Estuaries

Vol. 27, No. 2, p. 283-295

April 2004

Watershed Landscape Indicators of Estuarine Benthic Condition

STEPHEN S. HALE~*,JOHN F. PAUL~, and JAMES F. HELTSHEs
1 U.S. EnrJ~on~lclllal ~FOtes

agggls
Office of teesearch and Development (NHFJ~RL), Atlantic
Ecolog~ Dir~sion, 27 Tarzwelt Drive, Narragansett, Rhode Island 02882
2 U.S. Environmental Protection Agency, t~esearch Triangle Park, N~rth Carolina 27711
s Department of Computer Science and Statistics, University of Rhode Island, Ir
Rhode
Island 02881
ABSTRACT: Do land use and cover characteristics of watersheds associatedwith small estuaries exhibit a strong enough
signal to make landscape metrics useful for identifying degraded bottom communities? We tested this idea with 58 pairs
of small estuaries ( < 2 6 0 km 2) and watersheds in the U.S. Mid-Atlantic coastal plain (Delaware Bay to Chesapeake Bay).
We considered 34 landscape metrics as potential explanatory variables and seven estuarine parameters as response
variables. We d e v e l o p e d three logistic regression models: one to calculate the probability of degraded benthic environmental quality (BEQ), as defined by chemical parameters, and two for the probability of degraded estuarine bottom
communities, o n e using a benthic index (BI) and a s e c o n d using the total number of bottom-dwdling species (TNBS,
consisting of benthic macroinvertebrates and fishes). We evaluated the discriminatory power of the m o d e l s with ROC
(receiver operating characteristic) curves of sensitivity and specificity. All three m o d e l s s h o w e d excellent discrimination
of high and low values. A m o d e l using the sum of all human land uses and percent wetlands correctly classified B E Q in
86% of the eases; low benthic index and low total number of bottom s p e c i e s were each associated with degraded B E Q
(p < 0.01). T h e BI model u s e d percent riparian urban, riparian wetlands, and agriculture on steep slopes (76% correct
classification) and correctly predicted high-low benthic index of an independent data s e t 79% of the time (p < 0.05).
T h e T N B S m o d e l used percent wedands, riparian wedands, and riparian agriculture (74% correct classification). Watersheds with higher percentages of urban and agricultural land uses were associated with lower benthic environmental
quality, benthic index, and biodiversity, whereas those with higher percentages of w e d a n d s w e r e associated with higher
numbers. A~ human d e v e l o p m e n t of watersheds increases, statistical prediction rules d e v e l o p e d from landscape metric~
could be a cost-effective m e t h o d to identify potentially threatened estuaries.

r o n m e n t (Deegan et al. 1997; Breitburg 2002) and

are useful in environmental m o n i t o r i n g (e.g.,
Smith et al. 1999; D e s m o n d et al. 2002). Fish are
relatively easy to sample and identify, are economically important, and occupy top trophic levels that
require intact ecosystems in o r d e r to thrive. Few
long-term m o n i t o r i n g studies have included b o t h
benthic invertebrates and fishes (Desmond et al.

Introduction

Watersheds, delivering freshwater, nutrients, and

organic matter, are the lifeblood of estuaries. But
h u m a n alteration of watersheds often leads to
changes in loading of nutrients, organic matter,
and sediments (Valiela et al. 1992; O'Neill et al.
1997; Wahl et al. 1997;Jones et al. 2 0 0 0 ; J o r d a n et
al. 2008); increased loading of contaminants and
p a t h o g e n s (Siewicki 1997; Inglis and Kross 2000;
Mallin et al. 2000); and changes in water flow
( H o p k i n s o n and Vallino 1995; O'Neill et al. 1997;
J o n e s et al. 2000). Land use changes are predicted
to have a dramatic global impact on biodiversity in
the coming century, particularly n e a r water bodies
where h u m a n s are concentrated (Sala et al. 2000).
In estuaries, benthic invertebrate communities
reflect ecological b o t t o m conditions and have long
b e e n used for environmental m o n i t o r i n g (e.g.,
Pearson and Rosenberg 1978; Weisberg et al. 1997;
Gallagher and Keay 1998; Dauer et al. 2000; Inglis
and Kross 2000). Estuarine fish assemblages are
also influenced by the quality of the b o t t o m envi* Corresponding author;
hale.stephen@epa.gov

tele:

9 2004 Estuarine Research Federation

401/782-3048;

2002).
Land use and cover characteristics of watersheds
can affect the condition of estuarine b o t t o m envir o n m e n t s and communities by s e d i m e n t contamination (Gomeleo et al. 1996; Paul et al. 2002; Morrisey et al. 2003) and have adverse effects on benthic organisms and communities (Porter et al.
1997; Dauer et al. 2000; Inglis and Kross 2000; Letberg et al. 2000; Morrisey et al. 2008). Increased
watershed d e v e l o p m e n t has b e e n associated with
lowered estuarine species diversity, altered food
webs, and altered benthic c o m m u n i t y composition
(Dauer et al. 2000; L e r b e r g et al. 2000). T h e m o r e
extensive literature on linkages between landscapes and freshwater biological effects, such as the
effect of urbanization on stream biological integrity (Karr and Ghu 2000), has b e e n recently reviewed by Gergel et al. (2002) and discussed by

e-mail:

283

284

s.s.

Hale et al.

H u g h e s and H u n s a k e r (2002). Estuarine fish assemblages and n u m b e r of species also r e s p o n d to

stressors with a strong watershed influence such as
hypoxia (Breitburg 2002), quality of b o t t o m habitat ( D e e g a n et al. 1997), a n d stream discharge
( D e s m o n d et al. 2002). A l t h o u g h c o m p o s i t i o n and
condition of estuarine b o t t o m c o m m u n i t i e s are inf l u e n c e d by m a n y n o n w a t e r s h e d factors as w e l l - including tidal circulation, invasive species, harvesting, storms, and s e d i m e n t r e s u s p e n s i o n - - o u r
working hypothesis was that the signal of landscape
influences in small estuaries (<260 km 2) is strong
e n o u g h to be used to identify d e g r a d e d b o t t o m
communities.
T h o u s a n d s of stations in estuaries a r o u n d the
U.S. coasts have b e e n s a m p l e d since 1990 by the
coastal c o m p o n e n t of the U.S. E n v i r o n m e n t a l Protection Agency's E n v i r o n m e n t a l M o n i t o r i n g and
Assessment P r o g r a m (U.S. EPA EMAP) as p a r t of
its b r o a d e r p r o g r a m of assessing the e n v i r o n m e n tal condition of the n a t i o n ' s aquatic resources
(U.S. EPA 2002). T h e p r o g r a m has also collected
data f r o m landscapes a n d freshwater streams. For
estuaries, EMAP has focused on the condition of
the sediments, b o t t o m water, and b o t t o m communities. EMAP uses a probability-based survey design that allows inferences a b o u t the total p o p u l a tion of small estuaries in an area, but does n o t necessarily sample every estuary. S o m e e n v i r o n m e n t a l
m o n i t o r i n g p r o g r a m s find it desirable to identify
all estuaries that fall below s o m e level of expectation, so that r e m e d i a l steps can be taken. As a complete census of all estuaries would be too expensive, predictive m o d e l s are n e e d e d . Data on land
use a n d cover, hydrography, elevation, and r o a d s
are readily available for the U.S. (National L a n d
Cover Data [NLCD] u n p u b l i s h e d data; U.S. Geological Survey [USGS] u n p u b l i s h e d data), and
m a n y aspects of l a n d s c a p e p a t t e r n that potentially
affect water quality can be d e t e r m i n e d f r o m landscape metrics calculated f r o m these data (Jones et
al. 2000). I f these metrics could be used in a m o d e l
that identified potentially d e g r a d e d estuaries, a targeted sampling p r o g r a m m i g h t be m o u n t e d for
those estuaries.
Levels of metals a n d organic c o m p o u n d s in sedi m e n t s of small sub-estuaries in C h e s a p e a k e Bay
are strongly associated with the p r e s e n c e of u r b a n
lands within 10 km of stations ( C o m e l e o et al.
1996). A study of 75 watersheds in the Virginian
B i o g e o g r a p h i c Province showed that this held
across a b r o a d e r g e o g r a p h i c area and that levels of
c o n t a m i n a t i o n decreased as the p e r c e n t a g e of
n o n f o r e s t e d wetlands in the watershed increased
(Paul et al. 2002). Morrisey et al. (2003) f o u n d
h i g h e r chemical c o n t a m i n a n t levels in u r b a n i z e d
estuaries n e a r Auckland, N e w Zealand, than in ru-

ral ones and u r b a n - r u r a l differences in benthic

faunal assemblages. It has b e e n suggested that mac r o b e n t h i c r e s p o n s e may be a m o r e sensitive and
reliable indicator of adverse effects than water or
s e d i m e n t quality data b e c a u s e the loss of biodiversity and the d o m i n a n c e of a few pollution-tolerant
species in polluted areas may simplify the food web
to the p o i n t of irreversibly c h a n g e d ecosystem processes ( L e r b e r g et al. 2000).
T h e p u r p o s e of our study was to d e t e r m i n e
w h e t h e r landscape metrics alone could be used to
discriminate d e g r a d e d and n o n d e g r a d e d estuarine
b o t t o m c o m m u n i t i e s a n d if so, w h e t h e r we could
develop a general m o d e l that could be used over
b r o a d areas. We used logistic regression m o d e l s to
calculate the probabilities of d e g r a d e d benthic env i r o n m e n t a l quality (BEQ), as defined by i n d e p e n d e n t chemical p a r a m e t e r s , a n d d e g r a d e d b o t t o m
c o m m u n i t i e s , as defined by a b e n t h i c i n d e x (Paul
et al. 2001) and by the total n u m b e r of m a c r o i n v e r t e b r a t e a n d fish species. O u r p r i m a r y interest
was the b e n t h i c index. We evaluated the indicators
we derived f r o m the logistic regression m o d e l s by
using ROC (receiver operating characteristic)
curves, which assess the accuracy of an indicator
in reflecting s o m e d i c h o t o m o u s r e s p o n s e (Murtaugh 1996). We investigated w h e t h e r it was useful
to c o m b i n e land use a n d cover data with elevation
and h y d r o g r a p h i c data to derive land use a n d cover p e r c e n t a g e s specific to slope a n d riparian zones.
We also used our surrogate landscape m o d e l to
predict a high-low benthic index for an i n d e p e n d e n t data set.
Methods

