversity of regional groups of populations (Lande and

Barrowclough, 1987; Scudder, 1989; Tallmon et al, 2000), and thus they merit some level

of protection.

The presence of fish appeared to alter the behavior of larval salamanders. The

probability of encountering “hidden” larvae was greater in lakes with non-reproducing

fish than in fishless lakes. “Hiding” behavior in larval A. macrodactylum may be a means

to avoid predation risks from predatory fish. Fish presence in ponds reduced activity of

ambystomatid larvae in the water column (Semlitsch, 1987, Stangel and Semlitsch, 1987;

Figiel and Semlitsch, 1990), increased refuge use or time spent in refuge (Sih et al., 1992;

Jackson and Semlitsch, 1993), increased nocturnal activity (Sprules, 1974; Taylor, 1983a;

Stangel and Semlitsch, 1987; Sih et al., 1992), or restricted larvae to a narrower range of

available habitat (Taylor, 1983b; Tyler et al., 1998b).

Time spent in refuge to avoid encounters with predatory fish can reduce forage

opportunities of larval salamanders and limit larval growth and survival (Semlitsch, 1987,

1988; Sih et al., 1988; Figiel and Semlitsch, 1990; Resitarits, 1995; Tyler et al., 1998b).

Slower growth rates in larval salamanders may impair survival either by increasing length
19

of the larval period, thus increasing susceptibility to mortality factors in the aquatic

environment, or decreasing larval body size at metamorphosis, and so possibly increasing

susceptibility to terrestrial threats.

The probability of encountering a “hidden” larva in NOCA lakes was higher for

large larvae (TL > 60 mm) than for small larvae (TL < 60 mm; Table 2). Amphibians

may be more susceptible to predation during metamorphosis (Wassersug and Sperry,

1977; Arnold and Wassersug, 1978), and may become more secretive. Larger A.

macrodactylum larvae likely were closer to metamorphosis than were small larvae in

NOCA lakes, thus possibly explaining size dependent differences in behavior.

Higher probability of encountering large A. macrodactylum larvae classified as

“hidden” than small larvae also may be related to experience with predators. Larger A.

gracile larvae displayed a more developed flight response than smaller A. gracile larvae

that may have resulted from larger individuals having more experience with predators

(Taylor, 1983a). Sih et al. (1988) noted that emergence rates from refuge should decrease

as prey increase experience with predators. Larger (and older) larval A. macrodactylum

may have been more conditioned to the presence of predators than small larvae as a

consequence of longer exposure to predators. These observations suggest that small A.

macrodactylum have less of a propensity to seek refuge in substrates during daylight than

larger larvae and, as a result, small larvae may be more vulnerable to fish predation than

large larvae. Intense predation on small larvae could be a major cause for differences in

densities between fishless lakes and lakes with fish.
20

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26

Figure 1. Relationships between larval Ambystoma macrodactylum density and total

 Kjeldahl-N concentration (a) and pH (b) for 16 fishless lakes and 15 lakes with

 non-reproducing fish.
27
28

Figure 1a.

0

10

20

30

40

50

60

70

0 0.01 0.02 0.03 0.04 0.05 0.06 0.07 0.08 0.09 0.1

Total Kjeldahl-N concentration (mg/L)

Salamander Density (#/100m)

Fishless

Non-Reproducing Fish

Figure 1 (continued). Relationships between larval Ambystoma macrodactylum density

 and total Kjeldahl-N concentration (a) and pH (b) for 16 fishless lakes and 15

 lakes with non-reproducing fish.
29
30

Figure 1b.

0

10

20

30

40

50

60

70

5.5 6 6.5 7 7.5 8 8.5

pH

Salamander Density (#/100m)

Fishless

Non-Reproducing Fish
Table 1. Fish data was obtained from stocking records provided by NOCA personnel. Maximum depth (Max. Z)  (Elev.) are given in meters. Average stocking density is fry or fingerling/ha with range shown in parenth average interval between fish stockings is given in years.

 Last Average Average Interval Number 

Lake Sampled Elev. Max. Z Species1 Stocking Density between Stockings StockinRD3* 1999 802 8.8 NAMR13-1* 1998 1800 2.0 NAMC1 1998 1762 3.0 NAMC2 1998 1800 11.0 NAMSH4 1998 1635 8.9 NAML1 1998 1476 1.2 NAML4 1998 1583 6.4 NAMC27 1998 1488 8.8 NA1NA= fishless lake, Rb1= Mt. Whitney rainbow trout, Rb2=Packer rainbow trout, Ct=Twin Lakes cutthroat trout*Previously stocked fishless lake.? – denotes unknown figure.
Table 1 (continued). Fish data was obtained from stocking records provided by NOCA personnel. Maximum dep

 elevation (Elev.) are given in meters. Average stocking density is fry or fingerling/ha with range shown  average interval between fish stockings is given in years. Last Average Average Interval Number 

Lake Sampled Elev. Max. Z Species1 Stocking Density between Stockings StockinMR2 1999 1873 1.5 NAMR3 1999 1873 2.5 NAMR8 1999 1970 3.5 NAMM7 1999 1642 1.9 NAMM6 1999 1504 11.9 NADD8 1999 1600 1.9 NAEP3 1999 1299 3.7 NAFP9 1999 1662 3.4 NA1NA= fishless lake, Rb1= Mt. Whitney rainbow trout, Rb2=Packer rainbow trout, Ct=Twin Lakes cutthroat trout*Previously stocked fishless lake.? – denotes unknown figure.
Table 1 (continued). Fish data was obtained from stocking records provided by NOCA personnel. Maximum dep

 elevation (Elev.) are given in meters. Average stocking density is fry or fingerling/ha with range shown i

 average interval between fish stockings is given in years.

 Last Average Average Interval Number 

Lake Sampled Elev. Max. Z Species1 Stocking Density between Stockings StockinML2 1998 1687 27.4 Rb1 117.1 ( 88.2-147.1) 4.0 3 ML3 1998 1967 15.2 Rb1 85.6 ( 76.9-103.1) 5.0 3 MR12 1998 1981 4.0 Rb1 311.7 (166.7-500.0) 6.0 3 MR13-2 1998 1789 5.0 Rb1 190.3 ( 58.3-362.5) 4.7 4 MR15-1 1998 1922 27.0 Rb2 125.0 0.0 1 MM11 1998 1974 7.6 Rb1 310.7 0.0 1 M19 1998 1427 24.0 Gt 120.6 (108.0-140.0) 5.3 4 DD1 1998 1496 2.4 Gt 260.0 (260.0-260.0) 8.0 2 1NA= fishless lake, Rb1= Mt. Whitney rainbow trout, Rb2=Packer rainbow trout, Ct=Twin Lakes cutthroat trout*Previously stocked fishless lake.? – denotes unknown figure.
Table 1 (continued). Fish data was obtained from stocking records provided by NOCA personnel. Maximum dep

 elevation (Elev.) are given in meters. Average stocking density is fry or fingerling/ha with range shown i

 average interval between fish stockings is given in years.

 Last Average Average Interval Number 

Lake Sampled Elev. Max. Z Species1 Stocking Density between Stockings StockinMR9 1999 1813 4.9 Rb1 100.0 ( 88.2-111.8) 5.0 2 MC7 1999 1556 27.0 Rb1 196.3 (119.4-247.7) 4.7 4 M1 1999 1159 4.3 Rb1 155.6 ( 93.8-248.1) 6.3 4 LS3-FS 1999 1369 6.7 Rb1 ? ? ? LS3 1999 1365 5.2 Ct/Rb1 173.3 (166.7-291.7) 6.7 5 DD5 1999 1531 5.2 Gt 62.5 ( 57.5-76.9) 5.0 4 EP5-1 1999 1543 6.0 Rb1 130.4 (111.1-147.0) 5.3 4 1NA= fishless lake, Rb1= Mt. Whitney rainbow trout, Rb2=Packer rainbow trout, Ct=Twin Lakes cutthroat trout*Previously stocked fishless lake.? – denotes unknown figure.
Table 2. Comparison of 95% confidence intervals (shown in parentheses) between larval Ambystoma macrodacty individual fishless lakes (NF) and of lakes with non-reproducing fish (NRF) was used to indicate differ fishless lakes and lakes with fish. Larval densities for 16 fishless lakes were derived from a multiple re with total Kjeldahl-N (TKN) concentration and pH as independent variables. Larval densities in 15 lak reproducing fish were averaged. Fish Category Lake TKN pH Observed density Predicted densityNF MC27 0.015 6.25 0 0.018 (-0.007, 0.277)

FP9 0.02 7.2 0 0.000 (-0.008, 0.024)aDD8 0.02 7.1 0 0.000 (-0.008, 0.031)aML1 0.03 7.65 0 0.002 (-0.008, 0.063)MM7 0.03 7.1 1 0.032 (0.003, 0.125)EP3 0.03 7.1 0 0.032 (0.003, 0.125)ML4 0.035 7.75 0 0.011 (-0.007, 0.129)

aPredicted fishless lake density less than 0. NRF density significantly greater than density in fishless lake.bMR2 density significantly higher than NRF density.
Table 2 (continued). Comparison of 95% confidence intervals (shown in parentheses) between larval Ambystoma  densities of individual fishless lakes (NF) and of lakes with non-reproducing fish (NRF) was used to in between fishless lakes and lakes with fish. Larval densities for 16 fishless lakes were derived from a m formula with total Kjeldahl-N (TKN) concentration and pH as independent variables. Larval densities  reproducing fish were averaged. Fish Category Lake TKN pH Observed density Predicted densityNF (continued) MSH4 0.035 7.4 0 0.036 (0.002, 0.163)

MR8 0.04 6.9 0 0.292 (0.097, 0.844)MC1 0.04 6.5 3 0.727 (0.151, 3.371)MC2 0.045 6.5 16 1.579 (0.329, 7.431)MM6 0.05 7.1 2 0.888 (0.291, 2.667)MR13-1 0.055 6.7 6 4.711 (1.110, 19.878)MR3 0.06 6.4 14 19.852 (2.703, 145.392

aPredicted fishless lake density less than 0. NRF density significantly greater than density in fishless lake.bMR2 density significantly higher than NRF density.
Table 2 (continued). Comparison of 95% confidence intervals (shown in parentheses) between larval Ambystoma  densities of individual fishless lakes (NF) and of lakes with non-reproducing fish (NRF) was used to in between fishless lakes and lakes with fish. Larval densities for 16 fishless lakes were derived from a m formula with total Kjeldahl-N (TKN) concentration and pH as independent variables. Larval densities  reproducing fish were averaged. Fish Category Lake TKN pH Observed density Predicted densityNF (continued) RD3 0.07 7.825 32.75 3.834 (0.340, 42.172)

MR2b 0.09 7.1 65 417.3 (27.98, 6222.3)

NRF average 1.594 (0.033, 3.154)aPredicted fishless lake density less than 0. NRF density significantly greater than density in fishless lake.bMR2 density significantly higher than NRF density.
38

Table 3. The probability of encountering “hidden” larval Ambystoma macrodactylum

 during snorkel surveys was affected by larval total length and whether 

 observations were made in a fishless lake (NF) or in a lake with non-

 reproducing fish (NRF). Probabilities were derived from logistic regression

 analysis.

Fish Total Probability of

Category Length Larva “Hidden”

NRF > 60 mm 0.9326

NRF < 60 mm 0.5592

NF > 60 mm 0.6339

NF < 60 mm 0.1369
39

CHAPTER 2

Changes in the Behavior of Ambystoma gracile Larvae 

After the Removal of Fish from a Mountain Lake

Robert L. Hoffman1, Torrey J. Tyler2, William J. Liss2, and Gary L. Larson3

1

 College of Oceanic and Atmospheric Sciences, 104 Ocean Admin, Oregon State

University, Corvallis, OR 97331

2

 Department of Fisheries and Wildlife, 104 Nash Hall, Oregon State University,

Corvallis, OR 97331

3

 USGS Forest and Rangeland Ecosystem Science Center, 3200 SW Jefferson

Way, Corvallis, OR 97331
40

ABSTRACT

Ambystoma gracile (Baird) larvae were surveyed in two adjacent lakes in North

Cascades National Park Service Complex, Washington, USA, between 1994 and 1999.

One lake (Upper Panther) was fishless. The other lake (Lower Panther) was inhabited by

introduced trout (Oncorhynchus clarki). The objective of this research was to identify any

changes in larval salamander behavior after fish removal from Lower Panther was

completed in June 1997. We investigated the diel habits and spatial use of larvae in each

lake before and after fish removal. Ambystoma gracile in Upper Panther were readily

observed during day surveys in immediate shoreline, 2 m, and 5 m transects, and were

active day and night during the entire period. Prior to fish removal, larvae in Lower

Panther were primarily observed during night surveys and restricted to the immediate

shoreline habitat. After fish removal, the percent of larvae observed during day surveys

increased significantly as did the percent of larvae observed in 2 m and 5 m transects.

Changes in Lower Panther indicate that larval behavior becomes less restricted and

secretive after fish are removed. This response is indicative of the ecological release of A.

gracile larvae from the threat of predation by introduced trout. 
41

INTRODUCTION

Prey attributes that decrease predation risk include unpalatability, reduction or

restriction of activity level, and occupation of habitats that may be ephemeral, stressful

for predators, or have complex structure that provides refuge from predation (Sih, 1987).

