Sources and Distribution of Organic Compounds Using Passive Samplers in Lake Mead
National Recreation Area, Nevada and Arizona, and Their Implications for Potential
Effects on Aquatic Biota
Michael R. Rosen,* David A. Alvarez, Steven L. Goodbred, Thomas J. Leiker, and Reynaldo Patio U.S. Geological Survey
M.R. Rosen, Nevada Water Science Center, U.S. Geological Survey, 2730 N. Deer Run
Copyright 2010 by the American Society of Agronomy, Crop Science Rd., Carson City, NV 89701. D.A. Alvarez, Columbia Environmental Research Center,
Society of America, and Soil Science Society of America. All rights U.S. Geological Survey, 4200 New Haven Rd., Columbia, MO 65201. S.L. Goodbred, U.S.
reserved. No part of this periodical may be reproduced or transmitted Geological Survey, Modoc Hall, 3020 State University Dr. E., Sacramento, CA 95819-
in any form or by any means, electronic or mechanical, including pho- 6129. T.J. Leiker, U.S. Geological Survey, Box 25046, MS 407, Denver, CO 80225-0046;
tocopying, recording, or any information storage and retrieval system, current address: Univ. of Colorado at Denver, Dep. of Pharmacology, 12081 E. 17th
without permission in writing from the publisher. Ave., Aurora, CO 80045. R. Patio, U.S. Geological Survey, Texas Cooperative Fish &
Wildlife Research Unit, Texas Tech Univ., Lubbock, TX 79409-2120.
Published in J. Environ. Qual. 39 (2010).
doi:10.2134/jeq2009.0095 Abbreviations: BB, Boulder basin; BMI, Basic Metals, Incorporated; DDT,
Freely available online through the author-supported open-access option. dichlorodiphenyltrichloroethane; EDC, endocrine-disrupting compound; GB, Gregg
Published online 13 Nov. 2009. Basin; LVB, Las Vegas Bay; LVVD, Las Vegas Valley Drive; OA, Overton Arm; PAH,
Received 11 Mar. 2009. polycyclic aromatic hydrocarbon; PCB, polychlorinated biphenyl; POCIS, polar organic
*Corresponding author (mrosen@usgs.gov). chemical integrative sampler; PRC, performance reference compound; SOC, synthetic
ASA, CSSA, SSSA organic compound; SPMD, semipermeable membrane device; USGS, U.S. Geological
677 S. Segoe Rd., Madison, WI 53711 USA Survey; WB, Willow Beach.
that might not be detected using traditional sampling methods. the concentration of some compounds being significantly reduced
The objective of this paper is to demonstrate the utility of using while other compounds are relatively unaffected.
SPMDs and POCIS for detecting lateral and vertical changes in Semi-permeable membrane devices were deployed in a ver-
concentrations and composition of SOCs within a large reser- tical profile in LVB because, of the three main surface water
voir (hereafter called a lake), Lake Mead, Nevada and Arizona, inputs to the lake (Las Vegas Wash, Virgin/Muddy Rivers, and
USA, that receives different types and amounts of contaminants the Colorado River), LVB was likely to have the highest con-
from various perennial streams and from sources within or on centrations of organic contaminants due to the urban influ-
the lake (Lico and Johnson, 2007). Our hypothesis is that higher ence from Las Vegas Wash. Furthermore, LaBounty and Burns
concentrations of SOCs will be found downstream of munici- (2005) demonstrated that plumes of Las Vegas Wash water
pal and urban sources than areas that do not have urban con- enter LVB at different depths in the water column at different
taminant sources. We hypothesize that these compounds can be times of the year and that these plumes are persistent for some
traced within the lake laterally and vertically. Potential sources of distance into the lake. In the spring, during the time the SP-
contaminants within the Lake Mead National Recreation Area MDs were deployed, Las Vegas Wash water is warmer than the
include urban runoff, regional or local atmospheric deposition, lake but generally enters the bay as bottom flow or interflow
tertiary-treated waste water inflows, urban return-flow discharge because Las Vegas Wash water has higher dissolved solids con-
from ground water, and in-lake combustion from watercraft en- centrations than LVB. This leads to unstable inflow conditions
gines. By deploying passive samplers throughout the water col- of Las Vegas Wash water into Las Vegas Bay at this time of the
umn and throughout the lake at other sites, a better assessment year (LaBounty and Burns, 2005) and indicates that, during
of organic contaminants entering Lake Mead can be determined. deployment of the SPMDs for this study, the position of SOCs
When SPMDs are deployed in lakes, they are generally posi- in the water column may have varied.
