J. N. Am. Benthol. Soc., 2004, 23(1):114-125
© 2004 by The North American Benthological Society
Relationship of declining mussel biodiversity to stream-reach and
watershed characteristics in an agricultural landscape
K. Elizabeth Poole1 and John A. Downing2
Ecology, Evolution, and Organismal Biology, Iowa State University, 353 Bessey Hall, Ames,
Iowa 50011 USA
Abstract.
Freshwater mussels are among the most rapidly declining components of global biodi
versity, but causes of local species disappearances are frequently unknown. We estimated decadescale local extinction by resampling 118 stream reaches representing the best mussel habitat across
a region that was once rich in species and is now mostly converted from prairies and riparian
woodlands to intensive agriculture (Iowa, USA). Average species richness was reduced from >5 to
<2 species, maximum richness was reduced from 22 to 15 species, and all mussel species were
extirpated from 47% of the reaches since 1984 to 1985. More than half of the sites lost >75% of their
species. Although 5 of the species were found at 20% to 140% more sites in 1998 than 1984 to 1985,
29 species (83%) decreased an average of 80% in geographic coverage, whereas 8 species were com
pletely lost from these stream sites. Correlation analyses with reach and watershed characteristics
determined using GIS and local sampling methods linked the greatest declines to rarity of streamside
woodlands, high siltation, and most intensive agricultural land uses, i.e., where conditions had
changed most from the historical land cover. The surveys indicated a very large extinction debt has
been created by large-scale habitat modification over the last century and ongoing agricultural land
uses.
Key words:
agriculture, biodiversity, extinction debt, GIS, habitat, land use, mussels, riparian, spe
cies richness, streams.
Global biodiversity is declining through ex
social implications. Few studies have, however,
panding and accelerating local extinctions of
been able to measure rates of recent local de
species.
Although biodiversity is generally
cline against a background of prior field surveys
threatened in fresh waters (Miller et al. 1989),
that would enable linkage of species-loss rates
to changed environmental conditions.
mussel populations have been declining for de
cades (Matteson and Dexter 1966), are decreas
ing precipitously in North America (Suloway
1981), and are among the most seriously im
pacted aquatic animals worldwide (Bogan 1993,
Williams et al. 1993). The rate of mussel extinc
tion (1.2% per decade) is substantially higher
than all other aquatic and terrestrial faunal
groups (Ricciardi and Rasmussen 1999). Fresh
protracted period because of a time lag between
habitat loss and eventual population collapse
(Cowlishaw 1999). For the long-lived fauna,
such as freshwater mussels, a century of land
scape change has likely created a major extinc
water mussels have been important economical
ly for cultured pearl production (Anthony and
Downing 2001), are ecologically important as
primary consumers, detritivores, filter feeders,
and nutrient sinks (McMahon 1991), and may
be among the oldest living animals on earth
(Anthony et al. 2001). Their loss from aquatic
systems would have economic, ecological, and
1 Present address: Office of Environmental Services,
Iowa Department of Transportation, 800 Lincoln Way,
Ames, Iowa 50010 USA. E-mail:
kelly.poole@dot.state. ia. us
2 To whom correspondence should be addressed.
E-mail: downing@iastate.edu
Populations of mussels and other aquatic fau
na that have survived extensive loss of suitable
habitat often face continued extinction over a
tion debt (sensu Tilman et al. 1994, Hanski and
Ovaskainen 2002).
Changes in large-scale watershed character
istics can affect community composition and en
vironmental conditions (Frissell et al. 1986, Davies et al. 2000). Likewise, habitat degradation
and fragmentation often drive declines in local
and regional biodiversity. Located in the heart
of the Mississippi watershed, the State of Iowa
(USA) has been an historic area of high mussel
diversity (Pennak 1989). Within the past centu
ry, the entire state has been converted from tall
grass prairie with rivers surrounded by dense
riparian woodlands (Andreas 1875) to a highly
114
2004]
Declining mussel biodiversity in streams
115
100 -n
land surface
80 —
o
in farms
60
CO
wetlands
o
SS
drained
40
20 —
1840
I
I
I
1880
1920
1960
2000
Year
Fig. 1. Changes in the Iowa landscape from the mid 1800s to present. The % of the total land area in farms,
including only farms in actual use (i.e., "improved land in farms"), was taken from the United States Agricul
tural census data (http://fisher.lib.virgmia.edu/census/) through 1950. More recent data on land use were taken
from historical census figures (1987, 1992, and 1997 reports) from United States Department of Agriculture's
Census of Agriculture (http://govmfo.kerr.orst.edu/php/agri/index.php) and United States Bureau of the Census
(1964, 1987). Wetland drainage data were taken from Shaw and Fredine (1956).
degraded
agricultural
landscape
(Thompson
1992) with widespread riparian deforestation.