Many amphibian species have noxious and/or toxic skin secretions that reduce their

palatability to predators (Duellman and Trueb, 1986). These secretions are less developed

in larval amphibians (Formanowicz and Brodie, 1982; Duellman and Trueb, 1986), and,

thus, larvae rely on behavioral adaptations to escape threats of predation (Sih, 1987; Kats

et al., 1988). In the presence of predators, larvae may alter their use of microhabitats

(Kiesecker and Blaustein, 1998) and increase their use of structural components of

habitat (e.g., coarse woody debris, rock-talus, and aquatic vegetation) as refugia (Kats et

al., 1988; Sih et al., 1988; Tyler et al., 1998b). Larvae have also been shown to become

more secretive, shift their diel patterns of behavior (Taylor, 1983; Resetarits, 1995), and

increase the tendency to display flight behavior (Taylor 1983). 

Laboratory studies have shown that larval ambystomatids increase their use of

refuge in the presence of fish. In artificial ponds with fish, larval ambystomatids increase

their time spent in refuge (Sih et al., 1992; Jackson and Semlitsch, 1993), and restrict

their activity to a narrower range of available substrates (Semlitsch, 1987; Stangel and

Semlitsch, 1987; Figiel and Semlitsch, 1990; Tyler et al., 1998b). However, little is

known about larval salamander refuge use in response to the presence of fish in natural

systems. Taylor (1983) observed lower densities and less activity of larvae in lakes with

fish in comparison to lakes without fish. While investigating startle responses of two

larval Ambystoma gracile (Baird) populations, he observed that higher numbers of larvae
42

were present in the shallow, nearshore areas of a lake with fish than in a fishless lake.

Taylor (1983) speculated that the shallow areas of the fish lake may have offered greater

refuge from fish predation.

Another behavioral adaptation of ambystomatid larvae is increased nocturnal

activity in the presence of fish. Stangel and Semlitsch (1987) noted decreased diurnal

activity in larval Ambystoma talpoideum (Holbrook) in artificial ponds with fish. The

addition of predatory fish to stream pools decreased the diurnal activity of larval

Ambystoma barbouri Kraus and Petranka (Sih et al., 1992). Several field studies have

indicated that A. gracile larvae shift toward increased nocturnal activity when fish are

present in lakes (Efford and Mathias, 1969; Neish, 1971; Efford and Tsumura, 1973;

Sprules, 1974; Taylor, 1983). In view of these results, the objective of this research was

to document the diel distributions of A. gracile larvae in a lake before and after fish

removal.

METHODS

Upper Panther (the control lake) and Lower Panther (the treatment lake) are

separated by about 4 m and are located at an elevation of 1031 m within the boundaries

of the North Cascades National Park Service Complex (NOCA), Washington, USA.

Upper Panther is smaller (surface area = 0.1 ha; maximum depth = 3 m) than Lower

Panther (surface area = 0.3 ha; maximum depth = 5.8 m). Flocculent organic material is

the predominant substrate present in the deeper, offshore area of each lake. Both lakes

have shorelines consisting of bedrock, talus, and woody debris, although Lower Panther

contains more woody debris than Upper Panther. Lower Panther has additional shoreline

areas of overhanging vegetation and undercut banks.
43

Both lakes have a history of cutthroat trout (Oncorhynchus clarki) introductions.

Beginning in 1990, removal of fish from the lakes by angling and gillnetting was

initiated. Gillnets were set extending from the lake shoreline to the center of the lake.

Each gillnet was 42 m long and 2 m deep with four sections of monofilament panels of

12.5 mm, 18.5 mm, 25 mm, and 33 mm mesh. The last trout were removed from Upper

Panther in July 1992. In Lower Panther, trout were stocked twice following fish removal

efforts. In September 1990, trout were stocked at a density of 750 fry/ha in an attempt to

introduce a known number of fish into the lake. In 1994, an unauthorized stocking of

trout occurred at an unknown density. Using mark-recapture methods we estimated that

there were 320 trout/ha in Lower Panther in 1992 (Gresswell et al., 1997), and 250

trout/ha in 1996 (Torrey Tyler, unpublished data). Fish have not been collected or

observed in Lower Panther since seven fish were removed in June 1997.

From 1994 through 1999, densities of A. gracile larvae in both lakes were

estimated from snorkel surveys (Tyler et al., 1998a). In Lower Panther, surveys were

conducted along four 25 m segments randomly selected along the lake’s perimeter. In

Upper Panther, the entire lake perimeter (100m) was snorkeled. All surveys were

conducted parallel to the shoreline. The same shoreline segments were sampled on all

subsequent sampling visits.

Three types of surveys were performed during each sampling visit (Tyler et al.,

1998a). Search surveys were conducted near to (i.e., within approximately 1 m) and

along the immediate shoreline of each lake. Substrate materials (e.g., talus, woody debris,

organic detritus, and aquatic vegetation) present in this nearshore area of each lake

created a relatively complex structured habitat potentially useful to larvae as refuge.
44

Larvae were often obscured from the snorkeler’s view by these materials. Therefore,

during search surveys, snorkelers searched through these substrate materials for larvae

and recorded the number of larvae observed. Search surveys were only conducted during

mid-afternoon. Two-meter surveys were conducted approximately 2 m from shore where

water depth was typically ∃1 m. During two-meter surveys, snorkelers counted the

number of larvae they could observe without disturbing nearshore substrates within an

area extending from their 2 m offshore position toward the shore. Five-meter surveys

were conducted approximately 5 m from shore where water depth was typically ∃2 m.

During five-meter surveys, snorkerlers counted salamanders without disturbing substrates

within an area extending approximately 1.5 m to each side of the snorkeler’s longitudinal

axis. Two-meter and 5 m surveys were performed once during mid-afternoon, and again

30 min after sunset with the aid of a handheld dive-light. Since 2 m and 5 m surveys were

conducted without disturbing substrate materials, these surveys only censused larvae

observed in the open and not obscured from the snorkeler’s view by substrate materials.

The sequence of surveys proceeded from 5 m to 2 m to search. Sampling was conducted

systematically so as to avoid recounting larvae potentially flushed from shoreline refugia

and moving out to deeper areas of the lake.

Salamander surveys were typically conducted twice a year during the period from

mid-June to late August. Both lakes were sampled only once in 1994 due to a forest fire.

Equipment failure prevented night surveys during the August 1996 sampling. Nine day

surveys and eight night surveys were completed for each lake.

Two-meter and 5 m surveys were combined to investigate differences between

day and night larval relative densities in each lake when fish were present in Lower
45

Panther (i.e., 6/94 - 6/97) and after fish were no longer collected or observed in Lower

Panther (i.e., 7/97 - 8/99). The combined survey counts were expressed as the percent of

all larvae that were observed during the day versus at night. Paired T-tests were

performed to test for significant (i.e., p # 0.05) within and between lake differences in the

percent of larvae observed during day surveys before and after fish were removed from

Lower Panther. In each lake there were four dates before fish removal when both day and

night surveys were completed (i.e., n = 4) and four day and night survey dates after fish

removal (i.e., n = 4). 

To investigate differences in the number of larvae observed in the immediate

shoreline area of each lake before and after fish removal, survey counts were expressed

as the percentage of total larvae (i.e., search + 2 m + 5 m surveys) observed per day

search surveys. The rational for comparing search surveys with combined 2 m and 5 m

surveys was as follows: search surveys expressed the number of larvae associated with

refuge in each lake, while 2 m and 5 m surveys represented the number of larvae in the

open and typically not near refuge. Mann-Whitney tests were used to test for significant

within lake differences (i.e., p # 0.05) in the percent of larvae observed during day search

surveys before (i.e., 6/94 - 6/97) and after (i.e., 7/97 - 8/99) the removal of fish from

Lower Panther. Paired T-tests were used to examine between lake differences. There

were five day survey dates prior to fish removal (i.e., n = 5) and four day survey dates

after fish removal (i.e., n = 4) for each lake.

NCSS 2000 (Hintze, 1998) was used to calculate Paired T-test and Mann-Whitney

test results. 
46

RESULTS

The percent of larvae observed during day versus night surveys in Lower Panther

was quite low (i.e., 1% - 6%, average = 4%; Figure 1) when fish were present in the lake

(i.e., 6/94 - 6/97; surveydates = 4); whereas the percent of larvae observed during day

surveys after fish were removed (i.e., 7/97 - 8/99; surveydates = 4) increased significantly

to 29% - 48% (average = 41%)(Paired T-test, p = 0.002). In Upper Panther, typically

30% - 50% (average = 40%) of the total number of larvae counted during day and night

surveys were observed during the day (Figure 1). Furthermore, no significant difference

in the relative percentage of larvae observed in Upper Panther during the day occurred

before (surveydates = 4) versus after (surveydates = 4) fish were removed from Lower

Panther (Paired T-test, p = 0.46). Comparisons between lakes showed that the relative

percentage of larvae observed during the day in Lower Panther (surveydates = 4) was

significantly lower than in Upper Panther (surveydates = 4) prior to fish removal from

Lower Panther (Paired T-test, p = 0.002); whereas after fish removal the two lakes did

not significantly differ (Paired T-test, p = 0.71; surveydates = 4 in both lakes)(Figure 1).

Day search surveys revealed within and between lake differences in the

proportion of A. gracile larvae observed in the immediate shoreline areas of each lake.

There was a significant decrease in the proportion of larvae observed during the day in

the immediate shoreline area of Lower Panther after all fish had been removed from the

lake (i.e., by June 1997)(Mann-Whitney test, p = 0.01). Prior to fish removal (i.e., 6/94 -

6/97; surveydates = 5) the percent of larvae observed was above 80% (range = 80% - 99%;

average = 87%) and then dropped below 50% (range = 14% - 49%; average = 30%) after

fish were removed (i.e., 7/97 - 8/99; surveydates = 4)(Figure 2). In fishless Upper Panther,
47

the percent of larvae observed in day search surveys ranged from 16% - 52% (average =

33%), and was typically < 40% of all larvae observed (i.e., search + 2 m + 5 m

surveys)(Figure 2). The percent of larvae observed in Upper Panther search surveys

conducted prior to when fish were removed from Lower Panther (range = 16% - 44%,

average = 28%; surveydates = 5) did not differ significantly from the percentage observed

after fish were removed from Lower Panther (range = 26% - 52%, average = 39%;

surveydates = 4; Mann-Whitney test, p = 0.11). Between lake comparisons showed that the

percentage of larvae observed in the immediate shoreline area of each lake differed

before but not after fish removal from Lower Panther. Prior to fish removal a

significantly greater mean percentage of larvae were observed in Lower Panther search

surveys than in Upper Panther search surveys (Paired T-test, p = 0.002; surveydates = 5 for

each lake)(Figure 2). After fish removal the average percentage of larvae observed in

search surveys did not significantly differ between lakes (Paired T-test, p = 0.12;

surveydates = 4 for each lake)(Figure 2). 

DISCUSSION

This study provides experimental evidence based on whole-lake manipulations

that indicates that A. gracile larval behavior differs between lakes with and without fish.

This study also documents the response of A. gracile larvae to the removal of fish from a

lake. Prior to the removal of all trout from Lower Panther, A. gracile larvae tended to be

primarily active at night. Larvae were mostly restricted to the shallow, shoreline area of

the lake that contained substrates that created complex habitat structure. This structure

provided refuge for larvae from predation by trout. During this same period, salamander

larvae in fishless Upper Panther were active day and night and were observed throughout
48

the lake. In this context, the secretive and restricted behavior of A. gracile larvae in

Lower Panther can be seen as indicative of an anti-predator response to the presence of

fish in the lake.

Previous studies have observed that A. gracile larvae in response to the threat of

predation by trout may decrease their diurnal activity and restrict the number and types of

habitats they occupy in a lake. Efford and Mathias (1969) attributed the secretive and

wary behavior of A. gracile larvae in Marion Lake, British Columbia, Canada, to

predation by trout. In ponds and lakes containing fish in British Columbia and Oregon, A.

gracile larvae are almost exclusively nocturnal (Efford and Mathias 1969; Sprules 1974;

Taylor, 1983). Liss et al. (1995) found that although A. gracile larvae could be detected

during day surveys in some NOCA lakes with fish, most of these larvae were observed in

refuges (e.g., woody debris, rock-talus, undercut banks). At one NOCA lake containing

fish, counts of larvae at night were ten times greater than day counts. Taylor (1983)

reported that in three lakes with fish in the Oregon Cascade Mountains, A. gracile larvae

were detected only in nearshore refugia where the water was #1.3 m deep. Tyler et al.

(1998b) determined that A. gracile larvae in experimental ponds with fish utilized a

narrower range of available habitats (e.g., rock and wood) than did larvae in fishless

controls. In contrast to the nocturnal and secretive behavior of larvae in lakes with fish, A.

gracile larvae in fishless lakes tend to be readily detected during the day, more active

throughout a lake, and do not appear overly wary or secretive in behavior (Sprules 1974;

Taylor 1983).

