Trace Elements in Plankton, Benthic Organisms, and Forage Fish of Lake Moreno, Northern Patagonia, Argentina

Page 1

Trace Elements in Plankton, Benthic Organisms, and ForageFish of Lake Moreno, Northern Patagonia, Argentina

Maria A. Arribére & Linda M. Campbell &Andrea P. Rizzo & Marina Arcagni &Jorge Revenga & Sergio Ribeiro Guevara

Received: 24 July 2009 /Accepted: 13 January 2010 /Published online: 17 February 2010# Springer Science+Business Media B.V. 2010

Abstract The Northern Patagonian Andean rangeshared by Chile and Argentina has numerous glacialoligotrophic lakes protected in a series of NationalParks. Recent baseline surveys indicated that concen-trations in muscle and liver tissues from various fishspecies from across Nahuel Huapi and Los Alerces

National Parks in Argentina were comparable orhigher than similar fish species from other parts ofthe world. As a result, Lake Moreno, in Nahuel HuapiNational Park, was chosen to investigate multipleelement sinks, trends, and transfer in a representativePatagonia aquatic food web. The metals and metal-loids Ag, As, Ba, Br, Cs, Co, Cr, Fe, Hg, K, Na, Rb,Se, and Zn were analyzed in three size planktonfractions, submerged macrophytes, biofilm, insectlarvae, amphipods, decapods, gastropods (snails),annelids (earthworms), and forage fish. Except fornanoplankton (10–53 μm; small-celled algae, rotifers)and microplankton (53–200 μm; larger algae, ciliates,zooplankton nauplii), which share elemental compo-sitional similarities, each taxon category had its owndistinctive compositional pattern, revealed by princi-pal component analysis. Nano- and microplanktontend to be relatively elevated in some metals,including As, Co, Cr, Fe, Hg, Zn, and Rb, followedby biofilm. Shredder-scrapper Trichoptera (caddis-flies) have higher concentration of most of the studiedelements than other insect larvae taxa, especiallycarnivorous Odonata (Anisoptera, dragonflies), whichwere associated with lower elemental contents. Thosetrends point to an overall tendency for biodiminishingelement concentrations with trophic level in thebenthos of Lake Moreno.

Keywords Metals . Aquatic food web . LakeMoreno .

Functional feeding groups

Water Air Soil Pollut (2010) 212:167–182DOI 10.1007/s11270-010-0330-3

M. A. Arribére (*) :A. P. Rizzo :M. Arcagni :S. Ribeiro GuevaraLaboratorio de Análisis por Activación Neutrónica, UAIN,Centro Atómico Bariloche,Comisión Nacional de Energía Atómica (CNEA),Bustillo 9500,8400 Bariloche, Argentinae-mail: [email protected]

M. A. ArribéreInstituto Balseiro, Universidad Nacional de Cuyo y CNEA,Bustillo 9500,8400 Bariloche, Argentina

L. M. CampbellDepartment of Biology and School of EnvironmentalStudies, Queen’s University,Kingston, ON K7L 3N6, Canada

A. P. RizzoCONICET,Buenos Aires, Argentina

M. Arcagni : J. RevengaCentro Regional Universitario Bariloche (CRUB),Universidad Nacional del Comahue,Quintral 1250,8400 Bariloche, Argentina

Page 2

1 Introduction

The Northern Patagonian Andean mountain range(39° to 45° S, 71° W; 500 to 3,554 m a.s.l.), shared byChile and Argentina, have numerous glacial lakes,which drain toward the Atlantic and Pacific oceans.Both countries have established national parks alongtheir shared border to protect the “Lake District.” TheNahuel Huapi National Park (NHNP) on the Argen-tine side encompasses 785,000 ha, including drainagebasins of three major river systems.

Because of its isolation and low population density,this area has been historically protected from anthro-pogenic contamination, with the most importantsource of metals being from the frequent Andesvolcanic activity (Stern 2004; Campbell et al. 2007).However, over the past 60 years, the human populationin the region has rapidly increased by a factor of ten.Tourism, both from within Argentina and outside,fishing, and recreational water sports are importantsources of revenue and are fuelling a major populationgrowth with subsequent increase in environmentalcontaminants. Recently, a baseline survey indicated thatmetal (Cs, Fe, Br, Se, Rb, Na, and Zn) concentrations inmuscle and liver tissues from various fish species fromacross Nahuel Huapi National Park and the neighboringLos Alerces National Park were comparable or higherthan similar fish species from other parts of the world(Ribeiro Guevara et al. 2004; Campbell et al. 2005;Arribére et al. 2006; Arribére et al. 2008). The actualtrophodynamics and metal transfer routes within foodwebs leading to fish still require analysis and quanti-fication for better management of the economicallyimportant sport fisheries.

Lake Moreno, a double-basined lake situated byLake Nahuel Huapi and the City of San Carlos deBariloche, provides an ideal case study due to itsaccessibility and similarity to other less accessiblelakes of Nahuel Huapi National Park. The aim of thisstudy is to investigate metal trends and transferthrough the lower food web of Lake Moreno usingmultivariate approaches and how that relates to metalconcentrations in sportfish.

2 Methods

Study Site Lake Moreno (41°5′ S; 71°33′ W, 758 m a.s.l.), in Nahuel Huapi National Park, is an hour-glass-

shaped warm monomictic and ultraoligatrophic sys-tem. It is stratified from late spring to early autumnwith a thermocline at about 30 m depth. The twobasins, Lake Moreno West (MW) and Lake MorenoEast (ME), are connected by a short narrow channel(Fig. 1). Lake Moreno West, in turn, is connected toLake Nahuel Huapi, the largest lake of the Park(560 km2), through a short channel. Table 1 shows themain characteristics of both basins.

Lake Moreno West has a highly irregular coast line,with peninsulas, bays, and flooded areas, surrounded bytemperate rainforest dominated by Nothofagus dombeyiand Austrocedrus chilensis (Queimaliños et al. 1999).The coast line of Lake Moreno East is more regularand present rocky beaches, and the drier rainforest–steppe ecotone vegetation coverage in the surroundingsof the lake is less dense. This region is increasinglybecoming periurban, with family housing and hoteldevelopment along the shores, in addition to a rainbowtrout fish farm in ME.

