Ecological Indicators 6 (2006) 644–663
This article is also available online at:
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Using multiple indicators to evaluate the ecological integrity
of a coastal plain stream system
Robert A. Zampella *, John F. Bunnell, Kim J. Laidig, Nicholas A. Procopio
Pinelands Commission, P.O. Box 7, 15 Springfield Road, New Lisbon, NJ 08064, USA
Accepted 17 August 2005
Abstract
We demonstrate the use of multiple indicators to characterize the ecological integrity of a coastal plain stream system in the
New Jersey Pinelands in relation to human-induced watershed alterations. The individual indicators include pH, specific
conductance, stream vegetation and stream-fish, impoundment-fish, and anuran assemblages. We evaluate and compare the
utility of the individual and multiple environmental and biological indicators and present a relatively straightforward method for
ranking sites. Specific conductance and pH measured at 88 monitoring sites varied in relation to the percentage of altered land
(developed land and upland agriculture) within the associated watersheds. All three environmental variables were associated
with variations in the composition of stream vegetation and stream fish, impoundment fish, and anuran assemblages. With the
exception of impoundment fish, the association between altered land and the multiple-indicator scores based on the two waterquality indicators and the four biological indicators was stronger than that displayed by any of the individual variables.
# 2005 Elsevier Ltd. All rights reserved.
Keywords: Pinelands; Multiple indicators; Ecological integrity
1. Introduction
The use of biological indicators to assess the health
of aquatic systems represents an important water
resources management tool (Karr and Chu, 1999;
Simon, 2003). Fish have been used as indicators of
aquatic degradation throughout North America
(Fausch et al., 1990; Karr and Chu, 1999; Karr
et al., 1986; Simon, 1999). Aquatic and wetland
vegetation have been employed less frequently for this
* Corresponding author.
E-mail address: [email protected] (R.A. Zampella).
purpose (O’Connor et al., 2000; Stewart et al., 2003;
Vaithiyanathan and Richardson, 1999). Although
amphibians may be good indicators of environmental
conditions (Hecnar and M’Closkey, 1996; Wake,
1991), anuran (frog and toad) assemblages have rarely
been used to assess biotic integrity (Moyle and
Randall, 1998). Several studies have considered
multiple indicators (Allen et al., 1999; Berkman
et al., 1986; Moyle and Randall, 1998; Stewart et al.,
2003; Wang and Lyons, 2003; Yoder and DeShon,
2003), but none have used water-quality, fish, anurans,
and stream vegetation to evaluate the ecological
integrity of stream systems.
1470-160X/$ – see front matter # 2005 Elsevier Ltd. All rights reserved.
doi:10.1016/j.ecolind.2005.08.027
R.A. Zampella et al. / Ecological Indicators 6 (2006) 644–663
New Jersey Pinelands (Pine Barrens) streams
draining forested watersheds are typically acidic and
nutrient-poor (Morgan and Good, 1988; Zampella,
1994). In contrast, streams draining developed lands
and upland agriculture display elevated pH and
dissolved solid concentrations (Johnson and Watt,
1996; Morgan and Good, 1988; Watt and Johnson,
1992; Zampella, 1994). Previous Pinelands studies
have shown that specific conductance, pH, stream
vegetation, and fish and anuran assemblages are each
good indicators of land-use-related watershed disturbance in Pinelands streams (Dow and Zampella, 2000;
Zampella and Bunnell, 1998, 2000; Zampella and
645
Laidig, 1997). Both pH and specific conductance are
highly correlated with concentrations of nitrogen and
phosphorus (Zampella, 1994), two nutrients that are
probably limiting in the region’s dystrophic waters.
Additionally, Morgan (1985) associated the increase in
pH in degraded Pinelands waters with enhanced
primary productivity and nitrogen assimilation. Biological communities in acid-water Pinelands reference
sites are characterized by native species, whereas
nonnative plants and animals are found in streams with
elevated pH and specific conductance values.
In this study, we demonstrate the use of multiple
indicators to characterize the ecological integrity of
Fig. 1. Regional location of the Mullica River Basin in the New Jersey Pinelands.
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R.A. Zampella et al. / Ecological Indicators 6 (2006) 644–663
coastal plain streams in the New Jersey Pinelands in
relation to human-induced watershed alterations.
Ecological integrity, which includes both biotic and
environmental factors, is a broader concept than biotic
integrity, which concerns only the status of biological
communities (Stevenson, 1998; Stevenson and Pan,
1999). The individual indicators include pH, specific
conductance, stream and impoundment fish, anurans,
and stream vegetation. We evaluate and compare the
utility of the individual and multiple environmental
and biological indicators and present a relatively
straightforward method for ranking sites.
2. Methods
2.1. Study-area description
Stream surveys were conducted in the 1474 km2
Mullica River Basin, which is the largest watershed in
the New Jersey Pinelands (Fig. 1). Groundwater
discharge from the unconfined Kirkwood-Cohansey
aquifer, which underlies the entire basin, accounts for
nearly 90% of average annual stream flows (Johnson
and Watt, 1996; Rhodehamel, 1973). The watershed,
which comprises several major tributaries (Fig. 2),
displays a diverse range of natural and humandominated landscapes (Fig. 3). The major tributary
basins studied were the Hammonton Creek and Lower
Mullica River tributaries, Nescochague Creek, Sleeper
Branch, Upper Mullica River, Batsto River, Wading
River, Oswego River, and Bass River. Distinct landuse patterns characterize the major tributary basins,
providing a study in contrast between heavily altered
landscapes and extensive forests. Most developed land
and upland agriculture is found in the headwater areas
of the western stream systems, whereas most wetland
agriculture, which includes cranberry and blueberry
farms, is located in stream systems on the eastern side
of the basin. Nearly all lakes in the basin are on-stream
impoundments, including those created by past
industrial and agricultural activities (Wacker, 1979).
Ammonia and total phosphorus are exceptionally
low in most Mullica River streams. Zampella et al.
Fig. 2. Major Mullica River Basin tributary systems.