ESTUARINE DATA

T h e area of this study was the U.S. Mid-Atlantic

coastal plain f r o m Delaware Bay to C h e s a p e a k e
Bay, which has similar climate, g e o m o r p h o l o g y ,
and b i o g e o g r a p h y (Paul 2001). Data for this work
came f r o m two EMAP studies in the mid-Atlantic
coastal area: the Virginian Province study (VP) of
1990-1993 (Strobel et al. 1999; Hale et al. 2002)
and the estuaries c o m p o n e n t of the Mid-Atlantic
I n t e g r a t e d Assessment (MAIA) of 1997-1998 (Strobel et al. 2000; Kiddon et al. 2003). A third study,
the National Coastal Assessment (NCA), b e g a n in
2000 (EMAP u n p u b l i s h e d data). All three used
c o m p a t i b l e probability-based s a m p l i n g designs and
c o m p a r a b l e field and analytical m e t h o d s . T h e s e
overlapping studies gave us a m o d e l validation data
set that was i n d e p e n d e n t of the m o d e l calibration
data set. M e a s u r e d variables included water quality
( t e m p e r a t u r e , salinity, clarity, dissolved oxygen, nutrients), s e d i m e n t c o n t a m i n a t i o n , s e d i m e n t toxicity, c o m p o s i t i o n of benthic and b o t t o m fish com-

Watersheds and Benthic Condition

TABLE 1. Estuarine p a r a m e t e r s for 58 estuaries in the Vn-gin i a n Province study d a t a set. B e n t h i c p a r a m e t e r s are b a s e d on
the m e a n of t h r e e grabs.
Mean
Estuary area, k i n 2
Station d epth, m
# b e n t h i c species
# benthic organisms
B e n t h i c biornass, g
# fish species
Total # i n d i v i d u a l fish
B e n t h i c I n d e x (BI)
TNBS ~

33.3
4.3
9.8
178.7
0.15
5
136
0.29
15.0

Median Minimum Maximum

26.0
3.9
9.3
84.2
0.07
5
62
0.28
14.3

TNBS (Total n u m b e r of b o t t o m species)

+ # fish species.

1.9
1.5
0.0
0
0
0
0
2.20
0.3

148.9
10.6
32.3
2,888.8
2.42
11
739
8.48
41.3

# b e n t h i c species

munities, and fish tissue c o n t a m i n a n t s and external pathology. T h e VP s a m p l e d 425 probabilitybased stations d-ore C a p e Cod, Massachusetts, to
C a p e Henry, Virginia; MAIA sampled a r o u n d 900
stations f r o m the Delaware River to A l b e r m a r l e Pamlico Sound; and NCA has s a m p l e d t h o u s a n d s
of stations in all states. From these studies, we used
the small (<260 km ~) estuarine systems, which included subestuaries, small bays, tidal rivers, a n d
coastal ponds.
Benthic samples in VP a n d MAIA were collected
using a stainless steel Young grab that s a m p l e d a
surface a r e a of 440 cm ~ (Strobel et al. 1999; Kidd o n et al. 9003). T h e s a m p l e was sieved t h r o u g h a
0.5-ram screen and p r e s e r v e d in 10% formalinrose bengal solution. In the laboratory, the samples
were t r a n s f e r r e d to an ethanol solution, sorted by
species, c o u n t e d , a n d weighed. Fish were collected
by trawling on the b o t t o m 10 m i n u t e s against the
tide between 0.5 and 1.5 m s 1 (1--3 knots) with a
15-m, high-rise otter trawl with a 2.5-cm cod e n d
mesh. A l t h o u g h we r e f e r to fishes c a u g h t in the
otter trawl as b o t t o m species, several species were
c a u g h t that are not strictly associated with the bottom.
Paul et al. (2001) d e v e l o p e d an i n d e x of benthic
c o m m u n i t y condition (BI) for the VP that can be
used over the full r a n g e of salinity a n d s e d i m e n t
grain size f o u n d in the province. It consists of salinity-normalized G l e a s o n ' s D ( n u m b e r of species
divided by log of n u m b e r of individuals), salinityn o r m a l i z e d a b u n d a n c e of tubificid oligochaetes,
a n d a b u n d a n c e of spionid polychaetes. T h e index
is a c o n t i n u o u s variable, with negative values indicating d e g r a d e d sites a n d positive values indicating
n o n d e g r a d e d sites. It correctly classified 87% of
r e f e r e n c e a n d 90% of d e g r a d e d sites, and comp a r e d well with an i n d e p e n d e n t b e n t h i c i n d e x dev e l o p e d specifically for C h e s a p e a k e Bay (Ranasign h e et al. 2002).
For biological r e s p o n s e variables (Table 1), we

285

evaluated this b e n t h i c index, the sum of benthic

m a c r o i n v e r t e b r a t e a n d fish s p e c i e s (which we
called the total n u m b e r of b o t t o m species, or
TNBS, even t h o u g h these species are limited to the
invertebrates >0.5 m m a n d the fishes caught in a
2.5-cm cod end m e s h ) , a b u n d a n c e and biomass of
b e n t h i c invertebrates, and a b u n d a n c e of fishes. Alt h o u g h different i n v e r t e b r a t e and fish taxa res p o n d differently (and these responses are n o t necessarily m o n o t o n i c along a pollution gradient), increasing pollution and h u m a n alteration generally
decreases biodiversity of b o t h benthic invertebrate
(Pearson and R o s e n b e r g 1978; D a u e r 1993; Gallagher a n d Keay 1998; Inglis and Kross 2000;
Clarke and Warwick 9001) and fish ( D e e g a n et al.
1997; Smith et al. 1999; Breitburg 2002) c o m m u nities. A m o d e l that included watershed land use
characteristics a n d water d e p t h explained a significant a m o u n t of variance in an i n d e x of ecosytem
integrity for n o r t h e r n C h e s a p e a k e Bay that comb i n e d benthic a n d fish assemblages ( J o r d a n a n d
Vaas 9002).
WATSRSttSI) DATA
We delineated watershed b o u n d a r i e s for each of
the 60 small VP estuaries in the study area, using
A r c / I n f o GIS software with U.S. Geological Survey
(USGS) 1:100,000 Digital Elevation M o d e l (DEM)
data. We i n t e r p r e t e d the b o u n d a r i e s on-screen using DEM-derived shaded relief m a p s a n d hydrogr a p h y (USGS 1:100,000 Digital Line G r a p h ) as
b a c k g r o u n d s . For s o m e areas with little t o p o g r a p h ic relief, we used USGS 1:24,000 Digital Raster
Graphics to h e l p define the watershed. After eliminating watersheds that were nested in o t h e r watersheds (and t h e r e f o r e n o t i n d e p e n d e n t sampies), we were left with 58 VP watersheds (Fig. 1).
T h e y s p a n n e d wide varieties and ranges of land
cover and land use types, f r o m salt m a r s h and uplands like those on the lower eastern shore of
C h e s a p e a k e Bay to u r b a n i z e d watersheds like those
in the Baltimore area. To obtain an i n d e p e n d e n t
validation data set, we also delineated watersheds
for estuaries that h a d a MAIA station but no VP
station (Fig. 1).
L a n d s c a p e m e t r i c s c a m e f r o m J o n e s et al.
(1997), who had used data f r o m several sources,
particularly the 30-m National L a n d Cover Data
(NLCD u n p u b l i s h e d data), to p r o d u c e a landscape
atlas for the Mid-Atlantic area. T h e y calculated
four g r o u p s of landscape metrics: landscape characteristics, riparian characteristics, physical characteristics, and h u m a n stresses. I n p u t included 30m land use a n d cover, 1:100,000 elevation, 1:
100,000 hydrography, and 1:100,000 roads; the outp u t consisted of 29 l a n d s c a p e metrics (Table 2).
Because these landscape metrics can explain m u c h

286

s.s.

Hale et al.