Iowa is among the most agriculturally produc
The extinction effect of large-scale landuse
change of the last century has not yet been fully
were already locally extinct or in danger of local
realized; thus, the least-changed landscapes are
likely to harbor faunal remnants that are declin
ing more slowly and are more protected from
the continued impacts of agricultural perturba
tion. Therefore, our goal was to estimate the re
lationship of local extinction rates to the char
acteristics of the changed landscapes. We resampled 118 historic reference sites to document
changes in mussel species richness over the last
decade. Our specific objectives were 1) to quan
tify change in species richness between 1984 to
1985 and 1998; 2) to determine the relationships
between site-specific, stream-reach characteris
tics (e.g., current instream habitat and riparian
conditions) and changes in species richness; and
3) to analyze the relationships between current
watershed characteristics (e.g., land use and ge
ology) and rates of change in species richness at
extirpation.
the whole-watershed scale.
tive of the Mississippi River watershed states
with ~90% of its 14.5 million hectares in agri
cultural production.
Conversion of natural landscapes to agricul
tural lands is driving a great deal of habitat deg
radation and reduced biodiversity. In Iowa, for
example, >95% of the land area had been con
verted to farms by 1925 and >90% of the wet
lands had been drained by 1956 (Fig. 1). Be
cause such profound landscape modification
can lead to declining biodiversity, an extensive
assessment of Iowa's mussel fauna was under
taken from 1984 to 1985 to estimate species rich
ness in the highest-quality habitats. At that time,
nearly half of the 55 historically known species
(Drew 1890, Frest 1987) of Iowa stream mussels
116
K. E. Poole and J. A. Downing
Methods
[Volume 23
sign (Hayek and Buzas 1997) and extensive vi
sual and tactile surveys over several hours of
Changes in species richness
searching of epibenthic and endobenthic habi
tats, stream banks, and shores. Sampling was
Mussel species richness was surveyed by the
continued until long after no new species could
Iowa Department of Natural Resources at 171
be located within the stream reach, so the 1998
sites throughout the state in 1984 to 1985 (Frest
sampling was nearly exhaustive. Identifications
1987). More than 1000 sites were initially visu
were verified by comparing specimens with
ally assessed. Many entire streams were com
photos of voucher shells held at the Illinois Nat
pletely devoid of mussels, but the 171 sites cho
ural History Survey (Champaign, Illinois).
sen had the best remaining mussel habitat in the
Every effort was made to access the same
state. Mussels were becoming rare, even in 1984
sites sampled in 1984 to 1985. If access to the
to 1985, so they were sought by searching sites
previously surveyed stream segment was pre
that appeared to be "least impacted" (Frest
vented, surveys were done as close as possible
1987), considering riparian and water-quality
to each original site, in the most favorable mus
characteristics. Least-degraded sites were locat
sel habitat. The same access points were used
ed by examining most large streams in the state
in both 1984 to 1985 and 1998 for 104 of the 118
every 8 km along their length, medium streams
sites resurveyed. However, surveys were done
every 5 km, and small streams every 3.5 km.
in a different direction at 14 of these sites (e.g.,
Road or bridge access points were usually used
upstream versus downstream), most commonly
to examine streams, but offroad travel and boat
at sites where grazing and instream fencing pre
access were sometimes used. Most of the road
vented access to the same segment. It is there
or bridge access points in the state were exam
fore possible that declines in species richness at
ined and mapped (Frest 1987). Stream condition
these 14 alternative sites may have been under
was assessed at each access point based on sub
estimated.
strate, water clarity, aquatic vegetation, other
bottom fauna, and flow. A site was designated
Locations of sites and species assemblages are
not revealed here to protect the species against
for sampling if evidence of living mussels or re
illegal collection. These data have been depos
cently dead shell material was found along
ited with the Iowa Department of Natural Re
stream banks and in the shallow waters. Living
sources and are legally protected under the US
mussels were censused by hand collection at
Endangered Species Act.
