at SciVerse ScienceDirect

Environmental Pollution 163 (2012) 109e116

Contents lists available

Environmental Pollution

journal homepage: www.elsevier .com/locate/envpol

Contaminant exposure in relation to spatio-temporal variation in dietcomposition: A case study of the little owl (Athene noctua)

Aafke M. Schipper a,*, Sander Wijnhoven b, Hans Baveco c, Nico W. van den Brink c

aRadboud University Nijmegen, Institute for Water and Wetland Research, Department of Environmental Science, P.O. Box 9010, 6500 GL Nijmegen, The NetherlandsbNetherlands Institute of Ecology (NIOO-KNAW), Centre for Estuarine and Marine Ecology, Monitor Taskforce, P.O. Box 140, 4400 AC Yerseke, The NetherlandscWageningen University and Research Centre Alterra, P.O. Box 47, 6700 AA Wageningen, The Netherlands

a r t i c l e i n f o

Article history:Received 25 July 2011Received in revised form6 December 2011Accepted 11 December 2011

Keywords:CadmiumExposure modelingFunctional responseSoil contaminationWildlife

* Corresponding author.E-mail address: A.Schipper@science.ru.nl (A.M. Sc

0269-7491/$ e see front matter � 2011 Elsevier Ltd.doi:10.1016/j.envpol.2011.12.020

a b s t r a c t

We assessed dietary exposure of the little owl Athene noctua to trace metal contamination in a DutchRhine River floodplain area. Diet composition was calculated per month for three habitat types, based onthe population densities of six prey types (earthworms, ground beetles and four small mammal species)combined with the little owl’s functional response to these prey types. Exposure levels showed a strongpositive relationship with the dietary fraction of earthworms, but also depended on the dietary fractionof common voles, with higher common vole fractions resulting in decreasing exposure levels. Spatio-temporal changes in the availability of earthworms and common voles in particular resulted inconsiderable variation in exposure, with peaks in exposure exceeding a tentative toxicity threshold.These findings imply that wildlife exposure assessments based on a predefined, average diet compositionmay considerably underestimate local or intermittent peaks in exposure.

� 2011 Elsevier Ltd. All rights reserved.

1. Introduction

Persistent environmental contaminants can accumulate in foodchains and pose toxicological risks to wildlife (Pascoe et al., 1996;Van den Brink et al., 2003; Smith et al., 2009). Food chain accu-mulation is governed not only by the environmental concentrationsof the contaminants, but also by the composition of the food web,as diet and prey items differ in the degree towhich they accumulateenvironmental contaminants (Schipper et al., 2008a). Hence,exposure levels are influenced by the availability of different dietand prey items as well as the foraging strategy and functionalresponse of the receptor species exposed. It has recently beenshown, for example, that the wood mouse (Apodemus sylvaticus),which has an opportunistic feeding strategy, has different accu-mulation patterns than the less opportunistic common vole(Microtus arvalis) (Van den Brink et al., 2011). Yet, although the dietof a target species may vary with habitat and through time (Preziosiand Pastorok, 2008), dietary exposure of wildlife to environmentalcontaminants is commonly estimated under the assumption ofa fixed, predefined dietary composition (e.g., Jongbloed et al., 1996;Pascoe et al., 1996; Hope, 2005; Smith et al., 2009; Sala et al., 2010),which may affect the accuracy of wildlife exposure assessments.

hipper).

All rights reserved.

The aim of the present studywas to investigate dietary exposureof wildlife to environmental contaminants in relation to spatio-temporal variation in diet composition. To that end, we assessedthe dietary exposure of the little owl (Athene noctua) to trace metalcontamination in a floodplain area along the Rhine River. The littleowl was selected because of its opportunistic feeding strategy andbecause its ecological characteristics are relatively well-known. It isthe smallest owl species breeding in the Netherlands, weighingbetween 155 and 210 g (Van den Brink et al., 2003). The species isterritorial and year-round residential (Groen et al., 2000) and hasa preference for open landscapes with scattered trees to breed in,agricultural areas like arable land and orchards, and open forests(Heinzel et al., 1972). Being an opportunistic feeder, the little owlforages on a wide range of prey types, including mammals, smallbirds, amphibians and invertebrates (Schönn et al., 1991; Groenet al., 2000; Hounsome et al., 2004). The common vole is gener-ally the most important prey species in terms of biomass, followedby mice and other vole species (Schönn et al., 1991). However,terrestrial invertebrates, in particular earthworms and beetles, arealso an important part of the little owl’s diet (Van Zoest and Fuchs,1988; Schönn et al., 1991; Hounsome et al., 2004). The species tendsto adapt to the local availability of prey, resulting in relatively largespatio-temporal variation in diet composition (Schönn et al., 1991).

In the Netherlands, the floodplains along the Rhine River are animportant breeding habitat for the little owl (Groen et al., 2000).These areas are contaminated with a mixture of sediment-bound

Fig. 1. Sampling sites and habitat types in the ‘Wolfswaard’ study area.

A.M. Schipper et al. / Environmental Pollution 163 (2012) 109e116110

pollutants and hence pose a potential toxicological risk to thebreeding individuals or their young. In our study the focus was oncadmium (Cd), as this contaminant in particular has been associ-ated with potential toxicological risks for wildlife in Rhine Riverfloodplains (Kooistra et al., 2001; Van den Brink et al., 2003).Cadmium exposure levels for the little owl were calculated basedon its daily intake of contaminated prey from three distinct habitattypes in a floodplain area along the Nederrijn River, which is one ofthe main Rhine River distributaries in the Netherlands. Dietcomposition was calculated based on monthly population densityestimates of earthworms, ground beetles and four small mammalspecies, combined with the little owl’s functional response to thesedifferent prey types. Cadmium concentrations in invertebrate preywere derived from soil concentrations. Concentrations in verte-brate prey species were calculated based on their assimilation ofcadmium from contaminated food. In this paper, we present anddiscuss the results of our calculations and address general impli-cations for wildlife exposure and risk assessment.

2. Methods

2.1. Study area and habitat types

The ‘Wolfswaard’ study area (51�570190 N; 5�390300 E) is located south of the cityof Wageningen along the Nederrijn River. It is part of a larger floodplain area that isembanked by a winter dike. Within the study area there is a minor embankmentparallel to the river at a distance of approximately 200 m from the middle of thechannel (Fig. 1). The main part of the study area is covered by semi-natural

Table 1Physicalechemical soil properties of the habitat types in the ‘Wolfswaard’ study area.