After all of the fish were removed from Lower Panther by June 1997, the

behavior of A. gracile larvae changed and became strikingly similar to the larval behavior
49

in fishless Upper Panther (Figs. 1 and 2). In essence, upon the removal of fish from

Lower Panther the proportion of larvae observed in the lake during day surveys increased

as did the proportion of larvae observed in the transects (i.e., 2 m and 5 m) further from

the shoreline of the lake. To our knowledge, the present study is the first to indicate that

A. gracile larval behavior can shift following the removal of fish from a lake. The change

in the level of diurnal activity and location of larvae in Lower Panther might be explained

as a form of ecological release, and more specifically as a release from predation. In

general, ecological release is expressed when prey exhibit density compensation and/or

habitat expansion upon reduction of the level of interspecific competition or predation

within an ecosystem (MacArthur et al., 1972; Cox and Ricklefs, 1977; Ricklefs, 1979).

The suppressed species can become more abundant, more active, and less restricted in the

habitats it is able to occupy or exploit. For instance, sea urchin sizes and densities were

higher on Kenyan reefs where the exploitation of predatory fish was high as compared to

reefs where exploitation was low (McClanahan and Muthiga 1988). Furthermore, species

richness and total abundance of young-of-the-year non-piscivorus fishes were greater on

predator removal coral reefs than on control reefs (Caley 1993). In a study examining

ecological release in amphibians, the relative abundance of green frogs (Rana clamitans

Latreille) in Point Pelee National Park, Ontario, Canada, increased four-fold after the

extirpation of the green frogs’ potential competitor and predator, the bullfrog (Rana

catesbeiana Shaw; Hecnar and M’Closkey 1997).

The shift in A. gracile larval behavior in Lower Panther occurred relatively soon

after the last fish were removed from the lake. Ambystoma gracile larvae can co-exist

with introduced trout in mountain lakes albeit at lower densities than in lakes without
50

trout (Liss et al., 1995; Robert Hoffman and Torrey Tyler, personal observations). They

survive in lakes with trout by becoming secretive and wary, and by restricting their

diurnal activity to lake habitats that provide refuge from predation. Being able to coexist

with introduced trout enhances this species’ ability to reestablish potentially threatened

populations upon the removal or extinction of fish from a lake. This outcome is certainly

encouraging as resource managers attempt to deal with issues related to declining

amphibian populations in the western United States. Future research should include

additional amphibian species, especially those that may be less able to coexist with

introduced fish (e.g., Ambystoma macrodactylum Baird; see Tyler et al., 1998a), so that

we may better understand the full potential of amphibian population recovery associated

with the removal of introduced fish from mountain lakes.

ACKNOWLEDGMENTS

This research was funded by the United States Geological Survey, Biological

Resources Division. The authors would like to thank Mike Collopy and the USGS Forest

and Rangeland Ecosystem Science Center for support of this project; Bruce Freet, Reed

Glesne, and park personnel of North Cascades National Park Service Complex; and

Elisabeth Deimling and Gregg Lomnicky for their assistance in completing the field work

associated with this study.
51

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Caley, M.J. 1993. Predation, recruitment and the dynamics of communities of coral-reef

fishes. Marine Biology 117:33-43.

Cox, G.W. and R.E. Ricklefs. 1977. Species diversity and ecological release in Caribbean

land bird faunas. Oikos 28:113-122.

Duellman, W.E., and L. Trueb. 1986. Biology of Amphibians. The John Hopkins

University Press, Baltimore, Maryland, U.S.A. 670 p.

Efford, I.E., and J.A. Mathias. 1969. A comparison of two salamander populations in

Marion Lake, British Columbia. Copeia 1969:723-735.

Efford, I.E., and K. Tsumura. 1973. A comparison of the food of salamanders and fish in

Marion Lake, British Columbia. Transactions of the American Fisheries Society

102:33-47.

Figiel, C.R., and R.D. Semlitsch. 1990. Population variation in survival and

metamorphosis of larval salamanders (Ambystoma maculatum) in the presence

and absence of fish predation. Copeia 1990:818-826.

Formanowicz Jr., D. R. and E. D. Brodie, Jr. 1982. Relative palatabilities of members of

a larval amphibian community. Copeia 1982:91-97.

Gresswell, R.E., W.J. Liss, G.A. Lomnicky, E.K. Deimling, R.L. Hoffman, and T. Tyler.

1997. Using mark-recapture methods to estimate fish abundance in small

mountain lakes. Northwest Science 71:39-44.

Hecnar, S.J. and T. M’Closkey. 1997. Changes in the composition of a ranid frog

community following bullfrog extinction. American Midland Naturalist 137:145-

150.
52

Hintze, J.L. 1998. NCSS 2000. Kaysville, Utah.

Jackson, M.A., and R.D. Semlitsch. 1993. Paedomorphosis in the salamander Ambystoma

talpoideum: effects of a fish predator. Ecology 74:342-350.

Kats, L.B., J.W. Petranka, and A. Sih. 1988. Antipredator defenses and the persistence of

amphibian larvae with fishes. Ecology 69:1865-1870.

Kiesecker, J.M., and A.R. Blaustein. 1998. Effects of introduced bullfrogs and

smallmouth bass on microhabitat use, growth, and survival of native red-legged

frogs (Rana aurora). Conservation Biology 12: 776-787.

Liss, W.J., G.L. Larson, E.K. Deimling, R. Gresswell, R. Hoffman, M. Kiss, G.

Lomnicky, C.D. McIntire, R. Truitt, and T. Tyler. 1995. Ecological effects of

stocked trout in naturally fishless high mountain lakes: North Cascades National

Park Service Complex, WA, USA. Technical report NPS/PNROSU/NRTR-95-03.

National Park Service, Pacific Northwest Region, 909 First Avenue, Seattle, WA

98104.

MacArthur, R.H., J.M. Diamond, and J.R. Karr. 1972. Density compensation in island

faunas. Ecology 53:330-342.

McClanahan, T.R. and N.A. Muthiga. 1988. Changes in Kenyan coral reef community

structure and function due to exploitation. Hydrobiologia 166:269-276.

Neish, I.C. 1971. Comparisons of size, structure, and distributional patterns of two

salamander populations in Marion Lake, British Columbia. Journal of the

Fisheries Research Board of Canada 28:49-58.

Nussbaum, R.A., E.D. Brodie, and R.M. Storm. 1983. Amphibians and Reptiles of the

Pacific Northwest. The University Press of Idaho, Moscow, Idaho. 332 p.
53

Resetarits, Jr., W.J. 1995. Competitive asymmetry and coexistence in size-structured

populations of brook trout and spring salamanders. Oikos 73:188-198.

Ricklefs, R.E. 1979. Ecology, second edition. Chiron Press, Inc., New York. 966 p.

Semlitsch, R.D. 1987. Interactions between fish and salamander larvae: costs of predator

avoidance or competition? Oecologia 72:481-486.

Sih, A. 1987. Predators and prey lifestyles: an evolutionary and ecological overview. In

Kerfoot, W.C. and A. Sih (eds.), Predation: Direct and Indirect Impacts on

Aquatic Communities, p. 203-224, University Press of New England, Hanover,

New Hampshire, U.S.A. 386 p.

Sih, A., J.W. Petranka, and L.B. Kats. 1988. The dynamics of prey refuge use: a model

and tests with sunfish and salamander larvae. American Naturalist 132:463-483.

Sih, A., L.B. Kats, and R.D. Moore. 1992. Effects of predatory sunfish on the density,

drift, and refuge use of stream salamander larvae. Ecology 73:1418-1430.

Sprules, W.G. 1974. The adaptive significance of paedogenesis in North American

species of Ambystoma (Amphibia: Caudata): an hypothesis. Canadian Journal of

Zoology 52:393-400.

Stangel, P.W., and R.D. Semlitsch. 1987. Experimental analysis of predation on the diel

vertical migrations of a larval salamander. Canadian Journal of Zoology 65:1554-

1558.

Taylor, J. 1983. Orientation and flight behavior of a neotenic salamander (Ambystoma

gracile) in Oregon. American Midland Naturalist 109:40-49.
54

Tyler, T., W.J. Liss, L.M. Ganio, G.L. Larson, R. Hoffman, E. Deimling, and G.

Lomnicky. 1998a. Interaction between introduced trout and larval salamanders

(Ambystoma macrodactylum) in high-elevation lakes. Conservation Biology

12:94-105.

Tyler, T.J., W.J. Liss, R. L. Hoffman, and L.M. Ganio. 1998b. Experimental analysis of

trout effects on survival, growth, and habitat use of two species of Ambystomatid

salamanders. Journal of Herpetology 32:345-349.
55

Figure 1. Percent of Ambystoma gracile observed during day (versus night) 2 m

and 5 m surveys in Lower Panther and Upper Panther Lakes. No fish were 

observed in Lower Panther Lake after June 1997. FR indicates when Lower 

Panther Lake was considered fishless.

Date

6/94 6/95 8/95 6/96 8/96 7/97 6/98 8/98

Diurnal Observations (as % of total)

0

10

20

30

40

50

60

70

80

90

100

Lower Panther

Upper Panther
56

Figure 2. Percent of Ambystoma gracile larvae observed in the immediate shoreline areas

of Lower Panther and Upper Panther Lakes during day search versus day 2 m + 5 m surveys

No fish were observed in Lower Panther Lake after June 1997. FR indicates when Lower 

Panther Lake was considered fishless.

date

6/94 6/95 8/95 6/96 8/96 7/97 6/98 8/98 8/99

Search Survey Observations (as % of total)

0

10

20

30

40

50

60

70

80

90

100

Lower Panther

Upper Panther
57

CHAPTER 3

Distributions and Abundances of Larval Salamanders (Ambystoma macrodactylum)

and Large Copepods (Diaptomus sp.) in Relation to Introduced Trout and Abiotic

Factors in Mountain Lakes of North Cascades National Park Service Complex

William J. Liss1, Gary L. Larson2, Lisa Ganio3,

Torrey J. Tyler1, Robert L. Hoffman4

1 Department of Fisheries and Wildlife, Oregon State University, Nash Hall 104,

Corvallis, Oregon 97331, USA.

2 USGS, Forest and Rangeland Ecosystem Science Center, 3200 SW Jefferson Way,

Corvallis, Oregon 97331, USA.

3 Department of Forest Sciences, Oregon State University, Corvallis, Oregon 97331,

USA.

4 College of Oceanic and Atmospheric Sciences, 104 Ocean Admin, Oregon State

University,Corvallis, OR 97331, USA.
58

ABSTRACT

From 1989 through 1999 we conducted research to determine the impacts of stocked

trout on native biota in mountain lakes in North Cascades National Park Service Complex

(NOCA), located in the Northern Cascades Province of northern Washington, USA. We

performed a meta-analysis of data for larval salamanders for all lakes sampled from

1990-1994 and 1998-1999 (n = 63 lakes) and data for crustacean zooplankton for all

lakes sampled from 1989-1994 (n = 70 lakes). The purpose of the analysis was to

determine the influence of a suite of abiotic factors on the distributions and abundances

of larval Ambystoma macrodactylum and diaptomid copepods, and to test whether

observed larval abundances of A. macrodactylum and densities of large diaptomid

copepods differed among fishless lakes, lakes with non-reproducing trout populations

that are periodically stocked with fry at low densities, and lakes with reproducing trout

populations that tend to reach high fish densities. For fishless lakes (n = 28), observed

larval salamander abundance was positively related to total Kjeldahl-N (TKN)

concentration and water temperature. Larval abundances were low and no differences in

abundances were detected among fishless lakes (n = 17) and lakes with non-reproducing

(n = 10) or reproducing (n = 9) trout populations when lake TKN concentration was 

< 0.045 mg/L. For lakes with TKN ≥ 0.045 mg/L, lakes with reproducing trout

populations (n = 8) had significantly lower abundances of larvae than fishless lakes (n =

11) and lakes with non-reproducing trout populations (n = 7). Observed larval

abundances in fishless lakes and lakes with non-reproducing trout populations did not

differ significantly in lakes with TKN ≥ 0.045 mg/L. However, larval abundances in

fishless lakes with TKN ≥ 0.055 mg/L (n = 8) were significantly greater than abundances
59

in lakes with non-reproducing trout populations over the same TKN range (n = 4),

although sample size of lakes with non-reproducing trout populations was small. Analysis

using a general linear model with reproductive status of the fish population as a

categorical variable revealed that large copepod density was influenced by maximum

lake depth, total phosphorus concentration, and water temperature. Of these three abiotic

variables only temperature was a significant factor when the presence/absence and

reproductive status of the fish population in lakes were considered. Large copepod

densities were significantly different between fishless lakes and lakes with reproducing

trout populations for temperatures > 12°C. There were no significant differences in large

diaptomid densities between fishless lakes and lakes with non-reproducing trout

populations. These results suggest that larval salamanders and large crustacean

zooplankton may be at greatest risk from introduced trout in lakes with reproducing fish

populations that have TKN concentrations ≥ 0.045mg/L and water temperatures > 12°C.

