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Estuaries Vol. 20, No. 1, p.

149-158 March 1997

An Estuarine Benthic Index of


Biotic Integrity (B-IBI) for
Chesapeake Bay
STEI'HEN B. WEISBERG L9 LINDA C . SCHAFFNER
j. A N A N D A RANASINGIIE ROBERT J. DIAZ
Versar, Inc. School of Marine Science
9200 Rumsey Road The College of William and Mary
Columbia, Maryland 21045 Gloucester Point, Virginia 23062

DANIEL M. DAUER JE~'FREY B. FRITHSEN


Department of Biological Sciences Versar, Inc.
Old Dominion University 9200 Rum~wy Road
Norfolk, Virginia 23529 Columbia, Maryland 21045
ABSTRACT: A multimetric b e n t h i c i n d e x o f biotic integrity (B-IBI) was d e v e l o p e d u s i n g data f r o m five C h e s a p e a k e
Bay s a m p l i n g p r o g r a m s c o n d u c t e d b e t w e e n 1972 a n d 1991. Attributes o f the i n d e x were selected by c o m p a r i n g the
r e s p o n s e o f 17 candidate m e a s u r e s o f benthic condition (metrics) between a set o f minimally a f f e c t e d reference sites
a n d at all o t h e r sites f o r w h i c h d a t a were available. This p r o c e d u r e was c o n d u c t e d independently for each o f s e v e n
habitats d e f i n e d by salinity a n d substrate. Fifteen o f the 17 candidate metrics d i f f e r e d significantly b e t w e e n r e f e r e n c e
sites a n d o t h e r sites for at least o n e habitat. N o meeric d i f f e r e d significantly in all s e v e n habitats; however, f o u r metrics,
species diversity, a b u n d a n c e , biomass, a n d p e r c e n t o f a b u n d a n c e as pollution-indicative taxa, d i f f e r e d in six habitats.
T h e i n d e x was calculated by scoring each selected metric as 5, 3, or 1 d e p e n d i n g on w h e t h e r its value at a site approx-
imated, deviated slightly f r o m , or deviated greatly f r o m conditions at the best r e f e r e n c e sites. Validation b a s e d on
independent data collected b e t w e e n 1992 a n d 1994 indicated that the i n d e x correctly distinguished slxessed sites f r o m
r e f e r e n c e sites 93% o f the time, with the highest validation rates o c c u r r i n g in high salinity habitats.

Introduction cause, unlike most pelagic fauna, benthic assem-


blages r e f l e c t local e n v i r o n m e n t a l c o n d i t i o n s
Benthic invertebrates are used extensively as in-
(Gray 1979). T h e structure o f benthic assemblages
dicators o f estuarine e n v i r o n m e n t a l status and
responds to many kinds o f stress because these as-
trends because n u m e r o u s studies have demonstrat-
sentblages typically include organisms with a wide
ed that b e n t h o s respond predictably to many kinds
of natural and a n t h r o p o g e n i c stress (Pearson and range of physiological tolerances, feeding modes,
Rosenberg 1978; Dauer 1993; T a p p e t al. 1993; Wil- and trophic interactions (Pearson and Rosenberg
son and Jeffrey 1994). Many characteristics of ben- 1978; Rhoads et al. 1978; Boesch and Rosenberg
thic assemblages make them useful indicators (Bil- 1981).
yard 1987), the most i m p o r t a n t o f which are relat- Although descriptions of benthic assemblages
ed to their exposure to stress and the diversity of have been useful for characterizing environmental
their response. Exposure to hypoxia is typically conditions and gradients at local scales, benthic as-
greatest in near-bottom waters and a n t h r o p o g e n i c semblages have not yet b e e n used to their full po-
c o n t a m i n a n t s o f t e n a c c u m u l a t e in s e d i m e n t s tential as indicators in regional-scale studies o r
where b e n t h o s live. Benthic organisms generally studies o f entire estuaries because the structure of
have limited mobility and c a n n o t avoid these ad- benthic assemblages also reflects natural variation
verse conditions (Wass 1967). This immobility is related to salinity, sediment type, latitude, and
advantageous in e n v i r o m n e n t a l assessments be- d e p t h (Boesch 1973, 1977; Dauer et al. 1984, 1987;
Holland et al. 1987; Schaffner et al. 1987; Snel-
grove and Butman 1994: H e i p and Craeymeersch
C o r r e s p o n d i n g author. 1995). Benthic assemblages rarely are used to as-
-~Present address: S o u t h e r n California Coastal Water Re- sess ecological condition across habitats because of
search Program, 7171 Fenwick Lane, Westminster, California
92683; tele 714/894-2222; fax 714/894-9699; e-mail stevew@ the difficulty in separating variation in the condi-
sccwrp.org. tion o f the assemblage caused by habitat differ-

9 1997 Estuarine Research Federation 149


"150 S.B. Weisb0rg et al.

TABLE t_ Data sources used in developing the Chesapeake Bay B-IBI.


Number of
Sampling Gear and Summer
Data .'-;oulce Time Period Sampling Krea (rod Samples References

Chesapeake Bay Benthic 1984-1994 Petite Ponar (0.025) 1,814 Ranasingheet al.
Monitoring Program, Maryland Van Veen (0.1) (1994a)
Box Corer (0.022)
Chesapeake Bay Benthic Monitoring
Program, Virginia 1985-1994 Box Corer (0.0184) 180 Dauerand Alden (1995)
EPA's Environmental Monitoring and
Assessment Program (EMAP) 1990-1993 Van Veen (0.044) 293 Paul et al. (1992)
James River Study 1971-1972 Ponar (0.05) 28 Diaz (1989)
Wolf Trap 1987-1991 Box Corer (0.063) 4 Schaffner(unpublished data)

