Spatial and Temporal Trends of Freshwater Mussel ...

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Spatial and Temporal Trends of Freshwater Mussel Assemblages Spatial and Temporal Trends of Freshwater Mussel Assemblages

in the Meramec River Basin Missouri USA in the Meramec River Basin Missouri USA

J E Hinck

Stephen E McMurray

Andrew D Roberts MSU Graduate Student

M Christopher Barnhart Missouri State University

Christopher G Ingersoll

See next page for additional authors

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Recommended Citation Recommended Citation Hinck Jo Ellen Stephen E McMurray Andrew D Roberts M Christopher Barnhart Christopher G Ingersoll Ning Wang and Tom Augspurger Spatial and temporal trends of freshwater mussel assemblages in the Meramec River basin Missouri USA Journal of Fish and Wildlife Management 3 no 2 (2012) 319-331

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Authors Authors J E Hinck Stephen E McMurray Andrew D Roberts M Christopher Barnhart Christopher G Ingersoll Ning Wang and Tom Augspurger

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Surveys

Spatial and Temporal Trends of Freshwater MusselAssemblages in the Meramec River Basin Missouri USAJo Ellen Hinck Stephen E McMurray Andrew D Roberts M Christopher BarnhartChristopher G Ingersoll Ning Wang Tom Augspurger

JE Hinck CG Ingersoll N WangUS Geological Survey Columbia Environmental Research Center 4200 New Haven Road Columbia Missouri 65201

SE McMurrayMissouri Department of Conservation Central Regional Office and Conservation Research Center 3500 East Gans RoadColumbia Missouri 65201

AD RobertsUS Fish and Wildlife Service 101 Park DeVille Drive Columbia Missouri 65203

MC BarnhartMissouri State University Department of Biology 901 South National Avenue Springfield Missouri 65897

T AugspurgerUS Fish and Wildlife Service 551-F Pylon Drive Raleigh North Carolina 27636

Abstract

The Meramec River basin in east-central Missouri has one of the most diverse unionoid mussel faunas in the centralUnited States with 40 species identified Data were analyzed from historical surveys to test whether diversity andabundance of mussels in the Meramec River basin (Big Bourbeuse and Meramec rivers representing 400 river miles)decreased between 1978 and 1997 We found that over 20 y species richness and diversity decreased significantly in theBourbeuse and Meramec rivers but not in the Big River Most species were found at fewer sites and in lower numbers in1997 than in 1978 Federally endangered species and Missouri Species of Conservation Concern with the most severetemporal declines were Alasmidonta viridis Arcidens confragosus Elliptio crassidens Epioblasma triquetra Fusconaiaebena Lampsilis abrupta Lampsilis brittsi and Simpsonaias ambigua Averaged across all species mussels were generallybeing extirpated from historical sampling sites more rapidly than colonization was occurring An exception was one reachof the Meramec River between river miles 284 and 595 where mussel abundance and diversity were greater than inother reaches and where colonization of Margaritiferidae Lampsilini and Quadrulini exceeded extirpation The exactreasons mussel diversity and abundance have remained robust in this 30-mile reach is uncertain but the reach isassociated with increased gradients few long pools and vertical rock faces all of which are preferable for musselsComplete loss of mussel communities at eight sites (16) with relatively diverse historical assemblages was attributed tophysical habitat changes including bank erosion unstable substrate and sedimentation Mussel conservation effortsincluding restoring and protecting riparian habitats limiting the effects of in-stream sand and gravel mining monitoringand controlling invasive species and protecting water quality may be warranted in the Meramec River basin

Keywords extirpation field survey freshwater mussels status Unionoidea

Received May 8 2012 Accepted August 14 2012 Published Online Early August 2012 Published December 2012

Citation Hinck JE McMurray SE Roberts AD Barnhart MC Ingersoll CG Wang N Augspurger T 2012 Spatial andtemporal trends of freshwater mussel assemblages in the Meramec River basin Missouri USA Journal of Fish andWildlife Management 3(2)319ndash331 e1944ndash687X doi 103996052012-JFWM-038

Copyright All material appearing in the Journal of Fish and Wildlife Management is in the public domain and may bereproduced or copied without permission unless specifically noted with the copyright symbol Citation of thesource as given above is requested

The findings and conclusions in this article are those of the author(s) and do not necessarily represent the views of theUS Fish and Wildlife Service

Corresponding author jhinckusgsgov

Journal of Fish and Wildlife Management | wwwfwspubsorg December 2012 | Volume 3 | Issue 2 | 319

Introduction

Native unionoid mussels (Mollusca Bivalvia Union-oidea Carter et al 2011) are important components ofaquatic ecosystems Global declines have resulted innative mussels being identified as the most imperiledfaunal group in North America which emphasizes theneed for their protection and conservation At least 26and probably 40 of the 300 North American taxahave become extinct in the past 100 y and it appearsthat 25 of the mussel fauna will be lost within thenext 30 y (Haag 2009) Presently 73 mussel species areclassified as federally threatened or endangered pur-suant to the US Endangered Species Act (ESA 1973 asamended) with 7 additional species as candidates forlisting in the United States (US Fish and Wildlife Service2011) Declines in mussels have been attributed tovarious factors including sedimentation channelizationdredging impoundment construction and operationpollution and invasive species (Lydeard et al 2004)

At least 69 species of native mussels have historicallyoccurred in Missouri (Missouri Department of Conserva-tion 2008) The Meramec River basin in east-centralMissouri contains one of the most diverse mussel faunasin the central United States with 40 species (Buchanan1980 Roberts and Bruenderman 2000) several of whichare listed as federal or state endangered species Thestatus of mussels in the basin was initially surveyed in1977ndash1978 following proposals to construct multipleflood-control dams in the Meramec River basin (Bucha-nan 1980) A second survey was conducted in 1997 toaddress concerns about declines in mussel diversity andabundance (Roberts and Bruenderman 2000) The musselcommunity in the Big River the largest tributary of theMeramec River was of specific concern because of lead-zinc and barite (barium sulfate) mining that occurred inthe upper and middle reaches of the Big River watershedHistorical mining has been implicated in heavy metalcontamination of aquatic biota including mussels in theBig River (Niethammer et al 1985 Czarnezki 1985 1987Schmitt et al 1987 Gale et al 2002 Besser et al 20072009a 2009b)

In addition to mining other threats to musselconservation exist in the Meramec River basin Althoughwater quality is considered good compared with otherbasins in the state point and nonpoint source pollutionfrom hundreds of dischargers occurs within the basin(Annis et al 2009) Construction activities to accommo-date human population growth especially in the lowerportion of the basin can also impact water qualitythrough hydrologic alteration and by increasing inputs ofsediments and contaminated runoff Livestock grazinglogging and in-stream gravel mining are major activitieswithin the basin that have the potential to impact musselpopulations through runoff erosion sediment produc-tion and nutrient loading

The objective of this study was to analyze data fromhistorical surveys to document and evaluate trends inspatial and temporal diversity and abundance of musselsin the Meramec River basin (Buchanan 1980 Roberts and