Larval salamanders also appear to be at risk in lakes with non-reproducing trout

populations that have TKN concentrations ≥ 0.055mg/L. Native biota appear to be at

minimum risk in lakes with TKN concentrations < 0.045 mg/L regardless of fish

presence/absence or reproductive status.
60

INTRODUCTION

Most mountain lakes in the western USA were originally fishless and considered

“barren”. These lakes were stocked with fish during the early to mid-20th century

primarily to provide recreational angling opportunities (Bahls 1992). Although mountain

lakes in the western USA are popular locations for recreational angling, the possible

environmental impacts of introduced non-native fish on native biota are a concern. A

reduction in abundance or elimination of some species of frogs (e.g., Bradford, 1989;

Bradford et al., 1993; Fellers and Drost, 1993; Blaustein et al., 1994; Knapp and

Matthews, 2000), ambystomatid salamanders (Taylor, 1983a; 1983b; Tyler et al., 1998a),

and crustacean zooplankton (e.g., Starkweather, 1990; Stoddard, 1987; Donald et al.,

1994; Liss et al., 1998) have been attributed to the introduction of trout into mountain

lakes. Food web alterations in mountain lakes associated with the introduction of trout

also have contributed to changes in the nutrient dynamics of these lakes (e.g., Leavitt et

al., 1994).

Ambystomatid salamanders often are among the top vertebrate predators in

fishless mountain lakes in the Pacific Northwest (Taylor, 1983a; Tyler et al., 1998a).

Introduced non-native fish can limit the distribution of salamanders (Thompson et al.,

1980), restrict the range of habitats they utilize (Semlitsch, 1987; Stangel and Semlitsch,

1987; Figiel and Semlitsch, 1990; Tyler et al., 1998b), reduce growth by limiting larval

feeding opportunities (Semlitsch, 1987; Figiel and Semlitsch, 1990; Tyler et al., 1998b),

and reduce survival and local population abundance (Petranka, 1983; Taylor, 1983a,

1983b; Semlitsch, 1987, 1988; Sih et al., 1988, 1992; Tyler et al., 1998a, 1998b).
61

Diaptomid copepods are among the largest, most visible zooplankters in mountain

lakes (e.g., Dodson, 1970; Anderson, 1971; Stoddard, 1987; Donald et al., 1994; Liss et

al., 1998). Planktivorous predators such as some fish species and salamanders can prey

selectively on larger, more visible zooplankton and can reduce their abundance or

eliminate them from lakes (Dodson, 1970; Sprules, 1972; Zaret, 1980; Morin, 1987; Stein

et al., 1987; Gliwicz and Pijanowska, 1989). Impacts of planktivorous vertebrate

predators are thought to be greatest in lakes where predation intensity is high (e.g.,

Gliwicz and Prejs, 1977; Dodson, 1979; Zaret, 1980; McQueen et al., 1986; Post and

McQueen, 1987; Liss et al., 1998). Predation intensity on zooplankters can increase if a

community shifts in composition toward predator species that are more planktivorous

(e.g., Bays and Crisman, 1983; Hessen et al., 1995), if the size distribution shifts toward

smaller individuals that may be more prone to planktivory than larger individuals, or if a

planktivore population increases in abundance (e.g., Zaret, 1980; Carpenter et al., 1985). 

Abiotic factors such as lake depth can mediate interactions between vertebrate

planktivores and their zooplankton prey. In deep lakes, zooplankton may undergo vertical

migrations and escape predation from visually oriented predators (e.g., Zaret, 1980; Stich

and Lambert, 1981; Gliwicz and Pijanowska, 1988; Donald et al., 1994). Thus, impacts

of vertebrate predation on zooplankton are most likely to be observed in shallow lakes

where deep-water refugia may not be available (Gliweicz and Prejs, 1977; Donald et al.,

1994; Liss et al., 1998).

From 1989 through 1999, we conducted research to determine the impacts of

stocked trout on native biota in lakes in North Cascades National Park Service Complex

(NOCA), located in the North Cascades Province of northern Washington, USA.
62

Analyzing data collected from 1990-1994, Tyler et al. (1998a) found that the abundance

of larval long-toed salamanders (Ambystoma macrodactylum) in NOCA lakes was

positively related to lake productivity as indicated by total Kjeldahl-N concentration

(TKN). The effects of stocked trout on larval salamanders appeared to be related to a

lake’s TKN concentration and the reproductive status of the introduced trout population.

The abundances of salamander larvae in fishless lakes were significantly higher than

abundances in lakes with non-reproducing trout populations only in lakes with TKN >

0.09 mg/L (Tyler et al., 1998a). These populations were composed of fish that did not

reproduce in a lake but instead were periodically stocked as fry at low densities.

However, larval abundances in fishless lakes were significantly greater than in lakes with

reproducing trout populations in lakes with TKN ≥ 0.045 mg/L (Tyler et al., 1998a). At

TKN < 0.045 mg/L there were no significant differences in larval abundances among

fishless lakes, lakes with non-reproducing trout populations, and lakes with reproducing

trout populations. One difficulty with the Tyler et al. (1998a) study was that the sample

size of lakes with non-reproducing trout populations was small (i.e., n = 7). Chapter 1 of

this report presented the results of research conducted from 1998-1999 that was

specifically directed at assessing the impacts of non-reproducing trout populations on

larval salamander abundance and behavior. The results and conclusions of the work

conducted in 1998-1999 were consistent with the results of Tyler et al. (1998a). 

Liss et al. (1998) reported results of research on the potential effects of stocked

trout on crustacean zooplankton in NOCA lakes, sampled at least twice per year, from

1989-1994 (n = 28). They found that the density of large diaptomid copepods in lakes

with high densities of reproducing trout and maximum depths ≤ 10 m was significantly
63

lower than in deeper lakes (maximum depth > 10 m) with reproducing or nonreproducing trout populations. In lakes where conditions were suitable for the small

herbivorous diaptomid, D. tyrrelli, the small copepod was often abundant in lakes where

trout densities were high and large predaceous diaptomids were absent or in low

abundance.

This chapter presents a meta-analysis of the combined sets of data for larval

salamanders collected from 1990-1994 and 1998-1999 (n = 63 lakes), and data for

crustacean zooplankton for all lakes that were sampled from 1989-1994 (n = 70 lakes).

The purpose of this analysis is: 1) to determine the influence of a suite of abiotic factors

on the distributions and abundances of larval Ambystoma macrodactylum and diaptomid

copepods; 2) to test whether observed A. macrodactylum larval abundances and densities

of large diaptomid copepods differed among fishless lakes, lakes with non-reproducing

trout populations, and lakes with reproducing trout populations; 3) to compare the results

of the meta-analysis embodied in objectives 1 and 2 with the earlier work by Tyler et al.

(1998a), the results from Chapter 1 of this report (1998-1999), and the work by Liss et al.

(1998); and 4) to develop inferences concerning the influence of biotic and abiotic factors

on the relative risk of larval salamanders and large diaptomids from stocked trout in

NOCA lakes.

METHODS 

There are approximately 154 lakes in NOCA of interest to National Park Service

(NPS) and Washington Department of Fish and Wildlife (WDFW) managers. The lakes

range in elevation from 412 m to over 2000 m. We restricted our analysis to lakes higher

than 800 m, the elevation range where most of the lakes in NOCA occur. Although lakes
64

within NOCA are thought to be historically fishless, during the last century, many NOCA

lakes were stocked with trout, primarily Oncorhynchus clarki and O. mykiss, to provide

recreational angling opportunities. There are two species of ambystomatid salamanders

(Ambystoma macrodactylum and A. gracile) present in NOCA lakes. These species rarely

co-occur (Liss et al., 1995).

At NOCA, lakes with trout can be grouped by the reproductive status of the trout

population (Tyler et al., 1998a; Liss et al., 1998). In lakes where fish successfully

reproduce, trout often reach high densities and have a complex age and size structure

(Gresswel l et al., 1997). In mark-recapture studies of fish density in nine lakes with

reproducing trout, average fish density was 524 fish/ha for fish larger than 177mm total

length (range 250-724 fish/ha, except one lake at 98 fish/ha; Gresswell et al., 1997). In

lakes where trout do not successfully reproduce, fish were periodically stocked as fry or

fingerlings at low to moderate densities with intervals between successive stockings

averaging about five years (average stocking density in 37 NOCA lakes = 179 fry/ha;

range = 60-375 fry/ha; 1976 to 1993; Liss et al., 1998). The reproductive status of trout

populations in NOCA lakes was determined from NOCA records (Jarvis, 1987) and

verified with field observations. Lack of successful reproduction in a lake was inferred

from failure to observe fry or smaller fish, little variation in size and age structure of fish

captured by gill net and angling, and a lack of suitable spawning habitat. Gillnets were

fished for several hours in each fishless lake to confirm that fish were absent.

From 1990 through 1999, 28 fishless lakes, 17 lakes with non-reproducing trout,

and 18 lakes with reproducing trout were sampled to determine the effects of trout on

larval salamanders. These lakes represent 41% of the 154 NOCA lakes of interest to fish
65

NPS and WDFW managers. In addition, from 1989-1994, zooplankton were sampled in

32 fishless lakes, 17 lakes with non-reproducing trout populations, and 21 lakes with

reproducing trout populations, collectively representing 45% of the lakes of interest. The

number of lakes sampled in each fish category and the number of times that lakes in each

category were sampled varied over the course of the study (Tables 1 and 2). Lakes were

sampled between ice-out in late June or early July and the onset of inclement weather in

late September.

 Larval salamanders were censused by snorkel surveys (Tyler et al., 1998a).

Snorkel methods tend to under-represent small, cryptic, and benthic individuals in density

estimates (Helfman, 1983). Therefore, larval salamander abundance estimates from

snorkel surveys are conservative. Tyler et al. (1998a) found no difference in larval A.

macrodactylum abundance estimates between surveys conducted at night and during the

day. Therefore, the data used in the analysis were from snorkel surveys performed during

mid-afternoon.

In lake shoreline surveys conducted from 1990 to 1993, a snorkeler carefully

searched through substrate materials (talus, woody debris, fine organic matter, aquatic

vegetation) within 2 m of the shoreline and recorded the number of larvae observed and

the length of the shoreline sampled (Tyler et al., 1998a). From 1994 to 1999, snorkel

surveys were conducted over four 25 m segments of shoreline that were randomly chosen

along the perimeter of each lake. The same shoreline segments were snorkeled on each

successive sampling visit. 

Salamander species identification was made in the field based on larval

characteristics outlined in Corkran and Thoms (1996). When species identification could
66

not be ascertained in the field, representative larvae were captured and reared to

metamorphosis in a laboratory to confirm species identification.

To sample crustacean zooplankton in each lake, three replicate vertical tows were

taken near the deepest part of the lake with a 20 cm diameter number 25 (64 μm mesh)

zooplankton net, except in 1989 when only one vertical tow was taken. The net was

lowered to within one meter of the lake bottom and towed upward at a rate of about 0.5

m/sec. In the field, samples were preserved in 5% neutral sugar formalin (Haney and

Hall, 1973). In the laboratory, samples were split using a Folsom plankton splitter. A split

portion was poured into a settling chamber and left to settle for 24 hours. Organisms were

counted using an inverted microscope at l00X magnification. The average body length of

adult female crustacean zooplankters of each taxon was determined. Mean density of

adult crustacean zooplankton was calculated for each lake. 

Eleven abiotic variables were measured for each lake during each sampling visit.

A hand-held sonar gun was used to determine maximum depth of each lake. Lake

elevations were derived from 7.5 min USGS topographical maps, and lake surface areas

were determined by digitization of lake shorelines outlined on these maps. During each

sampling visit, water temperature was recorded and water samples were collected from

one meter below the lake surface over the lake’s deepest point. Water samples and

temperature recordings were gathered over the deepest point in each lake to standardize

sampling among lakes. Temperature measurements were taken during mid-afternoon with

an Omega 871 thermo-couple. Water samples were collected with a 1.5 L van Dorn-style

sampling bottle. One liter of collected water was filtered in the field using a 0.7 μm

Whatman GF/C mesh glass fiber filter. Water samples were frozen upon return from the
67

field to facilitate transport. Frozen filtered and unfiltered water samples were transported

to the Cooperative Chemical Analytical Laboratory at Oregon State University, Corvallis,

Oregon, for analyses of total phosphorus, total Kjeldahl-N, ammonium-N, and nitrate-

/nitrite-N concentrations, and for alkalinity, pH, and conductivity.

Statistical analyses were conducted using Statgraphics Plus Version 4 and SAS.

Log-transformed larval salamander abundances, log-transformed diaptomid copepod

densities, and abiotic variables were compared among fishless lakes, lakes with nonreproducing trout populations, and lakes with reproducing trout populations using the

Kruskal-Wallis test (α = 0.05). If a statistically significant difference was found, the

Mann-Whitney test was used to conduct pair-wise comparisons of the fish categories to

determine which categories were significantly different. The level of significance was set

at α = 0.017 to adjust for Type I error for the three pair-wise comparisons (α = 0.05/3).

Some variables were natural logarithm-transformed to satisfy the assumption of equality

of variance among fish categories.

Stepwise multiple regression was used for each fish category (fishless, n = 28;

non-reproducing trout, n = 17; reproducing trout, n = 17) to determine relationships

between abiotic factors and observed larval salamander abundance. MR 16, a lake with a

reproducing trout population, was eliminated from the data set because it had an

unusually low fish density (as determined by mark-recapture) relative to other lakes with

reproducing fish populations. The response variable for each regression was the natural

logarithm of average larval abundance in each lake. Similar data collected on multiple

occasions from the same lake were averaged to obtain a single value for each variable for

each lake. Explanatory variables were the average values for each of the 11 abiotic
68

variables for each lake. Stepwise selection of variables was terminated when variables

added to models were no longer significant at α < 0.05. 

