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Effects of spatio-temporal variation in food supply on redsquirrel Sciurus vulgaris body size and body mass and itsconsequences for some fitness components

Lucas A. Wauters, Marleen Vermeulen, Stefan Van Dongen, Sandro Bertolino,Ambrogio Molinari, Guido Tosi and Erik Matthysen

L. A. Wauters ([email protected]), A. Molinari and G. Tosi, Dept Environment-Health-Safety, Univ. of Insubria Varese, Via

J.H. Dunant 3, IT-21100 Varese, Italy. * M. Vermeulen and E. Matthysen, Dept of Biology, Laboratory of Animal Ecology, Univ.of Antwerp, Universitsplein 1, BE-2610 Antwerp, Belgium. * S. Van Dongen, Dept of Biology, Group of Evolutionary Biology,Univ. of Antwerp, Groenenborgerlaan 171, BE-2020 Antwerp, Belgium. * S. Bertolino, DIVAPRA Entomology and Zoology, Univ.of Turin, Via L. da Vinci 44, IT-10095 Grugliasco (TO), Italy.

Food availability is likely to influence body condition and, in turn, fitness. The intensity of this response may vary between populations of the same species on a small spatial and temporal scale. We used 5 yr of data from 6Eurasian red squirrel Sciurus vulgaris populations from the southern Alps to explore differences in body size andbody mass among neighbouring populations, in relation to habitat type and variation in food supply. We alsoinvestigated sexual dimorphism in these traits and whether phenotypic variation affects local survival and femalereproductive success. Mean hind foot length, a measure of body size, did not differ between sexes but differed

between areas. Seasonal variation in body mass was small with no evidence for fattening in autumn. Femaleswere slightly heavier than males, but this difference was largely explained by mass gain of females during reproduction. The size of conifer seed crops, the major food supply, varied strongly over years and betweenhabitats, but this variation corresponded only weakly with autumn body mass. Differences in size and massbetween populations were partially explained by habitat-related differences in body size and variability of seed-crops, suggesting differential selection for smaller squirrels in spruce-larch forests against selection for larger andheavier animals in mixed broadleaves and conifer forests and in Scots pine forests with more stable seedproduction. The probability of reproduction by females increased with body mass, but varied strongly betweenhabitats and years, with more females reproducing in years with rich seed-crops. In both sexes, body masspositively affected probability of settlement and length of residency. Our results suggest that in temporally variable environments that differ in overall amount of food resources, individual variation in body mass isrelated to habitat type, and that having a relatively high body mass, within each population, positively affectsmale and female settlement success and local survival, and female reproductive success.

The amount of food animals consume will affect theirfitness in various ways. Food assimilation producesenergy necessary for body growth and/or maintenanceof body condition and for reproductive investment, aswell as essential nutrients such as proteins, carbohy-drates, minerals, and vitamins (Robbins 1993, Cuthilland Houston 1997). A diet rich in lipids allows a highrate of energy intake and, in a large variety of species,the accumulation of fat reserves that cause a (seasonal)increase in body mass. In many vertebrates, a relatively

high body mass in relation to body size is an indicationof good condition: such individuals are more likely tosurvive critical periods of food shortage or extremeweather conditions (Blem 1990, Millar and Hickling 1990, Schulte-Hostedde et al. 2001). Moreover, heavieranimals often are more likely to reproduce successfully,particularly in female mammals, and tend to be bettercompetitors (social dominance) than conspecifics of smaller size or lesser body mass (Wauters and Dhondt1989a, 1995, Robbins 1993, Law 1995, Cuthill and