Bruenderman 2000) Specifically we hypothesized thatmussel diversity and abundance decreased between1978 and 1997 in the three largest rivers in the MeramecRiver basin Trends in diversity and abundance ofmussels particularly Missouri Species of ConservationConcern (SOCC which includes federal and statethreatened or endangered species) were summarizedby river and individual sites

Methods

Study areaThe study area (10255 km2) included the Meramec

River and two major tributaries the Bourbeuse River andthe Big River in the Ozark Plateau Province in east-central Missouri (Figure 1) The Meramec River flowsnortheast for 351 km from the Salem Plateau of theOzark Highlands to the Mississippi River downstream ofSt Louis Missouri The watershed of the upper Meramec(upstream of River Mile [RM] 95) is primarily forest andpasture with little urbanization whereas the lower basinis heavily populated The lower Meramec River is widerand flows more slowly than the upper river and itsextreme lower reaches are influenced by backflows ofthe Mississippi River The Bourbeuse River lies to thenorth of the Meramec River and flows northeast 240 kmthrough a largely rural area until reaching the MeramecRiver at RM 68 The Bourbeuse is considered a lowlandriver with normally high turbidity and the watershed isprimarily forest (55) and pasture (32 Homer et al2004) The Big River lies southeast of the Meramec Riverand flows north 225 km until reaching the Meramec Riverat RM 38 Land use in the Big River drainage is primarilyforest (72) and pasture (16) but the lower basin isbecoming rapidly urbanized Degradation of habitat andbiota including mussels due to historical mining in theBig River watershed has been well-documented (egBesser et al 2009b Roberts et al 2009 Allert et al 2010)

Sampling methodsBuchanan (1980) surveyed mussels at 198 sites in

1977ndash1978 (henceforth referred to as 1978) to determinethe distribution relative abundance and habitat require-ments for mussel species with an emphasis on fourSOCC (Cumberlandia monodonta Cyprogenia abertiLampsilis abrupta Leptodea leptodon) known or suspect-ed to occur in the Meramec River basin Streams weresampled every 8 km (5 miles) unless access was restrictedor mussels were absent at two consecutive sites

Roberts and Bruenderman (2000) surveyed mussels at50 sites in the Meramec River (n = 28) Bourbeuse River(n = 17) and Big River (n = 5) in 1997 Sites wherecurrently listed SOCC were found in the 1978 surveywere resampled along with new sites to updateknowledge of the status of the mussel fauna in theMeramec River basin (Roberts and Bruenderman 2000Figure 1) The two surveys used similar methodology toallow for comparisons Briefly sampling during bothsurveys was carried out by timed qualitative searcheswith the primary objective to locate rare and endangered

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mussel species over a broad spatial scale a design notuncommon to state and federal management agenciesMussels were collected by hand while snorkelingwading and diving We attempted to match samplingeffort (person-hours) of the 1978 survey for each site(expressed as catch per unit effort [CPUE] see below)Sampling effort (ie time spent sampling individual sites)differed between surveys which can lead to bias inspecies richness estimates (eg Huang et al 2011) butthe lower sampling effort for a site was not consistentbetween surveys In 1997 the entire sampling area of the1978 survey was searched If no mussels or suitablehabitat were encountered in 1997 sampling crewsmoved on to other sites rather than continuing tosearch unoccupied habitat for the mere purpose ofmatching 1978 sampling efforts (Roberts and Bruender-man 2000) Mussels were identified classified as livingdead weathered or subfossil and returned to thesubstrate The number of living individuals of eachspecies was recorded Sites were identified by river mile(eg RM 69) as opposed to metric units to facilitatecomparison with sample locations evaluated in previouspublications (Buchanan 1980 Roberts and Bruenderman2000) Results of these surveys have bias because

qualitative searches are more likely to locate musselspecies that are large surface-dwelling and havedistinctive shell sculpture than species that are smalldeeply buried and smooth-shelled (Vaughn et al 1997Strayer and Smith 2003) The seasonal vertical migrationof freshwater mussels (eg Perles et al 2003) may affectthe detectability of individual species However allsurveys were conducted during seasons consideredoptimal for observing freshwater mussel populations inMissouri (from spring through autumn) when watertemperature and photoperiod differ minimally in theMeramec River basin and during periods of low flowthereby minimizing the effects water clarity and depthwould have on detectability between the surveys

Several sites were resampled opportunistically atirregular intervals after 1997 (Figure 1) to search formussel broodstock for artificial propagation research(eg Barnhart 2009) Sites resampled after 1997 com-prising the Meramec RM 69 335 and 398 BourbeuseRM 246 539 and 663 and Big RM 103 627 and 657were included in this paper to evaluate temporal trendsof mussel distribution and abundance These additionalcollections used the same methodologies described forthe 1978 and 1997 surveys except sampling times were

Figure 1 Meramec River basin (Missouri) map showing sites sampled for freshwater mussels in 1978 and 1997 (gray boxes) andthose resampled after 1997 (black circles)

Mussel Trends in the Meramec River Basin JE Hinck et al

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not always similar During post-1997 collections theentire area identified as the mussel bed in 1978 and 1997was searched and all species and individuals encoun-tered were recorded Additional areas that may harbormussels but were possibly not sampled during 1978were also searched to maximize the likelihood ofencountering rare species

Data analysesWe used mussel survey data to estimate community

characteristics at individual sites (Data S1 SupplementalMaterial) We revised taxonomy where necessary tofollow current usage Metrics that we analyzed includedspecies richness CPUE (musselsperson-hour) and Shan-non diversity index (Shannon 1948) We calculatedcolonization proportion (Pc) and extirpation proportion(Pe) for each species and analyzed them by taxa (Vaughn2012) For each species colonization was the number ofsites colonized between 1978 and 1997 divided by thetotal number of sites unoccupied in 1978 Extirpationwas the number of sites that were occupied in 1978 onlydivided by the total number of occupied sites (1978occurrences plus 1997 occurrences) Examination ofrichness and CPUE data revealed that mussels inMeramec River between RM 284 and 595 were generallymore abundant and diverse than in other reaches in theMeramec River in 1997 Therefore we evaluated Pc andPe in these reaches separately (Table S1 SupplementalMaterial) Community composition metrics includedrelative abundance of SOCC and common species(Actinonaias ligamentina Amblema plicata) which weregenerally ubiquitous and abundant throughout theMeramec River basin We also computed the relativeabundances of certain taxa Nonnative Asian clams(Corbicula fluminea) were found at most sites but werenot included in the data analysis

We compared the CPUE between two groups ofspecies those in the tribe Lampsilini and those in thetribes Amblemini + Pleurobemini + Quadrulini (APQtaxa) We compared these two groups because of theirdiffering life histories and perceived differences in theirresponses to stress Lampsilini generally have relativelythin shells and are mobile Most lampsilines maturerapidly (within 2ndash3 y) are long-term brooders and aregenerally short-lived (10 y Haag and Rypel 2011) TheAPQ taxa are relatively heavy-shelled and less mobile asadults The APQ taxa are also slower to reach sexualmaturity (3 y) are short-term brooders and longerlived (several decades Haag and Rypel 2011) Healthymussel communities in the Mississippi River basingenerally have approximately equal numbers of Lampsi-lini and APQ taxa and skewed ratios of these taxa mayindicate a problem (H Dunn Ecological Specialists Incpersonal communication) The APQ taxa appear to bemore tolerant than Lampsilini of temperature changessiltation or water quality degradation (eg Tetzloff2001)