ences trom variation caused by natural and anthro- ties: selecting measures of benthic macroinverte-
pogenic stresses. In site-specific assessments o f ben- brate assemblages (referred to by Karr as metrics)
thic assemblages, the p r o b l e m o f a c c o u n t i n g for that differ between references and d e g r a d e d areas;
habitat-induced variation is minimized by using identifying quantitative thresholds that differenti-
nearby reference sites from the same kind o f hab- ate between d e g r a d e d and reference areas for each
itat. Benthic assessments also are used frequently selected metric; c o m b i n i n g metric scores to devel-
in studies of trends, where the p r o b l e m of habitat- op an index that identifies the condition o f the
i n d u c e d variation can be minimized by r e t u r n i n g assemblage at a site; a n d validating the index with
to the same site or area, an i n d e p e n d e n t dataset,
O n e a p p r o a c h used to integrate biotic responses Attributes o f the index were selected by com-
and a c c o u n t for natural habitat variations in the paring response o f the benthic assemblage be-
freshwater e n v i r o n m e n t is to define habitat-specific tween minimally affected reference sites and all
reference conditions (Karr 1991; Kerans a n d Karr o t h e r sites in o u r database. Reference sites were
1994; D e S h o n 1995). This a p p r o a c h defines ex- selected from o u r dataset by first eliminating sites
pected conditions at sites free o f a n t h r o p o g e n i c within highly developed watersheds and locations
stress, and then assigns categorical values for vari- near known point-source discharges. The remain-
ous descriptive metrics by c o m p a r i s o n with obser- ing sites were e x a m i n e d to identify those where no
vations at reference sites. T h e result is a multi-met- c o n t a m i n a n t e x c e e d e d L o n g et al.'s (1995) effects
ric index o f biotic condition, frequently referred range-median (ER-M) c o n c e n t r a t i o n , total organic
to as an index o f biotic integrity (IBI). We bor- c o n t e n t of the sediment was less than 2%, and dis-
rowed from that a p p r o a c h to develop a benthic solved oxygen c o n c e n t r a t i o n was consistently high.
index of biotic integrity (B-IBI) for use with sum- Dissolved oxygen c o n c e n t r a t i o n was considered to
m e r estuarine benthic c o m m u n i t i e s o f Chesapeake be consistently high if the site had no r e c o r d e d
Bay. m e a s u r e m e n t below 2 ppm, 90% o f the observa-
Methods tions were above 3 ppm, and at least 80% o f the
m e a s u r e m e n t s were above 5 ppm. Sites for which
Macrobenthic infaunal data from five Chesa-
less than five i n d e p e n d e n t oxygen m e a s u r e m e n t s
peake Bay sampling programs, each o f which used
were available were selected as reference sites only
a 0.5-mm sieve a n d identified organisms to the low-
if they were in a region classified by the Chesa-
est possible t a x o n o m i c level, were used to develop
peake Bay P r o g r a m as being free of" dissolved ox-
the B-IBI (Table 1). T a x o n o m i c inconsistencies
a m o n g p r o g r a m s were eliminated by cross-corre- ygen stress (Magnien et al. 1995). O n e of the sam-
lating the species lists, identifying differences in pling p r o g r a m s (EMAP) included a 10-d, acute
n o m e n c l a t u r e , and consulting the taxonomist for sediment bioassay using the a m p h i p o d Ampelisca
each p r o g r a m to resolve discrepancies. Data col- abdita for each site. Bioassay survival also had to
lected before 1992 were used to calibrate the in- exceed 80% o f control survival for sites sampled
dex; data collected between 1992 a n d 1994 were by this p r o g r a m to be selected as reference sites.
used to validate the index. If a sile was sampled Two criteria were used to c o m p a r e metric values
m o r e than once d u r i n g a summer, which we de- between reference sites and o t h e r sites in the cal-
fined as July 15 t h r o u g h S e p t e m b e r 30, only the ibration dataset. First, a M a n n - W h i m e y U-test was
first sample was used in the calibration dataset. used to test for differences in mean. Second, dis-
O u r analytical a p p r o a c h was similar to the o n e tributions were c o m p a r e d using a Kolmogorov-
Karr et al. (1986) used to develop c o m p a r a b l e in- Smirnov test. T h e latter criterion was particularly
dices for freshwater fish a n d involved four activi- i m p o r t a n t for the a b u n d a n c e a n d biomass metrics
Benthic Index for ChesapeakeBay 151

TABLE 2. Mean values by habitat for each candidate metric at reference sites (top number) and at all other sites (bottom number).
Shading in the Table: Top number boldface indicates pair is different by Mann-Whitney test; bottom number boldface indicates
different by Kolmogorov-Smirnov test. N/A = data unavailable for that habitat.
High High
Tidal Low Mesohaline Mesohaline Polyhaline Potvhaline
Freshwater Oligohaline Mesohalinc Sand Mud Sand Mud

Species l)iversity
Shannon-Weiner 1.89 2.49 2.41 3.35 2.84 4.06 3.55
1.90 1.84 1.84 2.44 1.66 2.88 1.10
Productivity
Abundance (# m ~) 3,849 2,052 1,954 2,765 1,319 4,122 2,770
6,713 3,163 2,669 3,541 1,681 2,878 2,140
Biomass (g dry) (wt m -2) 10.7 26.5 9.6 19.9 8.4 29.9 8.1
21.9 28.9 18.7 5.8 2.9 10.0 0.9
Species composition
9 Percent of biom~ss as 24.5 0.8 0.9 2.8 9 2.3 5.9
pollution-indicative taxa N/A 1 8.4 N/A 55.4 6.3 24.8
Percent of abundance 29.4 22.4 2.4 11.6 26.5 12.1 22.9
pollution-indicative taxa 45.9 27.8 19.1 19.3 48.7 32.4 58.9
Percent of biomass as 18 89.1 83 78.9 65.3 71.2 63.2
pollution-sensitive taxa N/A 66.9 26.9 N/A 20. l 66.1 40.4
Percent of abundance 12.8 44.8 30.6 40.3 29.5 48.5 39.9
as pollution-sensitive taxa 4.7 28.3 25.7 20.8 10.3 29.3 8.4
Trophic composition
Percent of abundance 15.1 11.8 22.9 37.4 23.1 35.3 41.8
as carnivores or omnivores 10.1 15 18.3 23.8 15.6 32.8 19,9
Percent of abundance 66.6 37.8 23.8 24.3 21.4 25.1 21.4
as deep deposit feeders 69.6 35.1 21.8 21.3 18 12.4 9.4
Percent of abundance 6.5 16.7 1.2 7.0 4.8 10.6 3.1
as suspension feeders 11.3 13.6 8.3 15.4 6.4 9.0 4.9
Percent of abundance 10.4 33.7 52.1 31.4 50.8 29.0 33.7
as interface feeders 8.4 35.2 48.1 39.4 46.7 35.3 39.1
Depth distribution below sediment-water interface
Percent of taxa 31.4 20.0 37.6 26.8 35.1 47.6 35.5
deeper than 5 cm N/A 4.2 18.1 N/A 19.9 47.1 15.2
Percent of taxa 8.7 6.7 20.0 8.2 10.7 22.0 9.3
deeper than 10 cm N/A 0 6.9 N/A 3.3 30.1 6.1
Percent of abundance 11.1 8.6 27.7 11.7 21.4 34.9 16.6
deeper than 5 cm N/A 0.7 8.9 N/A 5.2 32 7
Percent of abundance 1.9 1.5 8.(1 2.4 5.6 16.6 4.2
deeper than 10 cm N/A 0 1.1 N/A 0.8 16.3 2.4
Percent of biomass 14.1 10.0 68.8 63.6 61.6 58.3 42
deeper than 5 cm N/A 3 17 N/A 11.5 68.5 17.4
Percent of bioma~s 3.3 1.7 48.3 31.6 29.9 28.5 24.9
deeper than 10 cm N/A 0 3 N/A 1 33.8 10.6

