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European Journal of WildlifeResearch ISSN 1612-4642Volume 61Number 1 Eur J Wildl Res (2015) 61:57-62DOI 10.1007/s10344-014-0873-5

A new method for assessing food qualityin common vole (Microtus arvalis)populations

Eva Janova, Josef Bryja, David Cizmar,Ladislav Cepelka & Marta Heroldova

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ORIGINAL PAPER

A new method for assessing food quality in common vole(Microtus arvalis) populations

Eva Janova & Josef Bryja & David Cizmar &

Ladislav Cepelka & Marta Heroldova

Received: 3 December 2013 /Revised: 2 October 2014 /Accepted: 8 October 2014 /Published online: 21 October 2014# Springer-Verlag Berlin Heidelberg 2014

Abstract Food quality is an important factor influencing thedemography of small rodents. While there have been numer-ous studies on food supply during small mammal populationcycles, studies on quality of food consumed are rare due totechnical difficulties in estimating nitrogen in small samples,such as stomachs or faeces. In this study, we use a newmethod, near infrared reflectance spectroscopy (NIRS), forestimating nitrogenous compounds (NC) in stomachs of com-mon voles (Microtus arvalis). Samples were taken from twopopulations over two 3-year periods. Vegetation cover (man-aged alfalfa/set-aside field), and thus also food supply, dif-fered significantly between the two periods. In analysing theeffects of food supply and individual attributes (i.e. sex, bodysize, reproduction) on NC in stomachs, we were able to show

that nitrogen varied uniformly and that sex, body size andseason had no effect. No significant difference in NC intakewas observed between the two study periods, despite individ-uals being smaller and the population less abundant during thesecond period. During the peak densities, however, reproduc-ing females consumed foodwith a significantly higher level ofnitrogen than all other individuals. Our results indicate thatchanges in food supply do not affect the overall quality of foodconsumed but that maintenance of nutritional quality mayrequire higher energetic release, which may affect body con-dition. We confirm that NIRS represents a useful new toolopening new possibilities in small-mammal ecology studies.

Keywords NIRS . Nitrogen . Rodent . Food quality . Foodsupply

Introduction

Dietary quality is an essential driver in the performance ofindividuals, which in turn drives population dynamics (Kalela1962). As such, dietary studies have tended to concentrate onthe influence of food quality and quantity on populationdensity, life history and dynamics (e.g. Pitelka and Schulz1964; Tast and Kalela 1971; Hansson 1979; Batzli 1986;Wilson et al. 1993; Franois et al. 1997; Lin and Batzli 2001;Sibly and Hone 2002; Zhu et al. 2011).

The common vole (Microtus arvalis, Pallas, 1779) is themost common rodent species in Central Europe (Jacob andTkadlec 2010). Population development in vole species isaffected by seasonal changes in both habitat and food quality(Martinet and Spitz 1971; Haken and Batzli 1996; VonBlanckenhagen et al. 2007), with low quality and quantity offood resulting in decreased body size and local fluctuations inpopulation number (e.g. Cole and Batzli 1978; Briner et al.2007; Hansson 1999; Raoul et al. 2001; Tumur et al. 2005).

Communicated by C. Gortázar

E. Janova (*) : J. Bryja :M. HeroldovaInstitute of Vertebrate Biology, Academy of Sciences of the CzechRepublic, Kvetná 8, 603 65 Brno, Czech Republice-mail: janova.eva@seznam.cz

E. JanovaInstitute of Animal Genetics, Veterinary and PharmaceuticalUniversity, Palackého 1-3, 612 42 Brno, Czech Republic

E. JanovaCEITEC-VFU, University of Veterinary and PharmaceuticalSciences, Palackého tr. 1-3, 612 42 Brno, Czech Republic

J. BryjaDepartment of Botany and Zoology, Faculty of Science, MasarykUniversity, Kotlárská 2, 611 37 Brno, Czech Republic

D. CizmarCentral Institute for Supervising and Testing in Agriculture,Hroznová 2, 656 06 Brno, Czech Republic

L. CepelkaDepartment of Forest Protection and Wildlife Management, MendelUniversity in Brno, Zemědělská 3, 613 00 Brno, Czech Republic

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Nitrogen (N) is a fundamental element for organisms as it isessential for the production of many proteins and is requiredfor both body growth and reproduction (Karasov andMartinez del Rio 2007; Palo and Olsson 2009). It has longbeen considered a limiting resource for growth in herbivorepopulations (e.g. see the ‘nitrogen limitation hypothesis’ ofSchetter et al. 1998). Total dietary N (or crude protein [usuallyN×6.25]) is relatively easily measured by chemical analysisand is considered a good index of dietary quality in largerherbivores (Leslie et al. 2008; Verheyden et al. 2011). Inecological studies on rodents, however, quality of food con-sumed (i.e. stomach content analysis: energy value, N andfibre content) is more difficult tomeasure as samples are muchsmaller. To date, only one study has provided data on Ncontent in stomachs of common voles (Butet 1996).