We performed statistical analyses with Version 92 ofthe Statistical Analysis System (SAS Institute Cary NC)Only sites sampled in 1978 and 1997 were included inthe data analysis We calculated arithmetic means and

standard errors for community metrics by river andsurvey year and we evaluated differences using thenonparametric KruskalndashWallis test Community charac-teristics for sites resampled after 1997 were calculatedbut not tested statistically because of the variation insampling effort and limited number of sites howevertrends are described Additional distribution abundanceand diversity data for individual species and at individualsites are presented as supplemental information (FigureS1 Tables S1ndashS3 Supplemental Material)

Results

Community metric differences among rivers andbetween qualitative surveys

Species richness was lower in 1997 than in 1978 in theMeramec Bourbeuse and Big rivers (Table 1 Figure S1Supplemental Material) The differences were significantin the Meramec River (H = 784 P 001) and BourbeuseRiver (H = 1816 P 001) but not in the Big River (H =110 P = 029) which had the smallest number of sites(n = 5) Species richness was significantly greater in theBourbeuse River than in the Meramec River (H = 436P = 004) and Big River (H = 714 P 001) in 1978 butspecies richness did not differ among the three rivers in1997 (Table 1) Within the Big River most species werefound at RM 48 and 103 in 1997 with other sitescontributing little to richness (Figure S1 SupplementalMaterial)

The CPUE was lower in 1997 compared with 1978 in allrivers but was only significantly lower in the BourbeuseRiver (H = 1422 P 001 Table 1 Figure S1Supplemental Material) Among the three rivers theCPUE was significantly lower in Meramec River than inthe Bourbeuse River in 1978 (H = 999 P 001) TheCPUE did not differ among the three rivers in 1997 butwas generally lowest in the Bourbeuse River and BigRiver (Table 1) Local extirpation of living musselcommunities were noted at eight sites resampled in1997 including RM 1024 1065 1252 1451 and 1457in the Meramec River RM 04 in the Bourbeuse River andRM 627 and 1204 in the Big River

Mussel diversity (as Shannon diversity index) wassignificantly lower in 1997 compared with 1978 in theMeramec River (H = 728 P 001) and the BourbeuseRiver (H = 1140 P 001) the difference was notsignificant in the Big River where diversity was low in1978 (Table 1 Figure S1 Supplemental Material) Musseldiversity was significantly lower in the Big River than inthe Bourbeuse River in 1978 (H = 571 P = 002) butdifferences in diversity among the three rivers were notsignificant in 1997 (Table 1)

The percentage of the mussel community representedas SOCC did not differ significantly between surveys inthe Meramec Bourbeuse or Big rivers (Table 1) Howev-er SOCC comprised a significantly greater proportionof the mussel community in the Meramec River thanthe Bourbeuse River in 1978 (H = 1123 P 001) and1997 (H = 568 P = 002 Table 1) Sites with SOCCcomprising the majority of the mussel community in1997 were in the upper Meramec River (RM 1156 to

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1659) where overall species richness was low (Figure S1Supplemental Material) The SOCC exhibiting the mostsevere temporal declines in distributions at historicalsurvey sites are A viridis A confragosus E crassidens Etriquetra F ebena L brittsi L abrupta and S ambigua(Table S2 Supplemental Material)

Relative abundance of APQ taxa and Lampsilini wasnot significantly different between 1978 and 1997 in theMeramec Bourbeuse or Big rivers (Table 1) The APQtaxa comprised a significantly greater proportion of themussel community in the Meramec River than theBourbeuse River in 1978 (H = 1051 P 001) butAPQ abundance was not significantly different amongthe three rivers in 1997 (Table 1 Figure S1 SupplementalMaterial) Lampsilini relative abundance was significantlygreater in the Bourbeuse River than the Meramec River in1978 (H = 1553 P 001) and 1997 (H = 557 P = 002Table 1)

The relative abundance of common species (A plicataand A ligamentina) was lower in 1997 than in 1978 in theMeramec and Bourbeuse rivers but greater in the BigRiver but these differences were not statisticallysignificant (Table 1 Figure S1 Supplemental Material)In 1978 common species abundance was significantly

greater in the Meramec River than in the Bourbeuse River(H = 541 P = 002 Table 1) however differencesamong the three rivers were not significant in 1997

Extirpation and colonizationAveraged across species Pe exceeded Pc at sites in the

Meramec River Bourbeuse River and Big River (Figure 2)The only exception was for Margaritiferidae (C mono-donta) in the Meramec River The Pe among rivers werenot significantly different (H = 455 P = 010) but Pcwas significantly lower in the Bourbeuse River than in theMeramec River (H = 780 P 001) The Pe by taxaranged from 020 to 072 in the Meramec River 055 to100 in the Bourbeuse River and 0 to 068 in the BigRiver The Pc by taxa ranged from 0 to 028 in theMeramec River 0 to 009 in the Bourbeuse River and 0 to031 in the Big River (Figure 2) Differences in Pe and Pcwere significant in the Meramec River for Anodontini(H = 860 P 001) Lampsilini (H = 1996 P 001)Pleurobemini (H = 864 P 001) and Quadrulini (H =466 P = 003 Figure 2) In the Bourbeuse River Pe wassignificantly greater than Pc for Anodontini (H = 1198P 001) Lampsilini (H = 2512 P 001) andPleurobemini (H = 605 P = 001) Differences in the

Table 1 Mean (6SE range in parenthesis) species richness catch per unit effort (CPUE) and Shannon Diversity Index (SDI) formussel surveys in the Meramec River basin Missouri by year Community metrics including the relative abundance of MissouriSpecies of Conservation Concern (SOCC) species in the tribes Amblemini Pleurobemini and Quadrulini (APQ taxa) Lampsilini andcommon species (A plicata A ligamentina) are also presented Values for a parameter within each row followed by the same letterwere not significantly different among sites (P 005 KruskalndashWallis test) For each river 1997 values followed by an asterisk weresignificantly different from 1978 values for individual parameters (P 005 KruskalndashWallis test)

Parameter year Meramec River (n = 28) Bourbeuse River (n = 17) Big River (n = 5)

Species richness

1978 141 6 14 (0ndash28) A 184 6 12 (4ndash24) B 94 6 27 (1ndash16) A

1997 81 6 17 (0ndash26) A 69 6 13 (0ndash18) A 60 6 30 (0ndash15) A

CPUE (musselsperson-hour)