b e c a u s e t h e a n t i c i p a t e d r e s p o n s e a t d e g r a d e d sites b u t less s e n s i t i v e to s m a l l c h a n g e s i n h a b i t a t , s u c h
c o u l d b e h i g h e r o r l o w e r t h a n a t r e f e r e n c e sites, as s a l i n i t y a n d s u b s t r a t e t y p e ( W a r w i c k 19881.
d e p e n d i n g o n t h e s e v e r i t y o f t h e stress. Species were classitied into feeding guilds using
9W e t e s t e d 17 c a n d i d a t e m e t r i c s r e p r e s e n t i n g literature descriptions of feeding behavior (Jorgen-
m e a s u r e s o f s p e c i e s diversity, p r o d u c t i v i t y , s p e c i e s s e n 1966; B o u s f i e l d 1973; F a u c h a l d a n d J u m a r s
composition, depth distribution, and trophic com- 1979; D a u e r e t al. 1 9 8 1 ) ; a c o m p l e t e list o f t a x a
p o s i t i o n ( T a b l e 2). T o e n s u r e t h a t t h e i n t l e x w o u l d i n c l u d e d in e a c h g u i l d is a v a i l a b l e in R a n a s i n g h e
b e a p p l i c a b l e to a w i d e a r r a y o f d a t a s e t s , w e at- e t al. ( 1 9 9 4 b ) . I,ists o f p o l l u t i o n - i n d i c a t i v e ( T a b l e
t e m p t e d to i d e n t i f y m e t r i c s t h a t h a v e b e e n s h o w n 3) a n d p o l l u t i o n - s e n s i t i v e ( T a b l e 4) t a x a w e r e d e -
t o b e l e a s t s e n s i t i v e to c o l l e c t i o n g e a r ( E w i n g e t al. v e l o p e d u s i n g a t w o - s t e p p r o c e d u r e . First, c a n d i -
1988). Metrics based upon individual species were date taxa were identified based on known oppor-
a v o i d e d in f a v o r o f a s s e m b l a g e m e a s u r e s , w h i c h tunistic or equilibrium life-history characteristics
c a n b e e q u a l l y s e n s i t i v e to t h e e f f e c t s o f p o l l u t i o n ( B o e s c h 1973; G r a s s l e a n d G r a s s l e 1974; M c C a l l
152 S.B. Weisberg et al.

TABLE 3. Taxa defined as pollution-indicative in the Chesa- TAB1.E 4. Taxa defined as pollution-sensitive in the Chesa-
peake Bay B-IBI. peake Bay B-IBI.

Annelida : Polychaeta Annelida : Oligochaeta Coelenterata : Anthozoa Mollusca : Bivalvia