R.A. Zampella et al. / Ecological Indicators 6 (2006) 644–663
647
Fig. 3. Land-use in the Mullica River Basin. Unshaded areas represent upland and wetland forest, water, and barren land.
(2001) reported that median ammonia concentrations
were below detection (0.02 0.03 mg L 1) at all but
three of twenty-six Mullica River Basin sites sampled
from 1995 through 1998. Median orthophosphorus did
not exceed the 0.01 mg L 1 detection limit at any of the
18 sites where it was measured. Only one stream
received a direct wastewater discharge. Low ammonia
and phosphorus levels in streams lacking point-source
wastewater discharges are typical in the Pinelands
(Morgan and Good, 1988; Zampella, 1994). Median
nitrite + nitrate–nitrogen concentrations in undeveloped
Mullica River Basin streams were below detection
(0.05 mg L 1), whereas, the median concentration of
this nitrogen species in streams with more than 49%
altered land (developed land and upland agriculture) in
the associated drainage was 0.40 mg L 1.
2.2. Selection of survey sites
The major criteria used to select survey stations
were the drainage basin land-use characteristics and
accessibility. Sites were selected to include a range of
land-use conditions represented by the percentage of
developed land and upland agriculture, the two major
altered land uses in the Mullica River Basin. Most of
the sites surveyed in our previous studies (Zampella
and Bunnell, 1998, 2000; Zampella and Laidig, 1997)
were included and resurveyed during this study. Due to
access limitations on private lands, we did not conduct
surveys in portions of the Wading River basin. We
registered the location of each sampling station with a
global positioning system (GPS).
2.3. Water-quality
In 1999, we completed field measurements of pH
and specific conductance at 88 sites at or near where
stream vegetation, fish, or anurans were surveyed.
Specific conductance was measured with an Orion
model-122 meter and pH was measured with an Orion
model-250A meter. With a few exceptions, we
conducted monthly monitoring rounds during baseflow conditions over a 3–8 day period in June, July,
August, and October 1999. All available data were
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R.A. Zampella et al. / Ecological Indicators 6 (2006) 644–663
used to calculate median values for each sampling
site. Using Spearman rank correlation and graphical
analysis, we evaluated the relationship between pH
and specific conductance for the 88 biologicalsurvey sites and the percentage of altered land
(developed land and upland agriculture) in the
associated drainage basin.
We also used Spearman rank correlation to evaluate
the association between both pH and specific
conductance and nitrite + nitrate as nitrogen, calcium,
magnesium, chloride, and sulfate measured between
October 1995 and September 1998 under baseflow
conditions at 25 Mullica River basin stream stations
unaffected by point-source wastewater discharges
(Zampella et al., 2001). Sampling frequency varied
among sites. All correlations were based on median
values.
the NJDEP (1996). New and modified basin lines were
delineated using digital-topographic maps, ArcView,
and on-screen digitizing.
2.5. Biological-survey methods
2.5.1. Stream vegetation
We surveyed 72 stream vegetation sites from 1996
through 1999 employing methods similar to those
used by Zampella and Laidig (1997). Most sites
consisted of a 100 m long stream reach. Eight sites
were only 25 m long. The sampling area at each site
included the channel and a 2 m wide belt transect
along each bank. At each site, we surveyed channel
and bank plants on a single occasion during each of
three time periods (May–June, July–August, and
September–October) covering a single growing
season.
2.4. Land-use
Human-induced landscape alterations impact the
ecological integrity of water resources by affecting
food sources, water-quality, habitat structure, flow
regime, and biotic interactions (Karr, 1991). In the
Pinelands, land-use directly and indirectly influences
each of these factors. This single variable represents a
dominant environmental stress and provides a good,
overall surrogate for variations in aquatic habitats due
to human-induced alterations.
We prepared land-use profiles for each drainage
basin where water-quality samples were collected
using ArcView software (Environmental Systems
Research Institute Inc., Redlands, CA, 1988–1992)
and digital land-use/land-cover data obtained from the
New Jersey Department of Environmental Protection
(NJDEP, 1995/97 Land Use/Land Cover Update
2001). Land-use profiles for the nearest water-quality
monitoring site were used for each biological
monitoring site. The NJDEP data set classifies landuse/land-cover using a modified Anderson et al.
(1976) system. In this paper, we refer to the NJDEP
land-use classes of urban land, agriculture, and
agricultural wetlands as developed land, upland
agriculture, and wetland agriculture, respectively.
The combined area of developed land and upland
agriculture is referred to as altered land. Drainage
basin boundaries were prepared using ArcView
software and digital-hydrography data obtained from
2.5.2. Fish
Using fish sampling methods described by
Zampella and Bunnell (1998), we surveyed 64 stream
sites throughout the Mullica River Basin. At each
stream station, we sampled all habitats in a 100 m
long stream reach using a 4 mm mesh nylon seine.
Stream sites were sampled for 1 h on two to four
separate occasions (one site was sampled only once)
between May and October. We also sampled 30
stream impoundments with a seine on a single
occasion for a period of 1 h. One impoundment
was sampled on two dates. For each species, we
pooled the number of individuals collected at a site
during all visits conducted between 1992 and 1999.
We used these pooled data to determine presence/
absence and to calculate relative abundance. Juveniles that could only be identified to genus were not
included in subsequent data analyses.
2.5.3. Anurans
We conducted nighttime vocalization surveys
during the anuran-breeding season in 1993 and from
1996 through 1999 using methods similar to those
employed by Zampella and Bunnell (2000). We
visited the majority of sites monthly during a single
breeding season. The number of visits varied among
sites. Anurans heard at 78 permanent-water on-stream
sites were included in the analysis. The sites included
two abandoned cranberry bogs, two forested stream
R.A. Zampella et al. / Ecological Indicators 6 (2006) 644–663
crossings, 21 non-forested stream crossings, and 53
impoundments. Forested and non-forested stream
crossings were stream sites located at roads.