tioned only at one depth (Lico and Pennington, 1999; Lico, 2004; Previous investigations dating back to the mid-1990s have
Balmer et al., 2005), which may miss significant concentrations of shown evidence of endocrine disruption in aquatic biota
contaminants if the water column is not fully mixed and if there (mainly common carp [Cyprinus carpio]) in Lake Mead (Bev-
are plumes of high SOC concentrations flowing on the surface or ans et al., 1996; Patio et al., 2003; Leiker et al., 2009) mostly
the bottom. To our knowledge, this is the first time that SPMDs in LVB. However, sources of endocrine-disrupting contami-
have been used at multiple depths (more than two points) in a nants have not been fully determined in these previous studies.
lake. Determining the vertical distribution of SOCs is important This study provides delineation of SOCs sources to LVB and
in determining what parts of the food chain may be affected (ben- delineates SOC sources throughout the Lake Mead National
thic versus pelagic organisms), the fate and transport of SOCs in Recreation Area.
the lake, and the interaction with lake sediments.
Materials and Methods
Setting Semi-permeable membrane devices and POCIS were de-
Lake Mead is the largest reservoir by volume in the USA and ployed in early March 2006 at seven sites for 29 or 30 d (Fig.
was created in 1935 by the construction of Hoover Dam on the 1). Two sites in Las Vegas Wash were selected: one at Las Vegas
lower Colorado River between Nevada and Arizona (Fig. 1). Main Valley Drive (LVVD) upstream of any waste water treatment
inflows to the lake are from three rivers (Colorado, Virgin, and facility inputs and one near the end of the wash (Outlet). Four
Muddy) and from an urban tributary, Las Vegas Wash. Las Vegas sites were selected in Lake Mead: Las Vegas Bay (LVB), Over-
Wash is now perennial because of discharges from three municipal ton Arm (OA), Boulder Basin (BB), and Gregg Basin (GB).
waste water treatment facilities (see Fig. 1 for locations) and ur- A final site, Willow Beach (WB), was located downstream of
ban ground water return-flow discharge from irrigation of grassed Hoover Dam in the Colorado River. The Las Vegas Wash sites
areas within the city of Las Vegas (Covay and Leiker, 1998) and were chosen to bracket inputs upstream and downstream of
natural storm water runoff (Rosen et al., 2006). As the popula- the major municipal inputs (waste water, urban runoff, indus-
tion in the Las Vegas Valley began to increase in the 1940s, the trial inputs). Each site within Lake Mead was chosen to be
amount of treated waste water produced increased and in 1993 representative of potential inputs from each major sub-basin,
constituted about 96% of the annual discharge of Las Vegas Wash and the WB site was chosen to represent the output from the
(Bevans et al., 1996). By 2001, the mean flow of Las Vegas Wash system. Deployment periods varied by up to 1 wk (Table 1)
into Las Vegas Bay (LVB) was about 606,000 m3 d-1 (U.S. Bureau due to the distances involved in deploying the samplers and
of Reclamation, 2001). Waste water entering Las Vegas Wash is access to boats, but length of deployment was consistent (Table
treated to a high standard that includes reduction of nutrients and 1). Three SPMDs (91.4 cm of polyethylene layflat tubing filled
dissolved solids using grit removal, primary sedimentation, acti- with 1 mL of ultra-pure triolein each) and three POCIS (both
vated sludge with nutrient removal, and chemical-enhanced filtra- pharmaceutical and pesticide configurations) were deployed
tion and disinfection, with chlorine addition or ultraviolet light in one stainless steel canister at each site. At the LVVD and
treatment (http://www.nps.gov/lame/parkmgmt/upload/Scope_ Outlet sites, the deployment canisters were attached to metal
FEIS_Chp2.pdf). However, these treatments are not designed to rebar that was pounded into the bottom sediment of the Wash.