Near infrared reflectance spectroscopy (NIRS) is a non-destructive, emission-free and low-cost analytical techniquethat may reduce the use of conventional laborious methods forestimating N in long-term wildlife monitoring (Dixon andCoates 2009). Numerous studies have indicated that NIRScan be a valuable tool for estimating a variety of chemicalcomponents in soil or plant and animal tissue (e.g. Büning-Pfaue et al. 1998; Foley et al. 1998). As such, the method hasroutinely been used in the analysis of food components in thefaeces of a range ofmammal groups (Dixon and Coates 2009),including determination of dietary quality in domestic rumi-nants and estimation of faecal N in ungulates (e.g. Kamler andHomolka 2005; Kidane et al. 2008; Leslie et al. 2008). In thisstudy, we provide a first assessment of NIRS for analysis ofthe stomach contents of free-living common voles.

The model population used in this study was situated in anintensively managed alfalfa (Medicago sativa) field, and ex-hibited regular multi-annual population cycles. Followingfield set-aside, however, available vegetation changed, popu-lation fluctuations ceased and vole body size decreased(Heroldova et al. 2005; Janova et al. 2008). Hypothetically,this could have been caused by a decrease in the nutritionalcontent of available food. Our aim in this study was to eluci-date any relationship between food quality (represented bystomach N) in managed alfalfa and set-aside fields with sex,reproductive condition and individual body size between sea-sons and years.

Material and methods

Population sampling and vegetation cover

Voles were sampled by regular monthly snap-trapping fromMay 1996 to September 1998 and from May 2001 toSeptember 2003. Trapping took place in a 10 ha field nearthe town of Drnholec in southern Moravia, Czech Republic(48° 53′ 30″ N, 16° 27′ 30″ E). Snap traps were baited with

fried wicks and exposed for one night in lines of 100 traps 3 mapart (for more detailed information see Janova et al. 2008).During the first period of sampling (1996–1998), 90–95 % ofthe vegetation biomass in the field comprised intensivelymanaged alfalfa and the rest weedy species (Fig. 1). Duringthis period, vole population density was strongly cyclic; thepopulation increasing in 1996, peaking in 1997 and decliningagain in 1998. The last mowing of the field was done in thesummer 1998. During the second sampling period (2001–2003), the field was gradually abandoned and the proportionof alfalfa decreased from 90 % in 2001 to just 10 % in 2003(Fig. 1). As a result, large-scale population fluctuations ceasedand changes in abundance were limited to seasonal oscilla-tions (Janova et al. 2008).

In total, 2086 common voles were trapped during the study.All individuals captured were weighed, sexed, measured anddissected. The reproductive status of females was identified as‘breeding’ if embryos or placental scars were detected on theuterus. Males were determined as sexually active if the testic-ular index (length of testes × width in mm) reached 40 or more(Pelikan 1959). Stomachs were removed and dried, and thecontents were used for NIRS analysis if the volume wassufficiently large.

NIRS calibration and sample examination

In preparing stomach samples for analysis, the stomach wallwas first removed in order to provide a sample of pure stom-ach content. One of the sample’s sides was then levelledthrough abrasion, ensuring that (a) the area treated was largerthan the detection window of the NIRS equipment and (b) thesample was sufficiently thick that it could not be penetrated bya light beam. In total, 889 stomach samples met the abovecriteria (Table 1) and these were further analysed using theFOSS NIR System 6500 near infrared (NIR) spectrophotom-eter (wavelength range 1100–2500 nm). This produced aspectrum encompassing the complete physical and chemicalcomposition of the sample.

An NIR calibration model for nitrogen content was devel-oped using chemometric methods and least squares regression.The model used 34 stomach samples of known N content,measured using the Kjeldahl method (AOAC 1980). Thisproduced a simple coefficient of determinationwith anR2 valueof 0.841 and a standard error (SE) of 43.5. Following cross-validation, the R2 was increased marginally to 0.843 and SEreduced to 44.1 (see Kidane et al. 2008). Verification of thecalibration model was undertaken using EffiChem software(designed for validation of calibration curves), and 20 indepen-dent samples were not included in the calibration model.Comparison of the results from the conventional Kjeldahlmethod andNIRS provided statistically identical results; hence,NIRS was used for all further analysis. The NIR calibrationmodel was further used to estimate N content in all stomachs

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analysed. Food quality was expressed as total NC (N×6.25) asa percentage of total dry stomach content (sensu AOAC 1980).