Forested-stream crossings were bordered by trees,
and non-forested stream crossings were streams or
small (<0.5 ha) impoundments bordered by shrub or
emergent vegetation communities. Impoundments
were larger, open-water habitats. Abandoned cranberry bogs were former cranberry bogs or reservoirs
that succeeded to mixed shrub/emergent wetlands
with open-water. Presence/absence was determined
for each species heard at a site by pooling the results of
all surveys.
2.5.4. Inventories and voucher collections
The complete stream vegetation, fish, and anuran
survey data sets and distribution maps for each species
are presented in Zampella et al. (2001). We assembled
an herbarium collection that includes voucher specimens for most of the plant species encountered during
the Mullica River Basin stream surveys. We also
collected fish-voucher specimens for each stream site
and documented anuran vocalizations heard during
each site visit using cassette-tape recordings.
2.6. Biogeography
2.6.1. Stream vegetation
Following Ehrenfeld (1983), Morgan and Philipp
(1986), Zampella and Laidig (1997), and Laidig and
Zampella (1999), we used Stone (1911) to classify
plant species as native or not native to the Pinelands.
Stone (1911) describes plants as characteristic of the
Pine Barrens, characteristic of an adjacent region
referred to as the Middle District, or common to both
the Pine Barrens and the Middle District. Using
Gleason and Cronquist (1991), we classified species
that are not native to North America as exotic.
Taxonomic nomenclature follows Gleason and Cronquist (1991).
2.6.2. Fish
We adopted Hastings’ (1984) classification of
Pinelands fish species. He categorized Pinelands fish
as native, peripheral, or introduced. Peripheral species
are native to other parts of New Jersey and are found in
waters along the boundaries of the Pinelands.
Introduced species are not native to New Jersey.
649
Native species include those that are limited to the
Pinelands (restricted characteristic) and species that
are native to both the region and other parts of New
Jersey (widespread characteristic).
2.6.3. Anurans
Conant (1979) classified all anurans found in the
region as Pine Barrens, wide-ranging, or borderentrant species. Pine Barrens species are confined to
Pinelands habitats and wide-ranging species are
distributed throughout the Pine Barrens and other
parts of New Jersey. Border-entrant species, such as
the bullfrog (Rana catesbeiana), are normally unable
to enter the Pinelands except in habitats disturbed by
human activity. The bullfrog is associated with the
general absence of native carpenter frogs (Rana
virgatipes) and Pine Barrens treefrogs (Hyla andersonii) (Zampella and Bunnell, 2000). Taxonomic
nomenclature follows Conant and Collins (1998).
2.6.4. General Pinelands classification
For consistency, we refer to plant, fish, and anuran
species whose distribution is generally limited to the
Pinelands as restricted native species, species that are
native to both the Pinelands and other areas of New
Jersey as widespread native species, and species that
are native to regions outside the Pinelands as
nonnative species (Table 1).
2.7. Analysis of biological data
For each biological community type (stream
vegetation, stream fish, impoundment fish, and
anurans), we used detrended correspondence analysis
(DCA, Hill, 1979a; Hill and Gauch, 1980) and
TWINSPAN (Hill, 1979b) to ordinate and classify
species and sampling sites based on presence/absence
data. DCA is a simple and effective way of ordering
Pinelands communities in relation to human-induced
watershed disturbance gradients (Zampella and
Bunnell, 1998, 2000; Zampella and Laidig, 1997).
To limit the effect of rare species on the ordinations,
we included only species occurring at two or more
sites in the analyses. These analyses were completed
using PC-ORD, Version 4 (McCune and Mefford,
1999).
Sixty of the sixty-four stream fish survey sites were
included in an initial DCA ordination of fish species
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Table 1
Biogeographic classification for plant and animal species based on Stone (1911), Hastings (1984), and Conant (1979)
General Pinelands
classification
Plants (Stone, 1911)
Fish (Hastings, 1984)
Anurans (Conant, 1979)
Restricted native species
Widespread native species
Pine Barrens District species
Species common to the Pine Barrens
District and the Middle District
Species restricted to the Middle District
Restricted characteristic species
Widespread characteristic species
Pine Barrens species
Wide-ranging species
Peripheral and introduced species
Border-entrant species
Nonnative species
Nonnative plant species also include species described as exotic by Gleason and Cronquist (1991).
presence/absence data. The four omitted sites
included two where less than a 100 m section was
sampled and two sites where pH and specific
conductance data were not collected. This initial
ordination was affected by six outliers that compressed the order of the remaining 54 sites along the
first DCA axis. These six sites, which were
characterized by low pH, narrow-ditched channels,
small forested basins, and native fish assemblages,
were omitted from the final ordination.
Spearman rank correlation and graphical analysis
were used to determine if species composition,
represented by the DCA axes, varied in relation to
pH, specific conductance, and the percentage of
upland agriculture and developed land in a basin.
Wetland agriculture was not included because it
covered less than 10% of all but two stream drainages
and is generally not associated with elevated levels of
pH and specific conductance (Zampella et al., 2001).
Correlation analysis of the anuran-ordination scores
was limited to 41 sites where water-quality data were
collected. An alpha level of 0.05 was used in all
correlation analyses, which were completed using
Statistica 5.5 (StatSoft Inc., 2000). We used the
sequential Bonferroni method (Rice, 1989) to adjust
significance levels for each set of related Spearman
rank correlations.
2.8. Rating the ecological integrity of streams
Multiple-indicator, ecological integrity scores were
derived for 88 water-quality monitoring sites by
ranking pH values, specific conductance values, and
each set of community-ordination DCA scores,
converting each set of scores to a relative scale of
0–100, and using the rescaled scores of each variable
to calculate a median multiple-indicator score for
each site. High scores were assigned to sites with
low pH and specific conductance values and
biological communities characterized by native
species. In contrast, low ecological integrity scores
were assigned to sites with high pH and specific
conductance values and biological communities
with a higher percentage of nonnative plant or
animal species. Although only 41 anuran sites were
used in producing ecological integrity scores,
anuran sites were ranked using the order of 78
sites included in the DCA ordination. The rescaled
variable scores and the multiple-indicator scores
were used to characterize the ecological integrity of
each of the major tributary systems.