A general linear model was used to determine relationships between abiotic

factors and large copepod density. The response variable for the regression was the

natural logarithm of average copepod density. Fish category (fishless, non-reproducing

trout, reproducing trout) was used as a categorical variable. Explanatory variables were

the average values for each of the 11 abiotic variables for each lake. Terms consisting of

the interaction of fish category with each of the abiotic variables were also introduced.

All of the terms were placed in the full model and then removed in a stepwise fashion.

We removed non-significant interaction terms first. We then evaluated the significance of

the main effect of the abiotic variable in each non-significant interaction term and

removed it from the model if it was not significant. If an abiotic variable interacted

significantly with fish category we did not remove it from the model. The main effect of

fish category also was kept in the model. We used a contrast statement in SAS to

generate confidence intervals for differences in predicted values of the response variable

between fishless lakes and lakes with reproducing trout, and between fishless lakes and

lakes with non-reproducing trout for selected values of the explanatory variables. The

differences were deemed insignificant if the confidence intervals included zero. 

To determine if large diaptomid copepods affected the abundance of the small

herbivorous copepod, Diaptomus tyrrelli, we used a stepwise regression procedure

similar to the one used for large copepods. The natural logarithm of D. tyrrelli was the

response variable, fish category (fishless, non-reproducing trout, reproducing trout) was a
69

categorical variable, and the explanatory variables were the average values for each of the

11 abiotic variables for each lake. 

Pearson’s correlation matrices were developed to investigate significant

relationships between chemical and physical variables used in the regression analyses. A

sequential Bonferroni adjustment was performed on the Pearson’s correlation matrices to

eliminate Type I error and maintain table-wide significance at α = 0.05 (Miller, 1981;

Rice, 1989).

Stepwise multiple regression was used to determine relationships between

observed larval salamander abundance and the density of large diaptomid copepods. The

response variable was natural log-transformed large copepod density, and the explanatory

variables were abiotic variables and observed larval salamander abundance. Analysis was

conducted only for fishless lakes because larval A. macrodactylum were absent or present

in low abundance in lakes with fish (Tyler et al., 1998a). Larval salamander abundance

was estimated in 17 of the 32 fishless lakes in the zooplankton data set. Densities of

larval salamanders in fishless lakes ranged from zero to 73 larvae/100 m of shoreline.

RESULTS

Larval Salamanders

Observed abundances of larval salamanders varied considerably among all lakes,

and larvae were absent from many lakes in each fish category (i.e., fishless lakes, lakes

with non-reproducing trout populations, and lakes with reproducing trout populations)

(Figure 1). Larvae were present in 50% (n = 14) of fishless lakes sampled (n = 28), in

65% (n = 11) of lakes sampled with non-reproducing trout populations (n = 17), and in
70

24% (n = 4) of lakes sampled with reproducing trout populations (n = 17). Larval

abundances > 20 larvae/100 m of shoreline surveyed were found only in fishless lakes. 

There were significant differences in larval salamander abundances among

fishless lakes, lakes with non-reproducing trout, and lakes with reproducing trout

(Kruskal-Wallis; p = 0.016; Table 3). Lakes with reproducing trout had significantly

lower larval abundances than did fishless lakes (Mann-Whitney; p = 0.017) and lakes

with non-reproducing trout (Mann-Whitney; p = 0.004). Observed larval abundances did

not differ significantly between fishless lakes and lakes with non-reproducing trout

populations. Of the 11 abiotic variables, lake surface area (Kruskal-Wallis; p = 0.0008),

total phosphorus (Kruskal-Wallis; p = 0.036), and maximum depth (Kruskal-Wallis; p =

0.048) differed significantly among the fish categories (Table 3). The surface area of

fishless lakes was significantly smaller than the surface areas of lakes supporting nonreproducing trout populations (Mann-Whitney; p = 0.0008) and lakes with reproducing

trout populations (Mann-Whitney; p = 0.004). Lakes with non-reproducing trout were

significantly deeper than fishless lakes (Mann-Whitney; p = 0.017), but not significantly

deeper than lakes with reproducing trout. Fishless lakes had significantly higher total

phosphorus concentrations than did lakes with non-reproducing trout (Mann-Whitney; p

= 0.005). 

The observed larval salamander abundances in fishless lakes were positively

related to total Kjeldahl-N (TKN) concentration and water temperature (p < 0.0001, R2 =

0.59; Figure 2a and 2b): 

Ln (Density) = β0 + β1(TKN) + β2(TEMP)

 [where, β0 = -9.72±1.87; β1 =47.18±12.62; and β2 =0.48±0.15].
71

Of the abiotic variables, TKN concentration was the most strongly related to larval

abundance (R2 = 0.43). Temperature was less strongly related to larval abundance (R2 =

0.36). In the regression model, a slightly greater proportion of the total variation in larval

abundance was explained by TKN concentration (partial R2 = 0.36) than by temperature

(partial R2 = 0.29). In fishless lakes, TKN concentration was positively correlated with

total phosphorus (p < 0.0001) and water temperature was negatively correlated with

nitrate-/nitrite-N (p = 0.0040). Regression analysis did not calculate a significant equation

relating larval A. macrodactylum abundances to any of the 11 abiotic variables for lakes

with non-reproducing or reproducing trout populations. 

In fishless lakes, larvae were absent from 13 of the 17 lakes with TKN < ~ 0.045

mg/L (Table 4). Observed larval abundances in the remaining fishless lakes with TKN <

~ 0.045 mg/L were less than four larvae/100m of shoreline surveyed (Table 4 and Figure

2a). In contrast, larvae were present in ten of the 11 fishless lakes with TKN ≥ 0.045

mg/L, and were abundant (i.e., > 10 individuals/100 m of shoreline surveyed) in eight of

these lakes (Table 4 and Figure 2a). 

Given this relationship between abundance and TKN concentration, the larval

abundances of lakes with TKN ≥ 0.045 mg/L were compared among fish categories using

the Kruskal-Wallis test. For lakes within this TKN range, there were significant

differences in observed larval salamander abundances among fishless lakes, lakes with

non-reproducing trout, and lakes with reproducing trout (Kruskal-Wallis; p = 0.001).

Lakes with reproducing trout had significantly lower abundances (average = 0.14

larvae/100 m shoreline; median density = 0.12 larvae/100 m shoreline; n = 8; Table 4)

than fishless lakes (average = 28.5 larvae/100 m shoreline; median density = 19.5
72

larvae/100 m shoreline; n = 11; Mann-Whitney; p = 0.003) and lakes with nonreproducing trout populations (average = 4.71 larvae/100 m shoreline; median density =

2.5 larvae/100 m shoreline; n = 7; Mann-Whitney; p = 0.003). Larval abundances in

fishless lakes and lakes with non-reproducing trout populations did not differ

significantly in lakes with TKN ≥ 0.045 mg/L (Mann-Whitney; p = 0.046). However,

observed larval abundances for fishless lakes with TKN ≥ 0.055 mg/L (average = 37.1

larvae/100 m shoreline; median density = 31.6 larvae/100 m shoreline; n = 8) were

significantly greater than abundances in lakes with non-reproducing trout populations

over the same TKN range (average = 1.89 larvae/100 m shoreline, median = 1.9; MannWhitney test, p = 0.009), although sample size of lakes with non-reproducing trout was

small (n = 4). 

The surface areas of lakes with TKN ≥ 0.045 mg/L differed among fish categories

(Kruskal-Wallis; p = 0.0005). Fishless lakes were found to be significantly smaller

(average = 0.5 ha; median = 0.3 ha; n = 11) than lakes with non-reproducing trout

populations (average = 2.1 ha; median = 1.2 ha; n = 7; Mann-Whitney test; p = 0.006)

and lakes with reproducing trout (average = 6.1 ha; median = 4.2 ha; n = 8; MannWhitney test; p = 0.0005). Surface area did not differ significantly among the fish

categories for lakes with TKN < 0.045 mg/L (Kruskal-Wallis; p = 0.217).

Concentrations of TKN ≥ 0.045 mg/L tend to be found in shallower NOCA lakes

(~ < 10.0 m; Figure 3), which is generally consistent with the distribution of abundant

salamander populations (Figure 4). Shallow lakes where salamanders were not abundant

usually had low TKN (Table 4). Trout generally are not found in NOCA lakes with

maximum depths < 2.0 m.
73

Diaptomid Copepods

The largest crustacean zooplankters in NOCA are Diaptomus kenai (mean length

= 1.88 mm) and Diaptomus arcticus (mean length = 2.04 mm). Diaptomus kenai is the

most ubiquitous, occurring in 65% of all the lakes that were sampled. Diaptomus arcticus

is present in 9% of the sampled lakes. 

Large diaptomid copepod densities, like observed larval salamander abundances,

varied considerably among all sampled lakes (Figure 5). Large copepods were present in

61% (n = 19) of the fishless lakes sampled (n = 32), in 88% (n = 15) of sampled lakes

with non-reproducing trout populations (n = 17), and in 59 % (n = 12) of sampled lakes

with reproducing trout populations (n = 21). 

There were significant differences in large copepod densities among fishless

lakes, lakes with non-reproducing trout populations, and lakes with reproducing trout

populations (Kruskall-Wallis, p = 0.021; Table 5). The median density of large copepods

in lakes with non-reproducing trout populations was significantly higher than the median

density of large copepods in lakes with reproducing trout (Mann-Whitney; p = 0.003).

The median density of large copepods in fishless lakes was not significantly different

from median densities in lakes with non-reproducing or reproducing trout populations.

Lake surface area was the only abiotic variable that varied significantly among fish

categories. Lakes with reproducing trout populations were significantly larger than

fishless lakes (Mann-Whitney; p = 0.012).

Maximum depth, total phosphorus, and temperature were significant in the

general linear model created when the presence or absence of reproducing trout (RF) or

non-reproducing trout populations (NRF) in the study lakes were used as categorical
74

variables. The regression equation was:

Ln Density = β0 + β1NRF + β2RF + β3 MAXZ + β4 TEMP + β5 TP + β6 (TEMP*RF) + β7 (TEMP*NRF)

[where, β0= -6.070±1.038, β1= -1.644±2.086, β2=3.495±1.933, β3= 0.054±0.016, β4= 

0.329±0.075, β5= -98.967±37.569, β6= 0.192±0.169, and β7= -0.401±0.158].

In the regression model, RF and NRF were assigned a value of one when an observation

was from a lake with either reproducing trout (RF) or non-reproducing trout (NRF)

populations and a value of zero otherwise. There were no significant interactions between

maximum depth or total phosphorus and fish category, whereas the slope of the

relationship between diaptomid copepod density and temperature differed among fish

categories (p = 0.0132). In lakes with water temperatures > 12°C, large diaptomid

copepod densities were significantly different between fishless lakes and lakes with

reproducing trout populations (Table 6). There were, however, no significant differences

in large diaptomid copepod densities between fishless lakes and lakes with nonreproducing trout populations (Table 6) with water temperature >12°C. The range of

temperatures was comparable for lakes in each fish category.

Diaptomus tyrrelli density was positively related to TKN concentration, total

phosphorus, and water temperature, and negatively related to large copepod density (p <

0.00001; R2 = 0.57; n = 68). The regression equation was:

Ln Density = β0 + β1TKN + β2TP + β3TEMP + β4 ln (large diaptomid density)

 [where, β0= -8.48±0.86, β1= 20.44±5.72, β2= 73.46±35.06, β3= 0.20±0.067, 

 and β4= -0.30±0.09.]

There were no significant interactions between the any of the abiotic variables and fish

category. After accounting for all other statistically significant explanatory variables,
75

TKN concentration, large copepod density, and water temperature each explained about

the same amount of variation (partial R2

’s ranged from 0.13-0.17), and total phosphorus

explained 6% of the variation in D. tyrrelli density. Regression analysis did not calculate

a significant equation relating large copepod density to any of the abiotic variables or to

observed larval salamander abundance for the 17 lakes where larval abundances had been

determined.

DISCUSSION

Potential Interactions of Native Biota and Introduced Trout in NOCA Lakes

The distribution of larval Ambystoma macrodactylum among NOCA lakes > 800

m in elevation was patchy, even in lakes without fish. No larvae were observed in over

50% of the fishless lakes sampled. This patchiness suggests that environmental

parameters and their variation between lakes may influence salamander distribution. 

Total Kjeldahl-nitrogen (TKN) concentration was the abiotic variable most

strongly related to the observed abundances of salamander larvae in fishless NOCA

lakes. Tyler et al. (1998a), and Chapter 1 of this report, also found the positive

relationship between TKN concentration and larval salamander abundance in fishless

NOCA lakes to be significant. TKN concentration is a measure of ammonia plus all

organically derived nitrogen (Lambou et al., 1983). Although, organic nitrogen is not

readily utilized by autotrophs (Goldman and Horne, 1983), TKN concentration has been

identified as a good predictor of lake productivity as measured by chlorophyll density

(Lambou et al., 1983) or by total plankton biomass (Paloheimo and Fulthorpe, 1987),

especially when it is correlated with phosphorus and temperature, as it is in NOCA lakes.