1978 271 6 55 (0ndash112) A 641 6 135 (11ndash238) B 273 6 125 (2ndash70) AB

1997 245 6 81 (0ndash190) A 156 6 47 (0ndash67) A 148 6 98 (0ndash53) A

SDI

1978 174 6 011 (0ndash29) AB 199 6 008 (12ndash25) B 109 6 037 (0ndash21) A

1997 094 6 018 (0ndash25) A 120 6 018 (0ndash22) A 097 6 042 (0ndash20) A

SOCC abundance ()

1978 185 6 38 (0ndash59) B 28 6 09 (0ndash14) A 179 6 113 (0ndash57) AB

1997 301 6 85 (0ndash100) B 42 6 19 (0ndash29) A 153 6 149 (0ndash45) AB

APQ abundance ()

1978 456 6 41 (10ndash100) B 229 6 44 (0ndash36) A 380 6 198 (0ndash94) AB

1997 320 6 64 (0ndash91) A 187 6 50 (0ndash54) A 514 6 159 (20ndash71) A

Lampsilini abundance ()

1978 404 6 38 (0ndash87) A 669 6 42 (35ndash100) B 399 6 163 (5ndash100) AB

1997 453 6 74 (0ndash100) A 719 6 69 (0ndash100) B 477 6 163 (27ndash80) AB

Common species abundance ()

1978 369 6 43 (0ndash71) B 206 6 52 (0ndash59) A 337 6 207 (0ndash91) AB

1997 268 6 59 (0ndash71) A 130 6 38 (0ndash50) A 364 6 193 (0ndash66) A

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Big River were only significant for Anodontini (H = 792P 001 Figure 2)

The Pe and Pc of species within the Meramec Riverwere not consistent with patterns among river reaches(Figure 3) The Pe were consistently lower for all taxabetween RM 284 and 595 (range 0ndash050) compared withupstream (range 014ndash100) and downstream (range025ndash075) reaches differences were significant forAnodontini Lampsilini and Quadrulini (Figure 3) ThePc in the Meramec River were 0ndash031 upstream of RM595 (range 0ndash02 excluding Margaritiferidae) 011ndash035between RM 284 and 595 and 0ndash017 downstream ofRM 284 and these differences among reaches weresignificant for Anodontini Lampsilini and Quadrulini(Figure 3) The Pc was greater than Pe for LampsiliniMargaritiferidae and Quadrulini between RM 284 and595 but these differences were not significant

Species trends at sites resampled after 1997Sites resampled after 1997 generally showed contin-

ued mussel declines (Table 2) Changes in speciesrichness were difficult to assess given the variation insampling times in surveys conducted after 1997However few species were found at Bourbeuse RM246 in 2005 despite lengthy sampling efforts at thesesites (Table 2) Decreases in Shannon diversity index andCPUE were greatest for the most recent collections atMeramec RM 69 and 398 and Bourbeuse RM 246Conversely species richness CPUE Shannon diversityindex and community abundance measures have beenrelatively stable or increasing at Bourbeuse RM 539 andat Big RM 103

The APQ taxa were dominant at Meramec RM 69 andat Big RM 103 while lampsilines were the mostabundant tribe at other sites (Table 2 Figure 4) Relativeabundances of lampsilines and APQ taxa were stable atBig RM 103 while sites upstream were more variable(Table 2) The CPUE for these taxa at individual sites inthe Meramec River basin has fluctuated since 1997 butgenerally shows a decreasing trend (Figure 4) One post-1997 sampling event at Meramec RM 335 had CPUEsgreater than in 1997 Increased CPUE was generally fromthe presence of more Lampsilini (A ligamentina) TheCPUE has remained low at Bourbeuse RM 246 and 539since 1997 The CPUE between 2000 and 2008 hasremained lower than 1997 values in the Big River(Figure 4) Compared with sites in the Meramec andBourbeuse rivers the CPUE was low (8) at RM 627 and657 in the Big River regardless of sampling year

Discussion

Significant decreases in diversity and abundance andincreases in extirpation of species were evident athistorical survey sites in the Meramec River basin apattern that continues to be reported in multiple USriver systems (Warren and Haag 2005 Hanlon et al 2009Wendeln et al 2009 Haag and Warren 2010) Althoughmussel populations in the Meramec River basin appearmore stable in terms of diversity and abundance thanother regions (eg Abell et al 2000) decreases in SOCC

distribution indicate that increased mussel conservationactions in the basin may be warranted

Mussel distribution may change over time with naturalchanges in river morphology Resurveying 1978 sites in1997 cannot account for the formation of new musselhabitat (ie mussel beds) that may have occurred in the20-y time period between surveys the data only reflectchanges at the resurveyed sites New sites surveyed in1997 (Roberts and Bruenderman 2000) provide addition-al insight on mussel occurrence and the status of speciesbut these data cannot be used to determine whethernew beds have been formed The loss of entire musselbeds at eight sites in 20 y is a cause for concern to

Figure 2 Mean (6SE) extirpation (gray bar) and colonization(white hatched bar) proportions of freshwater mussel speciesby taxa and river in the Meramec River basin Missouri between1978 and 1997 Asterisks denote significant differencesbetween extirpation and colonization proportions within eachtaxa (P 005 KruskalndashWallis test) Missing bars indicate aproportion of zero unless otherwise noted Ambl AmbleminiAnod Anodontini Lamp Lampsilini Marg MargaritiferidaePleur Pleurobemini Quad Quadrulini

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resource managers because the natural process ofmussel bed formation would be slower These sites thatsupported diverse mussel beds in 1978 were found tohave unsuitable habitat in 1997 fine loosely packedgravel lack of any coatings of algae or diatoms on gravel(indicating that gravel is actively moving) and lack offiner substrates were observed in 1997 (Roberts andBruenderman 2000) Collection of mussels has not beenattempted at any of these eight sites since 1997

Mussels are being extirpated at historical samplingsites more rapidly than colonization is occurring Thistrend does not appear to be species related becausedifferences between Pe and Pc were significant for alltaxa High Pe values in part were related to lowpopulation sizes of species in 1978 (Gotelli 2001)Vaughn (2012) determined that local extirpation ofmussels over an 80-y time period in the Red Riverdrainage of Oklahoma and Texas was greatest in rarespecies and lowest in highly abundant species Rarespecies in the Meramec River basin did have high Pe

but extirpation at historical sampling sites was also highin abundant species including A plicata A ligamentinaL cardium P alatus and E dilatata Despite differencesin species composition and time between surveys Peand Pc of mussels in the Meramec River basin weresimilar to those reported by Vaughn (2012) Anexception to these trends occurred in the MeramecRiver between RM 284 and 595 where colonizationwas greater than extirpation for Anodontini Lampsiliniand Quadrulini

The three surveyed rivers of the Meramec River basindiffered in mussel composition and abundance but mostspecies were found at fewer sites and in lower numbersin 1997 compared with 1978 regardless of the riverAmblema plicata and A ligamentina commonly consid-ered to be habitat generalists dominated mussel-assemblage composition at most sites in the MeramecBourbeuse and Big rivers Mussels were most diverseand abundant in the Meramec River between RM 284and RM 595 while relatively few mussels were found in