3. Results
3.1. Water-quality
Analysis of the data collected at 25 USGS
monitoring stations between October 1995 and
September 1998 revealed a significant correlation
between pH and specific conductance and nitrite +
nitrate as nitrogen, calcium, magnesium, chloride, and
sulfate (Table 2). Analysis of the pH and specific
conductance data that we collected at 88 stream sites
in 1999 indicated that altered land (developed land and
upland agriculture) was associated with variations in
pH and specific conductance (Table 3). Both variables
generally increased as the percentage of altered land in
a drainage basin increased. The relationship between
the two water-quality variables and altered land was
similar to that obtained when using either developed
land or upland agriculture independently. We observed
an increase in conductance at very low pH values
(<4.5). Specific conductance and pH were higher on
R.A. Zampella et al. / Ecological Indicators 6 (2006) 644–663
651
Table 2
Spearman rank correlations between pH, specific conductance, and selected water-quality variables
Water-quality variables (mg L 1)
Specific conductance (mS cm 1)
pH
Nitrite + nitrate as N, dissolved
Calcium as Ca, dissolved
Magnesium as Mg, dissolved
Chloride as Cl, dissolved
Sulfate as SO4, dissolved
r
p
r
p
0.77
0.85
0.85
0.84
0.51
<0.001
<0.001
<0.001
<0.001
<0.01
0.73
0.93
0.92
0.94
0.73
<0.001
<0.001
<0.001
<0.001
<0.001
Water-quality data were collected between October 1995 and September 1998 at 25 U.S. Geological Survey monitoring sites in the Mullica River
Basin (Zampella et al., 2001). Sampling frequency varied among sites. All correlations, which were based on median values, are significant
(a = 0.05) with the sequential Bonferroni method.
the more heavily developed and farmed western side
of the Mullica River Basin. With two exceptions,
wetland agriculture covered less than 10% of the
stream basins included in the sample.
3.2. Biological surveys
The number of restricted native, widespread
native, and nonnative plant species were nearly
equally represented. Fourteen plant species were
exotics. Nonnative species were encountered more
frequently on the western side of the Mullica River
Basin.
3.2.1. Stream vegetation
We found a total of 305 vascular plants, including
232 herbaceous and 73 woody species, at the 72
stream sites (Table 4). Total and herbaceous plant
species richness ranged from 21 to 90 and 10 to 69,
respectively. The mean (1 S.D.) number of species
found at the 72 sites was 50 14. Median species
richness was also 50. Eighty species were represented
by a single-occurrence. Sixteen stream sites accounted
for more than three-quarter of these single-occurrence
plant species.
3.2.2. Stream fish
Twenty-one fish species were collected at the 64
stream sites, including thirteen native Pinelands
species (restricted and widespread), five peripheral
species, and two introduced species (Table 5). Species
richness ranged from 8 to 15 species. The mean (1
S.D.) and median number of species collected at the 64
sites was 9.3 2.6 and 10, respectively. Nonnative
species (peripheral and introduced) were collected at
24 stream sites but none of these species was
abundant.
Table 3
Spearman rank correlations based on original water-quality data, community-ordination scores, and multiple-indicator, ecological integrity
scores
Environmental
variable
Altered land (%)
Developed land (%)
Upland agriculture (%)
pH
Specific conductance mS cm
pH,
n = 88
1
0.84
0.84
0.76
–
0.44
Specific
conductance,
n = 88
Community-ordination scores (DCA axis 1)
Multiple-indicator
scores, n = 88
Stream
vegetation,
n = 72
Stream fish,
n = 54
Impoundment
fish, n = 30
On-stream
anurans,
n = 41
0.64
0.58
0.55
0.44
–
0.79
0.72
0.70
0.73
0.68
0.82
0.78
0.76
0.82
0.65
0.90
0.85
0.82
0.90
0.41
0.76
0.76
0.65
0.75
0.61
0.89
0.84
0.81
0.88
0.63
Altered land includes developed land and upland agriculture. Ranking sites from 0 to 100 to develop the multiple-indicator scores produced
correlations with signs opposite of those obtained using the original water-quality data and ordination scores (e.g., 0.90 vs. 0.90). All
correlations shown are significant (a = 0.05) with the sequential Bonferroni method.