A further indication of the usefulness of TKN concentration as a predictor of lake
76

productivity is the positive correlation between cladoceran zooplankton density and TKN

concentration in NOCA lakes (Tyler et al., 1998a). Through examination of salamander

stomach contents, Tyler et al. (1998a) found that larval A. macrodactylum in NOCA lakes

primarily consumed benthic macroinvertebrates and cladoceran zooplankton, particularly

Daphnia rosea. These positive relationships between TKN concentration and various

productivity attributes suggest that there is a positive link between lake primary and

secondary productivity and larval salamander abundance. 

Observed larval salamander abundances between fishless lakes and lakes with fish

also differed relative to the reproductive status of the fish population in lakes with fish.

For lakes with TKN ≥ 0.045 mg/L, fishless lakes and lakes with non-reproducing trout

populations had significantly higher larval abundances than did lakes with reproducing

trout populations. Fishless lakes with TKN ≥ 0.055 mg/L also had significantly higher

larval abundances than abundances in non-reproducing trout lakes with TKN ≥ 0.055

mg/L, although the sample size of lakes with non-reproducing trout was small (n = 4). In

a previous study (i.e., Tyler et al., 1998a), the difference in A. macrodactylum larval

abundance between fishless NOCA lakes and NOCA lakes with non-reproducing trout

was only significant for one non-reproducing trout lake with TKN ≥ 0.09 mg/L. Thus,

results of the present analysis identified a lower TKN concentration at or above which

larval abundances in fishless lakes were significantly higher than abundances in lakes

with non-reproducing trout populations. In none of the analyses were larval salamander

abundances significantly different among fish categories for lakes with TKN < ~

0.045mg/L. 

Large copepod densities among NOCA lakes were quite variable. Maximum lake
77

depth, total phosphorus, and water temperature were correlated with this variation in

large copepod density, although densities were significantly different only in the

interaction between water temperature and fish category. In lakes with average water

temperatures ≤ ~ 10° C, large copepods were virtually absent from lakes regardless of

fish category. In these lakes, cold temperatures may slow development and delay

maturation, making large copepod persistence difficult in lakes at elevations where the

ice-free season is relatively short (Allan and Goulden, 1980). However, large copepod

densities in lakes with average water temperatures > 12°C and that supported reproducing

trout populations were significantly lower than in fishless lakes with average water

temperatures > 12°C. These results suggest that at NOCA, large copepods occur more

often in lakes with higher water temperatures and that reproducing trout populations can

reduce the abundance of or possibly eliminate large copepods from these types of lakes.

Analysis of the interaction between maximum lake depth, total phosphorus, and

fish category indicated that the relationship between large copepod density and each of

these two abiotic variables did not vary significantly relative to the reproductive status of

the trout population in study lakes. However, Liss et al. (1998), analyzing a smaller

NOCA lake data set, did determine that large copepod densities in reproducing trout lakes

> 10 m maximum depth were significantly higher than densities in reproducing trout

lakes < ~ 10 m maximum depth. Donald et al. (1994), in lakes of the Canadian Rockies,

found differences in large zooplankton abundances between shallow fishless lakes and

shallow lakes with fish, but not in deep lakes. Perhaps large zooplankton (e.g., diaptomid

copepods) persist in deeper lakes with fish because in these systems they are able to

diurnally migrate to refuge in deeper water to escape vertebrate predation (e.g., Zaret and
78

Suffern, 1976; Stich and Lambert, 1981; Gliwicz and Pijanowska, 1988; Donald et al.,

1994). Large copepod density was negatively related to total phosphorus in fishless lakes

(Table 6). It is unclear why this relationship would be negative since NOCA lakes with

higher concentrations of total phosphorus support a greater total number of zooplankton

species, including more species of cladocerans and the small herbivorous diaptomid, D.

tyrrelli, than do lakes with lower total phosphorus concentrations (W. J. Liss,

unpublished NOCA data).

Diaptomus tyrrelli density in NOCA lakes was positively related to water

temperature, TKN concentration, and total phosphorus, and negatively related to large

copepod density (also, see Liss et al., 1998). It is unclear whether the inverse relationship

between small and large copepod density is a consequence of lake environmental

conditions “favoring” species of one size-group over another or due to predation of small

copepods by large copepods. It is well known that invertebrate predation can influence

the structure of zooplankton communities. For example, predacious large copepods (e.g.,

D. arcticus) can prey on smaller copepods (e.g., D. tyrrelli) and reduce their abundance

or eliminate them from lakes (e.g., Anderson, 1970; Dodson, 1970, 1974; Sprules, 1972;

Paul et al., 1995). However, a reduction in large copepod abundance by introduced fish

can be followed by a corresponding increase in small copepod abundance (Anderson,

1970). This relationship in NOCA lakes has been implied by observations that densities

of D. tyrrelli were typically high in relatively shallow (i.e., < ~ 10 m maximum depth)

lakes, with relatively high TKN concentration (i.e., > ~ 0.05 mg/L) and reproducing trout

populations, where large copepods were absent and assumed eliminated by the introduced

fish (Liss et al., 1998). These kinds of cascading effects in food webs may be most
79

evident in montane oligotrophic systems (Gliweicz and Prejs, 1977; Dodson, 1979;

McQueen et al., 1986; Neill, 1987; Carney, 1990); and in NOCA, potential representative

lakes include Dagger, Kettling, and Upper Triplet (Liss et al., 1998). 

There was no significant relationship between larval salamander abundance and

large copepod density in fishless lakes. Thus, in contrast to the apparent negative impact

of reproducing trout populations on large copepod density, larval A. macrodactylum

appear to have little impact on the abundance of large copepods. Although larval

salamanders prey on crustacean zooplankton in NOCA lakes (Tyler et al., 1998a),

analysis of stomach contents of larval A. macrodactylum from NOCA lakes found that

diaptomid copepods were present in only 16% of the stomachs examined and were not a

major food item.

Relative Risk to Native Biota From Introduced Trout in NOCA Lakes

TKN concentration and water temperature were measured, either through this

research or earlier lake surveys, in 83 of 154 NOCA lakes of interest to NPS and WDFW

managers. Salamanders or zooplankton were not sampled in many of the 83 lakes, and

these lakes do not include lakes where TKN concentration and water temperature were

measured but were known to contain Ambystoma gracile (Northwestern Salamander)

larvae. The 83 NOCA lakes were not randomly selected for sampling and thus may not

be representative of all NOCA lakes. These lakes, however, represent 54% of all NOCA

lakes of interest to managers and have biotic and abiotic characteristics that are broadly

representative of lakes in the northern Cascade Mountains.

The relative risk to native biota from introduced trout in NOCA lakes appears to

be associated primarily with lake TKN concentration, water temperature, and the
80

reproductive status of the trout population. Native biota appear to be at greatest risk in

NOCA lakes with the following attributes: 1) TKN concentration ≥ 0.045 mg/L; 2) water

temperature >12°C; and 3) a reproducing trout population (indicating a relatively high

density of fish). Six of the 83 NOCA lakes identified above had these attributes

(Appendix I, Table A). The range of larval A. macrodactylum abundances in these lakes

was quite low (i.e., 0 – 1.2 per 100 m survey), as were large copepod densities (i.e., 0 –

0.12 /L; Liss et al., 1998). These low abundances and densities appear to be indicative of

the capacity of reproducing trout to significantly reduce or eliminate larval A.

macrodactylum and large copepods from these lakes. In lakes with non-reproducing trout

populations, larval salamander abundances were not significantly lower than abundances

in fishless lakes until lake TKN concentration was ≥ 0.055 mg/L. Three lakes with nonreproducing trout populations had TKN ≥ 0.055 mg/L and water temperatures >12°C

(Appendix I, Table B).

Differences in larval salamander abundances among fishless lakes and lakes with

non-reproducing or reproducing trout were not statistically significant in lakes with TKN

concentration < 0.045 mg/L. Larval salamander abundances in lakes within this range of

TKN concentrations typically were quite low or larvae were not observed (Table 4).

Large diaptomid copepods, however, could be at risk in some of the lakes with

reproducing trout and water temperatures > 12°C (n = 6; Appendix I, Table B), but

apparently not in the lakes with non-reproducing trout. Thus, the native biotic community

could be at minimal risk in lakes with non-reproducing trout and TKN < 0.045 mg/L. 

Twenty-three of the 83 lakes with known TKN concentration and water

temperature had average temperatures < 10° C (Appendix I, Table C). Larval
81

salamanders were absent from most of these lakes regardless of whether fish were present

or absent (Table 4) and statistically significant differences in large copepods density

among fish categories were not detected.

Lakes with relatively high TKN concentrations (i.e., ≥ 0.045 - 0.055 mg/L) and

water temperatures (i.e., >12°C) likely are more productive habitat for native biota,

especially larval salamanders, than lakes with TKN concentrations and water

temperatures below these levels. Of the 83 lakes with known TKN concentrations, 23

(28%) had TKN concentrations ≥ 0.045mg/L and temperatures > 12° C, and of these 23

lakes only ten lakes were fishless (Appendix I, Table A). These “more productive” lakes

in NOCA, that are fishless, typically have relatively high larval salamander abundances

and these “large” populations may play an important ecological role in montane areas.

Large populations may be less vulnerable to extinction from stochastic events than

“small” populations (e.g., Shaffer, 1981; Goodman, 1987) and so could serve as

important sources of dispersing individuals (sensu Pulliam, 1988; Harrison, 1994) that

could colonize vacant habitats. Ambystoma macrodactylum apparently was able to

colonize lakes in the Rocky Mountains within 20 years following extinction of trout

populations in these lakes (Funk and Dunlap, 1999). Recolonization of habitats where

local population extinctions have occurred also depends on the degree of isolation (or

distance) between sources of dispersers and vacant habitats available for colonization

(Sjogren-Gulve and Ray, 1996; Funk and Dunlap, 1999). Many NOCA lakes occur in

relatively isolated watersheds. This isolation could make it difficult (in terms of time and

distance), if not impossible, for dispersers to emigrate to and colonize vacant habitat. Yet,

given that NOCA lakes with TKN ≥ 0.045 mg/L are apparently productive habitats for
82

native biota, and the likelihood that lakes with productive habitat for native biota

represent a relatively small fraction of all NOCA lakes, a prudent and precautionary

management strategy would be to maximize protection of all NOCA lakes with TKN ≥ ~

0.045.

Summary

The results of this analysis generally are consistent with the view that the impacts

of vertebrate predators on their prey vary along a gradient of increasing vertebrate

predation pressure (Stenson, 1972; Langeland, 1978; Dodson, 1979; Zaret, 1980;

McQueen et al., 1986; Post and McQueen, 1987; Liss et al., 1998), with effects on the

prey likely to be greatest in lakes with high vertebrate predation intensity (Gliwicz and

Prejs, 1977; Donald et al., 1994). The reproductive status of a trout population may serve

as a surrogate for predation intensity in NOCA lakes. Reproducing trout populations in

NOCA lakes tend to reach higher densities and have a more diverse age and size structure

than non-reproducing trout in lakes that are periodically and usually stocked with trout

fry or fingerlings at relatively low densities (Gresswell et al., 1997; Tyler et al., 1998a;

Liss et al., 1998). 

Environmental conditions, however, can mediate effects of vertebrate predators

on prey in NOCA lakes. The highly patchy distributions of larval salamanders and large

copepods at NOCA can be partly explained by variation in environmental conditions

among lakes. Both TKN concentration and water temperature were potentially important

in mediating predator effects in NOCA lakes. Larval salamanders and large copepods

may be at greatest risk from introduced trout in lakes with reproducing trout populations

that have TKN concentrations ≥ 0.045mg/L and water temperatures > 12°C. Lakes with
83

these conditions are likely to be relatively shallow (maximum depth < ~ 10m). Larval

salamanders also appear at risk in lakes with non-reproducing trout populations and TKN

concentrations ≥ 0.055 mg/L. Native biota appear to be at minimum risk in lakes with

TKN < 0.045 mg/L supporting non-reproducing trout.
84

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92

Figure 1. Observed larval Ambystoma macrodactylum abundances in NOCA lakes



































































































































14

6

3

5

6

8

3

0

13

4

0 0

0.00

2.00

4.00

6.00

8.00

10.00

12.00

14.00

16.00

0 > 0 - 5 > 5 - 20 > 20

Density (Individuals/100m shoreline)

Number of Lakes

 Fishless Lakes (n = 28) 

Non-reproducing Fish (n = 17)

 Reproducing Fish (n = 17)
93

Figure 2a. Relationships between larval Ambystoma macrodactylum abundances and total

Kjeldahl-N concentration for 28 fishless lakes,17 lakes with non-reproducing trout

populations, and 17 lakes with reproducing trout populations in North Cascades National

Park Service Complex, Washington, USA. 
94
95

0.00

10.00

20.00

30.00

40.00

50.00

60.00

70.00

80.00

0 0.05 0.1 0.15 0.2

TKN (mg/L)

Salamander Density (no./ 100m shoreline)

Fishless Lakes (n = 28)

Non-reproducing Fish (n = 17)

Reproducing Fish (n = 17)

Figure 2b. Relationships between larval Ambystoma macrodactylum abundances and

water temperature for 28 fishless lakes, 17 lakes with non-reproducing trout populations,

and 17 lakes with reproducing trout populations in North Cascades National Park Service

Complex, Washington, USA.
96
97

0.00

10.00

20.00

30.00

40.00

50.00

60.00

70.00

80.00

0.00 5.00 10.00 15.00 20.00 25.00

Water Temperature (centigrade)

Salamander Density (no./100m shoerline)

Fishless Lakes (n = 28)

Non-reproducing Fish (n = 17)

Reproducing Fish (n = 17)
98

Figure 3. Relationships between total Kjeldahl-N concentration and maximum depth for

83 NOCA lakes. Larval salamander abundances were not estimated in all 83 lakes.
99
100

0.000

0.020

0.040

0.060

0.080

0.100

0.120

0.140

0.160

0.180

0.0 5.0 10.0 15.0 20.0 25.0 30.0 35.0 40.0

Maximum Depth (m)

TKN (mg/l)

Fishless Lakes (n = 40)

Non-reproducing Fish (n = 22)

Reproducing Fish (n = 21)

Salamanders Not Abundant 

In Lakes 

With TKN < 0.045 mg/l

Fish Absent From Lakes

< 2.0 Maximum Depth 

Salamanders Not Abundant In 

Lakes With Maximum Depth > 11.0 m 

Figure 4. Relationships between larval salamander abundance and the maximum depth of

NOCA lakes.