Fig. 1. Estua~ne stations of the EMAP Via-ginian Province (VP) study and the Mid-Atlantic Integrated Assessment (MAIA) study
for the Delaware Bay m Chesapeake Bay area.
of the variation in stream nutrients and s u s p e n d e d
s e d i m e n t (Jones et al. 2001; Gergel et al. 2002),
we considered t h e m to be potential e x p l a n a t o r y
variables for estuarine ecological condition. We
used the Analytical tools I n t e r f a c e for L a n d s c a p e
Assessments (ATTILA) software, described by E b e r t
et al. (2002), with the National H y d r o g r a p h i n g Dataset (USGS u n p u b l i s h e d data), to calculate riparian metrics for the New Jersey side of Delaware Bay,
which were n o t in the original data set of J o n e s et
al. (1997). We also calculated p o p u l a t i o n density
for all watersheds, using county-level 1990 census
data ( E n v i r o n m e n t a l Systems Research Institute
[ESRI] 1998). We used A r c / I n f o to intersect the
o u t p u t f r o m ATTILA with our delineated estuarine
watersheds. We calculated five additional metrics:
the ratio of watershed a r e a to estuarine area, the
ratio of watershed a r e a to estuarine v o l u m e , and
three landscape p a t t e r n metrics, based on the definitions of O'Neill et al. ( 1 9 9 9 ) - - a v e r a g e p a t c h pe-

rimeter-area ratio, contagion, a n d fractal dimension. Estuarine v o l u m e was calculated by GIS f r o m

National O c e a n i c a n d A t m o s p h e r i c A d m i n i s t r a t i o n
digital charts a n d the National Geophysical Data
C e n t e r ' s H y d r o g r a p h i c Survey Database.
ANALYTICAL PROCEDURES
Model Variables

T h e calibration data set consisted of 58 pairs of

VP estuary-watershed data with 34 candidate landscape metrics a n d 7 candidate estuarine metrics,
In o r d e r to find the m o s t p a r s i m o n i o u s m o d e l s
that a d e q u a t e l y fit the data ( H o s m e r a n d L e m e show 2000), we selected subsets of the landscape
metrics to try as i n p u t to the logistic regression
models; we did this by eliminating several r e d u n dant metrics and those that had a p o o r relationship with the d e p e n d e n t variables. E x p l o r a t o r y
analysis of the landscape data revealed r e d u n d a n t

Watersheds and Benthic Condition

TABLE 2.

287

Landscape m e t r i c s for 58 w a t e r s h e d s of estuaries in the Via-ginian Province study d a t a set.

Area, krn 2
Peiimeter, tml
N-index ~
Forest, %
Wetlands, %
Urban, %
Agriculture, pasture, %
Agriculture, crops, %
Agriculture, total, %
Barren, %
U..index ~
Agriculture, crops, steep b, %
Agriculture, pasture, steep, %
Agriculture, total, steep, %
Riparian ~ human, %
Riparian, barren, %
Riparian, ag, pasture, %
Riparian, ag, crops, %
Riparian, ag, total, %
Riparian, urban, %
Riparian, wetlands, %
Riparian, forest, %
Riparian, natural, %
Stream length, kin
Road length, km
Road densitya
Percent impervious e
Stream-road crossings
Population densityr, persons km 2
Watershed area/estuary area
Watershed area, krn2/estuary volume, rn ~
Average patch perkmeter-area ratios
Con tagione
Fractal dknensions

Mean

Median

Minimum

Maximum

572.0
115.1
52
40
13
13
23
11
34
1
48
1
4
5
27
1
11
6
17
9
32
42
73
691.9
1,480.7
5.0
6
0.4
12.3
51.5
0.19
1,074.4
44.1
1.046

225.6
78.7
52
38
7
5
20
9
31
1
48
1
1
2
22
0
9
4
14
8
27
42
77
197.7
542.2
2.3
3
0.3
0.21
11.4
0.04
1,075.9
43.7
1.045

21.7
21.3
9
7
1
1
0
3
8
0
10
0
0
0
5
0
0
1
4
0
5
3
24
3.7
26.5
0.6
0
0.0
0.0
0.6
0.01
1,036.1
34.4
1.039

4,170.7
440.3
90
73
83
83
52
29
70
6
91
7
22
25
76
6
30
14
39
62
91
76
95
7,586.2
9,902.1
12.4
51
1.7
332.4
788.0
3.18
1,124.4
61.1
1.055

N_index is the sum of all natural land uses and U_index is the sum of all human uses (developed and agricultural lands).
b Steep slopes are defined as those >3%.
c. Riparian is defined as a 30-rn buffer on each side of a stream.
d Road density is total road length divided by watershed area.
e Percentage of impervious cover, based on land use type.
Population density based on county-level 1990 data.
Based on definitions of O'Neill et al. (1999).
landscape metrics (the landscape data had a high
degree of collinearity). For example, natural index
( N - i n d e x ) is t h e d i r e c t c o n v e r s e o f t h e h u m a n u s e
i n d e x ( U _ i n d e x ) , so o n l y o n e is n e e d e d . T h e n we
e x a m i n e d c r o s s - c o r r e l a t i o n s o f all l a n d s c a p e a n d
e s t u a r i n e v a r i a b l e s a n d r e t a i n e d o n l y t h o s e signifi c a n t at p < 0.2. W e also r a n t-tests o n t h e i n d e p e n d e n t v a r i a b l e s u s i n g h i g h a n d l o w classes o f d e pendent variables and kept only those independ e n t v a r i a b l e s w h e r e t h e r e was a s i g n i f i c a n t d i f f e r e n e e (p < 0.2). W e e n s u r e d t h a t e a c h o f t h e
remaining landscape metrics could plausibly lead
to a n e f f e c t o n t h e e s t u a r i n e b o t t o m e n v i r o n m e n t
in some documented fashion, For example, urban
a r e a s , t h r o u g h d i r e c t d i s c h a r g e a n d r u n o f f , l e a d to
elevated sediment contaminants in nearby estuar i n e d e p o s i t i o n a l a r e a s ( C o m e l e o et al. 1996; M o r r i s e y et al. 2 0 0 3 ) . T h e l a n d s c a p e m e t r i c s d r o p p e d
were: area, perimeter, N_index, % barren metrics,

stream and road length metrics, population density, t h e r a t i o s o f w a t e r s h e d a r e a to e s t u a r i n e a r e a

a n d to v o l u m e , a n d t h e t h r e e p a t t e r n m e t r i c s . T h e
r e m a i n i n g m e t r i c s w e r e u s e d as i n p u t to t h e logistic r e g r e s s i o n s ( s p e c i f i c s u b s e t s o f i n d e p e n d e n t vari a b l e s s h o w n i n R e s u l t s ) . O f t h e d e p e n d e n t varia b l e s , BI a n d T N B S c o r r e l a t e d w e l l w i t h s e v e r a l
l a n d s c a p e m e t r i c s a n d w e r e s e l e c t e d f o r f u r t h e r investigation. Benthic invertebrate biomass, mean
number per grab of individual benthic organisms,
and total number per trawl of individual fishes had
weak relationships with landscape metrics and
were not considered further.

Model Devetopraent
E c o l o g i c a l r e s p o n s e s a r e o f t e n b i n a r y , s u c h as
species presence-absence or oxic-anoxic sediments,
o r c a n b e l o g i c a l l y d i c h o t o m i z e d , s u c h as c h e m i c a l
c o n c e n t r a t i o n a b o v e o r b e l o w a w a t e r q u a l i t y stan-

288

S.S. Hale et al.

dard ( M u r t a u g h 1996). Such responses can be analyzed by logistic regression, which we used to calculate, given landscape metrics, the probability of
a d e g r a d e d estuarine b o t t o m community. Relationships between landscape metrics and aquatic systems often exhibit threshold responses (Gergel et
al. 2002). T h e m o d e l s were developed from the VP
calibration data set. We developed three logistic regression models, one with B E Q as the d e p e n d e n t
variable, one with gI, and one with TNBS. T h e dep e n d e n t variable, Y, can take on two values, Y - 1
if the event (a d e g r a d e d condition such as a low
BEQ_, gI, or TNBS) occurs and Y - 0 if the event
does not occur. Logistic regression generates an
estimate of the probability of (Y - 1) - p, for each
data p o i n t i - 1 . . . . . n. After assessing the goodness of fit of several multiple logistic regression
models we developed a rule for classification that
was based on a cutpoint k for the estimated 10t values. We used the value of k from the classification
table (SAS Institute 2002) that gave the highest total correct classification. This rule b e c a m e our indicator for the condition. O u r general rule was: if
ibm> k t h e n Y =
lorifib~< kthenY=
0;0.0 < k
< 1.0. Explanatory variables with p < 0.10 for
Wald's chi-square statistic were considered significant. We used the Akaike I n f o r m a t i o n Criterion to
select the best set of i n d e p e n d e n t variables for
each m o d e l and the H o s m e r - L e m e s h o w goodnessof-fit test ( H o s m e r and L e m e s h o w 2000; SAS Institute 2002) to d e t e r m i n e w h e t h e r the fitted m o d e l
was adequate.

Logistic Model f~r Benthic Environmental Quality

T h e condition of b o t t o m c o m m u n i t i e s is affected by the condition of their immediate environm e n t or h a b i t a t - - s e d i m e n t s and b o t t o m water. Watershed landscapes affect b o t t o m c o m m u n i t i e s to
the extent they affect habitat quality. T h e r e are
nonwatershed-related stressors in estuaries that affect benthic environmental quality, such as b o t t o m
water b r o u g h t in from elsewhere by tidal mixing.
But our null hypothesis was that the watershed
landscape played no part in the quality of benthic
environments.
We classified a priori the B E Q of a station as
degraded, n o n d e g r a d e d , or i n t e r m e d i a t e by applying the following criteria. A d e g r a d e d station was
one where at least one sediment c o n t a m i n a n t exceeded the biological effects range-median (ER-M)
criteria ( L o n g et al. 1995; L o n g et al. 2002), or ten
or m o r e exceeded the effects range-low (ER-L), or
there was s e d i m e n t toxicity with survival < 8 0 % , or
b o t t o m dissolved oxygen c o n c e n t r a t i o n was < 2 mg
1-h A n o n d e g r a d e d station had no ER-Ms, -<8 ERLs, no sediment toxicity, and > 5 mg 1-1 oxygen.
This identified 14 d e g r a d e d (low BEQ) and 15

n o n d e g r a d e d (high BEQ) stations. We used multiple logistic regression to try to distinguish the two
B E Q classes, using only the subsets of landscape
metrics as i n d e p e n d e n t variables. To see how the
biological metrics c o m p a r e d between the two B E Q
classes, we used a t-test to c o m p a r e the BI m e a n of
high B E Q stations with that of low B E Q stations.
We did the same for the total n u m b e r of b o t t o m
species. To examine how the composition of the
c o m m u n i t y assemblages varied by BEQ_, we used
n o n - m e t r i c m u l t i d i m e n s i o n a l scaling (NMDS),
with a Bray-Curtis similarity index on square roottransformed a b u n d a n c e data, and an analysis of
similarity, A N O S I M (Clarke and Warwick 2001) for
both the benthic c o m m u n i t i e s and the fish communities.