Ecography 30: 51 Á 65, 2007doi: 10.1111/j.2006.0906-7590.04646.x

Copyright # Ecography 2007, ISSN 0906-7590

Subject Editor: Douglas Kelt. Accepted 16 October 2006

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Houston 1997, Lin and Batzli 2001, Diaz and Alonso2003). Finally, in some species, animals in goodcondition are better at escaping predators and are lessvulnerable to parasites or diseases (Ostfeld et al. 1996,Van der Veen 1999, Wirsing et al. 2002). Inevitably,there are also costs associated with being heavier: largeror heavier animals have higher absolute energy require-ments than smaller conspecifics and therefore are forcedto forage more intensively to meet their energy demands. These increased foraging costs may augmentthe possibility of predation, aggressive encounters, andcontact with parasites (McNamara and Houston 1987).Hence, body condition will affect an animal’s behaviourand fitness, and understanding the relationships be-tween phenotypic characteristics and environmentalfactors that influence body condition is of generalinterest to ecologists.

Many ecologists have explored variation in body condition in relation to predation rate, age-relatedsurvival, and reproductive success in small and med-

ium-sized mammals (Wauters and Dhondt 1989a,1995, Becker 1993, Dobson and Michener 1995,Humphries and Boutin 1996, Green 2001, Wirsing et al. 2002). Most of these studies were relatively short-term and in a single population or habitat, and there arefew papers that explore effects of habitat-type and/orseasonal and annual variation in food resources onwithin and between population patterns of variation inbody condition (Andersson 1994, Moss and Croft1999, Naeff-Daenzer et al. 2001).

Differences in size or body mass between neighbour-ing populations may be the result of genetic variation

with individuals responding to differential selection forbody size and/or body mass on a small spatial and eventemporal scale (Hoffmann and Merila ¨ 1999, McAdamand Boutin 2003a, b, Garant et al. 2005). In North

American red squirrels Tamiasciurus hudsonicus , juve-nile growth in both body mass and size had significantamounts of genetic variation, but also experienced large,heritable maternal effects (McAdam et al. 2002). A long-term study on great tits Parus major showed thatdifferences in body mass at a small spatial-scale,between (sub)populations occupying different habitatswithin a large, contiguous forest, was an expression of

divergent evolution (Garant et al. 2005). In fact,evolutionary theory predicts that local, adaptive, popu-lation divergence will depend on the balance betweendiversifying effects of natural selection and the (oppo-site) homogenizing effect of dispersal, hence gene-flow (Endler 1986, Slatkin 1987). Therefore, it is importantto understand how body size and body mass vary among populations of a species occurring in differenthabitats in a limited geographical range, and how thesephenotypic traits change with fluctuating environmen-tal conditions (in particular fluctuations in foodavailability) within populations.

Here we use a 5-yr data set from 6 Eurasian redsquirrels Sciurus vulgaris populations from the southern

Alps to explore effects of habitat type, characterised by variation in type and overall availability of the majorfood supply (tree seeds), and effects of season and year,representing temporal variation in food supplies, onpatterns of variation in two phenotypic traits: body sizeand body mass. We also investigate sexual dimorphismin these traits. Finally, we explore whether phenotypicvariation affects length of residency (local survival) of males and females, and reproductive success of femalered squirrels.

Materials and methods

We selected 6 study areas within mature, secondary montane and subalpine mixed conifer forests of theItalian Alps, with elevations ranging from 1100 to 2100m a.s.l. (the upper tree-line). These areas are distributed

over 2 geographic regions: COG and RHE are locatedin the Cogne and Rhemes Valleys of the Gran ParadisoNational Park, in the western Alps, while Cedrasco(CED), OGA, Valfurva (VAL), and Bormio (BOR) arein the Valtellina Valley in the central Alps. Specificlocation and distances between study areas are presentedelsewhere (Fig. 1 in Trizio et al. 2005). RHE and VALare dominated by Norway spruce Picea abies , OGA by Scots pine Pinus sylvestris , and BOR by Arolla pinePinus cembra . COG is spruce-larch Larix decidua forestand at CED the forest is mainly composed by silver fir

Abies alba and spruce with small proportions of larch,

Scots pine, and some beech Fagus sylvatica at lowerelevations (Wauters et al. 2004a).