0.00

10.00

20.00

30.00

40.00

50.00

60.00

70.00

80.00

0.0 5.0 10.0 15.0 20.0 25.0 30.0 35.0 40.0 45.0 50.0

Maximum Depth (m)

Salamander Density (no./100m shoreline)

Fishless (n = 28)

Non-reproducing Fish (n = 17)

Reproducing Fish (n = 17)
101
102

Figure 5. Large copepod densities in NOCA lakes.
103
104



































































































































































13

10

6

2

1

2

9

4

0

2

9

10

0

2

0

0

2

4

6

8

10

12

14

0 > 0 - 0.5 > 0.5 - 1.0 > 1.0 - 2.0 > 2.0

Large Diaptomid Density (no./L)

Number of Lakes



 Fishless Lakes (n = 32)

Non-reproducing Fish (n = 17)

 Reproducing Fish (n = 21)
Table 1. The number of lakes in each fish category that were sampled for larval salamanders and cruseach year of the study. Some lakes were sampled in more than one year.

Year Fishless Lakes Non-reproducing Trout Reproducing Tr

Salamanders Zooplankton Salamanders Zooplankton Salamanders Zoo

1989

0 25

0 14

0 

1990

4

8

0

4

4

1991

2

8

2

3

6

1992 1 2 1 3

3

1993 10 13

6 15

8

1994

8

7 1 3

9

1995 1 0

0

1996 1 0

0

1997

3

4

0

1998

8

8

0

1999

8

7

0
Table 2. The number of lakes in each fish category sampled from 1 to 

≥ 5 times for larval salamander

zooplankton from 1990 through 1999. 

Samples Fishless Lakes Non-reproducing Trout Reproducing Tr

Salamanders Zooplankton Salamanders Zooplankton Salamanders Zoo

≥

5

3

6 1 4 1 

4

2

2

2

0

2

3

3

7

3 1 0

2

8

9

6

5

8

1 12

8

5

6

7
107

Table 3. Averages and medians of larval salamander abundances and abiotic variables for

lakes in each fish category. Statistical comparisons were made using Kruskal-Wallis tests,

α = 0.05. Pair-wise comparisons among fish categories were made using the MannWhitney test, α = 0.017.

Fishless Lakes Non-reproducing Trout Reproducing Trout

Variable Average Median Average Median Average Median P value

Density (No./100m shoreline) 11.5 0.25 2.69 0.71 0.06 0.0 0.016

Elevation (m) 1674 1652 1595 1556 1585 1629 0.472

Maximum Depth (m) 6.5 3.9 11 6.0 9.6 5.5 0.048

Surface Area (ha) 1.6 0.7 2.8 1.6 4.3 2.8 0.0008

TKN (mg/L) 0.052 0.04 0.044 0.03 0.040 0.03 0.489

TP (mg/L) 0.006 0.005 0.004 0.004 0.005 0.006 0.036

Nitrate-N (mg/L) 0.006 0.002 0.005 0.004 0.01 0.004 0.321

Ammonia-N (mg/L) 0.006 0.006 0.008 0.004 0.005 0.005 0.360

PH 7.07 7.1 7.04 6.6 7.24 7.3 0.141

Alkalinity (mg/L) 1.84 1.34 1.67 1.48 2.38 2.19 0.073

Conductivity (μS/cm) 18.82 13.38 14.57 11.33 20.59 17.8 0.147

Water Temperature (°C) 12.83 12.56 12.13 12.56 12.67 12.8 0.942
108

Table 4. Averages of larval salamander abundances and abiotic variables for lakes with TKN ≤ 0.045

mg/L and lakes with TKN > 0.045 mg/L from 1990-1999.

MAX SURFACE

LAKE ABUND ELEV DEPTH AREA TKN TP NO3 NH3 pH ALK COND TEMP

Fishless Lakes

MC27 0.00 1488 8.8 4.6 0.001 0.001 0.004 0.003 6.33 0.573 6.733 13.1

DD8 0.00 1600 1.9 0.9 0.020 0.005 0.032 0.013 7.10 1.180 18.000 6.5

FP9 0.00 1662 3.4 0.5 0.020 0.004 0.003 0.003 7.20 1.990 1.990 9.2

M6 1.00 1632 3.6 0.6 0.020 0.002 0.028 0.001 7.70 2.780 22.700 10.2

MC21-1 0.00 1528 5.0 1.2 0.020 0.007 0.000 0.002 6.60 0.820 21.800 5.8

MR11 2.15 1863 8.8 1.3 0.021 0.005 0.003 0.006 7.20 2.480 18.950 14.7

MM6 2.60 1504 11.9 4.1 0.028 0.005 0.005 0.004 7.14 1.918 15.320 9.9

EP3 0.00 1299 3.7 0.4 0.030 0.004 0.007 0.009 7.10 1.230 9.300 11.7

GM2 0.00 1664 47.3 16.1 0.030 0.005 0.000 0.007 7.00 1.030 6.500 15.2

MA3 0.00 2044 6.0 1.3 0.030 0.006 0.000 0.007 7.10 1.570 11.800 12.3

ML1 0.00 1476 1.2 0.2 0.030 0.005 0.024 0.009 7.65 3.155 33.250 8.9

MSH4 0.00 1635 8.9 1.4 0.033 0.005 0.019 0.007 7.30 2.097 18.500 10.4

ML4 0.00 1583 6.4 3.3 0.035 0.003 0.002 0.006 7.75 2.695 20.900 12.8

MA2 0.00 2127 10.0 1.0 0.040 0.009 0.000 0.007 7.10 1.350 9.800 11.4

MC1 3.50 1762 3.0 1.2 0.040 0.002 0.007 0.009 6.50 0.650 4.500 17.4

MR6 0.00 1693 2.1 0.6 0.040 0.008 0.003 0.004 7.55 3.220 32.550 12.9

MR8 0.00 1970 3.5 0.3 0.040 0.005 0.010 0.001 6.90 1.230 8.200 11.0

Average 0.54 1678.2 8.0 2.3 0.028 0.005 0.009 0.006 7.13 1.763 15.341 11.37

MC2 16.50 1800 11.0 1.2 0.045 0.003 0.001 0.004 6.50 0.675 7.600 19.1

MC4 0.00 1604 4.9 0.8 0.050 0.007 0.001 0.006 6.50 0.740 7.200 14.5

MM7 0.50 1642 1.9 0.8 0.055 0.005 0.003 0.005 7.20 2.110 16.550 11.0

MR13-1 13.03 1800 2.0 0.3 0.058 0.008 0.001 0.006 7.50 0.973 7.300 18.1

RD3 73.00 802 8.8 0.3 0.064 0.008 0.001 0.006 7.79 8.520 74.066 16.1

MR3 19.50 1873 2.5 0.2 0.080 0.009 0.002 0.010 6.30 0.598 3.523 15.1

MC10 59.00 1556 4.9 0.4 0.090 0.007 0.001 0.006 6.80 1.330 9.400 15.3

PM5-3 33.00 1382 3.0 0.1 0.095 0.007 0.001 0.006 6.60 0.985 6.700 17.0

MR12 63.85 1981 4.0 0.6 0.125 0.009 0.000 0.003 7.25 1.995 14.950 12.1

MR2 30.17 1873 1.5 0.3 0.137 0.015 0.000 0.006 7.36 2.316 17.830 15.5

SM1 5.00 2033 1.2 0.2 0.170 0.016 0.001 0.009 6.90 1.250 101.000 12.4

AVERAGE 28.50 1667.8 4.15 0.5 0.088 0.008 0.001 0.006 6.97 1.954 24.193 15.10
109

Table 4 continued

MAX SURFACE

LAKE ABUND ELEV DEPTH AREA TKN TP NO3 NH3 PH ALK COND TEMP

Non-reproducing Trout

ML3 0.00 1967 15.2 1.3 0.010 0.004 0.000 0.002 7.20 1.480 12.900 13.4

ML2 0.00 1687 27.4 3.4 0.015 0.003 0.006 0.028 7.90 2.725 28.350 9.4

MR15-1 0.00 1922 27.0 4.8 0.018 0.003 0.018 0.010 7.20 1.943 18.330 12.6

DD5 1.00 1531 5.2 5.2 0.020 0.004 0.007 0.003 6.70 0.930 7.000 4.3

EP5-1 0.00 1543 6.0 2.7 0.020 0.003 0.006 0.004 6.90 1.030 7.800 9.9

MC7 11.00 1556 27.2 6.7 0.020 0.004 0.007 0.003 7.00 1.670 25.300 6.3

MM11 0.00 1974 7.6 1.4 0.020 0.003 0.005 0.002 6.67 0.810 5.033 14.2

MR9 0.71 1813 4.9 1.7 0.027 0.006 0.002 0.007 6.93 1.293 9.867 12.3

MR13-2 0.10 1789 5.0 1.2 0.030 0.004 0.004 0.004 6.93 1.203 9.200 13.1

M19 0.00 1427 24.0 5.0 0.035 0.001 0.012 0.006 6.55 0.670 4.850 10.4

Average 1.28 1720.9 15.0 3.3 0.021 0.003 0.007 0.007 7.00 1.38 12.86 10.59

LS3 10.00 1365 5.2 1.2 0.045 0.004 0.004 0.004 6.45 0.835 6.350 12.5

M1 0.33 1159 4.3 1.6 0.050 0.004 0.001 0.003 6.87 1.443 11.333 13.7

MR11 15.08 1863 8.8 1.3 0.050 0.005 0.003 0.004 7.33 2.688 21.875 13.4

MR12 3.00 1981 4.0 0.6 0.060 0.004 0.001 0.014 7.10 1.530 11.050 16.1

LS3-FS 2.50 1375 6.7 1.2 0.085 0.002 0.004 0.010 6.95 1.615 12.850 9.9

DD1 1.00 1496 2.4 0.5 0.090 0.004 0.001 0.009 7.75 3.320 29.600 16.7

MM10 1.07 662 5.8 8.2 0.145 0.012 0.001 0.027 7.30 3.160 25.950 18.1

AVERAGE 4.71 1414.4 5.3 2.1 0.075 0.005 0.002 0.010 7.11 2.084 17.001 14.32

Reproducing Trout

MR15-2 0.00 1909 3.0 0.3 0.001 0.006 0.021 0.004 7.30 2.210 21.500 9.0

M21 0.00 1205 3.1 1.6 0.010 0.000 0.059 0.000 7.20 2.190 17.500 8.4

LS7 0.00 1510 7.9 2.8 0.020 0.002 0.005 0.005 7.30 1.780 17.800 12.5

M7 0.00 1363 11.0 3.2 0.020 0.003 0.001 0.001 7.10 1.340 10.900 12.5

MLY2 0.00 1629 4.3 2.5 0.025 0.007 0.009 0.005 7.20 2.640 22.050 9.4

CP1 0.00 1642 17.7 12.0 0.030 0.003 0.001 0.005 6.70 0.930 11.800 13.1

M23 0.00 1270 37.2 0.4 0.030 0.002 0.001 0.004 7.30 1.660 13.200 17.0

SM2-2 0.00 1988 4.3 1.0 0.030 0.009 0.027 0.003 7.60 3.340 29.550 10.6

EP9-1 0.00 1580 2.5 0.6 0.040 0.001 0.000 0.002 7.10 1.730 13.100 13.2

Average 0.00 1570.5 9.7 2.9 0.023 0.004 0.013 0.004 7.21 2.010 17.655 11.51

LS2 0.13 1243 4.9 1.0 0.045 0.007 0.002 0.006 7.64 5.837 52.941 12.9

PM3 0.00 1609 5.5 4.3 0.045 0.004 0.005 0.016 7.25 2.280 19.150 9.4

MR14 0.30 1717 10.4 6.3 0.048 0.006 0.004 0.003 6.95 1.340 10.400 11.8

MR10 0.12 1679 6.1 5.0 0.050 0.007 0.002 0.005 7.30 2.033 16.167 13.1

SM2-1 0.00 1931 2.1 1.0 0.051 0.006 0.008 0.004 7.30 3.260 28.750 13.8

MR5 0.40 1639 7.0 4.0 0.055 0.009 0.001 0.005 7.45 2.740 24.400 16.1

M20 0.00 1357 33.0 23.5 0.090 0.003 0.018 0.006 6.60 0.850 6.100 12.8

MR4 0.00 1679 4.0 3.6 0.115 0.010 0.001 0.010 7.85 4.300 34.800 19.9

AVERAGE 0.14 1606.4 9.6 6.1 0.065 0.007 0.005 0.006 7.30 2.909 24.794 14.33
110

Table 5. Averages and medians of zooplankton densities and abiotic variables for lakes in

each fish category. Statistical comparisons were made using Kruskal-Wallis tests, α =

0.05. Pair-wise comparisons among fish categories were made using the Mann-Whitney

test, α = 0.017.