AsabeUides oculata Aulodrilus limnobius Ceriantheopsis americanu5 Anadara ovalis
Capitella spp. A ulod~ilus paucichae/a Anadara transversa
Hypereteone heteropoda A ulodrilus pigueti Annelida : Polychaeta Cyrtopleura costata
Leitoscoloplo~ fragTlis Aulodrilus pluriseta Asychis elongata Dosinia discus
Paraprionospio pinnata Bothrioneurum vqdovskyanum Bhawania heteroseta Ensis directus
Streblospio benedicti FIaber cf. speciosu,~ Chaetopterus variepedatus Macoma balthica
,M'thropoda : ]nsecta L~ochaetides curvosetosus Clymenella toruata Mercenarza mercenaria
Isochaetides ]reyi Diopatra cuprea Mya arenaria
Chironomus spp. Limnodrilus hoffmeiste,q Glycera americana Rangia cuneata
Cladotanytarsu.~ spp. Potamothrix vejdovskvi Glycinde solitalia Spisula solidissima
Coelotanypus spp. Quistadvilus multisetosus l,oimia medusa Tagelus divisus
Glyptotendipes spp. Tubificid immatures without Mao'oclymer~ zonalis "lhgelus plebeius
Polypedilum tripodura capilliform chaetae Marenzelleria virdis Tellina agilis
Prockulius sublettei Mediomastus ambiseta
Tanypus spp. Mollusca : Bivalvia Echinodermata : Ophiuroidea
Nephtys picta
Mulinia klteralis Spiochaetopterus costarum Microphiopholis atra
Nucula proxima Spiophanes bombyx
Arthropoda
Alpheus heterochaelis
1977; R h o a d s et al. 1978; G r a y 1979; R h o a d s a n d
Biffarius bifo,mis
B o y e r 1982; W a r w i c k 1986; D a u e r 1993). S e c o n d , Callianassa setimanus
t h e list was v e r i f i e d a n d a m e n d e d by c o m p a r i n g Cyathura polita
t h e a b u n d a n c e o f e a c h t a x a at t h e r e f e r e n c e sites Listriella clymenellae
with a b u n d a n c e at sites f r o m t h e c a l i b r a t i o n d a t a - SquiUa empusa
set t h a t h a d k n o w n p o l l u t i o n stress. Sites in t h e
c a l i b r a t i o n d a t a s e t w e r e c o n s i d e r e d to b e p o l l u -
t i o n - s t r e s s e d if a n y s e d i m e n t c o n t a m i n a n t e x c e e d - 5 0 t h p e r c e n t i l e s w e r e s c o r e d as 3, a n d v a l u e s a b o v e
e d t h e L o n g et al. (1995) ER-M c o n c e n t r a t i o n a n d t h e 5 0 t h p e r c e n t i l e w e r e s c o r e d a s 5. M e t r i c s c o r e s
survival in s e d i m e n t t o x i c i t y tests was less t h a n 8 0 % w e r e c o m b i n e d i n t o an i n d e x by c o m p u t i n g t h e
of control (where toxicity data were available), or m e a n s c o r e a c r o s s all m e t r i c s f o r w h i c h t h r e s h o l d s
t o t a l o r g a n i c c a r b o n in t h e s e d i m e n t e x c e e d e d 3%, were developed. Assemblages with an average
o r d i s s o l v e d o x y g e n c o n t e n t was low. A site was c o n - s c o r e less t h a n t h r e e a r e c o n s i d e r e d s t r e s s e d , as
s i d e r e d to h a v e low d i s s o l v e d o x y g e n if t h e m e a - t h e y have m e t r i c values t h a t o n a v e r a g e a r e less
s u r e d c o n c e n t r a t i o n was b e l o w 0.5 p p m o n a n y oc- t h a n v a l u e s at t h e p o o r e s t r e f e r e n c e sites.
c a s i o n , o r b e l o w 2 p p m o n at l e a s t t h r e e d i f f e r e n t Two o f t h e m e t r i c s , a b u n d a n c e a n d b i o m a s s , re-
d a t e s w i t h i n a year. s p o n d b i m o d a l l y ; t h a t is, t h e r e s p o n s e c a n b e g r e a t -
M e t r i c s w e r e s e l e c t e d s e p a r a t e l y f o r e a c h o f sev- e r t h a n at r e f e r e n c e sites with m o d e r a t e d e g r e e s
e n h a b i t a t s ( T a b l e 5). T h e seven h a b i t a t s t r a t a w e r e o f stress a n d less t h a n a t r e f e r e n c e sites with h i g h e r
e s t a b l i s h e d by c l u s t e r analysis ( B r a y - C u r t i s similar- d e g r e e s o f stress ( P e a r s o n a n d R o s e n b e r g 1978;
ity c o e f f i c i e n t ; t l e x i b l e s o r t i n g ; 13 = - 0 . 2 5 ) o f t h e D a u e r a n d C o n n e r 1980; F e r r a r o e t al. 1991). F o r
c a l i b r a t i o n d a t a s e t to i d e n t i f y d o m i n a n t assem- t h e s e m e t r i c s , t h e s c o r i n g was m o d i f i e d so t h a t
b l a g e s in C h e s a p e a k e Bay, a n d by analysis o f vari- both exceptionally high (those exceeding the 95th
a n c e to d e t e r m i n e w h e t h e r salinity, g r a i n size, p e r c e n t i l e at r e f e r e n c e sites) a n d low ( < 5 t h per-
depth, and latitude differed significandy among c e n t i l e ) r e s p o n s e s w e r e s c o r e d as a 1. V a l u e s be-
g r o u p s o f sites d e f i n e d by t h e d i f f e r e n t assem- t w e e n t h e 5 t h a n d 25th p e r c e n t i l e s o r b e t w e e n t h e
b l a g e s ( R a n a s i n g h e et al. in p r e p a r a t i o n ) .
Thresholds for the selected metrics wcrc based TABI,E 5. Habitat definitions used in the Chesapeake Bay
o n t h e d i s t r i b u t i o n o f v a l u e s f o r t h e m e t r i c at t h e B-IBI (N/A = not applicable).
r e f e r e n c e sites. T h e IBI a p p r o a c h involves s c o r i n g Bottom Silt-clay
e a c h m e t r i c as 5, 3, o r 1, d e p e n d i n g o n w h e t h e r Salinity (<63 p.) Content
Habitat (%,c) by Weigh! (%)
its v a l u e at a site a p p r o x i m a t e s , d e v i a t e s slightly, o r
d e v i a t e s g r e a t l y f r o m c o n d i t i o n s at r e f e r e n c e sites Tidal freshwater 0-0.5 N/A
Oligohalirte >-0.'5-5 N/A
( K a r r et ai. 1986). T h r e s h o l d v a l u e s w e r e estab- I.ow Mesohaline ----5-12 N/A
l i s h e d as a p p r o x i m a t e l y t h e 5 t h a n d 5 0 t h ( m e d i a n ) High Mesohaline sand >-12-18 0-40
p e r c e n t i l e v a l u e s l o t r e f e r e n c e sites in e a c h h a b i - High Mesohaline mud >-12-18 >40
tat. F o r e a c h m e t r i c , v a l u e s b e l o w t h e 5th p e r c e n - Polyhaline sand -> 18 0~,0
Polyhaline mud >-18 >40
tile w e r e s c o r e d as 1; v a l u e s b e t w e e n t h e 5th a n d
Benthic Indexfor ChesapeakeBay 153