The proportion of spruce, silver fir, larch, Scots pine,and Arolla pine differed among study areas, but alsovaried within study areas at a fine-grained level. There-fore, to estimate seed availability as our measure of foodabundance, we first determined woodland compositionby establishing a 20)20 m (400 m2) vegetation plotaround each trapping station across the trapping grid(n020 Á 30). In each vegetation plot, we counted thenumber of trees of each species, and measured thediameter at breast height (DBH in cm) of 2 trees of

typical size for each species on the plot (forests consistedof large areas of even-age stands with trees of similarsize), hereafter called ‘‘sample trees’’ (Wauters et al.2005). Dead trees were recorded separately since theirpresence indicated a naturally structured forest. Eachyear in August, we counted green cones in the canopy of all coniferous sample trees from a fixed position using 10)40 binoculars and scaled to estimate the totalnumber of cones per tree (Wauters et al. 2005).Counted cones were multiplied by species-specificaverage number of seeds per cone (unpubl.) to obtainan estimate of annual seed production per tree in each

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vegetation plot. To combine data of different seedspecies, we converted the number of seeds tree(1 foreach species to energy values (kJ tree(1), using our ownvalues of seed-specific energy-content. We then multi-plied the number of trees of each species with thespecies-specific seed energy tree(1 to calculate seeddensity in each vegetation plot (multiplied by 25 andthus expressed in kJ ha (1). The mean value of allvegetation plots was calculated as the measure of averageannual tree seed abundance in each study area. Seedsproduced in the summer-autumn of year t wereconsidered available for the squirrels during the follow-ing ‘‘squirrel year’’ (Wauters and Lens 1995), i.e. from

August of year t to July of year t'1.In each study area, squirrels were live-trapped

bimonthly from April to October 2000 Á 2004, using 20 to 30 ground-placed Tomahawk traps (models 201and 202, Tomahawk Live Trap, WI, USA). Traps wereplaced on a grid, with distances of 100 Á 150 m betweentraps and average trap density of 0.6 Á 0.7 traps ha (1.

Traps were pre-baited with sunflower seeds and hazel-nuts 4 to 6 times over a 30-d period, and then baitedand set for 8 Á 12 d, until no new, unmarked squirrelswere trapped for at least 2 consecutive days. Traps,partly covered by dark plastic to give shelter from rainor cold, were checked 2 Á 3 times a day. Each trappedsquirrel was flushed into a light cotton handling bag with velcro-type fasteners or with a zipper (Koprowski2002), or a wire-mesh ‘‘handling cone’’ to minimizestress during handling, and individually marked using numbered metal ear-tags (type 1003 S, 10 by 2 mm,National Band and Tag, Newport, KY, USA). It was

weighed to the nearest 5 g using a Pesola spring-balance(Pesola, Baar, Switzerland), and the length of the righthind foot (without nail) was measured (0.5 mm) with a thin ruler (Wauters and Dhondt 1989a, b, 1995). Sex,age, and reproductive condition were recorded follow-ing Wauters and Dhondt (1995). Thus, we scored a female’s reproductive status as: 1) anoestrus (vulva small, no longitudinal opening, not lactating), 2)oestrus (or post-oestrus, vulva partly or strongly swollenwith longitudinal opening, enlarged belly during latepregnancy), or 3) lactating (nipples large, milk excre-tion can be stimulated, Wauters and Dhondt 1995,

Wauters and Lens 1995).

Indices of body condition

In mammals, fat reserves are considered the best index of condition but are extremely difficult to measure inthe field for live animals (Green 2001, Blackwell 2002).There are 2 common methods to derive an index of body condition in studies on vertebrates: a ratio of body mass on a measure of structural body size, using hind-foot length (Krebs and Singleton 1993, Jakob et al.