Floodplain (n ¼ 11) Pasture (n ¼ 7)

Mean SD Mean

pH 7.8 0.1 7.6Soil organic matter (%) 11.5 3.1 14.9Clay (%) 6.3 2.6 7.9Soil moisture (%) 36.0 7.7 36.3As (mg g�1 dry weight) 10.7 3.5 8.3Cd (mg g�1 dry weight) 1.90 0.85 0.91Cr (mg g�1 dry weight) 65.9 24.1 38.9Cu (mg g�1 dry weight) 50.0 18.6 31.9Hg (mg g�1 dry weight) 0.96 0.31 0.59Ni (mg g�1 dry weight) 24.6 6.7 25.3Pb (mg g�1 dry weight) 100.5 39.4 71.7Zn (mg g�1 dry weight) 284.2 93.6 172.9

grasslands and meadows, which are grazed by cattle. A small part of the area,which is surrounded by a hedgerow, is employed for sheep grazing and containssome scattered fruit trees. One of these trees provides a nesting site for a little owlbreeding pair. Based on differences in flooding frequency and land use, three habitattypes were distinguished (Fig. 1): the area between the river channel and the minorembankment (‘floodplain’), the grassland area protected from flooding by the minorembankment (‘pasture’), and the sheep meadow with scattered fruit trees(‘orchard’). At 30 sampling sites in the study area (Fig. 1), physicalechemical soilproperties were investigated as described in Schipper et al. (2010). Soil propertiesper habitat type are provided in Table 1.

2.2. Prey densities

Three prey categories were investigated: earthworms, ground beetles and smallmammals (voles, mice and shrews). Earthworms and beetles comprise importantinvertebrate prey for the little owl, whereas voles, mice and shrews are generallyamong the most important vertebrate prey items (Van Zoest and Fuchs, 1988;Schönn et al., 1991; Tomé et al., 2008). Prey densities (n m�2) were estimated permonth for each of the three habitat types. For earthworm and ground beetledensities, we used field data collected in the study area in 2007e2008. Earthwormdensity was determined by hand-sorting 30 � 30 � 20 cm soil cores collected from15 sampling sites. Ground beetle densities were derived from pitfall trap samplesobtained from 30 sites (Fig. 1). Small mammal densities were calculated based onmonitoring data obtained in a nearby floodplain area (Wijnhoven et al., 2006b). Foursmall mammal species were selected to represent the little owl’s vertebrate prey, i.e.,common vole (Microtus arvalis), bank vole (Clethrionomys glareolus), wood mouse(Apodemus sylvaticus) and common shrew (Sorex araneus). These species commonlyoccur in lowland Rhine River floodplains (Wijnhoven et al., 2005) and are confirmedto be part of the little owl’s diet (Van Zoest and Fuchs, 1988). Their presence in the‘Wolfswaard’ study area was confirmed by accidental by-catch in the pitfall trapsestablished for ground beetle collection. A detailed description of the prey densitycalculations is provided in Appendix 1 (Supplementary Material).

2.3. Calculation of daily intake

Cadmium exposure of the little owl was calculated per habitat type permonth asthe daily intake of cadmium, which was calculated based on the little owl’s dailyintake of food, its diet composition and the cadmium concentrations in the variousprey types (Eq. (1)). As wildlife commonly ingests soil while feeding (Beyer et al.,1994), the intake of cadmium directly from the soil was accounted for by addingthe amount of soil ingested as fraction of the total daily food intake. The daily foodintake (Eq. (2)) was estimated based on the little owl’s daily energy expenditure(DEE) combined with the energetic values of its prey types and the efficiency withwhich they are assimilated (Crocker et al., 2002):

DIt ¼ DFIt$

"Xmi¼1

�fi;t$Ci

�þ ðfs$CsÞ

#(1)

DFIt ¼ DEEPmi¼1

�fi;t$ECi$DMCi$FAE

� (2)

where DIt ¼ daily intake of cadmium in month t (mg d�1), DFIt ¼ daily food intake inmonth t (g d�1), fi,t ¼ weight fraction of prey type i in little owl’s diet in month t(dimensionless), Ci ¼ cadmium concentration of prey type i (mg g�1), m representsthe number of prey types, fs ¼ fraction ingested soil in the little owl’s diet(dimensionless), Cs ¼ cadmium concentration in soil (mg g�1), DEE ¼ daily energyexpenditure (kJ), ECi ¼ energy content of prey type i (kJ g�1 dry weight), DMCi ¼ drymatter content of prey type i (dimensionless), FAE ¼ food assimilation efficiency

Orchard (n ¼ 12) One-way ANOVA

SD Mean SD F p

0.1 7.5 0.1 10.55 0.0001.1 10.0 1.9 5.33 0.0111.3 6.1 2.2 1.59 0.2229.2 39.2 4.6 0.40 0.6722.3 5.8 1.6 10.02 0.0010.38 0.65 0.25 14.89 0.000

14.5 23.9 6.9 18.21 0.0008.2 25.3 10.0 9.93 0.0010.17 1.13 0.92 1.66 0.2087.5 17.3 4.2 5.75 0.008

25.4 59.5 14.2 6.22 0.00661.7 150.1 39.3 11.91 0.000

Table 2Regression equations for calculating cadmium concentrations in diet items.

Diet item Regression equationa Additional information and references

Vegetation log (Cdi) ¼ 0.17 þ 0.49$log (Cds) � 0.12pH � 0.28$log (SOM)

Regression equation for grass based on a nationwide database for the Netherlands(r2 ¼ 0.53) (Van Wezel et al., 2003).

Seeds Cdi ¼ 0.3$Cdgrass Based on the geometric means of cadmium concentrations measured in grass seeds(n ¼ 5) and grass (n ¼ 8) (Van den Brink et al., 2010).

Berries Cdi ¼ 0.4$Cdgrass Based on the geometric means of cadmium concentrations measured in berries (n ¼ 2)and grass (n ¼ 8) (Van den Brink et al., 2010).