75th a n d 95th percentiles were scored as 3, a n d assemblage. For instance, we selected either abun-
values between the 25th a n d 75th percentiles of dance-based or biomass-based metrics o f species
the values at r e f e r e n c e sites were scored as 5. composition, b u t n o t both. We also limited the in-
T h e i n d e x was validated by e x a m i n i n g its re- dex to a single depth-distribution metric, a n d sin-
sponse at a new set o f r e f e r e n c e sites a n d a new gle trophic c o m p o s i t i o n metric, within each habi-
set o f sites with known e n v i r o n m e n t a l stress. Data tat.
used for validation were collected between 1992 T h e B-IBI classified 93% of the validation sites
a n d 1994 a n d were i n d e p e n d e n t o f data used to correctly (Table 7). T h e lowest classification effi-
calibrate the index. Criteria for defining r e f e r e n c e ciency by habitat was 50% in high m e s o h a l i n e
sites a n d known stressed sites f r o m the validation sand, but this was based on only two samples. Clas-
dataset were the same as those described for the sification efficiency was generally p o o r e r in low sa-
calibration dataset. linities. Cumulative classification efficiency for hab-
T h e index was f u r t h e r validated by e x a m i n i n g itats with salinity less than 18%o was 84%, whereas
the consistency of the i n d e x response at sites that classification efficiency was 97% for salinities above
were s a m p l e d m o r e than o n c e d u r i n g a summer. 18%o (Table 7).
This test, suggested by Stewart a n d L o a r (1994) as T h e i n d e x was stable within the s u m m e r i n d e x
a prerequisite for biological indices, e x a m i n e s in- period, with an overall correlation o f 0.97 between
dex stability assuming that the quality o f the site the first a n d second s a m p l i n g visits to a site. T h e
should n o t c h a n g e appreciably d u r i n g the index correlation between the first a n d second sampling
period. visits was g r e a t e r than 0.9 in all habitats, a n d for
six habitats the correlation e x c e e d e d 0.95 (Table
Results 8). In all habitats except the oligohaline a n d me-
O n e h u n d r e d f o u r t e e n sites f r o m the Chesa- sohaline sand, m o r e than 80% o f the sites s a m p l e d
p e a k e Bay database m e t o u r criteria as r e f e r e n c e twice d u r i n g the same s u m m e r classified the same
sites for d e v e l o p i n g the B-IBI. At least 10 r e f e r e n c e (Table 8). Most o f the sites that classified differ-
sites were identified f r o m each habitat e x c e p t the ently between the two visits were sites for which
oligohaline habitat, for which only seven r e f e r e n c e index values were similar for b o t h visits but were
sites were available. Biomass a n d d e p t h metrics close to, a n d on either side of, the threshold value
could n o t be evaluated in the tidal freshwater a n d o f 3.
high m e s o h a l i n e sand habitats, t h o u g h , because
n o t all s a m p l i n g p r o g r a m s p a r t i t i o n e d samples by Discussion
d e p t h within the s e d i m e n t or m e a s u r e d biomass D e v e l o p m e n t o f the B-IBI was based u p o n quan-
individually by t a x o n o m i c groups. tifying established principles of benthic ecology,
Fifteen of the 17 candidate metrics differed sig- n o t on d e v e l o p i n g new ones. T h e principles were
nificantly in m e a n or in distribution between ref- based largely on the p a r a d i g m o f Pearson a n d Ro-
e r e n c e sites a n d all o t h e r sites in the calibration s e n b e r g (1978), which holds that b e n t h i c assem-
dataset for at least o n e habitat (Table 2). No metric blages r e s p o n d to i m p r o v e m e n t s in habitat quality
differed significantly in all seven habitats; however, in three progressive stages: the a b u n d a n c e o f or-
f o u r metrics, species diversity, a b u n d a n c e , biomass ganisms increases; species diversity increases as
a n d p e r c e n t o f a b u n d a n c e as pollution-indicative new taxa are able to survive at the site; a n d the
taxa, differed in six habitats. T h e n u m b e r of met- d o m i n a n t species at the site c h a n g e f r o m pollu-
rics that differed significantly between r e f e r e n c e tion-tolerant to pollution-sensitive species. In o u r
sites a n d all o t h e r sites was considerably g r e a t e r in work, this p a r a d i g m was s u p p l e m e n t e d with as-
high salinity t h a n in low salinity (Table 2). Four- s u m p t i o n s that the a b u n d a n c e a n d diversity o f spe-
teen o f the 17 metrics differed significantly at ref- cies o c c u r r i n g d e e p e r in the s e d i m e n t should be
e r e n c e sites in polyhaline m u d c o m p a r e d with only g r e a t e r at r e f e r e n c e sites than at d e g r a d e d sites
t h r e e in tidal freshwater, a n d o n e in the oligoha- (Warwick 1986; Schaffner 1990; D a u e r 1993) a n d
line habitat. that the distribution o f b e n t h o s a m o n g feeding
Table 6 lists the selected metrics a n d their guilds should be m o r e diverse at r e f e r e n c e sites
thresholds. We i n c o r p o r a t e d each metric that dif- (Word 1978).
fered significantly in six habitats into the index for Each of these principles was successful at distin-
all habitats because in each case the direction o f guishing r e f e r e n c e sites f r o m d e g r a d e d sites within
the r e s p o n s e was the same in the seventh habitat at least s o m e habitats o f C h e s a p e a k e Bay (Table 2).
a n d in m o s t cases the difference was significant at W h e n applied individually to the validation data-
a marginally lower a l p h a level. We also limited the set, however, n o n e o f the metrics derived f r o m
n u m b e r of r e d u n d a n t metrics within a habitat to these principles were as effective at distinguishing
avoid over-weighting individual p r o p e r t i e s o f the between r e f e r e n c e sites a n d d e g r a d e d sites as the
154 S.B. Weisberg et al.

TABLE 6. T l u e s h o l d s u s e d to score each metric o f the C h e s a p e a k e Bay B-IBI.