Figure 3 Mean (6SE) extirpation and colonization proportions of freshwater mussel species by taxa and reach of Meramec RiverMissouri between 1978 and 1997 Letters on top of bars indicated that colonization or extirpation were significantly different withineach taxa (P 005 KruskalndashWallis test) Missing bars indicate a proportion of zero unless otherwise noted Ambl Amblemini AnodAnodontini Lamp Lampsilini Marg Margaritiferidae Pleur Pleurobemini Quad Quadrulini

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Table 2 Summary of sampling time (minutes) species richness catch per unit effort (CPUE musselsperson-hour) ShannonDiversity Index (SDI) relative abundance () of Missouri Species of Conservation Concern (SOCC) species in the tribes AmbleminiPleurobemini and Quadrulini (APQ taxa) Lampsilini and common species (A plicata A ligamentina) in mussel surveys at specificriver mile (RM) locations in the Meramec River basin Missouri from 1978 to 2008

Site yearSampling

timeSpeciesrichness CPUE SDI

Relative abundance

SOCC APQ taxa LampsiliniCommon

species

Meramec River RM 69

1978 690 19 599 169 10 85 12 46

1997 900 13 281 133 21 91 7 64

2000 75 4 48 133 167 83 0 33

Meramec River RM 335

1978 1380 24 361 199 81 64 26 46

1997 1395 24 144 245 165 24 64 30

2002 90 10 153 225 130 48 43 22

2003 180 13 400 171 50 20 79 62

2007 240 8 75 139 67 30 70 73

Meramec River RM 398

1978 490 23 687 190 54 44 56 65

1997 990 22 362 189 27 29 71 66

2007 240 2 15 064 0 0 100 67

Bourbeuse River RM 246

1978 390 18 491 206 28 11 73 11

1997 310 12 89 210 44 7 70 2

2005 240 2 10 056 00 0 25 0

Bourbeuse River RM 539

1978 125 22 2381 239 34 40 53 27

1997 130 18 669 181 55 29 68 50

2001 400 20 236 242 51 49 45 15

2002 75 8 168 189 00 57 33 5

2005 300 20 418 203 96 29 67 40

Bourbeuse River RM 663

1978 510 21 465 222 10 45 50 11

1997 340 17 480 214 63 39 57 38

2008 120 8 350 178 00 46 54 34

Big River RM 103

1978 600 13 700 054 03 94 5 91

1997 300 15 526 169 08 71 27 66

2002 102 8 271 140 00 63 37 76

2007 110 11 404 166 14 66 34 66

2008 300 16 364 167 17 73 26 66

Big River RM 627

1978 150 6 84 143 571 10 29 00

1997 240 0 00 000 00 0 0 00

2008 250 1 02 000 00 0 100 100

Big River RM 657

1978 105 1 11 000 0 0 100 0

1997 160 4 75 119 45 20 80 0

2008 150 2 08 069 50 50 50 0

Mussel Trends in the Meramec River Basin JE Hinck et al

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the upper Meramec River and the upper Big River Thedifferences in mussel diversity and abundance amongrivers could be attributed to several factors includingdifferences in geology water flow water depth sub-strate sedimentation fish host assemblages and waterquality Loss of mussels in the upper Meramec Rivermay be related to gravel routing the process whereaccumulations of excess bed load move downstream andcause channel instability (Jacobson and Gran 1999) or tolack of fish hosts The low abundance and diversity ofmussels in the Big River coincide with mining impacts inthe upper basin (Roberts et al 2009) Besser et al (2009a2009b) reported that the metal-contaminated sedimentscollected from the Big River were toxic to mussels inlaboratory tests Further declines of mussel assemblagesin the lower Big River may be expected if mine wastescontinue to move downstream (Roberts et al 2009)Mine wastes moving out of the Big River and into theMeramec River also are a concern for resource managersbecause of the diverse mussel assemblages in theMeramec River downstream from its confluence withthe Big River

Given our current understanding of mussel diversityand abundance in the Meramec River basin severallocations could be considered for further evaluation tounderstand the reason they have maintained therelatively robust mussel communities historically presentMussel assemblages found in the Meramec Riverbetween RM 284 and RM 595 were generally morediverse and abundant compared with other areas bothupstream and farther downstream based on 1997collections This reach is one of the few in the basinwhere species colonization has exceeded extirpationThe exact reasons that mussel diversity and abundancehave remained robust in this reach is uncertain but it hasa considerable amount of anthropogenic impact bothinstream and in the adjacent watershed from miningcommercial and residential development stormwaterinputs and increased bed-load movement The reach isassociated at least in part with increased gradients fewlong pools and bluff faces that provide stability Multiplefactors may be influencing mussel assemblages givendifferences in Pe and Pc in other reaches of the MeramecRiver

Figure 4 Change in catch per unit effort (CPUE) by mussel taxa at 1978 sites in the Meramec River basin Missouri resampled after1997 RM river mile

Mussel Trends in the Meramec River Basin JE Hinck et al

Journal of Fish and Wildlife Management | wwwfwspubsorg December 2012 | Volume 3 | Issue 2 | 327

Several factors are suspected to have contributed tomussel declines in the Meramec River basin The loss ofriparian vegetation is the primary source of excesssedimentation in the basin resulting in increasedoverland erosion water temperatures stream bederosion and degradation channel degradation andaltered stream geomorphology (Roberts and Bruender-man 2000) Therefore restoring and protecting existingriparian habitats especially in the headwaters may helpto protect mussel populations in the Meramec Riverbasin Restoration efforts are currently underway in thebasin to reforest 50ndash100-foot buffer areas and limitlivestock watering areas along streams to improveaquatic habitat (K Flores Missouri Department ofConservation personal communication) The MeramecRiver basin has 31 active permits for in-stream sand andgravel mining with most concentrated in the MeramecRiver other in-stream sand and gravel mining isconducted by individuals for personal use or politicalsubdivisions (eg county highway departments) whichdoes not require permits It is unknown what effectgravel mines have had on mussel assemblages in theMeramec River basin but they have been directlyimplicated in the local extirpation of mussel communitiesfrom reaches of the Osage River in central Missouri(Grace and Buchanan 1981) Grace and Buchanan (1981)also reported that turbidity significantly increased andchannel depth was altered downstream of sand andgravel dredging operations Limiting the effects of in-stream sand and gravel mining could help reducesubstrate instability bank erosion sedimentation pol-lutant release (Brown et al 1998 Hubbs et al 2006) andthe risk of physical habitat changes to existing musselbeds