Logistic Models of Benthic Index and Total Number of

Bottom @ecies
To m o r e directly examine the relationship between watersheds and estuaries, we next used BI
and TNBS from all 58 stations as direct d e p e n d e n t
variables in logistic regressions. This a p p r o a c h
could be useful for a m o n i t o r i n g p r o g r a m that
does n o t have B E Q data such as s e d i m e n t contaminant levels. T h e BI was converted to a dichotom o u s variable (above or below zero). We transf o r m e d TNBS, also a c o n t i n u o u s variable, to dic h o t o m o u s categories by using the m e d i a n (15) of
the calibration data set as the threshold between
high and low species stations. T h e BI is probably a
better indicator than the TNBS because the index
is salinity-normalized, multimetric, and includes
a b u n d a n c e s for specific pollution-tolerant taxa as
well as diversity data. Several investigators have
f o u n d a g o o d relationship between multimetric
benthic indices and the quality of the estuarine
b o t t o m e n v i r o n m e n t (Weisberg et al. 1997; Van
Dolah et al. 1999; Paul et al. 2001; Llanso et al.
2002; Ranasignhe et al. 2002). We included the
biodiversity measure TNBS because it contains inf o r m a t i o n a b o u t fish assemblages and may be
m o r e intuitively u n d e r s t o o d by managers than a
statistical m u l t i m e t r i c i n d e x . J o r d a n a n d Vaas
(2000) also included data from b o t h benthic and
fish assemblages in their index of ecosystem integrity.

Evaluating Logistic Regression Models

We created classification rules (indicators) for
the logistic regression probabilities and evaluated
their discriminatory effectiveness with ROC curves
from signal detection theory. A g o o d indicator will
be both sensitive to the underlying condition of
interest and specific to that condition (Murtaugh
1996). T h e sensitivity of the indicator is the probability of a positive indicator, given that the true

Watersheds and Benthic Condition

289

TABLE 5. Estuarine a n d watershed p a r a m e t e r s for 19 estuaries in the Mid-Atlantic I n t e g r a t e d A s s e s s m e n t study data set. L a n d s c a p e
m e t r i c s shown only for those metrics u s e d in the b e n t h i c i n d e x logistic regression.

Estum-y area, k m ~
Station depth, m
# b e n t h i c species
# benthic organisms
Benthic biomass, g
Benthic I n d e x (BI)
Riparian, wetlands, %
Riparian, u r b a n , %
Agriculture, total, steep, %

Mean

Median

6.6
2.5
21.0
253.5
0.23
-0.03
54
10
4

5.8
2.1
11.0
174.0
0.08
0.27
50
4
1

r e s p o n s e is positive. T h e specificity is the probability of a negative indicator, given that the true
r e s p o n s e is negative. A plot of sensitivity versus
specificity (the R O C curve), shows the probability
of detecting true signal (sensitivity) a n d false signal
(specificity). T h e a r e a u n d e r the R O C curve c provides a m e a s u r e of the indicator's ability to discriminate between the observations that have the response (a low BEQ, BI, or TNBS) a n d those that
do not. T h e a r e a u n d e r the curve is e x p e c t e d to
be - 0 . 5 for a n o n - i n f o r m a t i v e indicator and 1 for
a p e r f e c t indicator ( M u r t a u g h 1996). An a r e a >0.7
is c o n s i d e r e d acceptable discrimination and an
area ->0.8 has excellent discrimination ( H o s m e r
a n d L e m e s h o w 2000).

Validating the Benthic Index Model

To validate the logistic m o d e l d e v e l o p e d with VP
data, we tested how successfully it could predict a
high or low BI in the MAIA estuaries. In o r d e r to
have i n d e p e n d e n t pairs of w a t e r s h e d - e s t u a r y , we
used only the 19 MAIA estuaries with no VP station
or with missing VP b e n t h i c data (Fig. 1, Table 3).
T h e actual BI for MAIA stations was calculated the
s a m e way as for VP stations (Paul et al, 2001; Kidd o n et al. 2003). We did not a t t e m p t to validate
the VP TNBS indicator with MAIA data because
TABLE 4.

L a n d s c a p e metrics u s e d in logistic regressions.

Landscape M e d i c

Mean
Mean
Percent Perce~
abe %r
~ge %r
Low
High
Qat%ory Category

BEQ
U-index
P e r c e n t a g e we tlan ds

63
4

43
19

29
29

BI
P e r c e n t a g e riparian u r b a n
P e r c e n t a g e riparian wetlands
P e r c e n t a g e total agric, steep slopes

14
27
7

6
35
5

53
55
58

TNBS
P e r c e n t a g e wetlands
P e r c e n t a g e riparian wetlands
P e r c e n t a g e riparian total agric.

6
22
19

19
41
15

55
51
51

Minimum

Maximum

1.6
0.6
1.0
15.0
0.01
-8.90
3
0
0

12.6
9.2
34.7
1,620.0
2.24
2.89
79
63
25

the latter had too m a n y missing values for fish sampling.

Results
LOGISTIC M O D E L FOR B E N T H I C
ENVIRONMENTAL Q U A L I T Y

A logistic regression used the U_index (sum of

all h u m a n land uses such as d e v e l o p e d a n d agricultural lands) and the p e r c e n t wetlands in the watershed (Table 4) to correctly classify 86% of the
29 d e g r a d e d - n o n d e g r a d e d stations with a sensitivi t , / o f 7 9 % and a specificity of 93% (Table 5). Measures of the association between landscape metrics
a n d B E Q were strong; the area u n d e r the R O C
curve (Fig. 2) was 0.95. T h e H o s m e r - L e m e s h o w
goodness-of-fit test showed that the m o d e l fit the
data well (null hypothesis of g o o d fit n o t rejected),
T h e m e a n U_index was significantly (p < 0.01)
m o r e (63 versus 43) and the m e a n p e r c e n t wetlands significantly less (4% versus 19%) for deg r a d e d station watersheds than for n o n d e g r a d e d
station watersheds. T u r n i n g to the second step of
the indirect a p p r o a c h , the biological metrics were
significantly (p < 0,01) worse at the d e g r a d e d stations: m e a n g I of 0.S versus 1.2 a n d m e a n total
n u m b e r of species of 11,8 versus 18,4, NMDS plots
of the benthic and the fish c o m m u n i t i e s also
showed significant (p < 0.01, ANOSIM) differences in c o m m u n i t y assemblages between the degraded and n o n d e g r a d e d stations (Fig. 3). T h e stress
levels indicated a good NMDS o r d i n a t i o n of the
c o m m u n i t y data. D o m i n a n t b e n t h i c and fish species at the n o n d e g r a d e d and d e g r a d e d stations are
shown in Table 6.

TABLE 5.

Logistic regression m o d e l results.

Model

point

Percera tage
Correct

Sensi
tivity

Sjoeci
ncuty

ROC c

Hemmer
Lemeshow

BEQ
BI
TNBS

29
58
51

0.68
0.46
0.54

86
76
75

79
67
84

93
81
65

0.95
0.81
0.85

0.38
0.79
0.57

Cur

290

s . s . Hale et al.

used the percentages of riparian urban, riparian

wetlands, and total agriculture on steep slopes (Table 4). T h e model correctly classified 76% of the
observations, with a sensitivity of 67% and a specificity of 81% (Table 5). T h e area u n d e r the ROC
curve (0.81) indicated excellent discriminatory
power between high and low BIs. T h e p e r c e n t riparian u r b a n and total agriculture on steep slopes
was h i g h e r for low BI stations than for high BI stations; the p e r c e n t riparian wetlands was lower (Table 4). T h e VP m o d e l correctly predicted highdow
BI in i n d e p e n d e n t estuaries (MAIA) 79% (p <
0.05) of the time (Table 7).
LOGISTIC MODEL FOR TOTAL NUMBER
OF BOTTOM SPECIES
Fig. 2. Receiver operating characteristic (ROC) curve for
benthic envh-onmental quality (BEQ) with Vh-ginian Province
data set.

LOGISTIC MODEL FOR BENTHIC INDEX

T h e r e were $2 stations with a low BI and 21 with

a high BI (5 of the original 58 had missing data).
T h e logistic m o d e l that best fit the data for the BI
A. Benthos

N
N

N D t~l i ~

I,iLI

D
D ED

D
D

Stress: 0.13
B. Fish

N
N ND

o$

DE)

N
[]

Stress: 0.15
Fig. 3. Non-pm-ametiic multidimensional scaling plots for
benthic community and fish community at degraded (D) stations (low BEQ) and nondegraded (N) stations (high BEQ).
Both communities showed a significant difference (p < 0.01,
ANOSIM) in community structure between degraded and nondegraded stations.