Fishless Lakes Non-reproducing Trout Reproducing Trout

Variable Average Median Average Median Average Median P value

Density (No. L-1) 0.343 0.039 0.487 0.364 0.113 0.0045 0.021

Elevation (m) 1630 1634 1529 1496 1576 1622 0.477

Maximum Depth (m) 9.1 5.0 11.0 7.6 15.2 9.2 0.154

Surface Area (ha) 3.5 1.0 2.0 1.4 7.6 3.8 0.026

TKN (mg/L) 0.049 0.033 0.040 0.033 0.041 0.040 0.997

TP (mg/L) 0.008 0.007 0.006 0.007 0.006 0.006 0.534

Nitrate-N (mg/L) 0.006 0.002 0.004 0.001 0.008 0.005 0.294

Ammonia-N (mg/L) 0.005 0.005 0.005 0.004 0.005 0.005 0.531

PH 6.94 7.0 7.05 6.95 7.11 7.25 0.350

Alkalinity (mg/L) 1.68 1.27 2.19 1.38 2.18 1.76 0.234

Conductivity (μS/cm) 16.82 12.19 22.01 17.20 19.97 15.93 0.534

Water Temperature (°C) 11.51 11.67 12.09 12.28 12.18 12.23 0.799
111

Table 6. Confidence intervals for differences in

predicted values of large copepod density between

fishless lakes (NF) and lakes with reproducing trout

(RF), and between fishless lakes and lakes with nonreproducing trout (NRF) for selected temperatures.

Confidence intervals that do not contain zero indicate

statistically significant differences and are denoted by

an asterisk.

Comparison Confidence Interval

RF vs. NF Lower Upper

6°C -0.969 3.149

10°C -1.561 0.535

12°C -2.167 -0.462*

14°C -3.192 -1.040*

15°C -3.810 -1.224*

NRF vs. NF

6°C -2.738 1.749

10°C -0.881 1.425

12°C -0.262 1.573

14°C -0.086 2.163

15°C -0.117 2.578
Appendix I. Table A. Lakes with TKN ≥ 0.045 mg/L and water temperature > 12°C. NF = fishless lake; NRF 

lake with non-reproducing trout; RF = lake with reproducing trout.

CODE FISH ELEV MAX Z S. AREA TKN TEMP TP NO3 NH3 PH ALK CMC1 NF 1762 3.0 1.2 0.050 17.40 0.002 0.005 0.011 6.53 0.673 MR13-1 NF 1800 2.0 0.3 0.051 14.97 0.008 0.003 0.007 7.05 0.882 MC4 NF 1604 4.9 0.8 0.051 12.40 0.005 0.002 0.012 6.23 0.560 RD3 NF 802 8.8 0.3 0.063 16.05 0.008 0.001 0.006 7.82 8.406 7PM53 NF 1382 3.0 0.1 0.084 17.00 0.007 0.001 0.005 6.53 0.910 FP6 NF 1690 3.4 0.5 0.090 11.90 0.006 0.001 0.007 6.70 0.940 MC10 NF 1556 4.9 0.4 0.090 15.30 0.007 0.001 0.006 6.80 1.330 MR3 NF 1873 2.5 0.2 0.097 14.25 0.010 0.002 0.009 6.33 0.637 MR2 NF 1873 1.5 0.3 0.119 14.98 0.014 0.001 0.006 7.28 2.318 SM1 NF 2033 1.2 0.2 0.154 16.05 0.020 0.001 0.006 6.85 1.211 LS3 NRF 1365 5.1 1.4 0.050 13.23 0.004 0.002 0.004 6.53 0.873 3M1 NRF 1159 4.3 1.6 0.050 13.67 0.004 0.001 0.003 6.87 1.443 MR11 NRF 1863 8.8 1.3 0.050 13.24 0.005 0.002 0.004 7.32 2.670 2M20 NRF 1357 33.0 23.5 0.053 12.15 0.003 0.016 0.010 6.55 0.769 MR12 NRF 1981 4.0 0.6 0.060 16.05 0.004 0.001 0.014 7.10 1.530 DD1 NRF 1496 2.4 0.5 0.075 15.37 0.004 0.001 0.007 8.07 3.494 3MM10 NRF 662 5.8 8.2 0.145 18.1 0.0115 0.001 0.0265 7.3 3.16 LS2 RF 1243 4.9 1.0 0.052 13.22 0.007 0.001 0.006 7.70 6.044 MR16 RF 1900 2.0 0.6 0.055 15.45 0.009 0.001 0.007 6.90 1.325 MR5 RF 1639 7.0 4.0 0.055 16.05 0.009 0.001 0.005 7.45 2.740 2MR10 RF 1679 6.1 5.0 0.057 12.87 0.009 0.001 0.005 7.25 2.055 SM2-1 RF 1931 2.1 1.0 0.066 12.20 0.010 0.005 0.004 7.37 3.538 3
MR4 RF 1679 4.0 3.6 0.143 16.08 0.011 0.001 0.008 7.88 4.803 3

Appendix I (continued)Table B. Lakes with TKN < 0.045 mg/L and water temperature > 12°C. NF = fishless lake; NRF = lakewith non-reproducing trout; RF = lake with reproducing trout.CODE FISH ELEV MAX Z S. AREA TKN TEMP TP NO3 NH3 PH ALK MC27 NF 1488 8.8 4.6 0.013 12.35 0.001 0.006 0.002 6.33 0.557 MC17-2 NF 1754 5.5 0.3 0.018 14.57 0.002 0.001 0.005 6.27 0.465 EP3 NF 1299 3.7 0.4 0.025 12.90 0.004 0.006 0.006 7.00 1.205 MC17-1 NF 1755 13.1 4.0 0.008 14.50 0.002 0.001 0.002 6.20 0.463 MA3 NF 2044 6.0 1.3 0.030 12.30 0.006 0.000 0.007 7.10 1.570 ML4 NF 1583 6.4 3.3 0.031 12.27 0.003 0.001 0.005 7.87 2.778 MC2 NF 1800 11.0 1.2 0.043 16.37 0.003 0.002 0.004 6.53 0.683 MM11 NRF 1974 7.6 1.4 0.019 13.35 0.006 0.004 0.003 6.63 0.754 MR15-1 NRF 1922 27.0 4.8 0.023 12.58 0.003 0.024 0.014 7.20 1.943 LS7 RF 1510 7.9 2.8 0.020 12.50 0.002 0.005 0.005 7.30 1.780 GM1 RF 1270 49.0 59.0 0.017 13.80 0.009 0.029 0.005 7.40 3.219 M7 RF 1363 11.0 3.2 0.020 12.50 0.003 0.001 0.001 7.10 1.340 CP1 RF 1642 17.7 12.0 0.021 12.20 0.005 0.011 0.004 6.60 0.760 M23 RF 1270 37.2 12.7 0.023 15.25 0.002 0.002 0.005 7.25 1.646 EP9-1 RF 1580 2.5 0.6 0.040 13.20 0.001 0.000 0.002 7.10 1.730 
Appendix I (continued)Table C. Lakes with water temperature < 12°C. NF = fishless lake; NRF = lake with non-reproducingtrout; RF = lake with reproducing trout.CODE FISH ELEV MAX Z S. AREA TKN TEMP TP NO3 NH3 PH ALK FP4 NF 1624 33.0 12.0 0.000 6.00 0.030 0.001 0.008 7.00 1.087 MC21-2 NF 1525 3.0 1.6 0.003 10.60 0.003 0.004 0.003 6.40 0.560 MC24 NF 1982 4.6 1.0 0.005 2.30 0.006 0.008 0.000 6.50 0.605 MS4 NF 1659 9.8 2.0 0.005 4.60 0.009 0.035 0.006 6.60 0.658 MC25 NF 2028 2.4 0.007 1.10 0.004 0.022 0.001 5.90 0.363 M6 NF 1632 3.6 0.6 0.018 10.95 0.002 0.024 0.003 7.60 2.950 DD8 NF 1600 1.9 0.9 0.020 6.50 0.005 0.032 0.013 7.10 1.180 MC21-1 NF 1528 5.0 1.2 0.020 5.80 0.007 0.000 0.002 6.60 0.820 MP8 NF 1566 3.7 0.9 0.020 10.40 0.004 0.004 0.003 6.80 0.900 MC17-4 NF 1754 4.3 0.8 0.021 11.70 0.003 0.001 0.005 6.07 0.449 MR6 NF 1693 2.1 0.6 0.027 11.63 0.008 0.002 0.003 1.73 3.220 ML1 NF 1476 1.2 0.2 0.030 8.23 0.005 0.022 0.007 7.87 3.203 MM6 NF 1504 11.9 4.1 0.030 10.70 0.005 0.003 0.005 7.18 1.998 PM4 NF 1610 4.3 3.0 0.031 3.40 0.005 0.014 0.000 7.10 1.935 MS1 NF 2063 137.0 65.1 0.033 5.00 0.005 0.018 0.004 6.60 0.705 MSH4 NF 1635 8.9 1.4 0.033 10.37 0.005 0.019 0.007 7.30 2.097 FP9 NF 1662 3.4 0.5 0.040 9.15 0.005 0.010 0.010 7.40 2.065 MA2 NF 2127 10.0 1.0 0.040 11.40 0.009 0.000 0.007 7.10 1.350 ML6 NF 1961 3.0 0.2 0.040 11.20 0.004 0.005 0.019 7.30 1.540 MM7 NF 1642 1.9 0.8 0.040 10.13 0.005 0.004 0.004 7.17 2.107 MR8 NF 1970 3.5 0.3 0.040 11.00 0.005 0.010 0.001 6.90 1.230 FP7 NF 1378 33.0 32.5 0.042 7.60 0.013 0.004 0.003 7.10 1.070 
Appendix I. (continued)Table C (continued). Lakes with water temperature < 12°C. NF = fishless lake; NRF = lake with nonreproducing trout; RF = lake with reproducing trout.CODE FISH ELEV MAX Z S. AREA TKN TEMP TP NO3 NH3 PH ALK MSH3 NF 1188 26.2 16.0 0.048 5.00 0.024 0.025 0.012 6.90 0.999 ML2 NRF 1687 27.4 3.4 0.013 8.43 0.003 0.004 0.019 7.80 2.838 PM1 NRF 1171 9.1 4.4 0.021 10.20 0.002 0.007 0.005 7.20 2.449 MR9 NRF 1813 4.9 1.7 0.024 11.88 0.006 0.002 0.007 6.93 1.293 EP5-1 NRF 1543 6.0 2.7 0.025 11.50 0.003 0.006 0.004 6.85 1.000 MC6 NRF 1601 21.3 5.2 0.032 11.05 0.002 0.013 0.010 6.65 0.788 MR13-2 NRF 1789 5.0 1.2 0.032 10.06 0.004 0.005 0.005 6.93 1.206 M19 NRF 1427 24.0 5.0 0.032 9.10 0.001 0.013 0.006 6.48 0.656 MC7 NRF 1556 27.2 6.7 0.035 9.80 0.006 0.004 0.006 7.15 1.790 DD5 NRF 1531 5.2 5.2 0.040 5.70 0.005 0.005 0.003 6.70 0.905 ML3 NRF 1967 15.2 1.3 0.040 10.25 0.004 0.001 0.006 7.30 1.570 MR1 NRF 2072 26.0 4.0 0.070 6.10 0.005 0.017 0.008 6.90 1.170 LS3-FS NRF 1375 6.7 1.2 0.085 9.90 0.002 0.004 0.010 6.95 1.615 MR15-2 RF 1909 3.0 0.3 0.005 8.95 0.006 0.021 0.004 7.30 2.210 M21 RF 1205 3.1 1.6 0.010 8.40 0.000 0.059 0.000 7.20 2.190 MC12 RF 1769 46.3 11.4 0.012 11.30 0.003 0.016 0.004 6.60 0.726 EP6 RF 1566 19.8 3.0 0.024 10.90 0.003 0.004 0.007 6.40 0.699 MLY2 RF 1629 4.3 2.5 0.036 11.15 0.006 0.005 0.005 7.25 2.775 DD4 RF 1174 19.0 5.2 0.040 6.30 0.003 0.016 0.010 6.50 0.890 SM2-2 RF 1988 4.3 1.0 0.043 11.37 0.011 0.020 0.004 7.73 3.614 PM3 RF 1609 5.5 4.3 0.045 9.05 0.004 0.006 0.010 7.23 2.119 MR14 RF 1717 10.4 6.3 0.047 10.73 0.007 0.002 0.004 6.99 1.378 MC11-1 RF 1616 14.0 5.6 0.050 9.30 0.007 0.001 0.011 6.70 0.840