Protecting water quality in the Meramec River basin isalso an important consideration for mussel conservationStudies to determine water-quality needs for musselshave been conducted and interpreted relative toconservation of populations in the Meramec River (Hincket al 2011) However parameters including temperaturepH alkalinity hardness dissolved oxygen turbidityconductivity ammonia nitrates and sulfates have beenmeasured only occasionally at mussel assemblages in thebasin (Roberts and Bruenderman 2000) More studies areneeded to determine the extent to which water quality isa limiting factor (Hinck et al 2011) The mining of heavymetals has negatively impacted biota in the Big Riverwhere zinc lead and cadmium deposited in streambedsediments have accumulated in biota downstream of themining district (Besser et al 2009b Roberts et al 2009Allert et al 2010) The failure of tailing pond damscontinual erosion of tailing piles and exposure to con-taminated sediments have eliminated much of thebenthic community including mussel populations inthe Big River (Schmitt et al 1987 Besser et al 2009a2009b Roberts et al 2009) Quantitative chemical-contaminant data specific to mussels in the Big Riverare limited to lead and cadmium concentrations in Lcardium (Czarnezki 1987 Schmitt et al 1987) In additionto lead mining contaminants from other point (egwastewater treatment plant) and nonpoint pollution

(eg urban and agricultural runoff) can also impact waterquality in the Meramec River basin Based on thetoxicological literature mussels are particularly sensitiveto ammonia copper zinc lead certain pesticidespharmaceuticals and personal care products (Augspur-ger et al 2007 Wang et al 2010 2011a 2011b)monitoring these compounds in water could be aconservation priority in the basin

Invasive species may also affect mussels in the basin Cfluminea is found in the Meramec Bourbeuse and Bigrivers and Dreissena polymorpha has been found in thelower Meramec River Researchers have hypothesizedthat invasive species may compete with native musselspecies for food and habitat (Neves 1987 Ricciardi 2003)introduce diseases and parasites (Neves 1987 Ricciardi2003) and directly affect native mussels because ofincreased ammonia production (Cherry et al 2005Cooper et al 2005) Programs to monitor invasivespecies in the Meramec River basin have not beenestablished Monitoring and controlling invasive speciescould be considered when developing strategies toprotect mussel diversity and density in the basin

Overall the loss of species and assemblages from 1978to 1997 is cause for concern to federal and state agenciesresponsible for mussel conservation in the MeramecRiver basin because local extirpation is not species-specific and is occurring at a relatively high rate The lossappears to be driven by physical habitat changesincluding bank erosion unstable substrates and sedi-mentation as well as chemical contamination frommining Further loss of mussel diversity and abundancemay be exacerbated if fish host assemblages changeinvasive species become established or water qualitydegrades Ultimately ecological problems in the head-waters of the basin need to be identified and remediedfor the long-term conservation of mussels throughoutthe Meramec River basin

Supplemental Material

Please note The Journal of Fish and Wildlife Managementis not responsible for the content or functionality of anysupplemental material Queries should be directed to thecorresponding author for the article

Figure S1 Comparison of mussels collected in 1978(gray) and 1997 (black) in the Meramec River basinMissouri Parameters include species richness catch perunit effort (CPUE) Shannon diversity index (SDI) relativeabundance of Missouri state species of conservationconcern (SOCC) relative abundance of common species(A plicata A ligamentina) and relative abundance ofLampsilini and species in the tribes Amblemini Pleur-obemini and Quadrulini (APQ taxa)

Table S1 Extirpation proportion (Pe) and coloniza-tion proportion (Pc) of unionid mussels in the MeramecRiver basin Missouri found in the Meramec Riverdownstream of RM 284 (n = 4) Meramec River betweenRM 284 and 595 (n = 8) and Meramec River upstream ofRM 595 (n = 16) Bourbeuse River (n = 17) and Big River(n = 5) based on qualitative survey data from 1978(Buchanan 1980) and 1997 (Roberts and Bruenderman

Mussel Trends in the Meramec River Basin JE Hinck et al

Journal of Fish and Wildlife Management | wwwfwspubsorg December 2012 | Volume 3 | Issue 2 | 328

2000) Bold values indicate that Pc was greater than Pefor the species

Table S2 Historical distribution of Missouri species ofconservation concern (SOCC) by river mile (RM) in theMeramec River basin Plain text species present in 1978only bold text species present after 1978 underlinedtext species not present in 1978 Footnotes indicate themost recent observation at sites resampled after 1997(Meramec RM 69 335 and 398 Bourbeuse RM 246539 and 663 Big RM 103 627 and 657) bolded sitenumbers with no associated footnote indicate that thespecies was last observed in 1997 The mean speciesrichness at a site with each SOCC is also presented (rangein parenthesis)

Table S3 Unionid mussels found in the MeramecRiver (n = 28) Bourbeuse River (n = 17) and Big River (n= 5) of the Meramec River basin Missouri based onqualitative survey data from 1978 (Buchanan 1980) and1997 (Roberts and Bruenderman 2000) Data presentedinclude the number of sites where the individuals werefound the number of individuals collected and the catchper unit effort (CPUE musselsperson-hour)

Supplemental Figure and Tables found at DOI httpdxdoiorg103996052012-JFWM-038S1 (114 KB DOCX)

Data S1 Field data from 1977 to 1978 and 1997surveys conducted in the Meramec Big and Bourbeuserivers Missouri sites were sampled for freshwatermussels

Found at DOI httpdxdoiorg103996052012-JFWM-038S2 (3415 KB XLSX)

Reference S1 Barnhart MC 2009 Propagation ofendangered native mussels for research and recoveryFinal Report completed for Missouri Department ofConservation and US Fish and Wildlife Service Colum-bia Missouri

Found at DOI httpdxdoiorg103996052012-JFWM-038S3 (389 KB PDF)

Reference S2 Besser JM Brumbaugh WG HardestyDK Hughes JP Ingersoll CG 2009b Assessment of metal-contaminated sediments from the Southeast Missouri(SEMO) mining district using sediment toxicity tests withamphipods and freshwater mussels Report submitted toUS Fish and Wildlife Service Columbia Missouri

Found at DOI httpdxdoiorg103996052012-JFWM-038S4 (1095 KB PDF)

Reference S3 Grace TB Buchanan AC 1981 Naiades(mussels) of the lower Osage River Tavern Creek andMaries River Missouri Jefferson City Missouri MissouriDepartment of Conservation

Found at DOI httpdxdoiorg103996052012-JFWM-038S5 (7005 KB PDF)

Reference S4 Hinck JE Ingersoll CG Wang NAugspurger T Barnhart MC McMurray SE Roberts ADSchrader L 2011 Threats of habitat and water-qualitydegradation to mussel diversity in the Meramec Riverbasin Missouri USA US Geological Survey Open-FileReport 2011ndash1125

Found at DOI httpdxdoiorg103996052012-JFWM-038S6 also available at httppubsusgsgovof20111125(504 KB PDF)

Reference S5 Missouri Department of Conservation2008 Missouri mussel conservation and managementplan Columbia Missouri Missouri Department of Con-servation Resource Science Division

Found at DOI httpdxdoiorg103996052012-JFWM-038S7 (1291 KB PDF)

Reference S6 Neves RJ 1987 Recent die-offs offreshwater mussels in the United States an overviewPages 7ndash18 in Neves RJ editor Proceedings of theworkshop on die-offs of freshwater mussels in the UnitedStates Blacksburg Virginia Virginia Tech Press

Found at DOI httpdxdoiorg103996052012-JFWM-038S8 (130 KB PDF)