A total of 31,590 individual benthic invertebrates

from 206 taxa were collected at the 58 stations.
Four taxa a c c o u n t e d for half of the individuals: oligochaetes, including Lirnnodr'ilus hoffme~isteri, the
polychaete Strebtospio bevtedicti, and the a m p h i p o d s
Cc*rophium lacustre and Leptoche~irusptumutosus. Other numerically a b u n d a n t species included the polychaetes Heteroraastus fitifo~mis, Marenzdteria viridis,
Tharyx spp., and Mediornastus arnbiseta, the amphipods Arapelisca abdita and A. vadorura, and the bivalve Macorna rnitchdli. Benthic biomass was dominated by the bivalves Rangia cuneata and family Tellinidae, oligochaetes, polychaetes, Cmophiurn spp.,
and Gyathura spp. A total of 11,906 individual fish
from 42 species were caught at the 58 stations. Seven species m a d e up 90% of the catch: white p e r c h
(MorGue americana), spot (Leiostoraus xanthurus),
h o g c h o k e r (Trinectes macutatus), brown bullhead
(Ameiurus nebulosus), Atlantic m e n h a d e n (Brevoe>
tia tyrannus), weakfish ( Cynosdon regalis), and Atlantic croaker ( Micropogonius undutatus).
T h e r e were 25 stations with low n u m b e r s of species and 26 with high numbers. T h e best fitting
logistic m o d e l for total n u m b e r of species used as
explanatory variables the percentages of wetlands,
riparian wetlands, and riparian total agriculture
(Table 4). T h e m o d e l successfully classified 75% of
the observations, with a sensitivity of 84% and a
specificity of 65% (Table 5). T h e area u n d e r the
ROC curve (0.85) showed excellent discrimination
between stations with a high n u m b e r of species
and those with a low number. This suggests that
estuaries in this area with h i g h e r n u m b e r s of species tend to have watersheds with h i g h e r percentages of whole-basin and riparian wetlands and lower percentages of riparian agriculture (Table 4).
Discussion
LINKS BETWEEN WATERSHEDS AND ESTUARINE
BOTTOM COMMUNITIES

Previous work has shown a strong relationship

between watershed landscape metrics and levels of

Watersheds and Benthic Condition

291

TABLE 6. Dominant benttfic invertebrate (top ten by abundance) and fish (top five by abundance) species at 15 nondegraded (high
BEQ) and 14 degraded (low BEQ) stations.
Nond%raded (High BEQ)

Degraded (Low BEQ)

I nver tebra.te Spe cie s

Abundance

Nemertine a
Annelida: Polychaeta
Heteromastus filiforwds
Mediomastus ambiseta
Streblo~pio benedicti
Paraprionospio pinnata
Annelida: Oligochaeta
Ofigochaeta

I nver tebra.~e Spe cie s

Abundance

67
129
87
67
62
85

Mollusca: Bivalvia
Macoma mitchelli
Arthropoda: Crustacea
Leptocheirus plum~los~s
Arthropoda: Malacosn-aca
Le~con american,s
C~athura polita

Hetero~ast~s filifi,rmis
Neantlzes succinea
Streblospio benedicti

154
32
42

Oligochaeta
Limnodril~s hoffmeisteri
Aulodrilus pig~ieli
Tubificidae

77
141
58
716

142

Macov~a mit&elli
Mus~li*zm si0p.

107

Leptodadrus plumulosus

37
62
482

58
50

Fish Species

Abundance

Fish Species

Abundance

Leiostom~s xan#~r~s
Trinectes ma~latus
CTnoscion regalis
Micropogonias undulatus
Peprilus alepidotus

421
401
91
55
22

M~rone americana
Dorosorna cepedianurn
Leiosto~ezs xantlaezrvzs
Ameiurus nebulosus
Trinectes ~aozlat,~s

1,600
235
176
125
122

estuarine s e d i m e n t c o n t a m i n a n t s ( C o m e l e o et al.
1996; Paul et al. 2002; Morrisey et al. 2008). O u r
results show that landscape metrics are also statistically related to the condition a n d biodiversity of
estuarine b o t t o m c o m m u n i t i e s (shown also by
Morrisey et al. 2008 for two u r b a n i z e d versus two
rural watersheds). L a n d s c a p e metrics a l o n e disc r i m i n a t e d low and high B E Q stations a n d the biological metrics were significantly worse at the low
B E Q stations. W h e r e B E Q w a s low, n u m e r i c a l d o m inants were pollution-tolerant or opportunistic species such as tubificid oligochaetes, including s
hoffmeisteri and the a m p h i p o d L. pluraulosus. T h e
n u m b e r s of m o r e pollution-sensitive species, such
as the bivalve M. mitchelti and the crustaceans Leucon americanus and Cyathura polita were r e d u c e d at
low B E Q c o m p a r e d to high B E Q stations. This is a
typical benthic c o m m u n i t y response, with crustaceans, e c h i n o d e r m s , and bivalves tending to d r o p
TABLE 7. Two-way contingency table for Mid-Atlantic Integrated Assessment (MAIA) benthic index.
Predicted MAIA Be nthic Index
NOI:

Degraded degraded

Actual MAIA
Benthic Index

Total

Degraded
Nondegraded

3
0

4
12

7
12

Total

16

19

out in favor of annelids at m o r e stressed stations

(Pearson a n d R o s e n b e r g 1978; D a u e r 1998; Gallagher a n d Keay 1998; Inglis a n d Kross 2000; Morrisey et al. 2008).
Estuaries that h a d watersheds with higher percentages of wetlands and lower p e r c e n t a g e s of urb a n a n d agricultural areas t e n d e d to have a h i g h e r
benthic index and h i g h e r biodiversity. D a u e r et al.
(2000) f o u n d that benthic conditions in Chesap e a k e Bay were negatively correlated with measures of watershed u r b a n i z a t i o n a n d positively correlated with p e r c e n t forest in the watersheds. Two
u r b a n i z e d estuaries in n o r t h e a s t e r n Australia had
m a r k e d l y different f a u n a assemblages than three
n o n u r b a n i z e d estuaries; the differences c o r r e l a t e d
strongly with the c o n c e n t r a t i o n s of h y d r o c a r b o n s ,
lead, a n d c o p p e r in the s e d i m e n t s (Inglis and
Kross 2000). Differences in benthic assemblages
between u r b a n i z e d and n o n u r b a n i z e d estuaries
were also f o u n d in N e w Zealand (Morrisey et al.
2008) a n d in South Carolina, where L e r b e r g et al.
(2000) f o u n d that m a c r o b e n t h i c diversity and
a b u n d a n c e were lower for tidal creeks with u r b a n
watersheds than for watersheds with s u b u r b a n land
use, primarily because crustaceans a n d bivalves
(particularly rare taxa) were m u c h r e d u c e d in the
foriiler.

Fish assemblages in our study also r e s p o n d e d to

292

s.s.

Hale et al.

e n v i r o n m e n t a l d e g r a d a t i o n - - w i t h slightly m o r e
species at high B E Q than at low B E Q stations and
a clear difference in assemblage c o m p o s i t i o n - - b u t
the results were m o r e a m b i g u o u s than for benthic
m a c r o i n v e r t e b r a t e s . Restricting o u r analysis to the
y e a r . r o u n d resident fish species listed by M u r d y et
al. (1997) did n o t clarify the story. White perch,
gizzard shad (Dorosoma cepediar~um), and brown
b u l l h e a d were a b u n d a n t at stations where B E Q was
low. O t h e r species that were a b u n d a n t where B E Q
was high, such as spot, h o g c h o k e r , a n d weakfish,
were not as a b u n d a n t where B E Q w a s low. N u m b e r
of fish species would be e x p e c t e d to be lower in
estuaries with hypoxic or anoxic b o t t o m waters, but
s o m e fish m a y briefly swim into a hypoxic area to
prey on oxygen-stressed invertebrates (Breitburg
2002). O u r criteria for d e t e r m i n i n g d e g r a d e d stations included o t h e r p a r a m e t e r s such as s e d i m e n t
c o n t a m i n a n t c o n c e n t r a t i o n s a n d s e d i m e n t toxicity,
a n d h o w fish r e s p o n d to these variables m a y be
m o r e complex. Rose (2000) n o t e d that the relationship b e t w e e n e n v i r o n m e n t a l quality and fishes
can be difficult to quantify; spatial h e t e r o g e n e i t y
of habitat can result in p o p u l a t i o n responses disp r o p o r t i o n a t e to e n v i r o n m e n t a l quality. O n the
o t h e r h a n d , fish species using s o u t h e r n N e w England estuaries as spavaling or n u r s e r y areas were
less a b u n d a n t in low quality habitat as c o m p a r e d
to m e d i u m quality habitat ( D e e g a n et al. 1997);
fish assemblages at a sewage outfall h a d significantly less species richness than control stations
(Smith et al. 1999); a n d fish assemblages in three
estuaries in s o u t h e r n California were m o r e predictable f r o m e n v i r o n m e n t a l variables than were
i n v e r t e b r a t e assemblages ( D e s m o n d et al. 2002).
Nets that capture younger, smaller, a n d p e r h a p s
m o r e s i t e - d e p e n d e n t fishes (e.g., D e e g a n et al.
1997) m a y provide a b e t t e r m e a s u r e than did the
2.5 c m - m e s h b o t t o m trawl we used.
An i m p o r t a n t caveat is that statistically a n d biologically m e a n i n g f u l associations between the indicator a n d r e s p o n s e are not necessarily causal.
T h e actual m e c h a n i s m s by which landscape characteristics lead to d e g r a d e d estuarine b o t t o m conditions have b e e n discussed by others (e.g., Valiela
et al. 1992; H o p k i n s o n and Vallino 1995; Basnyat
et al. 1999; D a u e r et al. 2000; J o r d a n et al. 2003),
a l t h o u g h m o r e study is n e e d e d (Gergel et al.