Ground beetles ln (Cdi) ¼ �0.27 þ 0.29$ln (Cds) Floodplain-specific equation; based on total cadmium concentrations measured in soiland beetles (Coleoptera) from a lowland floodplain of the Rhine River in the Netherlands(n ¼ 33, r2 ¼ 0.46, p < 0.01) (Schipper et al., 2008b).

Earthworms log (Cdi) ¼ 1.3 þ 0.32$log (Cds) Floodplain-specific equation; based on total cadmium concentrations in soil and in threecommon earthworm species from a lowland floodplain of the Rhine River in theNetherlands (n ¼ 67, r2 ¼ 0.05, p ¼ 0.07) (Van Vliet et al., 2005).

a Cdi¼ cadmium concentration in diet item i (mg g�1 dry weight); Cds¼ cadmium concentration in soil (mg g�1 dry weight); pH¼ soil pH (dimensionless); SOM¼ soil organicmatter content (%).

A.M. Schipper et al. / Environmental Pollution 163 (2012) 109e116 111

(dimensionless). Values for fs, DEE, ECi, DMCi and FAE were derived from the liter-ature (Table S5; Supplementary Material). The cadmium concentrations in soil(Table 1) were converted from dry weight towet weight values based on the averagesoil moisture content per habitat type.

The fraction of prey type i in the little owl’s diet in month t (fi,t) was calculated asthe functional response of the little owl to that prey type multiplied by the prey’sbody mass in order to obtain dietary fractions on a weight basis (Eq. (3)). Thefunctional response (Fi) describes the intake rate of prey type i in relation to thedensity of that prey type. We applied a so-called Type II response, assuming that thelittle owl spends its time on two mutually exclusive activities: searching for prey,expressed as the encounter chance (ei), and handling of prey (hi), which includeschasing, killing, consuming and digesting (Holling, 1959). The multi-species exten-sion of Murdoch (1973) was used to account for the different prey types included inthe little owl’s diet (Eq. (4)):

fi;t ¼ Fi;t$BMiPmi¼1 Fi;t$BMi

(3)

Fi;t ¼

Di;t$ei1þP�Di;t$ei$hi

�!

(4)

where Fi,t¼ functional response to prey type i inmonth t (n d�1), BMi¼ bodymass ofan individual of prey type i (g), Di,t ¼ density of prey type i in month t (n m�2),ei¼ encounter chance of an individual of prey type i (m2 d�1), and hi¼ handling timeof prey type i (d n�1). The encounter chance e depends on the area that a predatorinvestigates in its search for food. We assumed this area to be independent of thetype of prey. However, the more mobile a prey item, the more easily it may bedetected. As a larger home range implies more mobility and thus a higher encounterchance, we assumed the encounter chance of each prey type i to be proportional toits typical home range size, independent of its population density. Home range sizesand values for handling timewere derived from the literature (Table S5). Earthwormbody mass was obtained from study area-specific measurements; body mass valuesfor ground beetles and small mammals were derived from the literature (Table S5).

Cadmium concentrations Ci in small mammal prey were calculated from theirfeeding rate, the cadmium concentrations in their diet, their cadmium assimilationefficiency (AE) and elimination rate (k), and their age (A) when consumed by thelittle owl (Eq. (5)):

Table 3Cadmium concentrations (mg g�1 dry weight) in food and prey items calculated for the t

Diet item Calculated Reported Addi

Floodplain Pasture Orchard

Vegetation 0.12 0.082 0.078 0.047 (0.026e0.16) Geomet al.

Seeds 0.040 0.027 0.026 0.14; 0.17 Measconce

Berries 0.030 0.020 0.020 na e

Earthworms 24.5 19.4 17.4 16.9 (5.9e38.4) Mean(Wijn

Ground beetles 0.92 0.74 0.67 0.70 (0.30e1.80) Geomet al.

Bank vole 0.33 0.073 0.064 0.68 (0e11.4) MeanCommon shrew 4.52 3.57 3.20 3.49 (0.004e29.0) MeanCommon vole 0.12 0.07 0.07 0.98 (0.001e7.81) MeanWood mouse 1.53 1.19 1.07 2.03 (0.001e21.3) Mean

na ¼ not available.

Ci ¼ DFIiBMi

$hX�

fj;i$Cj�þ ðfs$CsÞ

i$AEiki

$�1� e�ki$Ai

�(5)

where Ci¼ cadmium concentration in prey type i (mg$g�1), DFIi¼ daily food intake ofprey type i (g d�1), BMi ¼ body mass of prey type i (g), fj,i ¼ fraction of diet item j inthe diet of prey type i (dimensionless), Cj ¼ cadmium concentration in diet item j(mg g�1), fs ¼ fraction ingested soil in the diet of prey type i (dimensionless),Cs ¼ cadmium concentration in soil (mg g�1), AEi ¼ cadmium assimilation efficiencyof prey type i (dimensionless), ki ¼ cadmium excretion rate of prey type i (d�1), andAi ¼ age (d) of prey type i when consumed by the little owl. Values of DFIi, fj,i, fs, AEiand ki were derived from the literature (Table S5). The typical age at which a certainprey species is consumed by a predator might be influenced by preferences for preyof certain age or weight classes, as well as processes in the prey populations(Goszczy�nski, 1977; Petrusewicz, 1983). As quantitative data for Ai were not avail-able, we used a generic value of 200 days. Cadmium concentrations in vegetable andinvertebrate diet items were derived from soil concentrations (dry weight) withregression equations or bioaccumulation factors obtained from the literature(Table 2). Floodplain-specific relationships were used where possible. Resulting dryweight concentrations were converted to fresh weight concentrations using drymatter content values (Table S5). Cadmium concentrations in diet and prey itemswere in line with values measured in comparable lowland floodplain areas of Rhineand Meuse (Table 3), indicating that our exposure calculations are based on realisticfood web contamination levels.