1996, Becker et al. 1998, Wirsing et al. 2002), or theresiduals of a regression of body mass (or log-trans-formed body mass) on size (Dobson and Michener1995, Wauters and Dhondt 1995, Guinet et al. 1998,Blackwell 2002, Schulte-Hostedde et al. 2005). In thefirst case, animals with a higher ratio are considered tobe in better condition than those with a lower ratio, andin the second case individuals with a positive residualvalue have a better condition than those with a negativeresidual value. However, mass/size ratios often arehighly correlated with body mass in small mammals(Lidicker and Ostfeld 1991, Schulte-Hostedde et al.2001), potentially biasing interpretations of body sizevariation among populations or sexes, or the effects of body size on fitness components (Wauters and Dhondt1989b, 1995). Moreover, many recent studies havecriticized the use of residuals as a condition measurebased on statistical assumptions inherent to deriving residuals from regression equations, or the lack of a relationship between residuals and true variation in fat

reserves, or because residuals are an inappropriatemeasure of condition when comparing several popula-tions, sexes, and/or age-classes that differ in body mass(Garcia-Berthou 2001, Green 2001, Blackwell 2002,Freckleton 2002). Thus for these biological andstatistical reasons, we chose to include foot length,our measure of structural body size, as a covariate inmultivariate models that tested for spatio-temporalvariation and possible gender differences in body mass, and in multivariate models that explored effectsof body mass on settlement, residency and reproduction(Garcia-Berthou 2001).

Statistical analyses

Variation in foot length and body mass were analysedwith linear mixed models (Anon. 1999, Verbeke andMolenberghs 2000), with area, sex, age, season, year(and, where relevant reproductive condition) as classvariables. Because this study was designed to monitorindividual body mass over longer periods of time, thesemodels were adjusted for repeated measures by expli-citly modeling residual correlation structure. In each

analysis we started from a saturated mean model (i.e.including all fixed effects and interactions) and com-pared models with different correlation structures.Model fit was compared using Schwarz’s BayesianInformation Criterion (BIC), where smaller valuesindicate better fit (Verbeke and Molenberghs 2000).

After selecting correlation structure of the residualcorrelation matrix, we continued testing fixed effectsusing Type-III SS and performed model selection using a backward procedure. Degrees of freedom and stan-dard errors of F- and t-tests were obtained using theKenward-Rogers method. Interpretation of final models

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was based on least square means (Verbeke andMolenberghs 2000). Distribution of residual values of each finally-selected model was explored using theShapiro-Wilk statistic (Verbeke and Molenberghs2000). When effects on body mass were explored,foot length was always included as a covariate to correctfor variation in body mass produced by variation inskeletal size as measured by foot length. Foot length of adults does not change over time, and variance fromrepeated measures was small (0.313) compared tovariance caused by individual differences in size(2.125), indicating that measurement error in footlength was much smaller than individual variation(87% of total variance). Therefore, we used only onevalue for individual foot length based on the mean of allmeasurements.

Since juveniles differed from adults and subadults inboth mass and foot length (see Results), they wereanalysed separately. Only at BOR, juveniles weretrapped in late spring, hence these were pooled with

summer captures to avoid confounding effects of seasonwith those of study area. Since most squirrels werecaught only once as juveniles, we tested variation in

juvenile body mass with a generalised linear model,using each individual only once.

We further explored to what extent variation in foodabundance could explain body-mass variation. In a firststep we calculated mean body mass for each combina-tion of year, season, and area, using only data of spring and autumn captures. We predict that average body mass in spring of year t will be correlated with seed cropsize of the previous year (t(1) and that average body

mass in autumn of year t will be correlated with seedcrop size of the same year (t) (Wauters and Lens 1995,

Wauters et al. 2004b). We also tested for a possibleeffect of the previous year’s seed crop on autumn body mass, since conifer seeds produced in mast years may still be harvested throughout the following year’ssummer and autumn (Wauters et al. 2005). Sincemeasurements of food abundance are year- and area-dependent, year and area are included in a linear mixedmodel as random variables.