2002).
EVALUATION OF ESTUARINE AND
LANDSCAPE METRICS

Biological r e s p o n s e variables for m e a s u r e s of

productivity ( n u m b e r s of individual organisms and
biomass) were n o t as useful in o u r study as were
the benthic i n d e x a n d n u m b e r of species. T h e
n u m b e r of individuals can be a m b i g u o u s because

it is affected by the n u m b e r of pollution-tolerant

and opportunistic species with h i g h r e p r o d u c t i o n
rates, which can r e a c h relatively high n u m b e r s in
m o d e r a t e l y polluted waters (Pearson a n d Rosenberg 1978; Weisberg et al. 1997; L e r b e r g et al.
2000). It is p r o b a b l y of limited value in characterizing the quality of estuarine habitat ( D a u e r 1998).
A b e t t e r metric of benthic condition may be the
relative a b u n d a n c e of pollution-tolerant species
and pollution-sensitive species ( D a u e r a n d Alden
1995; L e r b e r g et al. 2000). Weisberg et al. (1997)
f o u n d that the data distributions, b u t n o t the
means, of benthic a b u n d a n c e and biomass in Chesa p e a k e Bay were significantly different for polluted
and u n p o l l u t e d areas. D r o p p i n g biomass f r o m
their i n d e x r e d u c e d classification efficiency by only
1%. W h e r e a s the BI in o u r study used a b u n d a n c e s
(albeit only for two taxa), the total n u m b e r of bottom species m e a s u r e did not. NMDS o r d i n a t i o n
has the advantage of using relative a b u n d a n c e
f r o m all species in an assemblage.
A m o n g the l a n d s c a p e metrics, consistently g o o d
e x p l a n a t o r y variables included p e r c e n t urban, wetlands, a n d agriculture, particularly in riparian areas or, for agriculture, on steep slopes. Similar resuits have b e e n n o t e d by others in b o t h estuaries
(Basnyat et al. 1999; Meeuwig 1999; D a u e r et al.
2000; L e r b e r g et al. 2000; Morrisey et al. 2008) and
streams (O'Neill et al. 1997; Wahl et al. 1997; Karr
and C h u 2000; J o n e s et al. 2001; Gergel et al.
2002). M e c h a n i s m s by which u r b a n and agricultural lands deliver pollutants to estuaries a n d ways
in which wetlands a n d riparian z o n e s function as
buffers are well d o c u m e n t e d (e.g., Correll et al.
1992; Valiela et al. 1 9 9 2 ; J o r d a n et al. 2008). In o u r
study, the odds ratio f r o m the logistic regression
showed that for every 1% increase in the U-index,
a d e g r a d e d B E Q was a b o u t 10% m o r e likely. This
could be used to c o m p a r e watersheds or to anticipate what m i g h t h a p p e n as a watershed b e c o m e s
m o r e developed. P e r c e n t wetlands worked well as
a metric in the Mid-Atlantic coastal area; this
r a n g e d f r o m high values in small estuaries with extensive salt m a r s h e s to the o t h e r end of the spect r u m in estuaries so heavily u r b a n i z e d that any
original salt m a r s h e s h a d long since b e e n filled.
Metrics such as land use and cover p e r c e n t a g e s
in riparian areas a n d types of agriculture on steep
slopes provide m o r e specific spatial i n f o r m a t i o n
(location of streams a n d steep slopes) than do percentages for the entire watershed. Riparian metrics
may be useful additions because of the s h o r t pathway f r o m source to stream and the b u f f e r i n g capacity of vegetated riparian z o n e s (Correll et al.
1992; Basnyat et al. 1999; Gergel et al. 2002;
H u g h e s a n d H u n s a k e r 2002). T h e distance f r o m a
land use type to a stream or estuary matters be-

Watersheds and Benthic Condition

cause of the physical and chemical dynamics that

occur b e t w e e n source and destination (Correll et
al. 1992; C o m e l e o et al. 1996; Siewicki 1997; D a u e r
et al. 2000; Gergel et al. 2009). O u r results suggested that m o d e l s that include riparian and slope
i n f o r m a t i o n may be b e t t e r indicators of estuarine
condition than m o d e l s that use only total watershed metrics. Riparian and slope metrics are easy
to calculate using GIS tools, a n d the data n e e d e d
are readily a v a i l a b l e - - N a t i o n a l H y d r o g r a p h y Dataset for streams (USGS u n p u b l i s h e d data) and National Elevation Dataset for slopes (USGS u n p u b lished data).
T h e p e r c e n t a g e of watershed i m p e r v i o u s to rainwater has b e e n shown in several studies to be an
i m p o r t a n t landscape metric (e.g., Karr and C h u
2000; Gergel et al. 2002). In o u r study, p e r c e n t impervious h a d a significant (p - 0.08) negative correlation with the BI, a n d slightly i m p r o v e d the fit
of the BI m o d e l , but we did n o t include it for reasons of parsimony, as it was c o r r e l a t e d with p e r c e n t
urban. At the spatial scale of o u r data, n o n e of the
three landscape p a t t e r n metrics (average p a t c h per i m e t e r - a r e a ratio, contagion, and fractal dimension) showed m u c h p r o m i s e as e x p l a n a t o r y variables for estuarine biological metrics. T h e s e are
m o r e useful in characterizing the habitat of species
that live within the l a n d s c a p e than they are for water quality effects (O'Neill et al. 1999). It would be
m o r e interesting to look at p a t t e r n metrics for the
estuarine b e n t h i c habitat itself as e x p l a n a t o r y variables for species distributions.
LANDSCAPE METRICS AS A WAY TO IDENTIFY
DEGRADED ESTUARIES

Estuarine m e a s u r e m e n t s such as s e d i m e n t chemistry a n d b e n t h i c c o m m u n i t y structure can be expensive. Developing statistical p r e d i c t i o n rules with
readily available l a n d s c a p e data could be a costeffective way to screen for potentially d e g r a d e d estuaries. T h e logistic regression m o d e l d e v e l o p e d
with only VP data correctly predicted a low or high
MAIA BI 79% of the time. To m a k e a strong case,
however, a larger sample size that covers o t h e r
b i o r e g i o n s is n e e d e d . We p l a n to test the m o d e l
against o t h e r i n d e p e n d e n t estuaries within a n d
outside our study region w h e n NCA data b e c o m e
available, for they cover a m u c h b r o a d e r area. NGA
data will also be n e e d e d to try to validate the total
n u m b e r of b o t t o m species indicator. Before the logistic m o d e l s can be generally applied, they must
be evaluated in areas with a different mix of landscape characteristics a n d different prevalences of
estuarine responses.
No high BI MAIA estuaries were incorrectly predicted to be low by the g I model. However, it predicted a high BI for 4 of 7 MAIA estuaries that

293

actually h a d a low BI. We could m a k e the m o d e l

m o r e sensitive by lowering the cutpoint to try to
pick up these stations. However, these four estuaries t e n d e d to have small watersheds with relatively little h u m a n d e v e l o p m e n t . We suggest that the
actual BI was low b e c a u s e the estuary was influe n c e d by the hypoxic z o n e of the m a i n s t e m Chesa p e a k e Bay ( D a u e r a n d A l d e n 1995), a stressor
that, while certainly related to the overall watershed r u n o f f to C h e s a p e a k e Bay, had little to do
with the watershed of that particular small estuary.
( T h e predictive p e r f o r m a n c e of these m o d e l s
would p r e s u m a b l y i m p r o v e if a project had additional data available such as b o t t o m water dissolved
oxygen, s e d i m e n t c o n t a m i n a n t s , a n d p o i n t source
loadings.) Conversely, the TNBS m o d e l was g o o d
at detecting low species stations, but n o t particularly specific to them. This is acceptable if the objective is to find low species estuaries and the cost
of u n n e c e s s a r y sampling of high species stations is
moderate.
Indicators must be rigorously s c r e e n e d b e f o r e
they are put to use as m e a n i n g f u l surrogates for
the r e s p o n s e of interest ( M u r t a u g h 1996). Signal
detection t h e o r y has b e e n used extensively in m e d ical research but less in ecological studies (Murtaugh 1996). Medical studies, on a single species,
may have an easier time finding a gold s t a n d a r d of
actual condition t h a n ecological research. We evalu a t e d h o w well a logistic regression m o d e l worked
with a reasonably defined measure----BEQ., which
was defined by chemical m e a s u r e m e n t s . T h e n we
e x a m i n e d h o w well logistic regression worked with
less well-defined m e a s u r e s - - t h e BI and TNBS. Alt h o u g h areas u n d e r the R O C curves for BI a n d
TNBS indicated excellent discrimination of the response variables, an i m p o r t a n t question is how well
these indicators would work for o t h e r regions.
T h e y m a y work well in areas with similar mixes of
urban, agriculture, and wetlands (half the watershed a r e a in our study was developed), b u t n o t as
well in m o r e forested regions such as the G u l f of
Maine. T h e functional relationships between landscape metrics a n d stream water quality m a y be different in ecoregions with different landscape characteristics (Jones et al. 2000, 2001; G e r g e l et al.

2002).
L a n d s c a p e metrics of h u m a n use were associated
with d e g r a d e d benthic m a c r o i n v e r t e b r a t e a n d bottom fish assemblages in small estuaries. O u r results
indicate that landscape statistical p r e d i c t i o n rules
reflect a strong e n o u g h watershed signal to be a
cost-effective m e t h o d for a m o n i t o r i n g p r o g r a m to
use in deciding w h e t h e r to sample a particular estuary. Signal detection t h e o r y provides a rigorous
standard for evaluating potential ecological indicators and for j u d g i n g applicability to areas with

294

s.s.