Scoring Criteria
5 3 1
Tidal Freshwater
Shannon-Weiner -> 1.8 1.0-1.8 <1.0
A b u n d a n c e (# m-'-') ->1,000-4,000 500-1,000 or ->4,000-10,000 < 5 0 0 or ->10,000
Biomass ( g m -z) ->0.5-3 0.25-0.5 or ->3-50 <0.25 or ->50
A b u n d a n c e o f pollution-indicative taxa (%) -<25 25-75 >75
Oligohaline
Shannon-Weiner ->2.5 1.9-2.5 < 1.9
A b u n d a n c e (# m -2) ->1,500-3,000 500-1,500 or ->3,000-8,000 < 5 0 0 or ->8,000
Biomass (g m z) ->3-25 0.5-3 or ->25-60 <0.5 or ->60
A b u n d a n c e o f pollution-indicative taxa (%) -<25 25-75 >75
A b u n d a n c e o f pollution-sensitive taxa (%) ->40 10-40 <10
Low Mesohaline
Shannon-Weiner ->2.5 1.7-2.5 <1.7
A b u n d a n c e (# m -z) ->1,500-2,500 500-1,500 or ->2,500-6,000 < 5 0 0 or ->6,000
Biomass (g m -2) -> :>---10 1-5 or ->10-30 <1 or ->30
A b u n d a n c e o f pollution-indicative taxa (%) -<10 10-20 >20
Bioma.s.s o f pollution-sensitive taxa (%) ->80 40--80 <40
Biomass > 5 cm below sediment-water interface (%) ->80 10-80 <10
High Mesohaline sand
Shannon-Weiner ->3.2 2.5-3.2 <2.5
A b u n d a n c e (# m-o-) -> 1,500-3,000 1,000-1,500 or ->3,000-5,000 <1,000 or ->5,000
Biomass (g m -2) ->3-15 1-3 or ->15-50 <1 or ->50
A b u n d a n c e o f pollution-indicative taxa (%) -<10 10-25 >25
A b u n d a n c e o f pollution-sensitive taxa (%) ->40 10--40 <10
A b u n d a n c e o f carnivores a n d o m n i v o r e s (%) ->35 20-35 <20
High Mesohaline m u d
Shamlon-Weiner ->3.0 2.0-3.0 <2.0
A b u n d a n c e (# m -2) ->1,500-2,500 1,000-1,500 or ->2,500-5,000 <1,000 or ->5,000
Biomass ->2-10 0.5-2 or ->10-50 <1,000 or ->5,000
Biomass o f pollution-indicative taxa (%) -<5 5-30 > 30
Biomass o f pollution-sensitive taxa (%) ->60 30-60 <30
A b u n d a n c e o f carnivores a n d o m n i v o r e s (%) -<25 10-25 <10
Biomass > 5 c m below sediment-water interface (%) ->60 10-60 <10
Polyhaline s a n d
Shannon-Weiner ->3-5 2.7-3.5 <2.7
A b u n d a n c e (# m -z) ->3,000-5,000 1,500-3,000 or ->5,000-8,000 <1,500 or ->8,000
Biomass (g m -~ ->5-20 1-5 or ->20-50 <1 or ->50
Biomass o f pollution-indicative taxa (%) -<5 5-15 >15
A b u n d a n c e o f pollution-sensitive taxa (%) ->50 25-50 <25
A b u n d a n c e o f deep-deposit feeders (%) >25 10-25 <10
Polyhaline m u d
Shannon-Weiner ->3.3 2.4-3.3 <2.4
A b u n d a n c e (# m -2) ->1,500-3,000 1,000-1,500 or ->3,000-8,000 <1,000 or ->8,000
Biomass (g m -2) ->3-10 0.5-3 or ->10-30 <0.5 or ->30
Biomass o f pollution-indicative taxa (%) -<5 5-20 >20
Biomass o f pollution-sensitive taxa (%) ->60 30-60 <30
A b u n d a n c e of carnivores a n d o m n i v o r e s (%) ->40 25-40 <25
Taxa > 5 cm below sediment-water interface (%) ->40 10-40 <10

index that combines t h e m (Table 9). We attribute (Kerans and Karr 1994). Developing indices for es-
this to the staged response o f b e n t h o s to stress, in tuarine b e n t h o s is difficult because o f the lack o f
which different metrics display greater response information a b o u t the life history or pollution sen-
with different degrees o f p e r t u r b a t i o n (Pearson sitivity o f most species; such i n f o r m a t i o n is neces-
and Rosenberg 1978); this illustrates o n e o f the sary to develop metrics such as p e r c e n t o f individ-
strengths of a multimetric a p p r o a c h (Karr 1991). uals as pollution-indicative or pollution-sensitive
T h e use o f m u h i m e t r i c indices has been a d o p t e d taxa. Controlled e x p e r i m e n t a t i o n to assess the pol-
quite widely for fish but only recently for b e n t h o s lution tolerance o f individual taxa, which are nu-
Benthic Index for ChesapeakeBay 155