To investigate differences in body mass betweenanoestrus, oestrus, and lactating females (Wauters and

Dhondt 1989a), we used only the spring trapping data (April Á early May) of adult females since in this seasonwe trapped anoestrus females, females in early oestruswhose body mass was not or only slightly affected by pregnancy (intermediate litters with expected parturi-tion mid May Á mid June), and lactating females (spring litters, observed or expected parturition dates midMarch Á late April). We used a mixed linear model(122 observations of 96 adult females) to explore effectsof study area, reproductive status, foot length, and a foot length by study area interaction on variation inbody mass. In a second step, logistic regression was used

to examine the relationships between body mass, footlength, study area, year, and season (data over allseasons) as independent variables and the probability for adult female squirrels to reproduce as dependentvariable (Hosmer and Lemeshow 1989). The binary dependent variable (Yi) was scored 0 when reproductivecondition of a female was classified as anoestrus, it wasscored 1 when a female was classified as pregnant orlactating. Models were calculated with PROC GEN-MOD (Anon. 1999) by stepwise forward selection of significant independent variables (a00.05) (Hosmerand Lemeshow 1989). The probability for immigrantsubadult or adult squirrels to settle successfully (definedas presence in at least 2 trapping sessions) was alsoexamined by logistic regression by testing the samevariables and factors as for reproduction. In this case,the binary dependent variable was scored 0 when a squirrel was trapped only in a single trapping session(transient dispersing animals, Wauters and Dhondt1993), it was scored 1 when a squirrel settled. For each

individual, we used mean body mass over all captures.Squirrels that immigrated in 2004 were excluded fromthe analyses since trapping did not last long enough toclassify them as settlers or transients. In a next step,length of residency, or local survival (number of monthsbetween first and last capture), was estimated for thosesquirrels that were captured at least twice in the study areas (n0195). If data from animals first captured in2003 or 2004 and still present in autumn 2004 wereexcluded, sample size was reduced to 171 squirrels.However, general linear models based on the entire andon the reduced dataset gave similar results: therefore we

present only analysis for the entire dataset. Lengthof residency was ln-transformed to meet assumptions of normality (Shapiro-Wilk’s W 00.94). All tests of significance are 2-tailed and the significance level wasset at 0.05. Unless otherwise indicated values arepresented in the text as mean9SD.

Results

Food availability

Tree seed production varied between years and study areas (Fig. 1, 2-way ANOVA on Log-transformed foodabundance: year F5,2107.07, p00.0005, area F5,210

5.35, p00.0025). The largest seed-crops were pro-duced at CED and VAL, the smallest at BOR andOGA. The years 1999 and 2004 had the largest crops,while 2003 and especially 2000 had poor crops. Theyear-effect explained 41% of variation in food abun-dance and the area-effect 31%. Although the year by area interaction could not be tested, fluctuations inseed-crop size differed among study areas; in particularthe seed-crops of pines at OGA and BOR were less

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variable than spruce and larch crops at the other sites(Fig. 1).

Foot length and body mass

Between July 2000 and October 2004, 1360 measure-ments of foot length and 2189 of body mass were takenfor 520 and 544 red squirrels respectively. Mean footlength was 57.592.0 mm (range 46.0 Á 62.0 mm, 90%between 54.0 and 60.0 mm) and mean body mass was304937 g (range 90 Á 400 g) with 90% of measure-ments between 245 and 360 g. Both foot length andbody mass differed between the 3 age-classes (Mixed

ANOVA models with first order autocorrelation struc-ture, foot length, F2,12100190.8, pB0.0001, body mass F2,17390746.2, pB0.0001).