Hale et al.

differing prevalences
of the condition.
With the
dramatic
global impact on biodiversity from land
use changes
that are anticipated
in coastal areas
during the coming
century
(Lerberg
e t al. 2 0 0 0 ;
S a l a e t al. 2 0 0 0 ; D e s m o n d
e t al. 2 0 0 2 ; L l a n s o e t al.
2002), even estuaries
that are now in relatively
good condition
face additional
pressure from increased watershed
development.
Both the need for
monitoring
a n d i t s c o s t will i n c r e a s e .
That will
make predictive models such as the logistic regression indicators
described
here even more important.
ACKNOWLEDGMENTS
We gratefully acknowledge the n u m e r o u s people who collected a n d a s s e m N e d the EMAP Virginian Province a n d MidAtlantic I n t e g r a t e d A s s e s s m e n t data. We t h a n k D. Ebert a n d
EPA's L a n d s c a p e Ecology B r a n c h for p r o d u c i n g the l a n d s c a p e
metrics a n d D. McGovern a n d J. C o p e l a n d for delineating the
x*~tersheds a n d o t h e r GIS work. T h e m a n u s c r i p t was materially
i m p r o v e d f r o m reviews by D. Dauer, M. Nicholson, M. Pelletier,
L. Meng, a n d K. Rahn. A l t h o u g h the r e s e a r c h described in this
artide h a s b e e n f u n d e d in part by the USEPA, it h a s n o t b e e n
subjected to Agency review-. T h e r e f o r e , it does n o t necessarily
reflect the views o f the Agency. T h i s is c o n t r i b u t i o n n u m b e r
AED-03-016 of the USEPA, Office o f R e s e a r c h a n d Developmerit, National H e a l t h a n d E n v i r o n m e n t a l Effects Research
Laboratory, Atlantic Ecology Division, Narragansett, R h o d e Island.
LITERATURE C I T E D

~SNYAT, F~, L. D. TF~TeX, K. M. FL'ZNN, AND B. G. LocacaBY

1999. Relationships between landscape characteristics a n d
n o n p o i n t source p o l l u t i o n i n p u t s to coastal estuaries. Environ
mental Managemeat 23:539-549.
B~uRo,
D. 2002. Effects o f hypoxia, a n d the balance between hypoxia a n d e n r i c h m e n t , on coastal fishes a n d fisheries. Estuaries 25:767-781.
(XAR~, K. R. AND R. M. WARWICIC 2001. C h a n g e in m a ~ n e
c o m m u n i t i e s : An a p p r o a c h to statistical analysis a n d interpretation. PRIMER-E Ltd., Plymoudl, U.K.
Coz~v.s.v.o R. L.,J. E PaUL, R V. AuouST, J. COPELaYD, C. B a K e ,
S. S. HALE, AND R. L. LAa~mR. 1996. Relationships b e t w e e n
watershed stressors a n d s e d i m e n t c o n t a m i n a t i o n in Chesapeake Bay estuaries. Landscape Ecology 11:307-819.
CORRFam, D. L., T. E. JORDAN, AND D. E. WFs.s.v.R. 1992. N u t r i e n t
flux in a landscape: Effects of coastal l a n d u s e a n d terresWial
c o m m u n i t y mosaic on n u t r i e n t t r a n s p o r t to coastal waters.
Estuaries 15:431-442.
DAUER, D. M. 1993. Biological criteria, e n v i r o n m e n t a l h e a l t h
a n d estuarine m a c r o b e n d f i c c o m m t m i t y stxuctm-e. Marine Pdlution Bulletin 26:249-257.
DAUF_R, D. M. AND R. W. ALDF~, III. 1995. L o n g - t e r m trends in
the m a c r o b e n t h o s a n d water quality of the lower C h e s a p e a k e
Bay (1985-1991). Marine Pollution Bulletin 30:840-850.
DAUER, D. M., J. A. RANASINOHg, AND S. B. WHSBERG. 2000. Relationships b e t w e e n b e n t h i c c o m m t m i t y condition, water
quality, s e d i m e n t quality, n u t r i e n t loads, a n d l a n d use p a t t e r n s
in C h e s a p e a k e Bay. Estuaries 28:80-96.
DF~OAN, L. A., J. T. FINN, S. G. AWAZIAN, C. A. RYI)F~R-KIFY"FER,
AND J. BUONACCORSI. 1997. D e v e l o p m e n t a n d validation of an
estuarine biotic integrity index. Estuaries 20:601-617.
DESMOND, J. s., D. H. DEUTSOHMAN, AND J. B. ZEI)LEI< 2002.
Spatial a n d t e m p o r a l variation in estuarine fish a n d invertebrate assemblages: Analysis of an 1 I-year data set. Ear
25:
552-569.

EBERT, D. W., 12 G. WAD~, J. E. HAm~ON, AND D. H. Y ~ .

2002. Analytical tools interface for l a n d s c a p e a s s e s s m e n t
(ATTILA). Q u i c k Start Guide, Version 8.0. U.S. E n v i r o n m e n t a l
Protection Agency, Office of Research a n d D e v e l o p m e n t , Las
Vegas, Nevada.
ENVIRO~AL
SYSTEMS RESEARCH INsTrruTE (ESRI). 1998.
ESRI data a n d maps. ESRI, Redlands, CalKornia.
GALLAOH~, E. D. AND K. E. KEAY 1998. O r g a n i s m - s e d i m e n t c o n t a m i n a n t interactions in Boston Harbor, p. 89-170. In D.
D. S m l z e n b a c h a n d E. E. A d a m s (eds.), C o n t a m i n a t e d Sedim e n t s in Boston Harbor. MIT Sea G r a n t College P r o g r a m ,
C a m b r i d g e , Massachusetts.
G ~ o e g , S. E., M. G. ~Xrm,re~, J. R. MILLE~, J. M. MELACa%AND
E. H. STANLEY 2002. Landscape indicators of h u m a n i m p a c t s
to riverine systems. Aquatic Sciences 64:118-128.
HALE, S. S., M. M. H u o I ~ S , C.J. STROBVJ, H. W. BUYVUM,j. L.
COPELAND, AND J. F. PAUL. 2002. Coastal ecological data f r o m
the Virginian Biogeographic Province, 1990-1993. Ecology 83:
2942 a n d Ecological ArctEves E083-057.
HOPICnVSON,J1~., C. S. AND J. j. VALLINO. 1995. T h e relationships
a m o n g m a n ' s activities in watersheds a n d estuaries: A m o d e l
o f r u n o f f effects on p a t t e r n s of estuarine c o m m u n i t y metabofism. Estuaries 18:598-621.
HOS~a~R, J1~., D. W. AND S. LEa~F~SHOW. 2000. A p p l i e d Logistic
Regression, 2 n d edition. J o h n Wiley a n d Sons, New York.
HUOHKS, R. M. AZ,a) C. T. HUNSAKF~. 2002. Effects o f l a n d s c a p e
c h a n g e on aquatic biodiversity a n d biointegrity, p. 309-329 In
K. J. Gutzwiller (ed.), Applying L a n d s c a p e Ecology in Biological Conservation. Springes~Verlag, New York.
INOI~S, G. J. AND J. E. tC~oss. 2000. Evidence for systematic
c h a n g e s in the b e n t h i c f a u n a o f tropical estuaries as a result
o f urbanization. Marine Pollution Bulletin 41:367-376.
JoNEs, K. B., D. 12 H E o o ~ , 12 G. WAD~, A. C. NEAZE, D. W.
EBERT, M. S. NASH, M. H. MEHAFFEY, K. A. HERMANlV,A. R.
Svs.s.v., S. AUOUSTIN< I. A. GOODMAN, J. PEDFa~SeN, D. BOLOMEN, J. M. VIOER, D. Ct-KASqO,C.J. LIN, Y. ZHONO, J. }~IKER,
AND R. D. VAN REIVlORTEL. 2000. Assessing landscape condition relative to water resources in the western U n i t e d States:
A strategic a p p r o a c h . Eavironmental Monitoring" and Assessment
64:227-245.
JoNEs, K. B., A. C. NEALE, M. S. NASH, R. D. VAN REMORTEL, J.
D. WICY,ffKAM, K. H. Rirrreas, AND R. V. O'NKmL. 2001. Predicting n u t r i e n t a n d s e d i m e n t l o a d i n g s to s t r e a m s f r o m landscape metrics: A m u l t i p l e w a t e r s h e d study f r o m the U n i t e d
States Mid-Atlantic Region. Landscape Ecology 16:301-312.
JONES, K. B., K. H. R m r m a s , J. D. WIEIg.HAkiVI,R. D. TANIWY,SLEY,
J1<, R. V. O'NEILL, D. J. (kiALOtYD, E. R. S~TH, AND A. C.
NEALE. 1997. An ecological a s s e s s m e n t o f the U n i t e d States,
Mid-Atlantic Region: A l a n d s c a p e atlas. E P A / 6 0 0 / R - 9 7 / 1 3 0 .
U.S. E n v i r o n m e n t a l Protection Agency, Office o f Research
a n d D e v e l o p m e n t , W a s h i n g t o n , D.C.
JolmAN, S. J. AND R A. VAAS. 2000. An i n d e x of ecosystem integrity for N o r t h e n a C h e s a p e a k e Bay. Environmental Science and
Policy 3:$59-$88.
JORDAN, T. E., D. E. Wvt.t.v.R, AND D. L. CORRmm. 2003. Sources
o f n u t r i e n t inputs to the P a m x e n t River estuary. Estuaries 26:
226-243.
KaRR, J. R. AND E. W. CHU. 2000. Sustaining living rivers. Hydro
biologSa 422:1-14.
KIDDON, J. A., J. F. PAUL, H. W. BtYncuN, C. S. STROBEL, S. S.
HALE, D. COBB, AND B. S. BI~OWN. 2003. Ecological condition
o f U.S. Mid-Atlantic estuaries, 1997-1998. Marine Pollution Bulletin 46:1224-1244.
LF~,BF~RO, S. B., A. E HOLLAND, AND D. M. SANOER. 2000. Responses of tidal creek m a c r o b e n t h i c c o m m u n i t i e s to the effects o f w a t e r s h e d d e v e l o p m e n t . Estuaries 23:838-853.
LLANSO, R. J., L. C. SCOT< J. L. HUAND, D. M. D A t ; ~ , D. E.
RUSSFIL, AND F. W. Kurz. 2002. An estuarine b e n t h i c i n d e x