Reference S7 Roberts AD Bruenderman S 2000 Areassessment of the status of freshwater mussels in theMeramec River basin Missouri Jefferson City MissouriMissouri Department of Conservation

Found at DOI httpdxdoiorg103996052012-JFWM-038S9 (9674 KB PDF)

Reference S8 Roberts AD Mosby D Weber J Besser JHundley J McMurray SE Faiman JS 2009 An assessment offreshwater mussel (Bivalvia Margaritiferidae and Unionidae)populations and heavy metal sediment contamination in theBig River Missouri US Fish and Wildlife Service USGeological Survey and Missouri Department of Conserva-tion Columbia Missouri

Found at DOI httpdxdoiorg103996052012-JFWM-038S10 (3057 KB PDF)

Reference S9 Schmitt CJ Finger SE May TW KaiserMS 1987 Bioavailability of lead and cadmium from minetailings to the pocketbook mussel (Lampsilis ventricosa)Pages 115ndash142 in Neves RJ editor Rock Island IllinoisProceedings of the Workshop on Die-offs of FreshwaterMussels in the United States

Found at DOI httpdxdoiorg103996052012-JFWM-038S11 (3 MB PDF)

Acknowledgments

Funding for this project was provided by Area StrategicIntegrated Science and Technology Funds of the USGeological Survey

J Scott Faiman Jen Girondo and Kevin Meneauprovided additional information on native mussels in theMeramec River basin and Aaron Garringer produced themap Lynn Schrader helped with initial project coordina-tion Barry Poulton Christopher Schmitt two anonymousreviewers and the journal Subject Editor reviewed earlierdrafts of this paper

Any use of trade product or firm names is fordescriptive purposes only and does not imply endorse-ment by the US Government

References

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Mussel Trends in the Meramec River Basin JE Hinck et al

Journal of Fish and Wildlife Management | wwwfwspubsorg December 2012 | Volume 3 | Issue 2 | 329

Allert AL DiStefano RJ Fairchild JF Schmitt CJ Brum-baugh WG 2010 Effects of mining-derived metals oncrayfish in the Big River of southeast Missouri MissouriDepartment of Conservation Science Notes 51

Annis GM Diamond DD Garringer AJ 2009 Stream-reach specific watershed data threats to aquaticecosystem integrity Jefferson City Missouri FinalReport and Data for Missouri Department ofNatural Resources Available httpmorapmissourieduPublicationsaspxPublicationId = 60 (July 2012)

Augspurger T Dwyer FJ Ingersoll CG Kane CM 2007Editorial advances and opportunities in assessing thecontaminant sensitivity of freshwater mussel early lifestages Environmental Toxicology and Chemistry 262025ndash2028

Barnhart MC 2009 Propagation of endangered nativemussels for research and recovery Final ReportColumbia Missouri Missouri Department of Conser-vation and US Fish and Wildlife Service (seeSupplemental Material Reference S1 httpdxdoiorg103996052012-JFWM-038S3)

Besser JM Brumbaugh WG Allert AL Schmitt CJIngersoll CG 2009a Ecological impacts of lead miningon streams of the Missouri Ozarks toxicity of wholesediment and pore water Ecotoxicology and Environ-mental Safety 72516ndash526

Besser JM Brumbaugh WG Hardesty DK Hughes JPIngersoll CG 2009b Assessment of metal-contaminatedsediments from the Southeast Missouri (SEMO) miningdistrict using sediment toxicity tests with amphipodsand freshwater mussels Columbia Missouri Reportsubmitted to US Fish and Wildlife Service (seeSupplemental Material Reference S2 httpdxdoiorg103996052012-JFWM-038S4)

Besser JM Brumbaugh WG May TM Schmitt CJ 2007Biomonitoring of lead zinc and cadmium in streamsdraining lead-mining and non-mining areas southeastMissouri Environmental Monitoring and Assessment129227ndash241

Brown AV Lyttle KB Brown KB 1998 Impacts of gravelmining on gravel bed streams Transactions of theAmerican Fisheries Society 127979ndash994

Buchanan AC 1980 Mussels (Naiades) of the MeramecRiver basin Missouri Missouri Department of Conser-vation Aquatic Series 17

Carter JG Altaba CR Anderson LC Araujo R Biakov ASBogan AE Campbell DC Campbell M Jin-hua C CopeJCW Delvene G Dijkstra HH Zong-jie F Gardner RNGavrilova VA Goncharova IA Harries PJ Hartman JHHautmann M Hoeh WR Hylleberg J Bao-yu JJohnston P Kirkendale L Kleemann K Koppka J KrızJ Machado D Malchus N Marquez-Aliaga A Masse JPMcRoberts CA Middelfart PU Mitchell S NevesskajaLA Ozer S Pojeta J Jr Polubotko IV Pons JM PopovS Sanchez T Sartori AF Scott RW Sey II Signorelli JHSilantiev VV Skelton PW Steuber T Waterhouse JBWingard GL Yancey T 2011 A synoptical classificationof the Bivalvia (Mollusca) University of Kansas

Paleontological Institute Paleontological Contribu-tions 41ndash47

Cherry DS Scheller JL Cooper NL Bidwell JR 2005Potential effects of Asian clam (Corbicula fluminea)die-offs on native freshwater mussels (Unionidae) Iwater-column ammonia levels and ammonia toxicityJournal of the North American Benthological Society24369ndash380

Cooper NL Bidwell JR Cherry DS 2005 Potential effectsof Asian clam (Corbicula fluminea) die-offs on nativefreshwater mussels (Unionidae) II porewater ammo-nia Journal of the North American BenthologicalSociety 24381ndash394

Czarnezki JM 1985 Accumulation of lead in fish fromMissouri streams impacted by lead mining Bulletin ofEnvironmental Contamination and Toxicology 34736ndash745

Czarnezki JM 1987 Use of the pocket mussel Lampsilisventricosa for monitoring heavy metal pollution in anOzark stream Bulletin of Environmental Contamina-tion and Toxicology 38641ndash646

[ESA] US Endangered Species Act of 1973 as amended PubL No 93ndash205 87 Stat 884 16 USC 1531 et seq (Dec28 1973) Available httpwwwfwsgovendangeredesa-librarypdfESAallpdf

Gale NL Adams CD Wixson BG Loftin KA Huang Y 2002Lead concentrations in fish and river sediments in theold lead belt of Missouri Environmental Science andTechnology 364262ndash4268

Gotelli NJ 2001 A Primer of Ecology Sunderland MASinauer

Grace TB Buchanan AC 1981 Naiades (mussels) of thelower Osage River Tavern Creek and Maries RiverMissouri Jefferson City Missouri Missouri Departmentof Conservation (see Supplemental Material ReferenceS3 httpdxdoiorg103996052012-JFWM-038S5)

Haag WR 2009 Past and future patterns of freshwatermussel extinctions in North America during theHolocene Pages 107ndash128 in Turvey ST editor Holoceneextinctions Oxford UK Oxford University Press