Juveniles

Juveniles (n0110 measures, 54.092.5 mm, 46 Á 61 mm) were smaller than subadults (n0182, 56.991.6 mm, 53 Á 61 mm) and adults (n01068, 58.091.5mm, 53 Á 62 mm). Juveniles also weighed less (n0136,

209940 g, 90 Á 265 g) than subadults (n0278919 g,230 Á 340 g) and adults (n01789, 315925 g, 240 Á 400 g). As expected, juvenile body mass increased withfoot length (slope 3.8891.39). There was no differencein juvenile body mass between the sexes or between years(Table 1) but juveniles trapped in autumn were heavierthan those trapped in summer (Table 1, summer n051,197942 g, autumn n057, 221933 g). Moreover,

juveniles at RHE and BOR were heavier than at CED,

CED OGA BOR VAL RHE COG56

57

58

59

60

61

Footlength(mm)

FemalesMales

CED OGA BOR VAL RHE COG290

300

310

320

330

340

Bodymass(g)

Spring Summer Autumn300

305

310

315

320

Bodymass(g)

(a)

(b)

(c)

Fig. 2. Plots of body size measurements of male and femalered squirrels (mean'1 SE) as a function of study area orseason. (a) mean foot length per study area, (b) mean body mass per study area, and (c) mean body mass of adults andsubadults per season (years pooled).

1999 2000 2001 2002 2003 2004Year

0

1000

2000

3000

4000

5000

6000

7000

8000

9000

10000

Seed-crop

size(10

3kJ/ha)

COG

RHE

VAL

BOR

OGA

CED

Fig. 1. Tree seed production per year (mean'1 SE expressedin 103 kJ/ha (1) as a function of study area.

55



and those from RHE were also heavier than juvenilesfrom COG (Table 1, and Tukey-test for differencesbetween means, all pB0.05). Juveniles were of inter-mediate mass at OGA and VAL.

Foot length of subadult and adult squirrels

Variation in foot length among subadult and adultsquirrels was analysed with a stepwise backward linearmixed model (compound symmetry correlation struc-ture) exploring the effects of study area, sex, and yearand all interactions. The model was corrected forrepeated measures with foot length measured once ineach trapping period (1 Á 13 observations per individual,1045 observations from 433 different squirrels). Noneof the interaction terms were significant (all p0.10),and foot length did not differ between male and femalesquirrels (males, n0627, 57.891.5 mm, females, n0418, 57.791.5 mm, F1,42600.34, p00.56), oramong years (F4,61200.70, p00.59). However, sizeof squirrels differed between study areas (Fig. 2a,F5,427012.1, pB0.0001). Squirrels were larger atCED and smaller at RHE than at all other sites(differences of least square means, DLSM, all pB0.01). There were no differences between the other 4study areas (Fig. 2a, DLSM, all p0.05).

Variation in body mass

In a preliminary test, we compared within-seasonvariation in body mass at the individual level of

subadults and adults (variation among repeated mea-sures of an individual’s mass within one trapping session) with variation in body mass between seasons.To achieve this we constructed a linear mixed modelwith repeated measures at the individual level and eachseason (spring, summer, or autumn) treated as anindicator variable and added to the model as randomfactor (nested within individual), next to a randomfactor individual which models overall between-indivi-dual variation. Within-season variation in body masswas largest in spring (72.10), intermediate in summer

(63.57), and smallest in autumn (49.04). However,within-season variation at the individual level Á reflect-ing day to day variability in body mass Á was an orderof magnitude larger than between-season variation atthe individual level (variance component0174.4).

Average individual body mass across seasons andtrapping sessions varied even more strongly (variancecomponent0348.71).

We examined effects of age, sex, study area, season,and year as factors, and the season by sex, season by year, season by area, and area by year interactions onvariation in body mass of subadult and adult squirrels,using foot length as a covariate (Table 2). Interactionswere chosen because of predicted variation in seasonalpatterns of body mass changes between the sexes(season)sex, seasonal changes in body mass of femalesrelated to reproductive condition of pregnancy orlactation, Wauters and Dhondt 1989a, b, 1995),between years (season)year, spring, and summermass was expected to be lower after poor than good

seed-crops), and between areas (season)area, autumnmass-gain might be habitat-dependent, Wauters andDhondt 1989b, Lurz and Lloyd 2000). Finally, an area by year interaction examined if mass changes acrossyears differed between the study areas in relation tovariation in food abundance between areas (Fig. 1).Body mass increased 3.91 (90.70) g with each mmincrease of foot length (Table 2a). Corrected forvariation in foot length, adult squirrels were heavierthan subadults. Variation between years, seasons, andareas was complex, including interactions among thesefactors as well as interactions with sex (Table 2a, Fig.