Field Sampling Lakes Moreno West and East weresampled four consecutive seasons (spring, summer,autumn, and winter), from 2005 to 2006. The samplingsite chosen from Moreno West was on the westernmostside, with dense rainforest in the surroundings, wherethe lowlands are flooded in spring time during thesnow melting period (GP, in Fig. 1). The siteschosen on Moreno East were the North and Southmargins (S and N; Fig. 1), in rocky beaches. Thetraps on the North side were damaged duringsampling; this site was abandoned, remaining onlythe South margin site. All plastic and glass vesselsand bottles used in the field or in the laboratory werewashed for 15 days in 50% HNO3 and thoroughlyrinsed in ASTM grade 1 water before use. Filteringdevices and filters were washed in 50% HNO3

whenever possible. The filters (made out of the netmaterial NITEX®), which could not stand acidcleaning, were washed with EXTRAN® detergentand thoroughly rinsed, using a bath with ultrasound.

All sampled specimens were rinsed with lake waterto remove excess sediment and particulates, taken tothe laboratory immediately after sampling where theywere rinsed with ASTM-grade water, stored at −20°Cuntil freeze drying, and then homogenized usingTeflon and titanium tools.

The food web sampling focused on items impor-tant to the larger sport fish diet: galaxids (Galaxias

168 Water Air Soil Pollut (2010) 212:167–182

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maculatus), salmonid young of the year (YOY),decapods (Samastacus sp., Aegla sp.), amphipods(Hyalella sp.), insect larvae (Plecoptera, Ephemerop-tera, Odonata, Trichoptera, and Coleoptera), gastro-pods (Chilina sp.), and Hirudinea.

Galaxids, salmonid juveniles, and macrocrusta-ceans (Samastacus sp. and Aegla sp.) were caughtwith baited traps set out for 2 to 4 days in the littoralzone. Brook trout and rainbow trout juveniles rangedin length from 7 to 18 cm and were pooled by size.

Fig. 1 Map of the study area

Units Moreno East Moreno West

Areaa km2 5.4 4.8

Conductivity μS cm−1 37 37

Maximum deptha m 128 110

Average deptha m 69 60

Maximum lengtha km 4.4 4.7

Maximum widtha km 1.8 2.0

Surface temperature °C 8 (winter)–16.5 (summer) 8 (winter)–17.5 (summer)

pH 6.8 6.8

Chlorophyll ab μg L−1 1 1

Table 1 Chemical, physi-cal, and limnologicalparameters of Lake Moreno

a Quirós (1988)b Souza et al. (2007)

Water Air Soil Pollut (2010) 212:167–182 169

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Because of their abundance and small masses,galaxids were pooled into five size classes to ensuresufficient analytical mass: G1, 3 to 4 cm length; G2, 4to 5 cm; G3, 5 to 6 cm; G4, 6 to 7 cm; and G5>7 cm.Each pooled set consisted of ten to 30 individuals;and to check for individual variability, in the springseason, when the largest set of small fish was caught(belonging to groups G1, G2, and G3), three sets of30 fish of each group were prepared as independentsamples to search for sampling variability. Since theshell of adult decapods and gastropods is notcompletely digested by fish, the majority of Samas-tacus, Aegla, and Chilina samples were dissected formuscle and digestive tissues (hepatopancreas), whichwere analyzed separately. Only a few selected adultSamastacus and Aegla samples were analyzed whole.All other invertebrates, insect larvae, Hyalella, Hiru-dinea, and soft-shelled juvenile Aegla sp (<2 cm,collected in summer and fall), were collected by handalong the shoreline. Pooled samples were created withhomogenized whole-body organisms since fish candigest those organisms in its entirety.

Nanoplankton (10–53 µm; consisting of hapto-phyte, cryptophytes, dinoflagellates, and rotifers),microplankton (53–200 µm; consisting of largerphytoplankton, ciliates, and smaller zooplankton),and zooplankton (≥200 μm; consisting of largercopepods and cladocerans) were collected using aseries of conical NITEX® nets in four different sites.Since Moreno East has a rather regular basin with themaximum depth in the middle, a central samplingpoint was chosen (ME, Fig. 1). Three sampling siteswere chosen in Moreno West: a site where the lakereaches its maximum depth (PP), a shallow and rathernarrow bay (LL, 18 m deep), and an open bay on theWest side (MW) 45 m deep. Samples were collectedby vertical hauls from 50 m depth to the lake surfacein deeper sites (ME, PP) and from about 2 to 4 mabove the lake bottom in the shallower sites (LL,MW). All samples were concentrated in the laborato-ry by filtering through 0.2 μm Nucleopore® polycar-bonate acid-washed filters and freeze-dried untilconstant weight.

Submerged macrophytes, moss, and benthic algaewere collected by hand. Biofilm (composed of algae,bacteria, decomposing organic matter, and very finedetritical particulate) was very abundant in spring andsummer and was sampled by gently scraping thesurface of folded NITEX® nets set in the littoral zone,

macrophyte leaves, and rock surfaces with acid-washed plastic or titanium utensils. Biofilm wasscarce in autumn and winter, and it was not possibleto collect enough mass for analysis, with the onlywinter sample obtained after one unusually sunny andwarm week in Moreno East (S).

Elemental Analyses Aliquots of about 100 mg ofdried homogenized and powdered sample were sealedin SUPRASIL AN® quartz ampoules, irradiated for24 h, and analyzed by Instrumental Neutron Activa-tion Analysis (INAA) at the RA-6 nuclear researchreactor at Centro Atómico Bariloche. Ag, As, Ba, Br,Cs, Co, Cr, Fe, Hf, Hg, K, La, Na, Rb, Sb, Se, Sm, U,and Zn were measured for all samples, while Ca wasalso measured in macrocrustacean samples. Gamma-ray spectra were collected using an intrinsic HighPurity Germanium (HPGe) n-type detector, 12.3%relative efficiency, and a 4096-channel analyzer.Spectra were analyzed by using the GAMANALroutine included in the GANAAS package, distributedby International Atomic Energy Agency (IAEA).Corrections for spectral interferences were includedwhen necessary. The concentrations reported arereferred to dry weight basis. Standard referencematerials from the National Research Council ofCanada (NRCC)-DORM-2 Dogfish Muscle, NRCC-TORT-2 Lobster, NRCC-DOLT-2 Dogfish Liver, andfrom the International Atomic Energy Agency, IAEA-336 lichen material, IAEA-392 Algae material, aswell as sample replicates, were analyzed to check onthe quality of analysis. The analyses of the standardreference materials showed good agreement withcertified and informed values, and replicate sampleswere consistent.