TABI,E 7. Classification efficiency of the B-IBI for sites t-ore TABI.E 8. Classification consistency for sites visited more than
the validation dataset. once during a year.
Number of Percent Correctly Number of
Habitat Class Validation Samples Classified Site-Year
Combinations Percent of
Tidal freshwater 22 86.4 with Multiple Sites with Correlation
Summer Unchanged Between RGI
Oligohaline 5 80.0 ttabitat Class Samples Status Values
Low Mesohaline 29 82.3
High Mesohaline sand 2 50.0 Tidal freshwater 19 84.2 0.98
High Mesohaline mud 50 96.0 Oligohaline 34 76.5 0.97
Polyhaline sand 11 100.0 Low Mesohaline 103 92.2 0.98
Polyhaline mud 52 100.0 High Mesohaline sand 74 66.3 0.95
lligh Mesohaline mud 61) 85.0 0.96
Polyhaline sand 2 100.0 1.00
Polyhaline mud 35 97.1 0.91
m e r o u s for fish, a r e v e r y l i m i t e d f o r b e n t h o s . T h e
p o l l u t i o n t o l e r a n c e o f b e n t h o s typically is c a t e g o -
rized based on their life-history characteristics b a s e d p r i m a r i l y o n s t u d i e s c o n d u c t e d in h i g h salin-
( D a u e r 1993), w h i c h in s o m e cases a r e a m b i g u o u s ity h a b i t a t s (e.g., P e a r s o n a n d R o s e n b e r g 1978)
o r i n c o n s i s t e n t with t h e i r r e s p o n s e to p o l l u t i o n a n d m a y n o t b e e n t i r e l y a p p l i c a b l e to tidal fresh-
(Seitz a n d S c h a f f n e r 1995). water benthic communities. The principles devel-
O n e e x a m p l e o f this c o n f l i c t is o u r c l a s s i f i c a t i o n o p e d fox" n o n t i d a l f i ' e s h w a t e r e n v i r o n m e n t s (Ker-
o f t h e c a p i t e l l i d p o l y c h a e t e Mediomastus ambiseta as a n s a n d K a r r 1994; L e n a t a n d B a r b o u r 1994) d i f f e r
a pollution-sensitive taxon. Most previous studies s u b s t a n t i a l l y f r o m t h o s e u s e d in e s t u a r i e s .
h a v e i d e n t i f i e d this w i d e s p r e a d s p e c i e s as o p p o r - O n e c o n s t r a i n t u p o n u s i n g t h e B-IBI is t h a t it
t u n i s t i c a n d c h a r a c t e r i s t i c o f p o l l u t i o n - s t r e s s e d sites i n c l u d e s s e v e r a l m e t r i c s t h a t w e r e n o t m e a s u r e d by
( G r a s s l e a n d G r a s s l e 1984; D a u e r 1993), O u r c o m - all b e n t h i c s a m p l i n g p r o g r a m s in C h e s a p e a k e Bay.
p a r i s o n o f its a b u n d a n c e a t r e f e r e n c e sites a n d an- M a n y h i s t o r i c C h e s a p e a k e Bay c o l l e c t i o n e f f o r t s
t h r o p o g e n i c a l l y s t r e s s e d sites s h o w e d t h e o p p o s i t e d i d n o t m e a s u r e b i o m a s s , a n d few o n g o i n g e f f o r t s
( T a b l e 10). W e c h o s e to rely o n t h e e m p i r i c a l d a t a p a r t i t i o n t h e s a m p l e s by d e p t h , as is r e q u i r e d f o r
f r o m C h e s a p e a k e Bay in d e v e l o p i n g o u r i n d e x , b u t m e t r i c s in t h e h i g h e r salinity strata. To m i n i m i z e
suggest that the classification of taxa into such the effect of missing biomass data, abundance-
g r o u p s is a f r u i t f u l a r e a f o r c o n s i s t e n t , c o n t r o l l e d based substitutes for the pollution-indicative and
experimentation. p o l l u t i o n - s e n s i t i v e c a t e g o r i e s a r e g i v e n ( T a b l e 11)
A l t h o u g h t h e p r i n c i p l e s o n w h i c h t h e B-IBI is b e c a u s e t h e s e m e t r i c s w e r e also s i g n i l i c a n t in all
b a s e d w e r e effective f o r d i s t i n g u i s h i n g b e t w e e n habitats where biomass-based metrics were selected
sites o f h i g h a n d l o w quality, t h e y d i d n o t a p p l y f o r i n c l u s i o n in t h e i n d e x . T o assess t h e effi~ct o f
e q u a l l y well in all h a b i t a t s . T h e n u m b e r o f m e t r i c s m i s s i n g d a m o n r e l i a b i l i t y o f t h e i n d e x , we r e p e a t -
t h a t d i f f e r e d s i g n i f i c a n t l y b e t w e e n sites o f h i g h a n d ed the validation step without using biomass data,
low q u a l i t y in t h e c a l i b r a t i o n d a t a s e t was c o n s i d - did the same without the depth-related dam, and
e r a b l y s m a l l e r in t h e t i d a l f r e s h w a t e r a n d o l i g o h a - a g a i n w i t h o u t e i t h e r o f t h e s e . O u r o v e r a l l classifi-
l i n e h a b i t a t , a n d i n d e x v a l i d a t i o n e f f i c i e n c y was c a t i o n e f f i c i e n c y w h e n b i o m a s s m e t r i c s w e r e re-
p r o g r e s s i v e l y w e a k e r at l o w e r salinities. F u r t h e r - m o v e d fell f r o m 9 3 % to 9 2 % . D r o p p i n g t h e d e p t h -
more, our validation for the tidal freshwater habi-
tat was n o t r i g o r o u s b e c a u s e o u r v a l i d a t i o n d a t a s e t TABI.E 9. Classification efficiency for each of the metrics used
d i d n o t i n c l u d e a n y d e g r a d e d sites, a n d t h e t h r e s h - in the B-IBI based on the validation data set. Metric testing was
o l d v a l u e s we i d e n t i f i e d f o r t i d a l f r e s h w a t e r w c r c limited to habitats for which thresholds were established.
low r e l a t i v e to t h o s e u s e d f o r t h e o t h e r h a b i t a t s . Pc-rcent of
We s u g g e s t c a u t i o n in u s i n g t h e t i d a l f r e s h w a t e r Sites
Correctly
c o m p o n e n t o f t h e B-IBI u n t i l f u r t h e r v a l i d a t i o n Classified
with a m o r e c o m p l e t e d a t a s e t c a n b e a c c o m - Shannon-Weiner diversity 89.5
plished. Abundance 82.5
T h e l o w e r v a l i d a t i o n e f f i c i e n c y f o r t h e i n d e x as Biomass 81.6
a whole and the smaller number of metrics that Percent of abundance as pollution-indicative taxa 72.1
Percent of biomass as pollution-indicative taxa 87.5
w o r k e d i n d i v i d u a l l y in low s a l i n i t i e s m a y b e d u e to Percent of abundance as pollution-sensitive taxa 90.2
t h e i n h e r e n t l y d i f f e r e n t f a u n a t h a t i n h a b i t t h e low Percent of biomass as pollution-sensitive taxa 82.4
salinity h a b i t a t s (i.e., d o m i n a t e d by o l i g o c h a e t e s Percent of abundance as carnivores and omnivores 71.2
a n d i n s e c t s i n s t e a d o f p o l y c h a e t e s , bivalves, a n d Percent of abundance as deep deposit fi=eders 90.9
crustaceans). The principles of benthic ecology Percent of biomass deeper than 5 cm 90.9
Percent of taxa deeper than 5 cm 65.7
u s e d to g e n e r a t e t h e list o f c a n d i d a t e m e t r i c s w e r e
156 s . B . Weisberg et al.

TABI.E i0. C o m p a r i s o n o f a b u n d a n c e a n d frequency of o c c u r r e n c e of Mediomastus amtnseta at reference a n d d e g r a d e d sites in all


habitats in which they were collected.