eliminate all organic compounds from the effluent, resulting in The canisters were deployed approximately half way between
the surface of the water and the bed of the wash and were sub- anchor the vertical profile gradient study measured the vertical
merged throughout the sampling period. In Lake Mead, all of profiles water quality parameters such as temperature, specific
the canisters were suspended at 8 m depth from US Geologi- conductance, dissolved oxygen, and other parameters at 1-m
cal Survey (USGS) Water Quality Platforms (Rowland et al., intervals every 6 h. One string of SPMDs was deployed at 4,
2006) using a stainless steel cable and u-bolts. The platforms 8, 12, and 18 m depths. The second string of SPMDs was de-
are located in LVB, OA, and BB. Because there were no plat- ployed at 8, 12, and 18 m depth (Fig. 2). The second string
forms at the GB and WB sites, the deployment canisters were of SPMDs deployed at the same depths as the first string was
deployed using a buoy attached to a stainless steel cable. used as a replicate, although one string of SPMDs was about
Semi-permeable membrane devices were deployed in a ver- 4 m from the other on the platform. The deepest SPMD was
tical profile in LVB for 29 d concurrently with the lateral gradi- suspended just above a metal anchor that was placed at the
ent samplers. The USGS-LVB Water Quality Platform used to sedimentwater interface, which was located at 18 m depth.
Table 1. Sampling site identification and dates for the passive sampler deployment.
Site name Abbreviation Deployment date Retrieval date Days deployed
Las Vegas Wash (Las Vegas Valley Drive) LVVD 28 Feb. 2006 28 Mar. 2006 29
Las Vegas Wash (Northshore Drive) Outlet 28 Feb. 2006 28 Mar. 2006 29
Las Vegas Bay LVB 1 Mar. 2006 29 Mar. 2006 29
Boulder Basin BB 1 Mar. 2006 30 Mar. 2006 30
Overton Arm OA 2 Mar. 2006 30 Mar. 2006 29
Gregg Basin GB 7 Mar. 2006 5 Apr. 2006 30
Willow Beach WB 6 Mar. 2006 4 Apr. 2006 30
2009). Extracts from all POCIS samples were concentrated us- a wood treatment chemical (para-cresol); flame retardants (tris
ing a Kuderna-Danish evaporator and high-purity N2 before (chloroethyl) phosphate and others); an anti-rust and corro-
analysis using the GCMS system described above. sion inhibitor (5-methyl-1H-benzotriazole), which is also used
as an anti-freezing agent in cycling cooling water treatment;
Results and Discussion and 3,4-dichlorophenyl isocyanate, which is used to synthe-
size pharmaceuticals, pesticides, and lubricants and is used in
Lateral Distribution of Compounds Detected making plastics. Many of these compounds are from industrial
Las Vegas Wash Sites and urban uses (including the use of pesticides on turf grass)
Concentrations of SOCs and the types of compounds de- that enter Las Vegas Wash by runoff, shallow ground water and
tected in the two Las Vegas Wash samples were somewhat dif- atmospheric inputs, and irrigation with treated waste water
ferent. Although some compounds were found at both sites upstream of the site. The reason for the anomalously high es-
(Tables 3 and 4), the site downstream of the waste water treat- timated concentration (up to 50,000 ng per POCIS) in both
ment facilities generally had higher concentrations and 66% POCIS media of tris (2-butoxyethyl) phosphate (Table 4), a
more detections (35 detections of different SOCs) of those chemical used in flame retardants, is unknown. However, oth-
compounds than at the upstream site (21 detections of differ- er phosphate SOCs used as flame retardants are present, and
ent SOCs). At the LVVD site, the most abundant chemicals the chemicals were not found in the trip or extraction blanks;
measured in the SPMDs were PAHs, pesticides (benfluralin, therefore, the compounds observed are present in the environ-
chlorpyrifos, and trifluralin), and relatively low concentrations ment. One possible source of these compounds is runoff from
of flame retardants and the wood treatment pentachloroanisole areas treated with fire retardants during an urban fire.