3. Results

3.1. Prey densities and diet composition

On average, earthworms were the most important prey in termsof available biomass. They comprised over 60% of the available preybiomass in each of the three habitat types (Fig. 2). Ground beetles(approximately 20%) and common voles (approximately 15%) alsoaccounted for a relatively large part of the available prey biomass,whereas bank voles, wood mice and common shrews each

hree habitat types in comparison with values reported in the literature.

tional information and reference

ean (minemax) measured in grass in ‘Heteren’ floodplain; n ¼ 4 (Van den Brink, 2010)ured for seeds of Elytrigia repens in floodplains of the Meuse with soil cadmiumntrations of 1.6e12.3 mg kg�1 dry weight (Verkleij et al., 2000)

(minemax) measured in ‘ADW’ floodplain (regularly flooded sites only); n ¼ 12hoven et al., 2006a)ean (minemax) measured in ‘Gelderse Poort’ floodplain; n ¼ 3 (Van den Brink, 2003)(minemax) measured in ‘ADW’ floodplain; n ¼ 56 (Wijnhoven et al., 2007)(minemax) measured in ‘ADW’ floodplain; n ¼ 65 (Wijnhoven et al., 2007)(minemax) measured in ‘ADW’ floodplain; n ¼ 31 (Wijnhoven et al., 2007)(minemax) measured in ‘ADW’ floodplain; n ¼ 21 (Wijnhoven et al., 2007)

Fig. 2. Yearly mean available prey biomass distribution (%; left), diet composition (% weight; centre) and the contribution (%) of each prey type to the little owl’s daily intake (DI) ofcadmium (right) for the three habitat types in the ‘Wolfswaard’ study area.

A.M. Schipper et al. / Environmental Pollution 163 (2012) 109e116112

constituted less than 1% (Fig. 2). The diet composition of the littleowl showed a different pattern, with the common vole being themost important prey, accounting for approximately 50% of the diet(by weight) in each of the three habitat types, followed by earth-worms and ground beetles (Fig. 2). Thus, while earthwormsaccounted for most of the available prey biomass, the common volewas a more important food source. This is due to the influence ofthe functional response, which is stronger for common voles thanfor earthworms, resulting in a relatively large dietary fraction ofcommon voles at the prevailing prey densities (Fig. 3). Small

earthwormscommon volebank volewoodmousecommon shrewground beetles

0

20

40

60

80

100

120

0.0 0.2 0.4 0.6 0.8 1.0

0

10

20

30

40

50

0.0 0.2 0.4 0.6 0.8 1.0

Relative prey density

diet

ary

fract

ion

(%)

daily

inta

ke (µ

g·d-

1 )

Fig. 3. Dietary fraction (%; top) and daily cadmium intake (mg d�1; bottom) as functionof the density of each prey type in the floodplain habitat type. To facilitate comparison,the density of each prey type was varied relative to its yearly mean density (n m�2)with the densities of the other prey types fixed at their yearly mean values.

mammal species other than the common vole constituted a minorpart of the little owl’s diet, although their contribution was some-what larger in the orchard than in the floodplain and pasturehabitat types (Fig. 2). Due to prey-specific fluctuations in biomass(Fig. 4; Table S6), the diet composition of the little owl showedconsiderable temporal variation (Fig. 4). The contribution of smallmammals to the diet was particularly large during the wintermonths. Ground beetles were important mainly in spring andsummer and contributed little to the diet from September to April.The contribution of earthworms showed two peaks: a firstmaximum in early spring (FebruaryeMarch) and a second, gener-ally smaller peak in AugusteSeptember. The peak in early springwas particularly large for the floodplain, where earthwormsconstituted almost 80% of the little owl’s diet in February andMarch (Fig. 4).

3.2. Exposure to cadmium

The mean daily intake of cadmium was highest for the flood-plain habitat type, followed by the pasture and the orchard habitattypes (Fig. 5). The daily intake showed a strong positive correlationwith the fraction of earthworms in the little owl’s diet (r2 ¼ 0.91).On average, earthworms accounted for 83% of the daily cadmiumintake in the orchard and up to 93% of the daily intake in thepasture (Fig. 2). With the densities of all other prey types fixed attheir mean values, the daily intake corresponding with a meanearthworm density in the floodplain habitat type was nearlya factor of 6 higher than for a situation without earthworms (i.e.,worm density of 0; Fig. 3). In addition, there was a relativelystrong negative correlation between the daily intake and thedietary fraction of common voles (r2 ¼ 0.33), with daily intakevalues decreasing by a factor of 2 from zero to mean common voledensities (Fig. 3). Due to the dominant contribution of earthwormsto the total daily intake of cadmium, temporal variations in thedaily intake (Fig. 6) reflected the fluctuations in the earthwormshare of the diet (Fig. 4). The daily intake was mostly low for thewinter months (NovembereJanuary), when the fraction of

earthworms

common vole

bank vole

woodmouse

common shrew

ground beetles

Floo

dpla

inPa

stur

eO

rcha

rd

Diet compositionAvailable prey biomass

0%

20%

40%

60%

80%

100%

J F M A M J J A S O N D

0%

20%

40%

60%

80%

100%

J F M A M J J A S O N D

0%

20%

40%

60%

80%

100%

J F M A M J J A S O N D

0%

20%

40%

60%

80%

100%

J F M A M J J A S O N D

0%

20%

40%

60%

80%

100%

J F M A M J J A S O N D

0%

20%

40%

60%

80%

100%

J F M A M J J A S O N D

Fig. 4. Available prey biomass (left) and the little owl’s diet composition (right) for the habitat types ‘floodplain’ (top), ‘pasture’ (centre) and ‘orchard’ (bottom).

daily

inta

ke (µ

g·d-

1 )

0

50

100

150

200

250

300

J F M A M J J A S O N D mean

floodplainpastureorchardTDI

A.M. Schipper et al. / Environmental Pollution 163 (2012) 109e116 113

earthworms in the diet was negligible. High daily intake valueswere found for early spring, particularly for the floodplain habitattype, which coincided with the first dietary peak in earthworms.In summer and autumn (JuneeOctober), when the share ofearthworms was higher in the pasture than in the floodplain(Fig. 4), the daily intake was also highest in the pasture (Fig. 6).The daily intake values for the floodplain habitat type in Februaryand March were about twice as high as the tolerable daily intake(TDI) derived from a no observed adverse effect level (NOAEL) of8.0 mg g�1 d�1 for mallard ducks (Pascoe et al., 1996) combinedwith a safety factor of 10 to account for inter-species differences insensitivity (Morrissey et al., 2005). For the orchard and pasturehabitat types, all monthly daily intake values were below thiscritical toxicity level (Fig. 6).