Abundance (number m ~) Frequencyof OcetlrFr162


(Percent of Sites)
Habitat Dataset Reference Sites Degraded S i t e s Rt:ference
Sites DegradedSites
Polyhaline s a n d Calibration 1,004 0 72 0
Polyhaline m u d Calibration 693 15 58 4
High Mesohaline sand Calibration 849 23 58 46
High Mesohaline m u d Calibration 409 9 30 3
Polyhaline sand Validation 2,073 0 77 0
Polyhaline m u d Validation 2,287 77 71 10
High Mesohaline m u d Validation 2,221 26 66 9

related metrics also resulted in a r e d u c t i o n in clas- e n r i c h m e n t of total organic c a r b o n (TOC), and


sification efficiency f r o m 93% to 92%. R e m o v i n g c o m b i n a t i o n s o f these stresses. To increase the
biomass a n d depth-related metrics t o g e t h e r caused n u m b e r o f samples to address this question, we in-
n o f u r t h e r loss in classification efficiency. cluded samples f r o m the calibration dataset m e e t -
In e x a m i n i n g the validation results, we discov- ing o u r criteria as a n t h r o p o g e n i c a l l y stressed sites
e r e d a small n u m b e r o f instances in which just a in the analysis since these sites were used to only
few individuals caused the pollution-sensitive taxa a small d e g r e e in calibration. T h e B-IBI was most
metric to be scored as 5 when overall a b u n d a n c e effective at identifying hypoxia; it correctly identi-
in the sample was low. In such cases, a few stray fied m o r e than 95% o f hypoxic sites regardless of
organisms can artificially inflate the response. To w h e t h e r hypoxia o c c u r r e d alone or in c o m b i n a -
avoid this, we r e c o m m e n d assigning a m a x i m u m tion with o t h e r stresses (Table 12). T h e index iden-
score of 3 for the pollution-sensitive taxa metric if tified p o o r biotic conditions in the p r e s e n c e of
overall a b u n d a n c e at the site is less than at the c o n t a m i n a n t s a b o u t 90% o f the time but slightly
r e f e r e n c e sites (i.e., the 5th percentile IBI abun- less often w h e n c o m b i n e d with hypoxia or high
d a n c e threshold) for the habitat. T O C . Response to organic e n r i c h m e n t was poor-
O u r validation test showed a high overall classi- est; the i n d e x identified only a b o u t 70% o f the en-
fication efficiency, b u t it did n o t address w h e t h e r riched sites as having d e g r a d e d b e n t h i c c o m m u -
the i n d e x is equally sensitive to the m a n y different nities. T h e i n d e x may have b e e n less efficient at
types o f a n t h r o p o g e n i c stress o c c u r r i n g in Chesa- i d e n t i f y i n g o r g a n i c a l l y e n r i c h e d sites b e c a u s e
p e a k e Bay. To assess this, we r e p e a t e d the valida- c h a n g e s in the benthic assemblage at low levels of
tion step separately for several categories of stress, T O C e n r i c h m e n t are too small to be detected con-
including hypoxia, chemical c o n t a m i n a t i o n , a n d sistently with community-level attributes (Gray et
al. 1990). Alternatively, the d e c r e a s e d efficiency
may be a function of c h o o s i n g 3% T O C as a
TABLE 11. A b u n d a n c e - b a s e d t h r e s h o l d s that m a y be substitut- threshold for e n r i c h m e n t ; the efficiency o f the in-
ed for biomass-based thresholds.
dex increased to 100% as T O C levels e x c e e d e d
.'~2oring Criteria 4%.
5 3 1 S o m e a u t h o r s have suggested that hypoxic con-
I.ow Mesohaline ditions in p o r t i o n s o f C h e s a p e a k e Bay are caused
A h u n d a n c e o f pollution- by natural seasonal stratification o f the water col-
sensitive taxa (%) ->25 -5-25 <5 u m n r a t h e r than a n t h r o p o g e n i c influences (Offi-
High Mesohaline m u d cer et al. 1984; C o o p e r a n d Brush 1993). Only a
A b u n d a n c e of pollution- few of o u r sites were located in these deep, strati-
indicative taxa (%) --<5 5-30 >30 fied areas o f the bay, but we o b s e r v e d biotic re-
A b u n d a n c e of pollution- sponse to hypoxia to be the same, regardless o f the
sensitive taxa (%) ->60 30-60 <30 cause of the hypoxia. Thus, the index c a n n o t be
Polyhaline sand
A b u n d a n c e o f pollution- TABLE 12. Classification efficiency o f B-IBI by stressor, alone
indicative taxa (%) < 10 10-40 >40 a n d in c o m b i n a t i o n with o t h e r stressors.
Polyhaline m u d
Alone In Combination
A b u n d a n c e o f pollution-
indicative taxa (%) -<15 15--50 >50 Toxic c o n t a m i n a n t s 92.9% 88.1%
A b u n d a n c e o f pollution- Hypoxia 98.5% 96.4%
sensitive taxa (%) ->40 2..5-40 <25 Organic enrichment 68.8% 77.3%
Benthic Index for ChesapeakeBay 157

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tion can be used to identify areas of the bay most httion Bulletin 26:249-257.
in n e e d of m a n a g e m e n t action or to evaluate prog- DAUER, D. M. AND R. W. ALDEN. 1995. Long-term trends in tile
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ACKNOWI.EDGMENTS
Virginia Water Control Board, Richmond, Virginia.
We gratefully acknowledge the contributions of T. Morris, N. FAUCHALD, K. AND P. A. JUMARS. 1979. The diet of worms. A
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thank K. Summers for access to the EMAP data, which was an FFRRARO, S. P., R. C. SWARTZ, F. A. COLF, AND D. W. SCHULTS.
important part of our calibration and validation datasets. We 1991. Temporal changes in the benthos along a pollution
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Magnien, M. Luckenbach, K. Mountford, and C. DeI.isle for from sewage-industrial wastewater effects. Estuarine Coastal and
their comments on drafts of tile manuscript. Portions of this She~ Science '~3:383-407.
work were supported by contract no. 68-D9-0166 from the l;'nit- GRA.';SLE,J. E AND J. E GRASSI.E. 1974. Opl)ortunistic life his-
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Governor's Council on Chesapeake Bay Research; we thank our GRASSLE,J. E AND J. E GI~.~.SSLE. 1984. The utility of studying
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