(Table 3). Polar organic chemical integrative sampler (Table Caffeine was detected at more than 24 times the estimated
4) detections included fragrances (acetophenone and methyl concentration at the LVVD site (3400 ng per POCIS) com-
salicylate), which may be from natural sources; residues of pes- pared with below the treatment facilities (Outlet site on Fig.
ticide formulations (isoquinoline, 4-tert-octylphenol); caffeine; 1; 530 ng per POCIS) and was detected in LVB at 8 m depth
(140 ng per POCIS). It is not known why caffeine would be tions (34 and 38pg L-1, respectively) at the Outlet site. Chlor-
detected at higher concentrations at the LVVD site compared pyrifos, which was banned from household use as a pesticide
with the downstream site (no caffeine was detected in the in 2001 but is still used in agriculture, was found at the Outlet
blanks), but significant amounts of rubbish and human distur- site at an average concentration of 1000 pg L-1. The source of
bance are present down in and along Las Vegas Wash, and both chorpyrifos is not well controlled, but the US Environmen-
of these factors could be the cause of this detection. tal Protection Agency settled a court case against companies
Overall, the number of different compounds detected in in Nevada in 2007 that were illegally selling home gardening
the POCIS media at the LVVD site was 44% lower (nine com- products that contained chlorpyrifos (http://yosemite.epa.gov/
pounds) than at the Outlet site (16 compounds), although esti- opa/admpress.nsf/2dd7f669225439b78525735900400c31/
mated concentrations were higher at the LVVD site (mostly due d17cb018b06f48c485257394006970d7!OpenDocument).
to the high concentration of tris [2-butoxyethyl] phosphate). Chlorpyrifos was also found at the LVVD site upstream of the
The SOCs detected at the Outlet site are dominated by waste water treatment facilities and at the OA site (which is
the occurrence of two fragrance compounds, galaxolide and downstream of agricultural lands along the Virgin and Muddy
tonalide, which were not present at the upstream site during Rivers), but at lower concentrations (Table 3). This indicates
the deployment period. Other SOCs that could be associated that at least some of chlorpyrifos is locally derived and is not
with treated waste water discharge and were either not found all from washing of produce that was sprayed with chlorpyrifos
at the upstream site or are found at much lower concentrations in other parts of the country, as has been suggested by Benotti
are lindane (used in shampoo as a control for hair lice), flame et al. (2009) for the presence of atrazine found in waste wa-
retardants, and food preservatives. Lindane was also manu- ter and drinking water samples from non-agricultural regions.
factured at the Basic Metals, Incorporated (BMI) industrial Chlordane was manufactured at the BMI industrial site, and
site (Fig. 1; see Rosen and Van Metre, 2009, for more details) this is the likely source for this chemical. However, the con-
and could be a possible source. Also, two known endocrine- centration of chlordane compounds at the Outlet site is much
disrupting chemicals, trans- and cis-chlordane (Huang et al., lower (72pgL-1 combined) compared with the lindane con-
2004), which are isomers of the pesticide chlordane that was centration (410 pg L-1), indicating that lindane is more mobile
banned in the USA after 1988, were found at low concentra- (although it has a higher octanol/water partition value than
chlordane) from the BMI site than chlordane or that lindane Lake Mead and Colorado River Sites
containing shampoo from the waste water treatment facilities The four sampling sites within Lake Mead (LVB, OA, BB,
may be an additionalsource. and GB) showed much lower concentrations and number of
Osemwengie and Gerstenberger (2004) showed that grab SOCs detected than the Outlet site on the Wash (Tables 3 and
samples of water collected at monthly intervals in Las Vegas 4). As expected, the LVB site contained higher concentrations
Wash downstream of the waste water treatment facilities con- of certain SOCs and more detections (23 detections at 8 m
tained yearly average concentrations of 57,000 pg L-1 of galax- depth) than the three other sites in Lake Mead (Tables 3 and
olide and 34,000 pg L-1 of tonalide, with monthly values no 4). Las Vegas Bay also had an overall higher sum of concentra-
higher than 98,000 pg L-1 and 50,000 pg L-1 for galaxolide tions of SOCs than other sites in the lake (Fig. 3). The OA and
and tonalide, respectively. In our study, SPMD concentrations GB sites had relatively low concentrations and fewer detections
at the Outlet site were almost eight times higher for galaxolide (8 and 10 detections, respectively) than the LVB and BB sites
(400,000 pgL-1) but were similar for tonalide (41,000 pg L-1). (23 and 11 detections, respectively), but the GB site contained
However, the values are not directly comparable because SPMDs relatively high concentrations of petrogenic PAHs (naphtha-
sample water continuously over the deployment period; there- lene, 2-methylnaphthalene, 1-methylnaphthalene, and 2,6-di-
fore, average concentrations determined from these devices may methylnaphthalene) compared with other sites. The reason
be different from water samples taken at one point in time. for this is not clear but may be due to discharge of unburned
petroleum products from boat exhaust from boats with two- in deep water (>80 m depth) well away from swimming areas,
stroke engines near the site. It is unlikely that the high values had relatively few detections of SOCs (11 detections), with most
of petrogenic PAHs were caused by the boat used to deploy and concentrations less than 0.1 ng L-1 or 100 ng per POCIS. Of
retrieve the samples because the same boat was used at each site significance is the continued presence of galaxolide at a concen-
and it has a four-stroke engine, which would be less likely to tration of 1.3 ng L-1 more than 10 km into the lake. Osemwen-
discharge unburned fuel into the lake than a two-stroke engine gie and Gerstenberger (2004) found concentrations of galaxolide
(Lico and Johnson, 2007). near the shore in the outer part of LVB (Fig. 3) of 0.36 ng L-1,
The LVB site at 8 m depth showed the same SOCs (if de- indicating that galaxolide can be transported over large distances
tected) as the Outlet site (Tables 3 and 4) but at lower concentra- in water even though it is relatively hydrophobic.