0.0

0.5

1.0

1.5

2.0

2.5

3.0

Floodplain Pasture Orchard

Habitat type

0

40

80

120

160

200

soil concentrationdaily intake

daily

inta

ke (µ

g·d-

1 )

Cd s

oil(

µg·g

-1 d

ry w

eigh

t)

Fig. 5. Mean cadmium concentrations in the soil (mg g�1 dry weight) and the littleowl’s mean daily intake of cadmium (mg d�1) per habitat type.

Fig. 6. The little owl’s daily intake of cadmium (mg d�1) per habitat type per month.The yearly mean daily intake was included for comparison. TDI ¼ tolerable daily intake,based on a little owl body weight of 185 g, a no observed adverse effect level (NOAEL)for water fowl of 8.0 mg g�1 d�1 (Pascoe et al., 1996), and a safety factor of 10 to accountfor inter-species differences in sensitivity (Morrissey et al., 2005).

Table 4Diet composition estimated for the little owl in the ‘Wolfswaard’ study area, basedon the three habitat types (n ¼ 3), compared with dietary fractions reported for the‘Achterhoek’ region in the Netherlands (n ¼ 7). Values are specific to the breedingseason (April, May, June).

Diet item ’Wolfswaard’ ‘Achterhoek’a

mean range mean range

Earthworms 20.0 13.9e24.4 19.3 6.7e40.3Beetles 33.4 22.8e42.5 10.6 3.4e22.0Small mammals 42.1 34.1e55.2 34.4 15.4e60.0Mice 3.2 2.8e4.0 23.4 7.9e47.8Voles 38.9 31.3e51.3 11.0 3.1e21.4Shrews 4.4 1.5e8.1 0.1 0e0.4

Other e e 35.6 15.6e58.6

a From: Van den Bremer et al., 2009; Van Harxen and Stroeken, 2009.

A.M. Schipper et al. / Environmental Pollution 163 (2012) 109e116114

4. Discussion and conclusions

4.1. Diet composition

We calculated the little owl’s diet composition based on thepopulation densities of various prey types combined with the littleowl’s functional response to the prey. The resulting diet fractionsare difficult to verify, because temporally explicit floodplain-specific data on the diet of the little owl are, to our knowledge,not available. Comparison with data reported in other studies ishampered by differences in habitat characteristics, which mayintroduce significant variability in prey availability (Schönn et al.,1991). Moreover, dietary fractions reported in the literature mayvary due to differences in the underlying research methods. Forexample, pellet analysis tends to result in an underestimation of theearthworm share of the diet, as pellets contain mainly hard preyparts like bones and beetle shields, whereas soft tissue is hardlypreserved (Beersma et al., 2007). Notwithstanding such limitations,however, comparisonwith independent data may indicatewhetherthe dietary fractions estimated in our study are within realisticranges. On average, the common vole turned out to be the mostimportant prey species in terms of biomass (Fig. 2), which agreeswith the conclusion of Schönn et al. (1991). The share of smallmammals was particularly large in winter, whereas ground beetlesand earthworms tended to be more important in spring andsummer (Fig. 4). This is again consistent with the findings ofSchönn et al. (1991). They report that the invertebrate share of thediet is generally large in early summer, when themaximum densityof arthropods is present, whereas invertebrates tend to be replacedby small mammals during the winter months. A more detailedcomparison can be made with dietary fractions based on videorecordings of prey delivered to nesting sites in the ‘Achterhoek’region in the Netherlands (Van den Bremer et al., 2009; Van Harxenand Stroeken, 2009). As these observations were restricted to thebreeding season and much of the delivered prey was fed to thechicks, these dietary fractions may be biased by the needs of thechicks and possibly be less representative of the adults’ diet. Yet,the use of video recordings circumvents the limitations of pelletanalysis. Moreover, the two areas are expected to have similarhabitat characteristics, despite the absence of periodical flooding inthe ‘Achterhoek’ region, as both areas comprise small-scale agri-cultural landscapes with grassland and scattered trees (Van denBremer et al., 2009). The comparison shows that the diet calcu-lated in our study does not include all potential diet items (Table 4).Being an opportunistic feeder, the little owl has a wide range ofpotential prey, including not only small mammals, earthworms andground beetles, but also small passerines, amphibians, smallreptiles, snails, slugs, and arthropods like cockchafers, earwigs andcaterpillars (Schönn et al., 1991; Van den Bremer et al., 2009; VanHarxen and Stroeken, 2009). Neglecting these groups may resultin the fractions of the other prey being somewhat overestimated.Nevertheless, the major part of the diet recorded for the ‘Achter-hoek’ region was covered by the three prey groups included in ourstudy (Table 4). In both studies, small mammals accounted forabout one third of the diet, although the fractions of voles andshrews tended to be larger for the ‘Wolfswaard’ study area, whereasthe fraction of mice was larger in the ‘Achterhoek’ region. This maybe related to habitat differences between the study areas. Woodmice typically prefer shrubs and bushes (Wijnhoven et al., 2006b),whichmay bemore abundant in the ‘Achterhoek’ region than in the‘Wolfswaard’ area, as vegetation with a relatively high hydraulicroughness is commonly minimized in Dutch floodplains to preventobstruction of flood water (Makaske et al., 2011). The fraction ofbeetles was considerably larger in our study than reported for the‘Achterhoek’ region (Table 4). Although the ground beetle densities

calculated in our study are within the ranges of ground beetledensities reported elsewhere (Baars, 1979; Lang, 2000), the func-tional response calculations (Eq. (4)) rely on parameters that aredifficult to quantify, like the encounter chance and handling time.This may have introduced some uncertainty in the dietary fractions.Yet, as ground beetles contribute only little to the total daily intakeof cadmium (Fig. 2), the possible overestimation of the groundbeetle densities is expected to have only minor influence on theestimated exposure levels. The earthworm fractions calculated inthe present study were nearly similar to the earthworm fractionsreported for the ‘Achterhoek’ region (Table 4), indicating thatearthworm fractions were within realistic ranges at least for themonths April to June.