Haag WR Rypel AL 2011 Growth and longevity infreshwater mussels evolutionary and conservationimplications Biological Reviews 86225ndash247

Haag WR Warren ML Jr 2010 Diversity abundance andsize structure of bivalve assemblages in the SipseyRiver Alabama Aquatic Conservation Marine andFreshwater Ecosystems 20655ndash667

Hanlon SD Petty MA Neves RJ 2009 Status of nativefreshwater mussels in Copper Creek Virginia South-eastern Naturalist 81ndash18

Hinck JE Ingersoll CG Wang N Augspurger T BarnhartMC McMurray SE Roberts AD Schrader L 2011Threats of habitat and water-quality degradation tomussel diversity in the Meramec River basin MissouriUSA US Geological Survey Open-File Report 2011ndash1125 (see Supplemental Material Reference S4 httpdxdoiorg103996052012-JFWM-038S6) also avail-able httppubsusgsgovof20111125

Mussel Trends in the Meramec River Basin JE Hinck et al

Journal of Fish and Wildlife Management | wwwfwspubsorg December 2012 | Volume 3 | Issue 2 | 330

Homer C Huang C Yang L Wylie B Coan M 2004Development of a 2001 National Landcover Databasefor the United States Photogrammetric Engineeringand Remote Sensing 70829ndash840

Huan J Cao Y Cummings KS 2011 Assessing samplingadequacy of mussel diversity in wadeable Illinoisstreams Journal of the North American BenthologicalSociety 20923ndash934

Hubbs D McKinney D Sims D Lanier S Black P 2006Aggregate extraction impacts on Unionid musselspecies richness and density Proceedings of theAnnual Conference of Southeastern Association ofFish and Wildlife Agencies 60169ndash173

Jacobson RB Gran KB 1999 Gravel routing fromwidespread low-intensity landscape disturbance Cur-rent River basin Missouri Earth Surf Processes andLandforms 24897ndash917

Lydeard C Cowie R Ponder W Bogan A Bouchet P ClarkS Cummings KS Frest TJ Gargominy O Herbert DGHershler R Perez KE Roth B Seddon MB Strong EEThompson FB 2004 The global decline of nonmarinemollusks BioScience 54321ndash330

Missouri Department of Conservation 2008 Missourimussel conservation and management plan ColumbiaMissouri Missouri Department of Conservation Re-source Science Division (see Supplemental MaterialReference S5 httpdxdoiorg103996052012-JFWM-038S7)

Neves RJ 1987 Recent die-offs of freshwater mussels inthe United States an overview Pages 7ndash18 in NevesRJ editor Proceedings of the workshop on die-offs offreshwater mussels in the United States BlacksburgVirginia Virginia Tech Press (see Supplemental Mate-rial Reference S6 httpdxdoiorg103996052012-JFWM-038S8)

Niethammer KR Atkinson RD Baskett TS Samson FB1985 Metals in riparian wildlife of the lead miningdistrict of southeastern Missouri Archives of Environ-mental Contamination and Toxicology 14213ndash223

Perles SJ Christian AD Berg DJ 2003 Vertical migrationorientation aggregation and fecundity of the fresh-water mussel Lampsilis siliquoidea Ohio Journal ofScience 103(4)73ndash78

Ricciardi A 2003 Predicting the impacts of an introducedspecies from its invasion history an empirical ap-proach applied to zebra mussel invasions FreshwaterBiology 48972ndash981

Roberts AD Bruenderman S 2000 A reassessment of thestatus of freshwater mussels in the Meramec Riverbasin Missouri Jefferson City Missouri MissouriDepartment of Conservation (see Supplemental Mate-rial Reference S7 103996052012-JFWM-038S9)

Roberts AD Mosby D Weber J Besser J Hundley JMcMurray SE Faiman JS 2009 An assessment offreshwater mussel (Bivalvia Margaritiferidae andUnionidae) populations and heavy metal sedimentcontamination in the Big River Missouri US Fish andWildlife Service US Geological Survey and Missouri

Department of Conservation Columbia Missouri (seeSupplemental Material Reference S8 103996052012-JFWM-038S10)

Schmitt CJ Finger SE May TW Kaiser MS 1987Bioavailability of lead and cadmium from mine tailingsto the pocketbook mussel (Lampsilis ventricosa) Pages115ndash142 in Neves RJ editor Rock Island IllinoisProceedings of the Workshop on Die-offs of Freshwa-ter Mussels in the United States (see SupplementalMaterial Reference S9 httpdxdoiorg103996052012-JFWM-038S11)

Shannon CE 1948 A mathematical theory of communica-tion Bell System Technical Journal 27379ndash423 623ndash656

Strayer DL Smith DR 2003 A guide to samplingfreshwater mussel populations American FisheriesSociety Monographs 81ndash103

Tetzloff J 2001 Survival rates of Unionid speciesfollowing a low oxygen event Ellipsaria 318ndash19

US Fish and Wildlife Service 2011 Summary of listedspecies listed populations and recovery plans Avail-able httpecosfwsgovtess_publicpubBoxscoredo(June 2011)

Vaughn CC 2012 Life history traits and abundance canpredict local colonization and extinction rates offreshwater mussels Freshwater Biology 57982ndash992

Vaughn CC Taylor CN Eberhard KJ 1997 A comparisonof the effectiveness of timed searches vs quadratsampling in mussel surveys Pages 157ndash162 inCummings DS Buchanan AC Koch LM editorsConservation and management of freshwater musselsII Rock Island Illinois Proceedings of an UpperMississippi River Conservation Committee symposium

Wang N Consbrock RA Ingersoll CG Barnhart MC 2011aSensitivity of juvenile freshwater mussels (fatmucketLampsilis siliquoidea) to ammonia in chronic waterexposure with or without the presence of sedimentEnvironmental Toxicology and Chemistry 302270ndash2276

Wang N Ingersoll CG Ivey CD Hardesty DK May TWAugspurger T Roberts AD van Genderen E BarnhartMC 2010 Sensitivity of early life stages of freshwatermussels (Unionidae) to acute and chronic toxicity oflead cadmium and zinc in water EnvironmentalToxicology and Chemistry 292053ndash2063

Wang N Mebane CA Kunz JL Ingersoll CG BrumbaughWG Santore RC Gorsuch JW Arnold WR 2011bInfluence of dissolved organic carbon on the toxicityof copper to a unionid mussel (Villosa iris) and acladoceran (Ceriodaphnia dubia) in acute and chronicwater exposures Environmental Toxicology andChemistry 302115ndash2125

Warren ML Jr Haag WR 2005 Spatio-temporal patternsof the decline of freshwater musses in the Little SouthFork Cumberland River USA Biodiversity and Conser-vation 141383ndash1400

Wendeln KL Runkle JR Watters GT 2009 The freshwatermussels (Unionidae) of Twin Creek Southwest OhioJournal of Freshwater Ecology 24351ndash460

Mussel Trends in the Meramec River Basin JE Hinck et al

Journal of Fish and Wildlife Management | wwwfwspubsorg December 2012 | Volume 3 | Issue 2 | 331