each sampling site. Medium and large streams
were visited during periods of seasonal low wa
ter. One person searched for live, recently dead,
and juvenile mussels for several hours at each
Characteristics of sampling sites
The 1998 survey assessed stream-reach char
site. On large streams, the length of the stream
acteristics at each of 5 cross-stream transect
reach searched sometimes extended for 1.6 km.
points located along the survey segment at each
Species richness at each site was determined as
sampling site. Transects were positioned at the
the sum of all species represented by all live
upstream and downstream ends of the survey
mussels found.
segment, and at Va, Vi, and % of the distance
The 1998 resurvey was designed to be more
from the downstream and upstream ends. Two
thorough and lengthy at each of the 171 sites
water samples were collected at each site and
sampled in the 1984 to 1985 study (see Arbuckle
analyzed for total N (TN), total P (TP), total sus
and Downing 2002 for a full account of sam
pended
pling methods). Only 118 of the 1984 to 1985
(APHA 1998). Water chemical analyses charac
solids
(TSS),
and
alkalinity
(ALK)
sites could be resampled because of high water
terize
and access problems. These 118 sites were sys
streams and reaches because daily variations in
tematically surveyed by
only
large-scale
differences
among
3 people searching
water chemistry can be large. Stream shading
while moving upstream along a survey segment
was estimated using a concave spherical den-
at each site. Species richness at a site was in
siometer. Sediments were characterized at each
ferred from all the species catalogued in 60
site, following Brim Box and Mossa (1999), by
quadrat samples (Downing and Downing 1992)
visually estimating % substrate type (fine sedi
arranged in a restricted random sampling de
ment: <0.0625 mm, sand: 0.0625-2 mm, gravel:
2004]
Declining mussel biodiversity in streams
117
2—4 mm, and cobble: >64 mm) at each of the 5
Tools; Environmental Systems Research Insti
points across the stream (right and left banks,
tute: http://www.esri.com).
midpoint, and 2 quarter points) at each of the 5
transects for a total of 25 sampling points per
site. Stream depth was measured across the
Statistical analysis
channel at 3 points (mid-channel and 2 quarter
Species-specific patterns of appearance and
points) on each transect. Stream width was also
disappearance were analyzed by coding each
measured at each transect. Riparian composi
species-site combination as -1, 0, or +1 indi
tion was visually estimated and recorded as %
cating that species went from presence to ab
cropland, grassland, pasture, woodland, urban,
sence, stayed present, or went from absent to
and bluff. The entire state was composed of tall
present,
grass prairie with dense riparian woodlands in
1984-1985 to 1998. We felt that trends in biodi
1850 (Andreas 1875; Fig. 1), so current condi
versity would be most robustly analyzed as
tions at sampling sites are a good indictor of
changes in overall species richness because pres
habitat change over a scale relevant to the lon
ence-absence dynamics were frequently posi
gevity of mussels (Anthony et al. 2001).
Current watershed characteristics likely to in
of species were quantified to relate changes in
species richness to geology and altered land use.
The watershed boundaries (Hydrologic Unit
Code 11; Seaber et al. 1987) used in the analyses
were obtained from the Iowa Department of
Natural Resources (Des Moines, Iowa), and are
Geological
Survey hydrologic
units, a nationwide hierarchical system for de
fining watersheds. Geographic Information Sys
tems (GIS) analysis was used to prepare de
scriptions (including alluvial deposits, average
relief,
geologic
formations,
and
land use) for each watershed surveyed. Land
scape features were selected because of their po
tential to influence water quality. GIS data for
geology and land use allowed classification by
% area. There were 8 geologic formations, in
cluding 2
formations associated with major
aquifers (Mississippian, Silurian-Devonian),
and 6 landuse types: agricultural, urban, range
land, forest, water, and wetland. Watershed to
pography was calculated as average % slope for
each watershed. Watershed alluvium was cal
culated as % of total watershed area. GIS data
used in this analysis were acquired from the
Iowa Department of Natural Resources, Natural
Resource GIS library. GIS work was done fol
lowing the methods described by Arbuckle and
Downing (2002), using GIS software to prepare
the watershed
descriptions
sions,
Spatial
X-Tools,
the
period
from
tively correlated among several species, and
fluence either susceptibility or resistance to loss
topographic
over
preliminary multivariate analyses (e.g., cluster
analysis, principal components analysis) indi
Waterslwd chamcteiistics
based on US
respectively,
(ArcView exten
Analyst,
and
Spatial
cated that several species declined in concert
under various combinations of environmental
conditions.