2b). Overall, females were heavier than males (females,n0425, 316931 g; males, n0635, 305925 g), butsex-differences changed across seasons (Table 2a). Maleswere slightly heavier in spring and autumn (DLSMspring-summer p00.003, spring-autumn p00.25,summer-autumn p00.064), while females were heavierin spring and summer (Fig. 2c, DLSM spring-summerp00.60, spring-autumn p00.03, summer-autumnp00.01). Therefore, effects of study area, age, year,and season on body mass were subsequently examinedfor males and females separately.

Table 1. Average (9SD) foot length and body mass of juvenile red squirrels (n0108) per study area. Generalised linear modelexploring effects of foot length (as co-variate), study area, sex, year and season on variation in body mass.

Study area (n) CED (5) OGA (11) BOR (20) VAL (12) RHE (34) COG (26)

Foot length (mm) 55.392.5 54.492.7 56.192.7 54.391.0 54.391.0 54.391.0Body mass (g) 164931 198949 219929 199939 221938 205939Generalised linear modelSignificant parameters Non-significant parametersFoot length F1,10007.80 p00.006 Sex F1,9500.69 p00.41

Season F1,10009.96 p00.002 Year F4,9602.09 p00.09Area F5,10002.72 p00.024

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Males

On average, body mass of male squirrels increased by 3.81 (90.71) g with each mm increase of foot length(Fig. 3). Variation among study areas changed accord-ing to season and year (Table 2b, Fig. 4a, b). In thefollowing paragraphs we summarize the patterns basedon the significance of pairwise comparisons (details notshown).

In spring, body mass showed hardly any differencesbetween VAL, RHE, and COG, and in these popula-tions annual variation was absent or weak (all compar-isons p0.05, except COG-RHE 2002, p00.044;RHE 2003 Á 2004 p00.034; Fig. 4a). In the other 3study areas, annual fluctuations were more pronounced(Fig. 4a). At BOR, males were lighter in 2002 and 2004than in 2003, consequently, male squirrels at BOR weighed less in spring 2002 and spring 2004 thanconspecifics in all other populations (Fig. 4a). Malesquirrels tended to be heavier at CED than at other sitesin most years, but there was no significant differencebetween mean body mass of animals from CED andOGA in 2002 and 2003. Mass fluctuations over yearsdiffered between these two study areas.

In autumn, male body mass did not differ betweenBOR, VAL, RHE, and COG, except in 2002 when atCOG males weighed less than at VAL and RHE(DLSM, pB0.001, Fig. 4b). At VAL, males reachedhigher autumn mass in 2002 than in 2003 and 2004(DLSM, pB0.05, Fig. 4b). There was no significantbetween-year variation in autumn mass at RHE,

whereas at COG, mean autumn body mass was highestin 2004 and 2000, intermediate in 2003 and 2001, andlowest in 2002 (Fig. 4b). At CED, males weighed less in2001 than in all other years (DLSM, pB0.001), andfrom 2002 to 2004 they weighed more than males inthe other populations (DLSM, pB0.001, Fig. 4b). AtOGA, males weighed less in autumn 2000 and 2002

52 55 58 61 64

Foot length (mm)

220

270

320

370

420

Bo

dymass(g)

Females

Males

f

m

Fig. 3. Relationship between body mass and foot length formale and female red squirrels (subadults and adults) from six study areas in the Italian Alps. Regression lines: (m) malebody mass (slope t26605.38, pB0.0001), (f) female body mass (slope t17604.17, pB0.0001).