Data Analyses Bivariate correlation and principalcomponent analysis (PCA) were used to identifyassociation of food items as sources of an elementor set of elements. Bivariate correlation allowsidentifying elemental contents related to geogenicmaterial, especially in insect larvae and other sampleswhich could retain entrapped geological particulate.Since Ba was determined only in a limited number ofsamples of fish and macroinvertebrates due toanalytical detection limits, it was included in the PCanalysis when only macrophyte, biofilm, plankton,and insect larvae were considered. Cr contents insome samples were below all other measurements in

170 Water Air Soil Pollut (2010) 212:167–182

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any sample considered; for these cases, the detectionlimit was included as input data for the PCA. Fish Asand Ba were not included in the PCA because the datawere not available for all samples.

Previously published trace element data for sevenfish species and one native mussel species from thislake were also included in the data analyses to enabledirect comparison of invertebrate and fish data. Thefish species included are Diplomystes viedmensis(velvet catfish), Odontesthes hatcheri (creole silver-side or pejerrey), Oncorhynchus mykiss (rainbowtrout), Percichthys trucha (creole perch), Salmo trutta(brown trout), and Salvelinus fontinalis (brook trout),and the sampling and analysis details can be found inRibeiro Guevara et al. (2006), while sampling andanalysis information for the native mussel Diplodonchilensis were taken from Ribeiro Guevara et al.(2004). Since the literature reports that musselpredators consume only the soft tissue (Lara andMoreno 1995), data for mussels without valves werethe only included.

3 Results and Discussion

The lithophile and the rare earth elements (REE) ofthe lanthanide and actinide series, Hf, U, La, Sb, andSm, are highly correlated with each other in the lowerfood web species (bivariate analysis, r2>0.9). REEand other insoluble elements are sometimes found infish and decapod tissues, but in significantly lowerconcentrations than in other organisms such as insectlarvae. REE are lithophile elements associated withgeological material trapped within the sample andthus having little biological significance within softtissues of animals. As a result, REE were notconsidered in the subsequent statistical analysis.

The minimum, median, maximum, average, andstandard deviation of As, Ba, Br, Cs, Co, Cr, Fe, Hg,K, Na, Rb, Se, and Zn concentrations of each type oforganisms are shown in Tables 2, 3, and 4.

Table 5 compares the elemental contents measuredin this work with some data found in the literature forsimilar species. Although comparisons are not alwayspossible due to the heterogeneity of statisticalmeasurements (ranks and means), data suggestenriched Zn, Fe, and Hg concentrations in planktonfrom this work (with the exception of Zn in macro-

plankton) compared to other published data. Inbenthic organisms, Ephemeroptera and Hyalella sp.have higher Hg burdens, but contents in whole fishare similar or lower.

The primary producers fell across a broad range forall the other transitional and semi-metalloid elements.The first principal component of the PCA for theprimary producers and zooplankton showed distinc-tive separation of four groups (Fig. 2). The firstgroup, nano- (10–53 μm) and microplankton (53–200 μm), was clustered apart from the second groupconsisting of zooplankton (≥200 μm). Macrophytesand mosses formed a tight third cluster, while biofilmformed the fourth. Biofilm and nano- and micro-plankton samples tend to be richer in As, Ba, Co, Cr,Cs, and Fe and poorer in Br and Se. All planktonfractions are poorer in K compared to macrophytes,mosses, and biofilm and tend to be richer in Se andZn. The PCA components 1 and 2 plot for the insectlarvae show that insects are located between planktonsamples and macrophytes (below), having biofilm tothe right. Within this cluster, the five Odonatasamples fall to the left end of the distribution andshares similar PC1 scores with zooplankton. Trichop-tera is closer to the phytoplankton and biofilm PCscores. Plecoptera and Ephemeroptera samples liebetween Odonata and Trichoptera. According to thisplot, Trichoptera metal trends are more closelyrelated to biofilm, which suggests that Trichopteramay be obtaining their metal burdens from grazingon biofilm. Odonata are known to be predatory(Westfall and Tennesseen 1996), and the PC1 scoregradient from Trichoptera to Odonata suggests afeeding gradient from biofilm grazing to feedingupon other organisms. Relating PC1 with elements,an increase in carnivory is accompanied with adecrease in As, Ba, Co, Cr, Cs, and Fe and anincrease in Br. This biodilution effect in macro-invertebrates food chain has been observed by Faraget al. (1998) for As, Hg, and Zn and by Watanabe etal. (2008) among different functional feeding groupsof benthic macroinvertebrates.

The PC1 vs. PC2 scores for the non-insectinvertebrates, Hyalella, Hirudinea, Oligochaeta, andgastropods (Fig. 3a), in addition to primary producers,indicate that Hyalella samples are clustered close tothe macrophytes and zooplankton, while Chilina sp.,Oligochaeata, and Hirudinea cluster between the PCscores for zooplankton and micro- and nanoplankton.

Water Air Soil Pollut (2010) 212:167–182 171

Page 6

Tab

le2

Con

centratio

nsof

traceelem

entsin

plankton

,biofilm

,subm

ergedmosses,macroph

ytes,insectlarvae,Hyalella

sp.,andHirud

inea

from

LakeMoreno:

minim

um,median,

andmaxim

um

Trace

elem

entNanop

lank

ton

(N=22

)Microplankton

(N=22

)Macroplankton

(N=22

)Biofilm

(N=9)

Sub

merged

mosses

(N=3)

Sub

merged

macroph

ytes

(N=25

)

Trichop

tera

larvae

(N=18

)

Plecoptera

larvae

(N=8)

Eph

emerop

tera

larvae

(N=5)

Odo

nata

larvae

(N=5)

Coleoptera

Hirud

inea

(N=6)

10to

53μm

53to

200μm

>20

0μm

Min.–

median–

max.

Min.–median–

max.

Min.–median–

max.

Min.–

median–

max.

Min.–

median–

max.

Min.–

median–

max.

Min.–

median–

max.

Min.–

median–

max.