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Table 4
Plants included in the stream vegetation analysis
Species
Order
Species
Order
Species
Order
Danthonia sericea var. epilis
Schizaea pusilla
Utricularia cornuta
Lycopodium alopecuroides
Muhlenbergia torreyana
Drosera filiformis
Eriocaulon compressum
Carex trisperma
Cladium mariscoides
Carex exilis
Pogonia ophioglossoides
Utricularia fibrosa
Schizachyrium scoparium
Carex livida
Polygala cruciata
Betula populifolia
Muhlenbergia uniflora
Eriocaulon decangulare
Lyonia mariana
Xyris difformis
Zizania aquatica
Xyris smalliana
Eleocharis tuberculosa
Habenaria clavellata
Sarracenia purpurea
Drosera rotundifolia
Panicum virgatum
Iris prismatica
Vaccinium pallidum
Eriophorum virginicum
Andropogon virginicus var. abbreviatus
Rhynchospora alba
Cyperus dentatus
Hypericum densiflorum
Drosera intermedia
Gaylussacia dumosa
Carex striata
Eriocaulon aquaticum
Myrica pensylvanica
Vaccinium macrocarpon
Panicum spretum
Gaylussacia frondosa
Orontium aquaticum
Aster nemoralis
Leiophyllum buxifolium
Lobelia nuttallii
Calamagrostis cinnoides
Eleocharis robbinsii
Chamaedaphne calyculata
Gaultheria procumbens
Kalmia angustifolia
Bartonia virginica
Carex bullata
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
Eupatorium pilosum
Isoetes echinospora
Gaylussacia baccata
Rhynchospora capitellata
Nymphaea odorata
Rhexia virginica
Carex atlantica
Euthamia tenuifolia
Hypericum canadense
Smilax herbacea
Panicum ensifolium
Lilium superbum
Panicum scabriusculum
Proserpinaca pectinata
Carex folliculata
Potamogeton confervoides
Sassafras albidum
Rhynchospora chalarocephala
Dulichium arundinaceum
Eupatorium resinosum
Hypericum denticulatum
Panicum dichotomum
Nuphar variegata
Panicum verrucosum
Triadenum virginicum
Smilax pseudochina
Chamaecyparis thyoides
Glyceria obtusa
Pontederia cordata
Iris versicolor
Viola lanceolata
Aronia arbutifolia
Oxypolis rigidior
Agrostis perennans var. elata
Lysimachia terrestris
Rhododendron viscosum
Magnolia virginiana
Peltandra virginica
Scirpus cyperinus
Smilax glauca
Osmunda regalis
Lyonia ligustrina
Alnus serrulata
Viburnum nudum var. nudum
Vaccinium corymbosum
Aster novi-belgii
Liquidambar styraciflua
Acer rubrum
Clethra alnifolia
Eubotrys racemosa
Carex venusta
Quercus ilicifolia
Osmunda cinnamomea
76
77
78
79
80
81
82
83
84
85
86
87
88
89
90
91
92
93
94
95
96
97
98
99
100
101
102
103
104
105
106
107
108
109
110
111
112
113
114
115
116
117
118
119
120
121
122
123
124
125
126
127
128
Mitchella repens
Lycopus uniflorus
Juncus effusus
Ilex verticillata
Cephalanthus occidentalis
Carex albolutescens
Viburnum dentatum
Carex crinita
Eleocharis ovata
Bidens frondosa
Woodwardia areolata
Decodon verticillatus
Carex intumescens
Kalmia latifolia
Hypericum mutilum
Phragmites australis
Diospyros virginiana
Eupatorium dubium
Solidago rugosa
Thelypteris simulata
Toxicodendron radicans
Apios americana
Parthenocissus quinquefolia
Lindernia dubia
Erechtites hieracifolia
Polygonum hydropiperoides
Ludwigia palustris
Scutellaria lateriflora
Polygonum punctatum
Echinochloa muricata
Galium tinctorium
Lycopus virginicus
Microstegium vimineum
Onoclea sensibilis
Mikania scandens
Cyperus strigosus
Toxicodendron vernix
Asclepias incarnata
Vitis labrusca
Potamogeton epihydrus
Thelypteris palustris
Panicum clandestinum
Polygonum sagittatum
Bidens connata
Lobelia cardinalis
Boehmeria cylindrica
Rosa palustris
Rubus sp.
Callitriche heterophylla
Glyceria canadensis
Impatiens capensis
Taraxacum officinale
Dryopteris carthusiana
151
152
153
154
155
156
157
158
159
160
161
162
163
164
165
166
167
168
169
170
171
172
173
174
175
176
177
178
179
180
181
182
183
184
185
186
187
188
189
190
191
192
193
194
195
196
197
198
199
200
201
202
203
R.A. Zampella et al. / Ecological Indicators 6 (2006) 644–663
653
Table 4 (Continued )
Species
Order
Species
Order
Species
Order
Carex collinsii
Juncus pelocarpus
Ilex laevigata
Lachnanthes caroliniana
Juncus canadensis
Juncus militaris
Bartonia paniculata
Smilax laurifolia
Amelanchier canadensis
Sabatia difformis
Eleocharis flavescens var. olivacea
Utricularia geminiscapa
Pinus rigida
Eleocharis tenuis
Ilex glabra
Smilax walteri
Carex stricta
Sagittaria engelmanniana
Utricularia purpurea
Potamogeton oakesianus
Scirpus subterminalis
Panicum longifolium
54
55
56
57
58
59
60
61
62
63
64
65
66
67
68
69
70
71
72
73
74
75
Leersia oryzoides
Carex pensylvanica
Agrostis hyemalis
Andropogon virginicus var. virginicus
Quercus alba
Woodwardia virginica
Bidens coronata
Smilax rotundifolia
Spiraea tomentosa
Agrostis perennans
Rubus hispidus
Itea virginica
Nyssa sylvatica
Carex atlantica var. capillacea
Sparganium americanum
Cuscuta sp.
Eleocharis acicularis
Viola primulifolia
Agrostis hyemalis var. scabra
Carex canescens
Ilex opaca
Dioscorea villosa
129
130
131
132
133
134
135
136
137
138
139
140
141
142
143
144
145
146
147
148
149
150
Carex lurida
Glyceria striata
Polygonum cespitosum
Elodea nuttallii
Potamogeton pusillus
Sambucus canadensis
Lonicera japonica
Polygonum arifolium
Aster racemosus
Salix nigra
Cinna arundinacea
Oxalis stricta
Typha latifolia
Epilobium coloratum
Pilea pumila
Cardamine pensylvanica
Aralia nudicaulis
Bidens discoidea
Lemna sp.
Phalaris arundinacea
Ceratophyllum echinatum
Carex stipata
204
205
206
207
208
209
210
211
212
213
214
215
216
217
218
219
220
221
222
223
224
225
Species are ordered by raw DCA axis 1 ordination scores. Species found at a single site were not included in the ordination.