4.2. Exposure levels

For several of the input parameters required to calculate thelittle owl’s daily food intake (DFI), including the daily energyexpenditure (DEE), food assimilation efficiency (FAE) and theenergy content (EC) of prey (Eq. (2)), species-specific data werelacking. This is a common limitation in wildlife exposure modeling,where input data are nearly always incomplete, with large andunknown amounts of uncertainty (Loos et al., 2010). Yet, theresulting values for DFI, ranging from 51 to 83 g d�1, agreewell withthe range of 50e80 g d�1 as reported in the literature (Schönn et al.,1991). This indicates that our exposure estimates are based onrealistic estimates of the amount of food consumed. The little owl’sexposure to cadmium was mainly dependent on the dietary frac-tion of earthworms (Fig. 3). Earthworms are characterized byconsiderably higher cadmium concentrations than other preycategories (Table 3). Moreover, the energy content of earthworms isrelatively low (Table S5), implying that an increase in the dietaryfraction of earthworms coincides with an increase in the little owl’sdaily food intake (Eq. (2)), thus yielding a higher intake ofcadmium. Daily intake values were also clearly influenced by thepopulation densities of the common vole (Fig. 3). As common volesfeed predominantly on vegetation, they are characterized by rela-tively low body burdens of cadmium (Veltman et al., 2007;Wijnhoven et al., 2007). Hence, if the dietary fraction of commonvoles increases at the expense of the fractions of diet items withhigher cadmium body burdens (i.e., earthworms), the little owl’sdaily intake of cadmium decreases. So, despite its low cadmiumcontent, the common vole is an important factor in the assessmentof the little owl’s daily intake. This is clearly illustrated by the highdaily intake values for the floodplain habitat type in February andMarch (Fig. 6). The yearly winter flooding that is characteristic ofthe floodplain habitat type reduces the availability of smallmammals, as they survive only on high water free areas (Groenet al., 2000; Wijnhoven et al., 2005). Contrastingly, earthwormsare well adapted to survive in inundated soils, with survival timesranging up to several months (Roots,1956). The reduced availabilityof small mammals results in a larger share of earthworms in thelittle owl’s diet, yielding a peak in the daily cadmium intake. As theorchard and pasture habitat types are protected from flooding by anembankment, these habitat types were characterized by a largercommon vole biomass in February and March (Table S6). Thisresulted in larger dietary fractions of common voles (Fig. 4) andlower exposure levels (Fig. 6).

Exposure levels calculated in this study are specific to a yearwith a winter flood in the floodplain habitat type, i.e., a flood nottransgressing theminor embankment. However, the timing and themagnitude of the flood, and hence the influence on small mammaldensities, may vary between years. During years without a flood,the densities of common voles and other small mammals are ex-pected to be higher in the floodplain habitat type. This will lead to

A.M. Schipper et al. / Environmental Pollution 163 (2012) 109e116 115

a smaller share of earthworms in the little owl’s diet and a corre-sponding decrease in the contaminant exposure of the little owl.Contrastingly, a summer flood in the floodplain habitat type ora high-magnitude flood transgressing the minor embankment isexpected to result in an overall decrease of the small mammaldensities, hence an increase in both the dietary fractions of earth-worms and the exposure of the little owl to cadmium. Thus, year-to-year changes in the flooding regime may lead to fluctuationsin exposure levels in addition to the variation observed within oneyear.

4.3. Potential toxicological risks

In the floodplain habitat type, the daily cadmium intakeexceeded a tolerable daily intake (TDI) in FebruaryeApril (Fig. 6),indicating that negative health impacts of cadmium on little owlscannot be excluded in recently flooded and contaminated flood-plain areas. This is in agreement with the findings of Van den Brinket al. (2003), who concluded that cadmium in Rhine River flood-plains may pose a risk if little owls are feeding mainly on earth-worms. Groen et al. (2000) compared the little owl breedingsuccess between a floodplain nearby our study area (‘GeldersePoort’) and an uncontaminated reference area (‘Achterhoek’). Theyobserved reduced clutch size (3.0 compared to 4.4 eggs per pair)and reduced breeding success (1.5 compared to 2.3 young per pair)in breeding seasons following winter flooding. However, theseindications of toxic effects are difficult to verify. Because toxicitythresholds specific to the little owl are lacking, we used a NOAEL foranother avian species (adult mallard ducks, 8.0 mg g�1 d�1) andcombined it with a safety factor (10) to account for inter-speciesdifferences in sensitivity. The resulting tolerable daily intake (TDI)of 0.8 mg g�1 d�1 corresponds with a lowest observed adverse effectlevel (LOAEL) for mallard ducklings, which exhibited altered bloodchemistry and kidney lesions after 12 weeks of exposure (Pascoeet al., 1996). Further, the TDI is close to the threshold of0.54 mg g�1 d�1 as estimated for the American dipper Cinclusmexicanus (Morrissey et al., 2005). Yet, as species may considerablydiffer in their sensitivity to toxicants (Shore and Douben, 1994), it isunknownwhether these threshold levels provide valid benchmarksfor assessing toxic effects on the little owl. Moreover, reducedbreeding success in recently flooded floodplains, as observed byGroen et al. (2000), may relate not only to flooding-induced peaksin the intake of contaminants, but also to the reduced availability offood. In addition, the nutritional value of earthworms may beinferior to the quality of small mammals. Thus, changes in thequantity and quality of the food per se could also explain reducedclutch size and breeding success in recently flooded areas. Repro-ductive success in barn owls (Strix aluco), for example, has beenassociated with the numbers and availability of rodent prey,whereby decreasing numbers of fledged young have been observedin relation to decreasing rodent densities (Southern, 1970). Hence,for obtaining more accurate estimates of toxicological risks, it isvital to obtain more reliable information on the little owl’s sensi-tivity to toxicants.