Min.–median–

max.

Min.–

median–

max.

Min.–

median–

max.

Min.–

median–

max.

As

3.8–

8.2–23.0

4.9–7.0–

15.4

1.7–2.5–

4.1

1.7–

8.6–18.0

1.3–

4.1–

4.5

0.12–0

.69–

12.5

0.90–3

.6–6.6

0.44

–0.97–

7.1

0.67–1

.8–6.7

0.87–1

.14–

1.45

1.3–

1.4

1.02

–1.8–4.9

Ba

130–

320–2,290

73–222

–444

11–7

0–24

140–310–

440

91–99–

253

6.8–39

–174

210–290–460

12–7

8–780

36–83–

210

9.6–19.0–

28100–104

16–82–

430

Br

7.9–

23–5

310.5–2

9–138

110–270–

390

1.7–

11–3

0.5

7.4–

7.8–

262.5–21

–78

13–24–

4116–2

6–69

48–82–

100

45–65–

122

208–210

2.8–

16–2

6

Cs

0.48

–0.84–

3.24

0.29–0

.84–

1.98

0.069–

0.25–0

.45

0.51

–2.57–

3.13

0.51

–0.67–

1.01

0.024–

0.34–

0.82

0.19–0

.37–

0.64

0.092–

0.36

–0.93

0.18–0

.34–

1.19

0.084–

0.14

–0.24

0.26

–0.34

0.019–

0.094–

0.48

Zn

133–

450–3,810

110–

332–

1,500

60–2

50–2

3070–1

20–140

30–51–

6632–8

0–320

150–270–420

98–1

80–260

85–200

–510

38–82–

98104–105

85–480

–870

Co

1.5–

3.9–16

1.9–3.9–

220.44–0

.89–

2.12

5.0–

18.5–2

2.6

2.6–

5.0–

5.0

0.56–2

.0–9

.63.2–6.9–

12.1

0.39

–3.3–5

.31.3–3.7–

10.1

0.35–0

.89–

1.84

1.1–

1.2

1.7–

5.2–

9.6

Cr

8.7–

25–1

764.2–24–9

40.69–2

.5–7

.619–4

0–70

4.3–

7.4–

15.2

0.27–1

.9–6

.42.5–4.7–

10.4

0.95

–2.1–8

.30.92–5

.2–32

0.43–1

.3–

4.3

1.5–

2.4

0.23

–3.0–4.5

Fe

3,150–

8,100–

19,000

4,580–8,500–

54,800

430–1,100–

3,000

17,000

–44,700

–80,800

8,300–

6,800–

11,200

390–2,540–

8,700

3,500–7,700–

13,900

640–

2,900–

4,800

840–2,800–

8,700

1,000–

2,100–

9,300

370–430

1,120–

2,100–

7,400

Hg

0.25

–10.2–

258

0.08–1

.9–100

0.16–0

.60–

8.1

0.14

–2.4–5

.8<0.03

–0.12a

<0.05

–0.31–

7.5

0.083–0.31

–2.3

<0.070–

2.0–

2.4

0.16–0

.66–

1.4

0.095–

0.26

–1.6

<0.1–

0.2

<0.1–

0.25

–2.4

K0.18

–0.73–

2.18

0.37–0

.56–

1.50

0.31–0

.63–

0.87

0.59

–0.95–

1.6

0.400.69

–0.90

0.27–2

.2–7

.31.1–1.6–

2.2

0.82

–1.03–

1.18

1.1–1.2–

1.9

0.42–0

.67–

0.87

1.0–

1.1

0.71

–1.01–

1.17

Rb

6.9–

18.8–4

6.3

13–19–

462.2–14

–22

19–3

9–67

16–26–

39<0.4–

21–95

9.3–13.2–

17.8

7.0–

26–3

14.0–30–4

89.0–17.5–

2314–1

62.1–

5.8–

9.9

Se

<0.4–

1.53

–1.87

<0.2–1.44

–2.18

1.5–2.2–

2.56

<0.1–

0.40

–0.86

0.19

–0.21–

0.81

<0.02

–0.07–

0.33

0.44–0

.93–

1.6

0.54

–1.3–2

.80.76–1

.6–3.2

0.53–0

.74–

0.80

0.8–

1.3

1.5–

1.6–

3.2

Na

1,860–

6,400–

16,000

1,600–4,200–

23,600

510–3,600–

6,000

4,800–

11,400

–21,900

2,500–

4,200–

4,800

500–4,000–

36,000

3,500–5,100–

9,100

3,900–

5,500–

6,500

1,600–6,300–

11,600

3,500–

5,900–

8,400

9,600–

10,000

1,100–

5,600–

6,600

Allvalues

inmg/kg

indryweigh

tbasis

Nnu

mberof

samples

aA

unique

valueabov

edetectionlim

it

172 Water Air Soil Pollut (2010) 212:167–182

Page 7

Tab

le3

Con

centratio

nsof

traceelem

ents

inmuscleof

Samastacussp.,Aegla

sp.,andChilin

asp.;who

leSa

mastacussp.andAegla

sp.juveniles(length>2cm

)andadults;

Diplodo

nchilensis,Olig

ochaeta,

andHyalella

sp.from

LakeMoreno:

minim

um,median,

andmaxim

um

Trace

elem

entSa

mastacus

sp.(m

uscle,

N=9)

Samastacus

sp.(w

hole)

Samastacussp.

hepatopancreas

(N=8)

Diplodo

nsp.a

Chilin

asp.

(softtissues,

N=6)

Chilin

asp.

(who

le)

Aegla

sp.

(muscle,

N=3)

Aegla

sp.

(who

leadults)

Aegla

sp.

hepatopancreas

(N=3)

Aegla

sp.

(who

lejuveniles)

Hyalella

sp.(N

=9)

Olig

ochaeta

Min.–

median–

max.

Range

Min.–median–

max.

Range

Min.–

median–

max.

Range

Min.–median–

max.

Range

Min.–median–

max.

Range

Min.–

median–

max.