Changes in species richness (AR) from 19841985 to 1998 conditions were calculated as a
proportional change [AR = (RI998 - R1984.19S5)/
R1984-1985] at each sampling site. Relationships be
tween rates of change in species richness and
characteristics at sampling sites were deter
mined using multiple regression analysis. Initial
candidate variables in these regressions includ
ed mean stream width, mean stream depth, %
stream shading, % substrate composition, % ri
parian composition, TN, TP, TSS, and ALK.
Candidate variables were eliminated from the
regression by partial significance level (p > 0.05)
using variable selection by backwards elimina
tion.
In watershed analyses, the dependent variable
was arcsine
transformed mean proportional
change in average watershed species richness
(AR) calculated as the proportional change of
mean species richness of all sites within a wa
tershed [AR = (Rm& - R1984_iy85)//W1985]. The
AR values were transformed using an arcsine
transformation (Snedecor and Cochran 1989) to
the distributional problems associated
avoid
with percentages and proportions. Graphical
analysis (Draper and Smith 1998) indicated im
provement in the distribution of the residuals
after transformation. The influence of watershed
characteristics on changes in species richness
was also determined using multiple regression
analysis. The large number of candidate vari
ables in the watershed analyses (geologic for-
K. E. Poole and J. A. Downing
118
[Volume 23
mations, landuse GIS data) necessitated identi
sels in the past, or that many populations were
fication of a subset of independent variables,
on their way toward extinction triggered by
which was done with backward elimination
massive landuse change early in the 20th cen
multiple regression methods in 2 analyses: one
tury. Of the 118 sites surveyed, only 26 (22%)
to identify the most significant of the*8 geologic
had equal or greater species richness in 1998
than in 1984 to 1985, but 58% of the sites lost
formations and a second to identify the most
significant of the 6 landuse types. Candidate
>75% of the species richness that had been ob
variables were eliminated from the initial mul
served only slightly more than a decade before
tiple regressions based on partial significance (p
(Fig. 3A).
> 0.05). Having reduced the independent vari
The rates of loss of species (Table 1) bore no
ables to a statistically manageable subset, a final
evident relationship with characteristics of the
backward elimination multiple regression anal
species themselves (e.g., size, fish hosts, host
ysis was performed to determine the concurrent
specificity, etc.)- For example, Strophitus undu-
influence of watershed characteristics on AR.
latus was found at 33 fewer sites in 1998 than
previously, yet is likely to require no host fish
Results
Changes in species richness
(Parmalee and Bogan 1998). Amblema plicata
and Pyganodon grandis have a wide variety of
potential and available host fish, yet declined
widely (Table 1). Species of mussels increasing
Overall species richness in the 1998 survey
their distributions have between 2 and 20
was low compared to historic records (Drew
known hosts, belonging to 1 to 10 families of
fish. Instead, the sharp decline in species rich
1890, Frest 1987). We found a total of 27 mussel
species in 1998 (Table 1), which represents a loss
ness found in our study suggests that habitat
of 8 species from the state since 1984 to 1985.
conditions in Iowa have declined precipitously
The loss is a 22% decline in the total number of
over the century of change from tall grass prai
species observed in the 1984 to 1985 survey, and
rie with wooded bottom lands to intensive ag
is ~Vi the number of species estimated from his
toric museum collections to occur on inland
riculture with little riparian buffer.
streams (Frest 1987). Five of the species were
ence or absence of species at the 118 sites in
found at between 1 and 17 more sites in 1998
dicated that most species responded similarly
than 1984 to 1985 (+20% to +140%), but 29 spe
to
cies (83%) decreased an average of 80% (from
sites. Correlation analyses among species pres
-29% to -100%) in geographic coverage (Table
1). Mussel species richness at individual sites in
ence-absence scores (-1, 0, +1 indicating di
rection of change) across the 118 sites revealed
Correlations among rates of change in pres
environmental
degradation at individual
1984 to 1985 ranged from 0 to 22, averaging 5.4,
all but 2 of the 29 statistically significant cor
but in 1998 ranged from 0 to 12, averaging 1.9.
relations (p < 0.05; unadjusted for multiple
The average mussel species richness declined by
comparisons)
>50% over this period.