tions. Galaxolide and tonalide concentrations at 8 m depth were Although concentrations and detections of SOCs were
approximately 10% of the value at the Outlet site. If microbial low at the OA site, three pesticides were detected (chlorpyri-
degradation was important, the decay rates of these compounds fos, dacthal, and hexachlorobenzene). Dachtal and hexachlo-
would be expected to be different depending on which microbes robenzene were detected at all sites with similar low concen-
degrade them and the rates of decay for each microbe. The simi- trations (<100 pg L-1), indicating that the detections may be
larity in reduction rates indicating that dilution/sedimentation partly atmospherically derived from regional agricultural use.
is probably more important than microbial degradation in con- However, chlorpyrifos was detected at OA and not detected at
trolling the concentrations in LVB. The BB site, which is located BB, GB, or WB, indicating that agriculture along the Virgin/
Muddy River basin upstream of OA may be contributing small LaBounty and Burns (2005) showed that water from Las Vegas
amounts of pesticide compounds, like chlorpyrifos. Wash may have four distinct interflow depths during the same
The Colorado River site downstream from Hoover Dam sampling event and may vary longitudinally within a 24-h period.
(WB) had a slightly greater number of detections (n = 13) than Temperature and specific conductance measurements taken at the
BB, OA, and GB but at low concentrations. Petrogenic PAHs time of this studys SPMD deployment show that water at the
were detected at this site, probably due to a large amount of LVB site was slightly warmer and had higher specific conductance
boat traffic. Other compounds detected at this site are related on the bottom for most of the deployment period (Fig. 4A, 4B).
to flame retardants, plastics, and other chemicals that are not In addition, diurnal temperature variations, which are more than
generally associated with boats. 4C at the Outlet site in Las Vegas Wash (Fig. 4C), were more ap-
Overall, the OA, BB, and WB sites showed low concentra- parent in the bottom waters of the LVB site than at 8 m depth, in-
tions of SOCs, and the GB site contained petrogenic PAHs dicating that a plume of Las Vegas Wash water was descending to
at concentrations of some concern, with concentrations equal- the bottom of the bay for more than half the deployment period.
ing almost half of the chronic fresh water quality benchmark There were three trends in the vertical profiles, and they
(Suter, 1996). The LVB site had many more detections and at were generally consistent between the two vertical deployment
much higher concentrations than the other sites. The distribu- strings (Table 2): (i) The concentrations of galaxolide and to-
tion of the contaminants within the water column found at nalide were greater at the deepest sampling points (18 m) than
the LVB site was further examined to determine if SOCs were the middle and upper points (4, 8, and 12 m). In one deploy-
distributed homogenously throughout the water column. ment string, the concentrations increased progressively from the
upper SPMD to the bottom SPMD (Fig. 5A, 5B), and in the
Vertical Distribution of Hydrophobic Contaminants other nearby vertical deployment (which only had three depths),
The vertical and lateral distribution of physical, chemical, and the concentrations dropped with the SPMD at 12 m depth but
biological parameters (such as temperature, nutrients, selected in- were still highest at the bottom SPMD. (ii) Concentrations of
organic elements and compounds, bacteria, phytoplankton, and PAH were highest in the SPMDs near the surface and generally
zooplankton) in LVB and Boulder Basin has been documented decreased with depth (Fig. 6A, 6B). (iii) A degradation product
by LaBounty and Burns (2005). They were able to show that dur- of dichlorodiphenyltrichloroethane (DDT), o,p-DDE, and two
ing the spring, when the SPMDs were deployed in our study, the congeners of polychlorinated biphenyls (PCB138 and PCB 180)
point where inflow from Las Vegas Wash enters LVB is not con- were present only in the lower water column.