Range

As

0.38

–0.31–

1.00

1.3–

1.4

1.00

–1.55–

2.14

32–3

96.2–

7.2–

13.0

1.8–2.0

2.7–

3.1–

4.0

1.8–

1.9

1.3–

2.7–

6.1

2.3–

3.9

1.6–

2.8–

5.0

2.4–

5.6

Ba

4–13

–16

100–

104

10–2

1–26

1,610–1,620

20–4

1–130

180–

300

<20

92–110

22–4

7–49

70–1

6422

–92–530

710–

1,100

Br

28–5

5–99

208–

210

15–9

3–168

35–40

10–1

8–34

29–3

798

–110

–120

270–

304

80–115

–117

230–250

61–2

40–

309

17–2

5

Cs

0.28

–0.40–

0.49

0.26

–0.34

0.074–

0.20

–0.24

0.029–0.036

0.12

–0.20–

0.43

0.082–

0.090

0.31

–0.31–

0.32

0.12

–0.17

0.22

–0.32–

0.48

0.26–0

.28

0.17

–0.37–

0.93

0.85

–0.94

Zn

68–1

20–2

10104–

105

110–

180–

290

240–290

63–8

4–140

20–2

3241–

263–

264

73–8

671

–83–

100

74–7

535

–78–160

370–

810

Co

0.040–

0.086–0.23

1.1–

1.2

0.68

–2.3–3

.81.03–1

.14

0.77

–1.4–4

.60.84

–0.85

0.094–

0.095–

0.148

0.66

–0.73

0.51

–0.53–

2.3

0.82–0

.99

0.26

–0.90–

1.6

1.45

–1.54

Cr

0.066–

0.15

–0.73

1.5–

2.4

0.15

–0.33–

1.35

18–30

0.75

–1.7–

12.6

3.2–

3.8

<0.2–

0.26

1.0–

4.9

<0.01

–15.3

2.0–2.2

0.51

–1.00–

3.5

<5–

5.5

Fe

23–6

3–290

370–

430

58–2

80–1

,260

13,600–

14,000

1,500–

1,900–

7,700

1,300–

1,500

25–3

8–240

350–

440

69–1

70–4

,300

100–120

240–650–

1,140

770–

2,900

Hg

0.20

–0.29–

1.44

<0.1–

0.2

0.086–

0.48

–1.34

0.34–0

.39

0.11–0

.18–

3.4

0.46

–0.70

0.19

–0.30–

0.40

1.38

–1.42

0.047–

0.074–

0.138

<0.06

–0.35

0.066–

0.18

–1.7

<1–

2.4

K1.0–

1.5–

1.7

1.0–

1.1

0.45

–0.68–

0.92

–0.13

–0.44–

0.57

4.6–

3.6

1.28

–1.40–

1.42

0.41

–0.58

0.53

–0.63–

0.72

0.69–0

.69

0.59

–0.79–

0.90

2.7

Rb

14–2

1–25

14–1

68.9–

13–2

22.4–3.6

5.1–

13.9–

20.3

14–1

630.6–3

0.8–

31.4

13–1

821

–22–

2919–2

16.2–

18–2

421

–43

Se

0.55

–0.64–

1.44

0.8–

1.3

1.2–

2.5–

5.8

2.7–3.2

0.66

–1.03–

1.49

0.21

–0.34

1.93

–1.97–

2.02

1.00

–1.01

1.4–

2.4–

4.1

1.02–1

.04

0.10

–0.72–

1.9

<2–

3.9

Na

5,800–

8,600–

11,800

9,600–

10,000

2,700–

8,100–

15,000

2,500–2,700

2,400–

4,300–

8,400

1,600–

4,100

13,000

–14,500–

17,000

8,100–

12,000

7,100–

7,200–

14,200

1,000–

12,000

1,800–

5,700–

8,200

7,900–

11,000

Allvalues

inmg/kg

indryweigh

tbasis

Nnu

mberof

samples

aTaken

from

Ribeiro

Guevara

etal.(200

5)

Water Air Soil Pollut (2010) 212:167–182 173

Page 8

Tab

le4

Con

centratio

nsof

traceelem

entsin

adultfish

muscleandliv

erof

salm

onids,creole

perchandvelvet

catfish,

andwho

legalaxids

(length>3cm

)andsalm

onid

juveniles

from

LakeMoreno:

minim

um,median,

andmaxim

um

Trace

elem

entRainb

owtrou

t(m

uscle,

N=14

)Brook

trou

t(m

uscle,

N=13

)

Creoleperch

(muscle,

N=35

)

Velvetcatfish

(muscle,

N=8)

Galaxids(puyen

chico)

(who

le,

N=40

)

Rainb

owtrou

t(liver,N=14

)Brook

trou

t(liver,N=13

)Creoleperch

(liver,N=35

)Velvetcatfish

(liver,N=7)

Hom

ogenate

mad

eou

tof

7livers

Salmon

idjuveniles(w

hole,

N=6)

Min.–median–

max.

Min.–

median–

max.

Min.–

median–

max.

Min.–median–

max.