Multivariate analyses of species-specific rates
The most noticeable change in species rich
among species were positive.
of change using cluster analysis or principal
ness occurred in the % of sites with no living
components led to no clear conclusions, in part
species (i.e., sites where all species had become
extinct). In 1984 to 1985, living mussels were
because of the number of empty species-site
combinations. Most mussel species appeared to
absent from only 6% of the minimally degrad
respond similarly to degradation, and limita
ed sites surveyed (Fig. 2A), whereas in 1998
tions of the data set made analyses based on
47% had no living mussels (Fig. 2B). This mag
species-specific trends unclear. Thus, analysis
nitude of change in species richness over that
time period is alarming, especially because
of conditions associated with lost biodiversity
was subsequently done on rates of change in
these sites were originally chosen to represent
species richness rather than species-specific
the region's least degraded mussel habitat. This
changes in presence at sites.
result may indicate that the intensification of
Effects were greatest at the sites that had the
agricultural production over the last century in
highest species richness during the original
this region has removed a considerable number
1984 to 1985 sampling. The most speciose sites
of habitat patches that were suitable for mus
in 1984 to 1985 lost the most species by 1998
2004]
Declining mussel biodiversity in streams
119
Table 1. Occurrence of mussel species at 118 resurveyed stream sites, arranged in decreasing order of
number of sites from which each species was lost. "EX" indicates that the species was no longer found at any
of the sampled sites, "New" indicates that the species was not found during the initial 1984 to 1985 survey but
was found in 1998.
No. of sites
Species
1984-
Common name
1985
%
1998
Change
change
-49
Lampsilis cardium Rafinesque
Plain pocketbook
90
46
-44
Fusconaia flava Rafinesque
Wabash pigtoe
52
13
-39
Lampsilis siliquoidea Barnes
-75
Fatmucket
43
6
Amblema plicata Say
-37
-86
Threeridge
42
8
-34
Strophitus undulatus Say
-81
Squawfoot
35
2
-33
Lasmigona complanata Barnes
-94
White heelsplitter
51
20
-31
Pyganodon grandis Say
-61
Giant floater
45
15
Anodontoides ferussacianus Lea
-30
-67
Cylinder
26
2
-24
Lasmigona compressa Lea
-92
Creek heelsplitter
22
0
-22
Venustaconcha ellipsiformis Conrad
EX
Ellipse
24
2
Leptodea fragilis Rafinesque
-22
-92
Fragile papershell
25
5
-20
Obovaria olivaria Rafinesque
-80
Hickorynut
17
1
Quadrula pustubsa Lea
-16
-94
Pimpleback
30
15
-15
Toxolasma parous Barnes
-50
Lilliput
14
0
-14
Truncilla tnincata Rafinesque
EX
Deertoe
14
2
-12
-86
Truncilla donaciformis Lea
Fawnsfoot
14
3
-11
PotamihiS alatus Say
-79
Pink heelsplitter
11
3
Obliquaria reflexa Rafinesque
-8
-73
Threehorn warty-
10
3
-7
-70
back
Potamilus ohiensis Rafinesque
Pink papershell
12
5
Quadrula metanerva Rafinesque
-7
-58
Monkeyface
5
1
-4
-80
-4
-67
Utterbackia imbecillis Say
Paper pondshell
6
2
Lampsilis teres Rafinesque
Yellow sandshell
5
2
Quadrula quadrula Rafinesque
Mapleleaf
3
0
-3
Alasmidonta viridis Rafinesque
EX
Slippershell
2
0
-2
Ligumia recta Lamarck
EX
Black sandshell
7
5
Pleurobema coccineum Conrad
-2
-29
Round pigtoe
2
0
-2
Anodonta suborbiculata Say
EX
Flat floater
1
0
-1
EX
EX
-60
Fusconaia ozarkensis Call
Ozark pigtoe
1
0
-1
Pletliobasus cyphus Rafinesque
Sheepnose
1
0
-1
Lasmigona costata Rafinesque
Fluted-shell
5
6
1
EX
+20
Tritogonia verrucosa Rafinesque
Pistolgrip
5
6
1
Alasmidonta marginata Say
+20
Elktoe
7
9
Elliptio dilatala Rafinesque
2
+29
Spike
3
5
2
Quadrula nodulata Rafinesque
+67
Wartyback
0
6
6
Actinonaias ligamentina Lamarck
New
Mucket
12
29
17
+142
(Fig. 3B). Communities with low richness in
Site changes and habitat quality
1984 to 1985 may therefore have already been
affected by the more radical changes in land
use and water quality in these areas since the
early 1900s. Communities with the highest
richness in 1984 to 1985 may have been able to
survive the most severe degradation before
1984 to 1985, and were simply slower to de
cline following generalized landuse change.