Table 5
Fish species collected at 54 stream sites and 30 impoundments
Biogeography
Scientific name
Common name
Species code
Restricted native
Acantharchus pomotis
Ameiurus natalis
Aphredoderus sayanus
Enneacanthus chaetodon
Enneacanthus obesus
Etheostoma fusiforme
Mud sunfish
Yellow bullhead
Pirate perch
Blackbanded sunfish
Banded sunfish
Swamp darter
AcanPomo
AmeiNata
AphrSaya
EnneChae
EnneObes
EtheFusi
Widespread native
Anguilla rostrata
Enneacanthus gloriosus
Erimyzon oblongus
Esox americanus
Esox niger
Noturus gyrinus
Umbra pygmaea
American eel
Bluespotted sunfish
Creek chubsucker
Redfin pickerel
Chain pickerel
Tadpole madtom
Eastern mudminnow
AnguRost
EnneGlor
ErimOblo
EsoxAmer
EsoxNige
NotuGyri
UmbrPygm
Peripheral nonnative
Ameiurus nebulosus
Etheostoma olmstedi
Lepomis gibbosus
Notemigonus crysoleucas
Brown bullhead
Tessellated darter
Pumpkinseed
Golden shiner
AmeiNebu
EtheOlms
LepoGibb
NoteCrys
Introduced nonnative
Lepomis macrochirus
Micropterus salmoides
Pomoxis nigromaculatus
Bluegill
Largemouth bass
Black crappie
LepoMacr
MicrSalm
PomoNigr
Pomoxis nigromaculatus was limited to impoundments. Etheostoma olmstedi and Noturus gyrinus were limited to streams. Only species used in
the ordination are listed.
654
R.A. Zampella et al. / Ecological Indicators 6 (2006) 644–663
Table 6
Anuran species heard at 78 on-stream sites
Biogeography
Scientific name
Common name
Species code
Restricted native
Hyla andersonii
Rana virgatipes
Pine Barrens treefrog
Carpenter frog
HylaAnde
RanaVirg
Widespread native
Rana utricularia
Rana clamitans melanota
Pseudacris crucifer crucifer
Bufo woodhousii fowleri
Southern leopard frog
Green frog
Northern spring peeper
Fowler’s toad
RanaUtri
RanaClam
PseuCruc
BufoWood
Nonnative
Rana
Rana
Rana
Acris
Wood frog
Bullfrog
Pickerel frog
Northern cricket frog
RanaSylv
RanaCate
RanaPalu
AcriCrep
sylvatica
catesbeiana
palustris
crepitans crepitans
3.2.3. Impoundment fish
Twenty fish species were collected from the 30
stream impoundments, including 12 native Pinelands
species and eight nonnative species (Table 5). Species
richness ranged from 3 to 15 species. The mean (1
S.D.) and median number of species collected at the 30
impoundments was 8.2 (2.5) and 8.0, respectively.
Tadpole madtom was the only native Pinelands species
not found in the impoundments. Nonnative species
were found at 15 impoundments. An important
difference between the stream and impoundment
surveys was a greater frequency of occurrence and
greater relative abundance for pumpkinseeds (Lepomis
gibbosus), bluegills (L. macrochirus), and largemouth
bass (Micropterus salmoides) in impoundments.
3.2.4. Anurans
A total of 10 species were heard at the 78
permanent-water on-stream survey sites, including
two restricted native species, four widespread native
species, and four nonnative species (Table 6). Species
richness ranged from two to eight species. The mean
(1 S.D.) and median number of species heard was
4.0 1.4 and 4.0, respectively. Pine Barrens species
were heard at 68% of the sites and widespread species
at 100% of the sites. Nonnative species were heard at
46% of the sites. With one exception, the bullfrog, a
nonnative species, was present at every site where
other nonnative species occurred.
remarkably similar (Fig. 4). In each case, the first
DCA axis represented a strong community gradient
contrasting sites composed of native species assemblages with those that included nonnative species
(Fig. 5). This contrast is also reflected by the
TWINSPAN classifications (Fig. 4) which separated
a group of sites with a higher percentage of native
Pinelands species (Pinelands site class) from sites
characterized by a high percentage of nonnative
Pinelands species (non-Pinelands site class) (Fig. 4).
The percentage of restricted-native plant species
decreased along the stream vegetation community
gradient represented by the first DCA axis, whereas
the percentage of nonnative plant species increased
(Fig. 5). For stream fish and impoundment fish
communities, the first DCA axis contrasted stream
sites with fish assemblages composed entirely of
native species with those including both native and
nonnative species (Fig. 5). The percentage of
nonnative species increased along these community
gradients. Similarly, for anurans, the percentage of
nonnative species increased along the first DCA axis
whereas the percentage of restricted native species and
widespread native species decreased (Fig. 5). The
contrast between opposite ends of the community
gradient was the most dramatic for anurans due to the
absence of either Pine Barrens species or nonnative
species in the presence of the other.
3.3. Community gradients
3.4. Single-assemblage environmental
relationships
The patterns revealed by the DCA ordinations of
stream vegetation, fish, and anuran data were
For each community type, the order of sites along
the community gradient represented by the first axis
R.A. Zampella et al. / Ecological Indicators 6 (2006) 644–663
655
Fig. 4. DCA ordination diagrams for stream vegetation, stream fish, impoundment fish, and anuran monitoring sites in the Mullica River
Basin showing the TWINSPAN-derived Pinelands (closed squares) and non-Pinelands (open squares) site classes. The Pinelands class
includes sites with a higher percentage of native Pinelands species. Sites in the non-Pinelands class are characterized by a high percentage of
nonnative species.
of the DCA site-ordination (Fig. 4) was associated
with increasing pH, specific conductance, and the
percentage of developed land and upland agriculture
in the basin (Table 3). Stream sites on the right side of
the diagrams displayed higher pH and specific
conductance values and a higher percentage of
developed land and upland agriculture in the drainage
basin compared with those on the left side of the
diagrams. Sites on the extreme left side of the
diagrams represent reference sites, i.e., sites that are
minimally impacted by human-related watershed
disturbance.
The relationship between each community gradient,
represented by the first DCA axis, and altered land
(developed land and upland agriculture) was stronger
compared with that displayed by either upland
agriculture or developed land alone. None of the
community gradients was associated with the percentage of wetland agriculture in a drainage basin. The
contrasts revealed by the first axis of the DCA
ordinations were related to differences in the range
of watershed conditions associated with each plant and
animal species (Fig. 6). In no case was the second DCA
axis related to differences in water quality or land use.
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Fig. 5. Biogeographic composition of stream vegetation and stream fish, impoundment fish, and anurans assemblages at Mullica River Basin
monitoring sites. Sites are ordered by DCA axis 1 scores. Restricted native species are species whose distribution is generally limited to the
Pinelands, wide-ranging native species are native to both the Pinelands and other areas of New Jersey, and nonnative species are native to regions
outside the Pinelands (Table 1).