Min.–median–

max

Min.–median–

max

Min.–

median–

max

Min.–

median–

max

Min.–median–

max

Min.–median–

max

Ag

1.7–2.8–

5.2

0.33

–0.82–

2.5

0.06–0

.53–

2.6

0.02

1–

As

0.12

–0.26–

1.6

<0.1–

0.95

<0.1–

0.87

0.16–0

.33–

0.16

0.10

–0.62–

1.00

<0.1–0.82

0.19

–0.45–

1.6

<0.8–3.6

0.34

0.07

–0.052

Ba

<10

<10

<10

<10

3.7–

6.3–30

––

––

4.8

Br

13–23–36

7.4–

29–3

713

–22–46

31–3

9–64

10–22–

5535–6

6–84

12–58–94

35–4

7–79

9231

–32–47

Cs

0.41

–0.92–

2.0

0.38

–0.74–

1.6

0.57

–1.2–1

.90.63–0

.75–

0.93

0.08

9–0.27

–0.62

0.39–0

.60–

0.85

0.15

–0.39–

1.2

0.28–0

.61–

0.96

610.15

–0.19–0.26

Zn

13–18–22

13–1

7–28

24–2

6–36

23–3

0–52

100–

210–

330

117–16

0–23

978

–132–1

6040–7

2–12

310

810

0–12

0–22

0

Co

<0.2–

0.17

<0.2–

0.17

<0.01

–0.05

0.06

0–0.10

0–0.24

0.03

3–0.11–

0.32

0.16–0

.27–

0.68

0.15

–0.30–

0.60

0.11–0.51–

1.4

0.47

0.27

–0.33–

0.39

Cr

<0.2–

3.7

<0.1–

2.1

<0.5–

4.8

1.3–3.4–

5.4

0.09

–0.39–

1.2

0.10–0

.42–1.8

0.20

–0.55–

2.0

0.08–0

.23–

2.0

1.6

0.76

–1.6–3

.4

Fe

9.0–

18–3

311–24–

502–

12–2

727–4

6–67

51–720

–750

510–

780–

1,68

018

0–46

0–1,87

098–6

20–

1,98

079

047

–68–13

0

Hg

0.23

–0.43–

1.0

0.25

–0.89–

4.0

0.70

–1.2–3

.20.76–1

.2–2

.30.11–0

.29–1.3

0.06–0

.53–

1.06

0.20

–0.82–

7.1

0.19–0

.41–

0.85

1.6

0.05

9–0.10–0

.26

K(%

)0.87

–1.8–2

.21.6–

1.8–

2.2

1.2–

1.7–2.3

1.33–1

.49–

1.65

0.64

–1.4–1

.8–

––

–1.1–

1.4–1.7

Rb

32–45–61

32–4

4–66

33–4

5–62

27–3

2–38

8.9–

17–2

726–3

9–63

18–22–56

22–3

7–61

2920

–23–31

Se

0.60

–0.80–

1.1

0.80

–0.96–

1.1

0.86

–1.16–

1.58

0.82–0

.89–

1.04

0.88

–1.5–2

.213–1

9–97

3.0–

3.7–7.6

2.3–4.4–

8.0

5.4

0.94

–1.7–2

.2

Na

1,05

0–1,71

0–2,98

01,20

0–1,82

0–3,00

0

1,40

0–2,07

0–3,06

0

2,62

0–3,02

0–3,52

02,00

0–4,20

0–12

,800

2,78

0–4,80

0–5,95

02,32

0–3,88

0–7,09

0

2,07

0–3,67

0–6,56

0–

2,70

0–3,30

0–3,80

0

Allvalues

inmg/kg

indryweigh

tbasis.Datatakenfrom

Arribéreet

al.(200

6),Arribéreet

al.(200

8),andRibeiro

Guevara

etal.(200

5)

Nnu

mberof

samples

174 Water Air Soil Pollut (2010) 212:167–182

Page 9

Table 5 Concentrations of trace elements in plankton

Reference As Cs Zn Co Cr Fe Hg Rb Se Na (%)

Nanoplankton 3.8–23 0.48–3.2 130–3,800 1.5–15.7

8.7–176 3,200–19,000 0.25–260 6.9–46 0.39–1.9 0.19–1.6

Lake Piaseczno, Polanda 822.5 (FW) 0.3(FW)

2,202.5 (FW)

Lake Husainsager, Indiab 11–15 (FW)

Microplankton 4.9–15 0.29–2.0 110–1,530 1.9–21.7

4.2–94 4,600–55,000 0.08–99 13–46 0.38–2.2 0.15–2.4

20 lakes in USAc 3.2±4.2 230±310 3.6±7.6

Macroplankton 1.7–4.1 0.07–0.45

60–234 0.44–2.1

0.69–7.6 430–3,000 0.16–8.1 2.2–22 1.5–2.6 0.051–0.60

Lakes close to Sudburyd 0.017–0.08

1.7–10

Lake Eriee 0.8–3.9

Lake Balaton, Hungaryf 84±6 0.1±0.4 287±23 0.74±0.15

Lochnagar Lake, Scotlandg 234.4±82

223

20 lakes in USAc 0.88±1.09

250±610 1.2±1.8

Lake Baikal, Russiah 12.6 <0.07 161 0.12

Shahpura Lake, Indiai 188 24 5,390

Macrophytes 0.12–13 0.02–0.82

32–320 0.56–9.6

0.27–6.4 390–8,700 <0.05–7.5 4.6–95 <0.02–0.3

0.05–3.6

Lake Provala, Yugoslaviaj 18–132 10.0 1,325–1,831.7

Taupo Volcanic Zonek 12–1,222

7.6–34 29–586 0.09–55 1.3–3,400 1,200–12,000 0.06–1.3 31–267

0.12–1.0 0.46–1.21

Armenia and India lakesystemsl

85–586 1.88–55.0

8.0–3,380 18,000–112,000

Plecoptera larvae 0.43–7.1

0.09–0.93

98–255 0.39–5.3

0.95–8.3 640–4,800 <0.07–2.4 7.0–31 0.54–2.8 0.39–0.65

Ginzan creek, Japanm 0.31–13 78–1,800 0.10–4.0

Odonata 0.87–1.5

0.08–0.24

38–98 0.35–1.8

0.43–4.3 1,000–9,300 0.26–0.64 9.0–23 0.53–0.80

0.35–0.84

Lakes in Utah, USAn 1.9–11

Trichoptera 0.90–6.6

0.19–0.60

150–420 3.2–12 2.5–10.4 3,500–13,900 0.69–3.6 9.3–18 0.4–1.6 0.35–0.91

Ginzan creek, Japanm 1.2–33 130–2,900 0.18–6.1

Ephemeroptera 0.67–6.7

0.18–1.2 85–510 1.3–10 0.92–32 800–8,700 0.16–1.4 4.0–48 0.76–3.2 0.16–1.16

Lakes close to a smelterd 0.01–0.08 4.4–12.2

Ginzan creek, Japanm 1.2–21 81–12,300 0.23–4.8

Coleoptera

Lakes close to smeltersd 0.033 7.4

Mussels

Lake Balaton, Hungaryo 7.1–375 69.7–2,000 0.02–3.6

Missouri River Watershedp 129–812 1.16–2.00

Hyalella sp. 1.6–5.0 0.17–0.93

35–160 0.26–1.6

0.51–3.5 200–1,100 0.066–1.7 6.2–24 0.10–1.9 0.18–0.82

Hyalella azteca, lakes closeto smeltersd

0.008–0.035

0.95–6.0

Whole fish (galaxids + troutjuveniles)

0.07–1.0

0.089–0.62

100–330 0.03–0.39

0.09–3.4 50–750 0.059–1.3 8.9–31 0.88–2.2 0.20–1.3

Perca flavescens, lakes closeto smeltersd

380–2,400 2.7–10.7

Water Air Soil Pollut (2010) 212:167–182 175

Page 10

The gastropod and Hirudinea samples share negativecorrelations with K and positive correlations with Seand Zn. However, when examining PC3 scores(Fig. 3b), which correlates strongly with Br, (p value0.64), gastropods are separated from Hirudinea andOligochaeta, while the other macroinvertebrates retainsimilar associations with primary consumers. Hirudi-nea and Oligochaeta are both annelids, with Oligo-chaeta being detritivorous and Hirudinea acting asscavengers on other organisms. Interestingly, mostelements (except for Br, Co, and Fe) are similar orhigher in Oligochaeta than in Hirudinea, furthersupporting that detritus and biofilm are importantsources of elevated metals to the lower stages of thefood web. Smock (1983) also found that sediment-dependent organisms had the highest concentrationsof most elements.