Statistical analysis

As we included reproduction parameters in the statisticalmodel, both sexes were analysed separately in all subsequentanalyses. Habitat (alfalfa or set-aside), year and reproductionstatus (breeding/non-breeding females, sexually active/non-active males) were used as categorical variables, and theseason (number of days from the beginning of the year) andbody length being used as continuous predictors. The effect ofthese variables was ascertained using a generalised linearmixed model (GLM).

All statistical analyses were performed using the Statistica6.0 software package (Statsoft 2000).

Results

Of the 2086 common voles captured, only 889 had stomachslarge enough for examination using NIRS. NC levels wereestimated for 262 females and 146 males from the first sam-pling period and 323 females and 158 males from the secondperiod (Table 1). NC as a percentage of total dry-stomach

content varied between 9.3 and 57.7 %, with a mean of 30.8(SE±6.4) and a median of 30.4. Ninety-five percent of sam-ples ranged between 18.5 and 44.9 % NC/total dry biomass.

Multivariate analysis (GLM) for each sex separately indi-cated that body size, habitat type and date had no influence onNC content, though the effect of year in females was close tosignificance (χ2

5=8.832, P=0.065; Table 2). Reproductionhad no effect on male NC but was significant for female NC(χ2

1=6.331, P<0.05), with average NC in stomachs of non-breeding females being 29.8 % compared to 31.2 % in breed-ing females (Table 2).

There was no effect of habitat, date or body size observedon stomach NC, except when testing reproducing femalesonly, where GLM analysis revealed higher NC in stomachsfrom 1997, when population density in the alfalfa field was atits peak, than in other years (reproduction status × habitat;χ2

1=12.523, P<0.05; median 32.8 %). If 1997 was excludedfrom the GLM, however, there was no longer any significanteffect of reproduction status or year.

Discussion

In this study, we confirm that NIRS can be used successfullyfor estimation of NC in stomachs of small rodents. The results

Fig. 1 Changes in biomass ofplants on experimental field(g/m2)—according to Heroldovaet al. 2005

Table 1 The number of common vole (Microtus arvalis) stomachs analysed each year according to sex (males/females), year and sample month

Sample month

Year I II III IV V VI VII VIII IX X XI XII

1996 – – – – 2/5 2/8 4/14 13/16 0/1 – – –

1997 – – – 15/15 14/26 16/34 4/13 32/53 – 12/26 16/22 11/17

1998 1/0 4/2 – – – – – – – – – –

2001 9/19 – – – 6/14 9/11 4/43 15/18 15/14 14/25 13/15 2/1

2002 – – – 0/2 11/21 – 17/63 10/30 11/16 2/1 6/2 5/9

2003 1/3 2/1 1/0 0/1 – 1/0 1/1 0/3 3/10 – – –

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indicate considerable variation in stomach NC concentrationsbetween individuals, suggesting a varied diet composed ofdifferent food types (see Holisova 1959; Heroldova 1994).The NC content of stomachs of voles inhabiting the fields wassimilar to those living in the wood clearings (Cepelka et al.2014). In addition, our results confirm a relationship betweenstomach NC and energy demand during the intensive repro-ductive period in females. Such a relationship that was onlyconfirmed during the peak of the population cycle, whenreproduction was most intense, was rather surprising. Anincrease in demand for food with higher protein contentduring times of intensive reproduction has also been observed,however, in other rodent species (Holisova 1959; Obrtel andHolisova 1982; Cepelka et al. 2013). What is more, cannibal-ism or infanticide has frequently been observed during periodsof high rodent population density (Ebensperger et al. 2000);indeed, this may actually be the source of the high-proteindiet. An increase in dietary quality (N level) concurrent withincreasing common vole population density was also con-firmed by Butet (1996) using classical chemical analysis;though in this case, the influence of sex or female breedingstatus was not considered. Similarly, Palo and Olsson (2009)noted that density was positively related to stomach N con-centrations in bank voleClethrionomys glareolus populations.These results suggest, therefore, that improved dietary qualitymay have a strong positive effect on survival and/or reproduc-tion. During the second (set-aside) sampling period, stomachNC levels were not significantly correlated with either sex orbody size. Further, the ‘quality’ of food in the stomachs didnot change significantly, despite a considerable change in foodavailability following field set-aside and a consequent de-crease in population and body size. Similarly, Palo andOlsson (2009) observed no relationship between N concen-tration in C. glareolus stomachs and body mass variationbetween sites and between seasons.