3.5. Multiple-indicators of human-induced
watershed alterations
The number of biological indicators used to
calculate multiple-indicator, ecological integrity scores
ranged from one to four. Two biological indicators
contributed to ecological integrity scores at 59% of the
sites. One, three, and four biological indicators
contributed to ecological indicator scores at 16, 10,
and 15% of the sites, respectively. Because reference
sites characterized by native species typically had lower
DCA scores and pH and specific conductance values
compared with sites characterized by native and
nonnative species, ranking sites from 0 to 100 to
develop the multiple-indicator scores produced correlations with signs opposite of those obtained using the
original water-quality data and ordination scores (e.g.,
0.90 versus 0.90).
With the exception of impoundment fish (r = 0.90),
the association between altered land and the multipleindicator, ecological integrity scores (r = 0.89) was
stronger than that displayed by any of the individual
variables (Table 3). This was true even when
impoundment fish scores were excluded from the
calculation of the multiple-indicator, ecological
integrity scores. Correlations among the four sets
R.A. Zampella et al. / Ecological Indicators 6 (2006) 644–663
657
Fig. 6. The percentage of altered land (developed land and upland agriculture) associated with stream plants, stream fish, impoundment fish, and
anurans at sampling sites. Refer to Table 4 for names of plant species ordered along the first DCA axis, Table 5 for fish-name codes, and Table 6
for anuran-name codes. Box plots show the first, second (median), and third quartiles and the 10 and 90th percentile for altered land.
Table 7
Spearman rank correlations based on community-ordination scores and multiple-indicator, ecological integrity scores
Community variables
Stream vegetation DCA axis 1
Stream fish DCA axis1
Impoundment fish DCA axis 1
On-stream anurans DCA axis 1
Multiple-indicator scores
Community-ordination scores (DCA axis 1)
Stream vegetation,
n = 72
Stream fish,
n = 54
Impoundment
fish, n = 30
On-stream
anurans, n = 41
–
0.75
0.70
0.80
0.91
0.75
–
0.79
0.84
0.92
0.70
0.79
–
0.79
0.94
0.80
0.84
0.79
–
0.88
Multiple-indicator
scores, n = 88
0.91
0.92
0.94
0.88
–
Ranking scores from 0 to 100 to develop the multiple-indicator scores produced correlations with signs opposite of those obtained using the
original ordination scores (e.g., 0.90 vs. 0.90). All correlations shown are significant (a = 0.05) with the sequential Bonferroni method.
658
R.A. Zampella et al. / Ecological Indicators 6 (2006) 644–663
Fig. 7. Mullica River Basin multiple-indicator, ecological integrity scores. High ecological integrity scores generally represent sites with low pH
and specific conductance values and biological communities characterized by native species. Low scores typically represent sites with high pH
and specific conductance values and biological communities with a higher percentage of nonnative plant or animal species. Refer to Fig. 2 for
tributary basin names.
of community DCA ordination scores and between
these scores and the multiple-indicator scores were
high (Table 7).
3.6. Major tributary-basin characterizations
The highest multiple-indicator, ecological integrity
scores were associated with the Wading River, Oswego
River, and Bass River basins, which represented
Pinelands reference sites (Fig. 7). All three basins
were characterized by <10% altered land and generally
displayed the lowest median pH and specific conductance values in the Mullica River Basin (Fig. 8). All
streams and impoundment sites in the Wading River
and Oswego River basins supported native fish
assemblages and occupied a position at the undisturbed
end of the fish-community gradient (Fig. 8). With the
exception of one stream site where pumpkinseeds were
collected on a single sampling date, nonnative fish were
also absent from the Bass River basin sites. This
peripheral species may have entered the acid-water
stream from downstream tidal areas where it is known
to occur (Hastings, 1984). On-stream anuran sites in all
three systems were dominated by native species and
occupied a position at the undisturbed end of the
anuran-community gradient. Bullfrogs were absent
from all Wading River, Oswego River, and Bass River
basin sites that we surveyed. A high percentage of Pine
Barrens plants characterized the Wading River, Oswego
River and Bass River stream sites, and all sites were
associated with the undisturbed end of the stream
vegetation community gradient (Fig. 8). These three
reference site basins had the highest multiple-indicator,
ecological integrity scores in the Mullica River Basin
(Fig. 8).
The widest range of environmental and biological
conditions, reflected by both the individual- and
multiple-indicator scores, was found in the Batsto
River basin (Figs. 7 and 8). Specific conductance and
pH values ranged from those typical of Pinelands
reference streams to conditions characteristic of
highly altered waters. Streams and impoundments
in the tributaries of the heavily altered western portion
of the basin supported fish assemblages with a high
R.A. Zampella et al. / Ecological Indicators 6 (2006) 644–663
659
Fig. 8. Characteristics of the major Mullica River Basin tributary systems. Box plots show the first, second (median), and third quartiles and the
10th and 90th percentile for each variable. The number of stations (n) by tributary system is Oswego River (8), Bass River (2), Wading River (11),
Batsto River (24), Upper Mullica River (12), Lower Mullica River (9), Sleeper Branch (11), and Nescochague Creek (11).
660
R.A. Zampella et al. / Ecological Indicators 6 (2006) 644–663
percentage of nonnative species, whereas only native
fish were found in the forested eastern portions of the
basin. A similar pattern was observed for anurans and
stream vegetation. The multiple-indicator scores for
the Sleeper Branch and Upper Mullica River basins
also reflected a range of conditions (Figs. 7 and 8).
Both basins supported native and modified fish
communities and stream vegetation. Anuran assemblages in the Sleeper Branch and Upper Mullica River
basins generally represent altered conditions.