Stream sites often had riparian zones domi
nated by agricultural use and were generally
characterized by poor water quality (Table 2).
Multiple regression showed that the fraction of
remaining woodland in the riparian zone, and
the fractions of fine sediment, sand, gravel, and
cobble substrate were significantly (p < 0.05)
[Volume 23
K. E. Poole and J. A. Downing
120
2%
(11-15 spp)
1984-85 species richness
Fig. 2.
1998 species richness
Comparison of the % of 118 stream reaches surveyed in 1984 to 1985 (A) and 1998 (B) that had
various levels of mussel species richness.
positively related to AR (Table 3). Positive vari
gravel, and cobble substrates had the least se
able loadings in this context indicated smaller
vere rates of decline in mussel richness.
declines or improvements in biodiversity, so ar
Riparian woodlands had the strongest posi
tive partial effect on change in mussel species
nearly equal fractions of fine sediment, sand,
richness (Table 3) in multiple regressions. The
4
B
u\5 18\mwUn-r—■^OCDo*
60
GLos ain
ies
A
4_-CQD 0M-
40.Q
>,
o
c
1998)
eas with more riparian woodlands and more
20-
o
ex
9>
u.
-100
0
100
200
% change in species richness (AR)
1984-85 to 1998
Fig. 3.
0
5
10
15
20
25
Species richness 1984-85
Mussel species losses from 1984-1985 to 1998. A.—The frequency of sites having various levels of
% change in species richness between 1984 to 1985 and 1998. B.—Relationship between the average change in
species richness between 1984 to 1985 and 1998 and species richness levels at sites in 1984 to 1985. Numbers
plotted on panel B indicate the number of sites used to calculate each average. The solid line is a least-squares
regression describing loss of species richness (r2 = 0.89, p < 0.001, n = 118).
2004]
Declining mussel biodiversity in streams
Table 2.
121
Stream diaracteristics at the 118 resampled sites in Iowa, USA.
Variable
Minimum
Median
Maximum
Morphology and shading
Average depth (m)
0.12
Mean width (m)
4.5
28.4
Shading (%)
0
20
0.52
1.21
171
67
Substrate (%)
Fine
0
16
Sand
100
0
50
Gravel
100
0
7
Cobble
69
0
4
100
Riparian land use (%)
Cropland
0
0
Grassland
100
0
30
Pasture
100
0
0
Woodland
80
0
50
Urban
100
0
0
Bluff
100
0
0
40
103
203
305
Water diemistry
Alkalinity (mg/L)
Total N (mg/L)
Total P (|i.g/L)
Total suspended solids (mg/L)
1.7
5.2
17.8
<10
236
1128
1
25
285
effect is illustrated as a bivariate plot (Fig. 4A)
showing that only sites with >50% woodlands
in the riparian zone occasionally lost no species
or increased in species richness. The median
rate of species loss only approached 0 in stream
reaches with >80% wooded riparian zone. Ri
parian woodlands, previously the rule across
this landscape (Andreas 1875), are of immense
water-quality and biological benefit to stream
animals (Karr and Schlosser 1978, Allan 1995),
providing shading as well as water-quality pro
tection. Stream segments with the highest sub
strate diversity (i.e., including most equal frac
tions of fine sediment, sand, gravel, and cobble)
also showed smaller declines in mussel species,
suggesting that substrate heterogeneity is im
portant to mussels.
use, presence of alluvial deposits, and preva
lence of the Mississippian geologic formation
(Table 3). Intensive agriculture can adversely in
fluence water quality, so the negative partial ef
fect on change in species richness is not sur
prising. A bivariate plot of this partial effect
(Fig. 4B) shows that species richness increased
or was unchanged in watersheds where agri
cultural practices accounted for <25% of land
use.