4.4. General implications for wildlife exposure and risk assessment

In addition to spatio-temporal changes in prey densities, varia-tion in various other factors may induce variability in the little owl’sdaily intake. For example, temporal changes in the activity patternsof prey species may yield variation in the encounter change (ei),thus changing the little owl’s functional response and hence its dietcomposition. Cadmium concentrations in diet and prey items mayshow large inter-individual variation (Table 3), due to for exampleage differences (Wijnhoven et al., 2007; Schipper et al., 2008a),

which could also yield variation in exposure that has not beenaccounted for in our study. Despite these limitations, however, ourresults have a few general implications for wildlife exposure andrisk assessment. First, our findings illustrate that dietary exposureof wildlife to soil contamination is not directly related to thecontamination levels in soil. Whereas the cadmium concentrationin soil was more than a factor of 2 higher in the floodplain habitattype than in the pasture habitat type, the relative differencebetween the daily intake values of these two habitat types wasmuch smaller (Fig. 5). Moreover, for the months June to October,exposure levels were higher in the pasture than in the morecontaminated floodplain habitat type (Fig. 6), due to the largerdietary fraction of earthworms in the pasture (Fig. 4). Second, ourresults showed that not only highly contaminated but also rela-tively uncontaminated diet items are important in governingaccumulation patterns in food webs. The little owl’s exposure tocadmium not only showed a strong positive relationship with thedietary fraction of earthworms, but also depended on the dietaryfraction of common voles, with larger common vole fractionsresulting in decreasing exposure levels. These findings imply thatreliable information on the availability and contaminant concen-trations of prey and the foraging strategy of the receptor species isvital for obtaining realistic estimates of dietary exposure levels andrisks of secondary poisoning. Finally, our results showed thatcontaminant exposure of wildlife species with an opportunisticfeeding strategy may vary considerably due to spatial and temporalvariation in the availability of different diet items. The daily intakevalues calculated for the little owl (n ¼ 36; Fig. 6) were character-ized by an overall coefficient of variation of 113%. Temporal varia-tion was larger than spatial variation: differences in daily intakevalues between the habitat types ranged up to a factor of 4, whereastemporal differences within a specific habitat type ranged up toa factor of 58. Overall, there was a factor of 2e3 difference betweenthe yearly maximum and the yearly mean daily intake values. Themaximum daily intake values were exceeding a tentative toxicitythreshold, whereas the mean daily intake values were well belowthis critical level (Fig. 6). These findings imply that the use of spatio-temporally averaged exposure estimates may considerably under-estimate local and intermittent peaks in exposure, which is causefor concern in particular if acute or short-term toxicity thresholdsare crossed.

Acknowledgements

We would like to thank Annemariet van der Hout for the earth-worm sampling. Funding for AS was provided by The NetherlandsOrganisation for Scientific Research (NWO) within the LOICZprogram (project 014.27.007). Funding for NvdB and HB was ob-tained from the INSPECT project funded by the SNOWMANnetwork(www.snowmannetwork.com) and the DutchMinistry of EconomicAffairs, Agriculture and Innovation (project KB-17-002.01-003-ALT1). This is publication 5153 of the Netherlands Institute ofEcology (NIOO-KNAW).

Appendix. Supplementary material

Supplementary material associated with this article can befound, in the online version, at doi:10.1016/j.envpol.2011.12.020

References

Baars, M.A., 1979. Catches in pitfall traps in relation to mean densities of carabidbeetles. Oecologia 41, 25e46.

Beersma, P., Beersma, W., Van den Burg, A., 2007. Steenuilen. Tirion, Zutphen.Beyer, W.N., Connor, E.E., Gerould, S., 1994. Estimates of soil ingestion by wildlife.

Journal of Wildlife Management 58, 375e382.

A.M. Schipper et al. / Environmental Pollution 163 (2012) 109e116116

Crocker, D., Hart, A., Gurney, J., McCoy, C., 2002. Methods for Estimating Daily FoodIntake of Wild Birds and Mammals. Report PN0908. Central Science Laboratory,York.

Goszczy�nski, J., 1977. Connections between predatory birds and mammals and theirprey. Acta Theriologica 22, 399e429.

Groen, N.M., Boudewijn, T.J., De Jonge, J., 2000. De effecten van overstroming van deuiterwaarden op de steenuil. De Levende Natuur 5, 143e148.

Heinzel, H., Fitter, R.S.R., Parslow, J.F., 1972. The Birds of Britain and Europe, withNorth Africa and the Middle East. Collins, London.

Holling, C.S., 1959. Some characteristics of simple types of predation and parasitism.Canadian Entomologist 91, 385e398.

Hope, B.K., 2005. Performing spatially and temporally explicit ecological exposureassessments involving multiple stressors. Human and Ecological Risk Assess-ment 11, 539e565.

Hounsome, T., O’mahony, D., Delahay, R., 2004. The diet of little owls Athene noctuain Gloucestershire, England. Birds Study 51, 282e284.

Jongbloed, R.H., Traas, T.P., Luttik, R., 1996. A probabilistic model for deriving soilquality criteria based on secondary poisoning of top predators. II. Calculationsfor Dichlorodiphenyltrichloroethane (DDT) and cadmium. Ecotoxicology andEnvironmental Safety 34, 279e306.

Kooistra, L., Leuven, R.S.E.W., Wehrens, R., Buydens, L.M.C., Nienhuis, P.H., 2001.A procedure for incorporating spatial variability in ecological risk assessment ofDutch river floodplains. Environmental Management 28, 359e373.

Lang, A., 2000. The pitfalls of pitfalls: a comparison of pitfall trap catches andabsolute density estimates of epigeal invertebrate predators in arable land.Anzeiger fur Schadlingskunde 73, 99e106.

Loos, M., Schipper, A.M., Schlink, U., Strebel, K., Ragas, A.M.J., 2010. Receptor-oriented approaches in wildlife and human exposure modelling: a comparativestudy. Environmental Modelling and Software 25, 369e382.

Makaske, B., Maas, G.J., van den Brink, C., Wolfert, H.P., 2011. The influence offloodplain vegetation succession on hydraulic roughness: is ecosystem reha-bilitation in Dutch embanked floodplains compatible with flood safety stan-dards? Ambio 40, 370e376.

Morrissey, C.A., Bendell-Young, L.I., Elliotti, J.E., 2005. Assessing trace-metal expo-sure to American dippers in mountain streams of southwestern BritishColumbia, Canada. Environmental Toxicology and Chemistry 24, 836e845.

Murdoch, W.W., 1973. Functional response of predators. Journal of Applied Ecology10, 335e342.

Pascoe, G.A., Blanchet, R.J., Linder, G., 1996. Food chain analysis of exposure andrisks to wildlife at a metals-contaminated wetland. Archives of EnvironmentalContamination and Toxicology 30, 306e318.

Petrusewicz, K., 1983. Ecology of the bank vole. Acta Theriologica 28 (Suppl. 1),1e242.

Preziosi, D.V., Pastorok, R.A., 2008. Ecological food web analysis for chemical riskassessment. Science of the Total Environment 406, 491e502.