Overall, low multiple-indicator scores were
associated with the Hammonton Creek and Lower
Mullica tributary systems (Fig. 7). A majority of the
sites in these two basins were associated with the
disturbed end of the land-use, water-quality, stream
vegetation, fish-community, and anuran-community
gradients (Fig. 8). The Hammonton Creek sites
occupied an extreme position at the disturbed end of
the fish-community gradients. Bullfrogs were present at all impoundments in these drainage systems,
which supported some of the most dramatically
altered anuran communities found in the Mullica
River Basin.
The Nescochague Creek displayed the lowest
multiple-indicator scores (Figs. 7 and 8). The
composition of biological communities in the Nescochague Creek basin reflected the high percentage of
altered lands and modified water-quality that characterized this watershed (Fig. 8). As indicated by their
position on the fish-community gradients, stream and
impoundment assemblages in the Nescochague Creek
basin were among the most heavily modified
communities found in the Mullica River Basin. Most
of the stream sites in this basin were also characterized
by a high percentage of non-Pinelands plant species
and were associated with the more disturbed end of the
stream-vegetation community gradient. Like the
Hammonton Creek and Lower Mullica River tributary
basins, bullfrogs were present at all Nescochague
Creek impoundments surveyed and most anuran
survey sites were associated with the disturbed end
of the community gradients.
4. Discussion
Assessing ecological integrity in relation to aquatic
degradation and diagnosing the causes of degradation
are prerequisites for effective management of stream
ecosystems (Stevenson and Pan, 1999). Our study
supports previous studies indicating that changes in
pH and specific conductance are related to variations
in the percentage of developed land and upland
agriculture within Pinelands watersheds, and that all
three environmental variables are associated with
variations in the composition of stream vegetation,
stream fish, impoundment fish, and anuran assemblages (Dow and Zampella, 2000; Zampella and
Bunnell, 1998, 2000; Zampella and Laidig, 1997). The
relationships between and among environmental and
biological variables provided a clear assessment of the
status of several major tributaries of a major Pinelands
watershed.
By including both water-quality and biological
variables in our assessment, we avoided the debate
over whether ecological integrity is best measured
using stressor variables (e.g., factors that cause a
change in community composition) or response
variables (e.g., changes in species composition).
Furthermore, an assessment of ecological integrity,
which includes both biological and environmental
integrity, is broader than one that is based only on
biotic integrity, which concerns only the status of
biological communities (Stevenson and Pan, 1999).
Because the low pH of Pinelands surface waters is
considered a major factor preventing the establishment
of nonnative fish (Gonzalez and Dunson, 1987;
Graham, 1993; Graham and Hastings, 1984; Hastings,
1979, 1984; Zampella and Bunnell, 1998) and anuran
species (Bunnell and Zampella, 1999; Freda and
Dunson, 1986; Gosner and Black, 1957) in undisturbed
Pinelands waters, this variable appears to be both a
response to altered lands in a watershed and a stressor
that influences community composition. Clearly a
response variable, the association between specific
conductance and other water-quality variables, including calcium, magnesium, and nitrite + nitrate as
nitrogen, strongly suggests that conductance may also
serve as a surrogate for potential chemical stressors and
eutrophication. The same can be said for pH.
Our results support the contention that because
different biological indicators respond to human
disturbances at different scales (Karr and Chu,
1999), the use of a multiple-indicator approach
provides a broader assessment of ecological integrity
than one based on single indicators. With the
R.A. Zampella et al. / Ecological Indicators 6 (2006) 644–663
exception of impoundment fish, the association
between altered land and the multiple-indicator,
ecological integrity scores was stronger than that
displayed by any of the individual water-quality or
biological variables. The slightly higher correlation
between impoundment fish and altered land compared
to that for the multiple-indicator scores is probably
due to the nature of impoundment communities.
Except for tessellated darter, the nonnative fish
encountered in this study are more typical of Pinelands
lakes and ponds (Hastings, 1984) as well as lakes in
other regions (Halliwell et al., 1999). Artificial lentic
habitats may also favor introduced species (Moyle,
1986). Thus, the contrast between native and
nonnative fish species along the community gradient
was more pronounced for impoundments, suggesting
that impoundment fish may be a better biological
indicator of Pinelands watershed integrity than stream
fish.
The ranking method that we used to order sites
along a disturbance gradient was fairly simple and
straightforward. Fausch et al. (1990) described several
limitations associated with the use of multivariate
analyses, such as ordination, to develop indexes of
aquatic degradation, including the requirement that
reference sites and degraded sites be included in the
analysis. In our study, ordination provided a direct,
effective, and objective way of ranking the biological
data and associating the ranks with environmental
variables. The clarity of our results may be due to the
presence of strong community gradients that contrasted the Mullica River Basin reference sites and
degraded sites and by well-defined environmental
gradients. We found similarly strong community and
water-quality gradients in the Rancocas Creek Basin,
another major Pinelands watershed (Zampella et al.,
2003). Water-quality, fish, and anuran gradients are
not as pronounced in the Great Egg Harbor River
Basin, a third major Pinelands watershed, where there
are few reference sites and nonnative fish and anuran
species are more widespread (unpublished data). As
Karr and Chu (1999) suggested, the only way to
distinguish the biological signals associated with
resource degradation from those inherent in natural
variation is to sample across a range of human
influences, including reference sites and impacted
sites. Subregional differences in biology and sources of
pollution can complicate the use of biometrics within
661
the same physiographic province such as the southeastern Coastal Plain (Zampella and Bunnell, 1998).
We avoided this problem by limiting our relative
ranking to a limited, well-defined geographic area.
Finally, the characterizations of the major
Mullica River Basin tributary systems based on
the ranking of individual stream sites using either
single or multiple indicators provides a means for
resource managers to focus on those watersheds in
greatest need of remediation or protection. Viewing
each basin as a whole may provide greater insight
into the ecological status of stream systems than the
review of individual sites.
Acknowledgements
The study was supported with funds from the
National Park Service, the U.S. Environmental
Protection Agency, and the Pinelands Commission.
It was based on information presented in a report to the
Pinelands Commission on the status of the aquatic and
wetland resources of the Mullica River Basin. The
comments of two anonymous reviewers helped to
improve an earlier version of this manuscript.
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