Watersheds and Benthic Condition

o f biotic integrity for the Mid-Aflantic Region o f the U n i t e d

States. II. I n d e x d e v e l o p m e n t . E~tuaries 25:1231-1242.
LONG, E. R., M.J. I-IAMEEDI, G. M. SLOANE, AND L. B. R ~ . 2002.
C h e m i c a l c o n t a m i n a t i o n , toxicity, a n d b e n t h i c c o m m u n i t y indices in s e d i m e n t s o f the lower Miami River a n d adjoining
p o r t i o n s o f Biscayne Bay, Florida. Estuaries 25:622-637.
LONG, E. R., D. D. MAcDoNALD, S. L. SMITH, AND F. D. CALDER.
1995. I n c i d e n c e of adverse biological effects within r a n g e s of
c h e m i c a l c o n c e n t r a t i o n s in m a r i n e a n d estuarine sediments.
Environmental Managewent 19:81-97.
MAt.trN, M. A., K. E. WmLiat~, E. C. ESHaN, AND R. R LOWE.
2000. Effect o f h u m a n d e v e l o p m e n t on bacteriological water
quality in coastal watersheds. Ecological Applications 10:10471056.
MEEtrWlG, J. j. 1999. Predicting coastal eutroptfication f r o m
land-use: An empirical a p p r o a c h to small non-stratified estuaries. Marine Ecolog/ Progress Series 176:231-241.
MORRISEY, D. J., s. J. ~ n ~ r m , G. N. MmLs, R. B. WILLIAMSON,
AND B. E. Wise. 2003. Factors affecting the distribution of
b e n t h i c m a c r o f a u n a in estuaries c o n t a m i n a t e d by u r b a n r u n off. Marine Environ~wntal Research 55:113-156.
Mtn~Y, E. O., R. S. BIm)SONO, ANDJ. A. MUSlCI~ 1997. Fishes o f
C h e s a p e a k e Bay. S m i t h s o n i a n Institution Press, W a s h i n g t o n ,
D.C.
MURTAUGH, 1~ A. 1996. T h e statistical evaluation of ecological
indicators. Ecological Applications 6:132-139.
O'NF,mL, R. V., C. 22 HUNSAIW~, AND K. B. JON~. 1997. Monitoring e n v i r o n m e n t a l quality at the landscape scale. Bic~cience
47:513--519.
O'NEILL, R. V., K. H. Rin~LRS, J. D. WICI~IAN, AND K. B. JONES.
1999. L a n d s c a p e p a t t e r n metrics a n d regional assessment.
Ecosystem Heai~h 5:225-255.
PAUL, J. F., R. L. COMEI~O, AND J. COPVXAND. 2002. Landscape
metrics a n d estuarine s e d i m e n t c o n t a m i n a t i o n in the MidAtlantic a n d s o u t h e r n New E n g l a n d regions. Jc,grnal of Eavironmental Qualit7 31:836-845.
PAUL, J. F., K. J. ScoTt, D. E. CAIVIPBELL,J. H. GENTILE, C. S.
STROBEL, R. M. VALENTE, S. B. WEISBERG, A. E HOImAND, AND
J. A. RANASINGHE. 2001. Developing a n d applying a b e n t h i c
i n d e x of e s m a r i n e condition for the Vfl-ginian Biogeographic
Province. Ecological Indicators 1:83-99.
PAUL, R. W. 2001. Geographical signatures of m i d d l e Aflantic
estuaries: Historical layers. E~tuaries 24:151-166.
PF~J~ON, T. H. AND R. ROSFa,mERO. 1978. M a c r o b e n t h i c succession in relation to organic e n r i c h m e n t a n d pollution o f the
m a r i n e e n v i r o n m e n t . Oceanograp/zy and Marine Biology Annual
Review 16:229-311.
PORTER, D. E., D. EDWARDS, G. SCOTt, B. JONES, AND W. S.
STm~T. 1997. Assessing the i m p a c t s o f a n t h r o p o g e n i c a n d
p h y s i o g r a p h i c i n f l u e n c e s on grass s h r i m p in localized saltm a r s h estuaries. Aquatic Botany 58:289-306.
RANASlNGHE, J. A., J. B. FraT~SEN, F. W. Ktrrz, J. E PAUL, D. E.
RUSSELL, R. A. BA~UK, J. L. H'mAND, J. SCOTt, AND D. M.
DAUER. 2002. Application o f two indices of b e n t h i c c o m m u nity condition in C h e s a p e a k e Bay. Environ~netrics 13:499-511.
RosE, K. A. 2000. W h y are quantitative relationships between
envfl-onmental quality a n d fish p o p u l a t i o n s so elusive? Ecolog:
ical Applications 10:367-385.
SALA, O. E., E S. CHAPIN, I I I , j . j . Am~ESTO, E. BF~LOW, J. BLOOMrw.tn, R. D m z o , E. HtmFa~-SANWm_D, L. F. HtrWrNF~, R. B.

295

JACI(SON,A, KINZIG,R. LEEMANS, D. M. LODGE, H. A. MOONEY,

M. OESTEm~ELD, N. L. POW, M. T. S~ES, B. H. WALKEr, M.
WALKER, AND D. H. WALL. 2000. Global biodiversity scenarios
for the year 2100. Science 287:1770-1774.
SA8 INSTITUTE. 2002. SAS/STAT User's Guide, version 8. 8AS
Institute, Cary, N o r t h Carolina.
SmwmI~, 22 C. 1997. Envfl-onmental m o d e l i n g a n d e x p o s u r e ass e s s m e n t o f sediment-associated f l u o r a n t h e n e in a small, urbanized, non-riverine estuary. J~,~rnal of Experimental Marine

Biolog/ and Ecolog/ 213: 71-94.

SMITH, A. K., P. A. AJA~, AND D. E. ROBERTS. 1999. Spatial a n d
t e m p o r a l variation in fish a s s e m b l a g e s e x p o s e d to sewage a n d
implications for m a n a g e m e n t . MariNe Env#onmental Research
47:241-260.
STROBEL, C. J., H. W. Btncp_r~, S. J. B ~ ,
AND J. F. PATS. 1999.
E n v i r o n m e n t a l M o n i t o r i n g a n d A s s e s s m e n t Program: C u r r e n t
stares of Virginian Province (U.S.) estuaries. Env#onmental
Monitoring and Assessment 56:1-25.
STROBEL, C. J., J. F. PAUL, M. M. HUGHES, H. W. BI_rFFuM, B. S.
BROWN, AND J. K. SUMMERS. 2000. Using i n f o r m a t i o n on spatial variability of small estuaries in designing large geograptfic
scale estuarine m o n i t o r i n g p r o g r a m s . Environmental Monito~
ing and Assess~wnt 63:225-236.
U.S. ENVmONMFSrrAL I~OTECnON AOFX,TCu (U.S. EPA). 2002. Research Strategy. E n v i r o n m e n t a l M o n i t o r i n g a n d A s s e s s m e n t
Program. E P A / 6 2 0 / R - 0 2 / 0 0 2 . Office of Research a n d Develo p m e n t , U.S. E n v i r o n m e n t a l Protection Agency, Research Triangle Park, N o r t h Carolina.
VALIELA, I., K. FOREMAN, M. LAMoNTAONE, D. HF,RSH, J. COSTA,
R PECXOL, B. DEMEo-ANDRESON, C. D'AvANZO, M. BABION~,
C.-H. SHAM, J. BRAWLEY,AND K. LAJTII& 1992. C o u p l i n g s of
watersheds a n d coastal waters: Sources a n d c o n s e q u e n c e s of
n u t r i e n t e n r i c h m e n t in Waquoit Bay, Massachusetts. Estuaries
15:443-457.
VAN D o t a H , R. F.,J. L. H,mAsm, A. E H o L t ~ m , J . S. RosFa~, AZ~
T. R. SNOOTS. 1999. A b e n t h i c i n d e x of biological integrity for
assessing h a b i t a t quality in estuaries of the s o u t h e a s t e r n USA.
Marine Environmental Research 48:269-283.
WAHL, M. H., H. N. M c g v . t t . ~ , AND 22 M. W n . H ~ S . 1997. Patterns of n u t r i e n t loading in forested a n d u r b a n i z e d coastal
streams. Journal of Experimental Marine Biology and Ecology 213:
111-181.
WEISBERG, S. B., J. A. RANASINGHE, D. M. DAUEr, L. SCH3~FNER,
R. J. DIAZ. 1997. An estum-ine b e n t h i c i n d e x o f biotic
integrity. Estuaries 20:149-158.
SOURCES OF U N P U B L I S H E D MATERIALS
ENVIRONMENTAL MONITORING AND ASSESSMENT PROGRAM
(EMAP). U n p u M i s h e d Data. EMAP web site, 2002. U.S. Env i r o n m e n t a l Protection Agency. h t t p : / / w w w . e p a . g o v / e m a p
NATIONAL LANI) COVER DATA (NLCD). U n p u b l i s h e d Data. Multi-Resolution L a n d Characteristics C o n s o r t i u m web site, 2002.
http ://www. epa. g o v / m r l c / n l c d . h m a l
U.S. GEOLOGICAL StmwY (USCS). U n p u b l i s h e d Data. 2002 National H y d r o g r a p h y Dataset. h t t p : / / n h d . u s g s . g o v
U.S. GEOLOGIC,~L StmwY (USGS). U n p u b l i s h e d Data. 2002 National Elevation Dataset. htr

Received, Marc/z 6, 2003

Revised, Septewber & 2003
Accepted, October 13, 2003