Both alluvial deposits and the Mississippian
formation enhance groundwater quantity and
quality (Anderson 1998) and were associated
with lowest rates of decline probably because
they stabilize the hydrologic regime. The alter
ation of drainage in this agricultural area
through channelization and subsurface drain til
ing that accompanied wetland drainage has led
Watershed geology, land use, and cftanges in species
richness
Watersheds varied in average land use and
geology (Table 4). Multiple regression analysis,
done on the watershed-averaged changes in
richness showed that changes in richness were
most closely associated with agricultural land
to flashy hydrology that can decimate the
stream biota. Further, agriculture was most
prevalent in the watersheds where the area of
Mississippian formations were found in <10%
of the landscape. The combination of intense ag
ricultural land use and low potential for water
recharge (inferred by low fractions of Mississip
pian formations) results in suboptimal water
122
K. E. Poole and J. A. Downing
Table 3.
[Volume 23
Multiple regression analyses of changes in site- and watershed-specific species richness related to
stream reach and watershed characteristics. Change in stream-site mussel biodiversity was analyzed as the
change in species richness from 1984-1985 to 1998 (arcsine AR). Change in watershed mussel biodiversity was
measured as the change in average watershed biodiversity (arcsine AR). Positive regression coefficients indicate
that variables were positively correlated with the maintenance of biodiversity and negative coefficients indicate
a negative relationship with biodiversity. Partial ^-values indicate the size of statistical effects of the independent
variables when all other independent variables are considered, p indicates the probability that a partial f-value
of equal or greater magnitude would be obtained through chance alone. The regression analysis of stream reach
characteristics had R2 = 0.23, F = 6.39, p < 0.001, and n = 118. The regression analysis of watershed charac
teristics had R2 = 0.51, F = 9.52, p = 0.001, and n = 36. For stream reach regressions, sediment data were
entered as the fraction (i.e., 100% = 1.0) of the total sediment area in the stream reach, and riparian woodlands
were entered as the fraction of the total riparian area. For watershed regressions, geologic formations and
agricultural land use were entered as the fraction of the total watershed area.
Regression
coefficient
Independent variable
Partial t
V
Stream reach regression
-24.7
Intercept
1.1
4.98
<0.001
Gravel
23.9
2.33
0.022
Sand
23.2
2.26
0.026
Fine sediment
23.0
2.24
0.027
Cobble
23.1
2.24
0.027
Riparian woodland
Watershed regression
-0.85
Intercept
Mississippian geologic formation
Agricultural land use
Alluvial deposits
1.46
3.12
0.004
-2.21
-2.64
0.013
1.94
2.58
0.016
The results of the watershed analysis under-
quality and hydrologic conditions for mussels,
complete. This finding echoes the results of terrestrial studies of biodiversity in both long-
scored the positive influence of site-specific,
nonagricultural, geomorphic features like
(Cowlishaw 1999) and short-lived (Brooks et al.
1997) organisms. Land use has been fairly static
wooded riparian zones (Table 3). Both results
in this region for several decades (Fig. 1) and
are consistent with other recent analyses (Hog-
we observed the lowest rates of species loss in
garth et al. 1995) in indicating that agricultural
areas most similar to historic conditions. It thus
practices degrade mussel richness.