Comparing the PCA scores for similar size preys,whole decapods Samastacus and Aegla, Diplodon,

and whole galaxids (Fig. 4), it is evident that wholegalaxids cluster away from all decapods. The elemen-tal contents of whole adult Samastacus and Aegla aredistributed equally between muscle and hepatopan-creas, while all Aegla values cluster closely, regard-less of tissue type or life stage. Samastacus muscleand hepatopancreas samples spread over a widerange, and as expected, muscle samples of both Aeglaand Samastacus form two compact groups, duemainly to the low variability of contents amongsamples. Small galaxid samples are grouped next toSamastacus muscle samples, which tend to havelower contents of As, Cr, and Fe and larger amountsof Rb and Cs. Aegla muscle samples are separatedfrom Samastacus, with higher contents Br and Na.Mussel data have very high scores for PC1 (4.7 and5.8), due to the high Fe contents, which are ten timeshigher than any of the other crustaceans’ contents (thesamples were included in the analysis, although these

Table 5 (continued)

Reference As Cs Zn Co Cr Fe Hg Rb Se Na (%)

Freshwater fish, Great SaltLake Basins, USAq

0.31–1.2

77–696 0.7–2.9 0.04–0.19 2–5.1

Perch juveniles, Wisconsinlakes, USAr

0.13–0.92

Perch juveniles, N Fork,Alene river, USAs

89 0.21

Data in italics are from this work (overall range for all samples). All values in mg/kg, in dry weight basis, except where indicateda Radwan et al. (1990);b Prahalad and Seenayya (1989)c Chen et al. (2000)d Belzile et al. (2006)e Adams and Johnson (1977)f Balogh (1988)g Yang et al. (2002)h Ciesielski et al. (2006)i Shrivastava et al. (2003)j Stanković et al. (2000)k Robinson et al. (2006)l Vardanyan and Ingole (2006)mWatanabe et al. (2008)n Hillwalker et al. (2006)o Salánki et al. (1982)p Schmitt et al. (2007)qWaddell and Giddings (2004)rWatras et al. (1998)s Farag et al. (1998)

176 Water Air Soil Pollut (2010) 212:167–182

Page 11

data are not shown in the graph to have a better detailof the low scores zone). The hepatopancreas of bothspecies spread over a wider range, which is expectedsince their composition depends on the more recentpreys, with higher contents of Co, Cr, As, and Fe.

Originally, the PC analysis of the galaxid samplesdid not show any grouping regarding length or site.However, when the sampling season was factored in,galaxids collected in summer tend to have lower As,Br, K, Cs, Rb, and Zn contents compared to thosecollected in other seasons (shown in Fig. 5). Thegalaxid diet consists of microcrustaceans (copepodsand cladocerans) as well as chironomid larvae andpupae. Two explanations can be proposed for thismarked trend for summer samples: (1) Galaxids may beswitching to low-metal dietary items during the muchmore productive summer season; (2) faster growth andturnover in the summer season may be leading to thebiodilution by growth of accumulated metals.

The large fish muscle samples show a compactarray in the PCA plots, with all species clusteringtogether, likely due to the narrower range of theelemental contents for fish compared to plankton,macrophytes, insects, and biofilm. The whole fishdata were also analyzed by PCA. Most elementalconcentrations are lower in fish muscle and higher infish liver samples compared to food sources, exceptfor Rb, Cs, and K (Tables 2, 3, and 4). The PCA

scores for muscle and liver samples are shown inFig. 6a, b, respectively. Figure 6a indicates that velvetcatfish muscle samples are characterized by high Br,Na, and Fe compared to salmonids and creole perch,while creole perch muscle samples are characterizedby high Se and low Fe concentrations. Brook troutand rainbow trout muscle metal trends are quitesimilar, but when liver tissue is analyzed, brook troutliver contents are more similar to those of creoleperch, especially regarding non-essential Ag andessential Se (see Fig. 6b).

Some authors had found that the Rb to Cs contentratios were indicators of fish diet (Kanevskii andFleishman 1972; Chiasson 1991). Although stronglimitations of the use of Rb–Cs ratios as indicator offish diet in local fish were found (Ribeiro Guevara etal. 2006), in this work, the Rb–Cs ratios of eachgroup of items were computed by using linearregression. The Rb vs. Cs correlation is significantfor each of the food items. The Rb–Cs ratiosmeasured for each group are as follows: macrophytes,44; nanoplankton, 11; microplankton, 15; macro-plankton, 56; biofilm, ten; insect larvae, 24; non-insectmacroinvertebrates, 25; galaxiids, 26; salmonids andperch, 14. However, the ratios show no trend regardingthe trophic level, and while Rb and Cs had differingtrends in the food items ordering, Rb and Cs are stronglyrelated to K in fish muscle. Therefore, since Rb and Cs

-1 0 1 2 3 4-4

-3

-2

-1

0

1

2

As

Ba

Br

Co

Cr

CsFe

Hg

NaRb

Se

Zn

-1.0 -0.5 0.0 0.5 1.0-1.0

-0.5

0.0

0.5

1.0

K

nanoplankton, 10-53 µmmicroplankton, 53-200 µmmacroplankton, >200 µmperiphytonsubmerged macrophytes mossses Trichoptera sp. Odonata sp. Plecoptera sp.Ephemeroptera sp. Coleoptera sp.

scor

es P

C2

scores PC1

Fig. 2 PCA ordination of nano-, micro-, and macroplankton; submerged macrophytes; submerged mosses; biofilm; and insect larvae fromLake Moreno and biplot of the elements

Water Air Soil Pollut (2010) 212:167–182 177

Page 12

are correlated to K in fish muscle, the intake is probablyrelated to the chemical similarities of these elements toK, and the amount of Rb and Cs to be incorporateddepends on the availability of these elements in theenvironment.