Roots, B.I., 1956. The water relations of earthworms. 2. Resistance to desiccation andimmersion, and behaviour when submerged and when allowed a choice ofenvironment. Journal of Experimental Biology 33, 29e44.

Sala, S., Cavalli, M., Vighi, M., 2010. Spatially explicit method for ecotoxicologicalrisk assessment of pesticides for birds. Ecotoxicology and Environmental Safety73, 213e221.

Schönn, S., Scherzinger, W., Exo, K.-M., Ille, R., 1991. Der Steinkauz. Ziemsen Verlag,Wittenberg Lutherstadt.

Schipper, A.M., Loos, M., Ragas, A.M.J., Lopes, J.P.C., Nolte, B., Wijnhoven, S.,Leuven, R.S.E.W., 2008a. Modeling the influence of environmental heteroge-neity on heavy metal exposure concentrations for terrestrial vertebrates inriver floodplains. Environmental Toxicology and Chemistry 27, 919e932.2627e2628.

Schipper, A.M., Wijnhoven, S., Leuven, R.S.E.W., Ragas, A.M.J., Hendriks, A.J., 2008b.Spatial distribution and internal metal concentrations of terrestrial arthropodsin a moderately contaminated lowland floodplain along the Rhine river. Envi-ronmental Pollution 151, 17e26.

Schipper, A.M., Lotterman, K., Geertsma, M., Leuven, R.S.E.W., Hendriks, A.J., 2010.Using datasets of different taxonomic detail to assess the influence of floodplaincharacteristics on terrestrial arthropod assemblages. Biodiversity and Conser-vation 19, 2087e2110.

Shore, R.F., Douben, P.E.T., 1994. The ecotoxicological significance of cadmium intakeand residues in terrestrial small mammals. Ecotoxicology and EnvironmentalSafety 29, 101e112.

Smith, J.T., Walker, L.A., Shore, R.F., Durell, S., Howe, P.D., Taylor, M., 2009. Doestuaries pose a toxic contamination risk for wading birds? Ecotoxicology 18,906e917.

Southern, H.N., 1970. Natural control of a population of tawny owls (Strix aluco).Journal of Zoology 162, 197.

Tomé, R., Catry, P., Bloise, C., Korpimaki, E., 2008. Breeding density and success, anddiet composition of little owls Athene noctua in steppe-like habitats in Portugal.Ornis Fennica 85, 22e32.

Van den Bremer, L., Van Harxen, R., Stroeken, P., 2009. Terreingebruik en Voed-selkeus van Broedende Steenuilen in de Achterhoek. Report 2009/02. SOVONDutch Centre for Field Ornithology, Beek-Ubbergen.

Van den Brink, N.W., Groen, N.M., De Jonge, J., Bosveld, A.T.C., 2003. Ecotoxicologicalsuitability of floodplain habitats in the Netherlands for the little owl (Athenenoctua vidalli). Environmental Pollution 122, 127e134.

Van den Brink, N.W., Lammertsma, D.R., Dimmers, W.J., Boerwinkel, M.C., Van derHout, A., 2010. Effects of soil properties on food web accumulation of heavymetals to the wood mouse (Apodemus sylvaticus). Environmental Pollution 158,245e251.

Van den Brink, N.W., Lammertsma, D.R., Dimmers, W.J., Boerwinkel, M.C., 2011.Cadmium accumulation in small mammals: species traits, soil properties, andspatial habitat use. Environmental Science & Technology 45, 7497e7502.

Van Harxen, R., Stroeken, P., 2009. Prooiaanvoer bij de webcamuilen in 2009.Athene 14, 75e87.

Van Vliet, P.C.J., Van der Zee, S.E.A.T.M., Ma, W.C., 2005. Heavy metal concentrationsin soil and earthworms in a floodplain grassland. Environmental Pollution 138,505e516.

Van Wezel, A.P., De Vries, W., Beek, M., Otte, P.F.M., Lijzen, J.P.A., Mesman, M., VanVlaardingen, P.L.A., Tuinstra, J., Van Elswijk, M., Römkes, P.F.A.M., Bonten, L.,2003. Bodemgebruikswaarden voor landbouw, natuur en waterbodem. Tech-nisch`wetenschappelijke afleiding van getalwaarden, Report 711701031/2003.RIVM, Bilthoven.

Van Zoest, J.G.A., Fuchs, P., 1988. Jaaggedrag en prooiaanvoer van een steenuilAthene noctua broedpaar. Limosa 61, 105e112.

Veltman, K., Huijbregts, M.A.J., Hamers, T., Wijnhoven, S., Hendriks, A.J., 2007.Cadmium accumulation in herbivorous and carnivorous small mammals; meta-analysis of field data and validation of the bioaccumulation model OMEGA.Environmental Toxicology and Chemistry 26, 1488e1496.

Verkleij, J., Ten Bookum, W., Sneller, E., Bernhard, R., 2000. Mechanismen vanopname, accumulatie en toxiciteit van zware metalen bij uiterwaardenvegeta-tie. Vrije Universiteit Amsterdam/RIZA, Amsterdam/Lelystad.

Wijnhoven, S., Van der Velde, G., Leuven, R.S.E.W., Smits, A.J.M., 2005. Floodingecology of voles, mice and shrews: the importance of geomorphological andvegetational heterogeneity in river floodplains. Acta Theriologica 50, 453e473.

Wijnhoven, S., Van der Velde, G., Leuven, R.S.E.W., Eijsackers, H.J.P., Smits, A.J.M.,2006a. Metal accumulation risks in regularly flooded and non-flooded parts offloodplains of the river Rhine: extractability and exposure through the foodchain. Chemistry and Ecology 22, 463e477.

Wijnhoven, S., Van der Velde, G., Leuven, R.S.E.W., Smits, A.J.M., 2006b. Modellingrecolonisation of heterogeneous river floodplains by small mammals. Hydro-biologia 565, 135e152.

Wijnhoven, S., Leuven, R.S.E.W., Van der Velde, G., Jungheim, G., Koelemij, E.I., DeVries, F.T., Eijsackers, H.J.P., Smits, A.J.M., 2007. Heavy metal concentrations insmall mammals from a diffusively polluted floodplain: importance of speciesand location specific characteristics. Archives of Environmental Contaminationand Toxicology 52, 306e316.