appears that biodiversity may decline for de
cades following habitat alteration. These find-
Discussion
in8s a8ree with current theories suggesting that
previously abundant organisms with low dis-
Our results illustrate a severe decline in the
persal potential like freshwater mussels may
local biodiversity of freshwater mussels (cf. Ric-
pay a long-term extinction debt through local
ciardi and Rasmussen 1999), and suggest the
extinction (Tilman et al. 1994, Hanski and Ovas-
importance of proper management of surround-
kainen
ing terrestrial landscapes when planning con-
changes have been made. Increased mortality,
servation and restoration of aquatic ecosystems
decreased potential for recolonization, or in-
(Page et al. 1997). The significant relationships
creased fragmentation of the metapopulation
between changes in mussel biodiversity and re-
will likely accelerate widespread species losses,
sidual
streamside
woodlands,
and
between
Our
2002)
results
that
also
continues
suggest
long after the
that
landscape
changes in mean species richness of mussels
changes may be having more severe effects than
and most intensive agricultural land use indi-
biotic changes linked to species biology, at least
cate that the extinction debt is most severe
at this stage of retraction of regional biodiver-
where habitat destruction has been the most
sity. For example, the relative rate of decline in
2004]
Declining mussel biodiversity in streams
i
20
40
60
80
100
■
20
123
i
■
40
% agriculture in watershed
% woodland in riparian zone
r
60
Fig. 4. Relationships between rates of mussel species losses and stream reach and watershed characteristics.
A.—Relationship between the proportional change in mussel species richness (AR) and % riparian woodland
area surrounding each stream-reach site. Points above and below the horizontal line of no change indicate an
increase and decrease in mussel species richness, respectively. The solid line is the least-squares regression fit
to the data (r2 = 0.24, p < 0.01, n = 93). The gray line indicates trends in median rates of species loss for
stream reaches with various fractions of riparian woodlands. B.—Relationship between the proportional change
in mean watershed mussel species richness (AR) and % agricultural land use in the watersheds. Numbers in
circles indicate the number of sites included in each watershed mean. The vertical dashed line indicates 25%
agricultural area. The horizontal dashed line indicates no change in species richness. Points above and below
the horizontal line of no change indicate an increase and decrease in A/?, respectively. The solid line is the
least-squares regression fit to the data (r2 - 0.26, p < 0.01, n = 32).
geographic coverage of species seems to bear
little relationship with the number or specificity
rarely been examined explicitly, completely dif
ferent aspects of streams may be associated
of required host fishes (Table 1). Further, even
with mussel success at small and large scales
species normally thought to be ubiquitous and
(e.g., Strayer 1993, Strayer and Ralley 1993). It
resistant to decline (e.g., Uimpsilis siliquoiden, Py-
seems reasonable, however, that the character
ganodon grandis) showed great rates of decrease.
istics of whole watersheds should influence
Although we do not have enough data on fish
long-term resistance of mussel communities to
perturbation when viewed at the small scale.
distributions and abundances to do specific
analyses, there is little doubt that reproductive
problems related to glochidial attachment to fish
have also become more acute in this altered
landscape.
A major framework in stream ecology is the
Our analyses uphold this concept because wa
tersheds with the most habitat converted to
farmland had the greatest levels of decline in
richness. This effect is echoed at the smallest
scale by the association of deforested riparian
concept that small-scale characteristics are driv
zones in agricultural watersheds with declining
en by a hierarchy of nested effects deriving from
richness. Also at the smallest scale, the lowest
rates of declining biodiversity were associated
with diversity of substrata. Again, parallel ef
fects were detected on the watershed scale as
sociated with the Mississippian geologic system
and alluvial sediments that give rise to sub
strates less prone to siltation (Table 3). Our anal
yses uphold the hierarchical view of stream
the large-scale watershed (e.g., Frissell et al.
1986). This concept has been used to understand
species composition of undegraded
systems
(e.g., Poff 1997), and to provide a framework for
assessing impacts (e.g., Davies et al. 2000). Al
though the effect of scale on the detection of
relationships between mussels and habitat has
Tabu-: 4.
[Volume 23
K. E. Poole and J. A. Downing
124
Characteristics of the watersheds ana
lyzed in Iowa, USA. All variables are expressed as
percentages of watershed area except the % slope of
the watershed.
also thank James Anthony, Jennifer Coshland,
Ben Dodd, and Laurie Meythaler for help in the
field, Marion Conover and Daryl Howell for
support of this project, Kevin Cummings for
Minimum
Median
Maximum
Land use
taxonomic help, and Richard Norris and 3 anon
ymous reviewers for constructive comments on
earlier drafts.
Agricultural
12.9
62.4
88.1
Forest
0.0
0.6
2.0
Range land
8.6
26.9
50.7
Urban
0.2
0.7
8.3
Water
0.0
0.3
3.3
Wetland
0.7
7.1
40.0
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Received: 3 January 2003
Accepted: 7 November 2003