4 Conclusions

Except for nano -and microplankton, which tend togroup together in the PC analyses, all items showdistinctive compositional patterns, which can be

-1 0 1 2 3 4-4

-3

-2

-1

0

1

2

As

Br

Cr

Cs

Hg

NaRb

SeZn

nanoplankton microplankton macroplankton submerged macrophytes and mosses periphyton gasteropods (without shell) Hirudinea Amphipods Oligochaeta

scor

es P

C2

scores PC1

-1.0 -0.5 0.0 0.5 1.0-1.0

-0.5

0.0

0.5

1.0

FeCo

K

-1 0 1 2 3 4-3

-2

-1

0

1

2

scor

es P

C3

scores PC1

nanoplankton microplankton macroplankton submerged macrophytes and mosses periphyton gasteropods Hirudinea Amphipods Oligochaeta

-1.0 -0.5 0.0 0.5 1.0-1.0

-0.5

0.0

0.5

1.0

Cr

AsNa

CsRb

ZnHg

Se

Br

CoFe

K

a

b

Fig. 3 PCA ordination of Hyalella sp.; Hirudinea; gastropods;Oligochaeta; nano-, micro-, and macroplankton; submergedmacrophytes and mosses; and biofilm from Lake Moreno. a

PC2 scores vs. PC1, b PC3 scores vs. PC1. Biplot of theelements are shown to the right

178 Water Air Soil Pollut (2010) 212:167–182

Page 13

visualized as different groups in the biplots of theprincipal component scores.

Plankton, especially nano- and microplankton, isrich in some metals such as As, Co, Cr, Fe, Zn, andRb, followed by biofilm.

Biofilm is the more concentrated source of As, Co,Cr, Cs, Fe, Na, and Rb. Hg is also high in biofilmsamples, second only to nano- and microplankton. Onthe other hand, biofilm is low in Br and Se.

There is evidence that an increase in carnivory(trophic level) among the insects is accompanied by adecreased metal concentrations. Trichoptera havehigher concentration of most of the studied elementsthan the other insect larvae. This could be aconsequence of belonging to the functional feedinggroup of shredders–scrappers that feeds on biofilm,whose elemental contents are elevated compared toother primary producers. Carnivorous Odonata tends

-3 -2 -1 0 1 2-2

-1

0

1

2

4

5

As

Br

Co

Cr

Cs

Fe

Hg

K

Rb

Se

Zn

2

3

1

44

4

4

2

24

3

2

44 4 4

4

4

4

4

32

3

1

21

4 4

4

3

2

1

3

2

3

43

42

1

3

-0.2 0.0 0.2 0.4 0.6 0.8-0.6

-0.4

-0.2

0.0

0.2

0.4

0.6

0.8

1.0

Na

scor

es P

C2

scores PC1

GALAXIDS

1: summer2: autumn3: winter4: spring

Fig. 5 PCA ordination of whole galaxid samples indicating the sampling season. Biplot of the elements are shown to the right

-1.0 -0.5 0.0 0.5 1.0-1.0

-0.5

0.0

0.5

1.0

-1 0 1-1.5

-1.0

-0.5

0.0

0.5

1.0

1.5

2.0

2.5

3.0 Br

Co

Na

Se

Zn

CrHg

Rb

Cs

Fe

As

scor

es P

C2

scores PC1

Aegla sp. muscle Aegla sp. digestive gland Aegla sp. whole adults Aegla sp. whole juveniles Samastacus sp. muscle Samastacus sp. liver Samastacus sp. whole adults galaxids

Fig. 4 PCA ordination ofwhole galaxids; Aegla sp.muscle, digestive gland;whole Aegla sp. juvenilesand adults; and Samastacussp. muscle, digestive gland,and whole adults. Musselsoft tissues contents wereincluded in the analysis, andtheir PC1 scores lie between4.7 and 5.8

Water Air Soil Pollut (2010) 212:167–182 179

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-2 -1 0 1 2-2

-1

0

1

2

3

-3 -2 -1 0 1 2 3-2

-1

0

1

2

3

Br

Fe

Na

Se

Zn

Hg

Br

Fe

Na

Se

Zn

Hg

scor

es P

C3

scores PC2

-1.0 -0.5 0.0 0.5 1.0-1.0

-0.5

0.0

0.5

1.0

CsRb

K

scor

es P

C3

scores PC1

brown trout rainbow trout brook trout creole perch velvet catfish

-1.0 -0.5 0.0 0.5 1.0-1.0

-0.5

0.0

0.5

1.0

RbCs

K

-2 -1 0 1 2

-2

-1

0

1

2

-0.5 0.0 0.5 1.0-1.0

-0.5

0.0

0.5

1.0

AgSe

BrCr

FeHg

Na

ZnCsCo Rb

scor

es P

C2

scores PC1

brown trout rainbow trout brook trout creole perch

b

aFig. 6 PCA ordination ofadult fish muscle samples. aScores PC3 vs. scores PC1and scores PC3 vs. scoresPC2 for fish muscle; bscores PC2 vs. scores PC1for fish livers. Biplot of theelements are shownto the right

180 Water Air Soil Pollut (2010) 212:167–182

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to have lower elemental contents. Fish muscle, whichare the top predators of the studied species, have thelowest concentrations of most metals.

Aegla sp. soft tissues are richer in trace elementsthan Samastacus. Mussels have the highest contentsof iron, above the other items by a factor of 10.

Acknowledgments We acknowledge the assistance of Mr.Ricardo Sánchez in all the field work, Dr. M. Diéguez and Dr.C. Queimaliños for their help with the plankton samplers, Dr.R. Daga for the site characterization, Mr. J. Pérez duringplankton sampling, and the RA-6 reactor staff for the irradiationof the samples. This work was partially funded by projectsPICT2005 33838 and PICT2006 1051 of the ANPCyT(Agencia Nacional de Promoción Científica y Técnológica) ofArgentina.

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