A number of studies have confirmed an increase in therequirement for ‘quality’ food by females during reproduc-tion; Migula (1969), for example, confirmed the increasedenergetic demand in reproducing common voles in laboratoryexperiments. In our study, the nutritional value of food taken

(NC) remained similar between years and sampling periods(except during the peak year of 1997). In reproducing females,however, the need for a better quality of food was compen-sated for by increased alimentary tract capacity and improveddigestive ability (Heroldova and Janova 2010). This is inagreement with previous studies on the relationship betweenseasonal dynamics and size or mass of gastrointestinal tracts,which have indicated a heavy bias in favour of females(Holisova 1959; Myrcha 1964; Borkowska 1995). In thisstudy, despite a similar NC content in food digested by malesand females, the actual amount of nutrient absorbed in femalesis higher, thereby compensating for a higher nutrient demandrelated to reproduction investment (Gorman and Akbar 1993).

In the first (managed alfalfa) sampling period, green alfalfashoots were a preferred food supply for voles. During thesecond sampling period, however, the set-aside fields werecharacterised by increased plant diversity (i.e. weeds), includ-ing a range of phenotypically different plants, some of whichrapidly produced seed (Heroldova et al. 2005).

During both of the compared periods, classical NC analysisof some dominant species was done (our unpublished data).The meanNC level in alfalfa field in the first period was 21%.At the beginning of the succession stage, two species weredominant: Capella burza pastoris (mean NC=30 %) andStellaria media (mean NC=22 %). Their NC content wasroughly similar as the content in the managed alfalfa field.In more advanced succession, Amaranthus sp. (mean NC=17 %) and Chenopodium sp. (mean NC=18 %) were domi-nant with lower NC content. At the last stage of our study onset-aside plot, Bromus sp. dominated (mean NC=11) with lowNC level. Annual weedy species have, in contrast to managedalfalfa, shorter vegetation period and soon ripen to have seeds.The decrease in availability of juicy, green plant shoots, espe-cially during the summer, may have functioned as a stressfactor for voles, as could an associated increase in the abun-dance of other small mammal species (e.g. Apodemus sp.)resulting from the increased availability of seeds (see Hakenand Batzli 1996; Heroldova et al. 2005). Small mammals,such as voles, are generally strongly selective when given achoice of food, and the plants (or plant parts) selected are often

Table 2 Results of multivariate analysis (generalised linear mixed models) on the effect of a range of variables on nitrogen content in common volestomachs

Hab Year Date L R H×R Y×R

χ2 P χ2 P χ2 P χ2 P χ2 P χ2 P χ2 P

Df 1 5 1 1 1 1 1

F 1.466 >0.1 8.832 0.065 2.160 >0.1 1.930 >0.1 6.331 <0.05 7.591 <0.05 5.043 >0.1

M 0.882 >0.1 5.833 >0.1 0.473 >0.1 0.770 >0.1 0.817 >0.1 1.28 >0.1 3.534 >0.1

Variables analysed include habitat (Hab), year, date, individual length (L), reproduction status (R; breeding/non-breeding), interaction between habitatand reproduction (H×R) and interaction between year and reproduction (Y×R) in females (F), males (M) and degrees of freedom (Df). Significantdifferences are marked in italics

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low in phenol and fibre and high in protein (McKey 1979;Bergeron and Jodoin 1987; Hambäck et al. 2002). The simi-larity in NC intake over both sampling periods (except forbreeding females in cyclic populations) implies that voleswere able to maintain their nutritional status, despite thechange in conditions under set-aside, though this requiredgreater energetic effort. This could potentially have led tothe observed decrease in both population size and body size(Janova et al. 2008). For example, maintenance of nutritionalquality may have led to increased migration as voles travelledgreater distances to acquire appropriate food (Balmelli et al.1999). Indeed, low food availability has previously beenshown to negatively influence body size in a range of species(e.g. see Cole and Batzli 1978; Batzli 1986; Hansson 1999;Raoul et al. 2001; Tumur et al. 2005). It should be noted,however, that demographic changes may also be connectedwith factors other than food supply, including illness, stress,(non-food-related) migration and lack of shelter (e.g. seeClarke 1985; Tew and MacDonald 1993; Balmelli et al.1999; Maisonneuve and Rioux 2001; Hardy et al. 2005;Janova et al. 2010).

NIRS proved to be a useful tool for estimating commonvole food quality (represented by stomach NC) and its rela-tionship to various demographic factors. Overall, the methodresulted in a marked reduction in time taken for analysis andassociated costs. Future use of NIRS in such studies is expect-ed to open up new possibilities in small-mammal ecology.

Acknowledgments This study was supported by Project 521/08/P529of the Grant Agency of the Czech Republic (Czech Science Foundation).We would like to thank Jiri Kamler for his efficient help with nitrogenanalysis. All work in this study complied with the Council Directive 86/609/EEC—regulations on the experimental use of animals. In addition,the approval for all field experiments within this project was obtainedfrom the ethical committee of the Academy of Sciences. We thank Dr.Kevin Roche for improving the English language and for commenting theearlier version of the manuscript.

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