sistently at the top or bottom of the water column when it reaches Although it could be argued that the two vertical profiles
the bay due to increasing Las Vegas Wash water temperatures. of the fragrances were not consistent because the 12-m SPMD
had a variation of more than 40,000 pg L-1 between the two biota and affect the health of bottom-feeding fish and benthic
strings, it is clear that the bottom concentrations (at 18 m) are invertebrates present in LVB.
higher or at least as high as the upper SPMDs, indicating that
the profiles for the fragrances and the PAHs are different. The Implications for Fish Health
differences observed in the 12-m SPMDs are likely to be caused The health of the aquatic ecosystem is important in Lake
by variations in interflow from Las Vegas Wash over the deploy- Mead for two main reasons. First, Lake Mead, and in particular
ment period, which may have contributed contaminants to this LVB, is habitat for a population of federally listed razorback
interval differently due to placement of the SPMDs on opposite sucker (Xyrauchen texanus), which has had limited success in
sides of the platform. These contrasting profiles of fragrances and recruiting new adults into the population (U.S. Fish and Wild-
PAHs indicate different sources for these SOCs. The fragrances life Service, 1998); second, Lake Mead supports a substantial
are almost certainly coming from treated waste water discharge and internationally recognized fishery that accommodates
into Las Vegas Wash because they are not present in Las Vegas more than 500,000 anglers a year (Rosen et al., 2006).
Wash at the LVVD site, which is upstream of the waste water A study in the mid-1990s showed that common carp in Las
treatment facility inflows. The PAHs likely come from in-lake Vegas Wash and LVB have been exposed to endocrine-disrupt-
sources, such as boats, where higher concentrations should be ing compounds (EDCs), such as DDT, PAHs, and phthalates
concentrated at the surface of the lake. Lico and Johnson (2007) (Bevans et al., 1996), and that the endocrine systems in com-
have shown that boat traffic is the major source of PAHs in Lake mon carp was most likely altered due to long-term exposure
Mead, and our study shows that the highest concentrations in to these EDCs. The implications for altered endocrine systems
LVB occur near the surface of the lake, indicating boats as the in fish can affect reproduction and recruitment (Kime, 1998).
likely source. Concentrations of PAHs are high at the surface of Water samples collected from Las Vegas Bay in April 1997 con-
the lake even though volatilization and photolytic degradation of tained four xenoestrogen compounds (octylphenol, 27ngL-1;
PAHs lowers the concentration of many PAHs near the surface nonlyphenol, 750 ng L-1; polyethoxylates, 4850 ng L-1; and
of the lake (Lico and Johnson, 2007). 17a-ethinyl estradiol, 0.5 ng L-1) and one natural estrogen
Dichlorodiphenyltrichloroethane and PCBs are legacy (17b-estradiol, 2.2 ng L-1) (Snyder et al., 1999). Another study
compounds formerly manufactured in industrial complexes by Snyder et al. (2001) determined that the compounds with
that are located along Las Vegas Wash (Rosen and Van Metre, the highest estrogenic activity at Las Vegas Bay were two steroid
2009). The fact that they are present only at lower depths of the hormones: 17b-estradiol, a naturally occurring estrogen, and
bay may indicate that they are solely entrained in the plume of 17a-ethinyl estradiol, a synthetic estrogen used in oral contra-
Las Vegas Wash water that is plunging to the bottom of the lake ception. Fish exposed to ethinyl estradiol in concentrations as
or that there is a flux of these compounds from the sediment low as 0.5ng L-1 have shown evidence of endocrine disruption
to the lake over time. Additional work is being performed to (Purdom et al., 1994; Routledge et al., 1998; Bayley et al., 1999;
determine if such a flux exists. The occurrence of these com- Doyle and Lim, 2002; Thorpe et al., 2003).
pounds in the sediment (Covay and Beck, 2001; Rosen and Patio et al. (2003) demonstrated lower gonadosomatic in-
Van Metre, 2009) or near bottom water may expose aquatic dex in male carp from LVB compared with common carp from