Table 2. Mixed linear models investigating effects of study area, age, sex, year and season, interactions (see Results), and foot lengthas co-variate on variation in body mass of subadult and adult red squirrels. (a) Both sexes, using 2037 observations of 434individuals, (b) males, using 1253 observations of 253 individuals, and (c) females, using 784 observations of 181 individuals.a

Excluded from the model.

Fixed effects Statistics Interactions Statistics

(a) Sexes pooledFoot length F1,450045.9, pB0.0001Study area F5,418010.58, pB0.0001 Area)year F16,192304.38,pB0.0001Age F1,18170284.1, pB0.0001 Season)area F10,185403.95, pB0.0001Sex F1,381040.8, pB0.0001 Season)sex F2,1843010.95, pB0.0001Year F4,192209.49, pB0.0001 Season)year F8,178002.41, p00.014Season F2,185801.45, p00.23

(b) MalesFoot length F1,266028.9, pB0.0001Study area F5,230010.26, pB0.0001 Area)year F16,113003.39, pB0.0001Age F1,11240111.5, pB0.0001 Season)area F10,111704.70, pB0.0001Year F4,107707.54, pB0.0001 Season)year F8,107505.75, pB0.0001Season F2,1123011.7, pB0.0001

(c) FemalesFoot length F1,176017.4, pB0.0001 Area)year F16,72102.40, p00.0016Study area F5,17101.43, p00.22 Season)areaa F10,69601.74, p00.069

Age F1,6570171.9, pB0.0001 Season)year F7,67104.40, pB0.0001Year F4,70109.81, pB0.0001Season F2,66807.05, p00.0009

57



than in autumn 2003 and 2004 (DLSM, all pB0.05,Fig. 4b).

Females

Body mass of female red squirrels increased on average

by 4.45 (91.07) g with each mm increase of footlength (Fig. 3). For females, body mass, corrected forvariation in foot length, did not differ on averageamong study areas, but there was a significant study area by year interaction, suggesting that in some yearsfemales were heavier in some sites than in others (Table2c, Fig. 4c, d). Overall, females weighed less in 2000than in other years. The season by area interaction wasnot significant, indicating that trends of seasonal massvariation were similar for all study areas (Table 2c).

There were no differences between years in meanspring body mass of females in 3 populations (CED,

BOR, and COG), while in the other populations trendsdiffered. In OGA females weighed less in 2001 than in2003 and were heavier in 2002 and 2004. Females of the VAL population also were heavier in 2004 than in2003, but those from RHE weighed less in 2002 and2001 and mean body mass was highest in 2003 (Fig.4c). Only in 2002, females at RHE weighed less than atthe nearby COG study area (DLSM, p00.01, Fig. 4c).In 2002, the year with the highest average spring body mass, females from OGA population were heavier thanthose from BOR and RHE populations (Fig. 4c).

At CED, mean autumn body mass of females waslowest in 2002 and highest in 2004 when they also wereheavier than females from the BOR population, thatweighed less than all other populations (Fig. 4d). AtOGA mass variation between years was more pro-nounced and females were heavier from 2002 to 2004than in 2000 and 2001 (DLSM, all pB0.05, Fig. 4d).

Females from OGA were also heavier than those fromCOG in 2000, than females from COG and RHE in2001 and 2002 (DLSM, all pB0.05, Fig. 4d). At VAL,females weighed more in autumn 2004 than in otheryears. At RHE and COG patterns were similar: femalered squirrels reached the highest autumn body mass in2004, followed by 2003 and 2002, they weighed less in2000 and 2001 (DLSM, all pB0.05, Fig. 4d).

Body mass patterns and food availability

We examined whether annual and site-related variationin body mass could be explained by variation in the sizeof tree-seed crops for each sex separately. Since wepredicted that body mass in spring was affected by theseed crop of the previous year, but autumn body massby the seed crop of the same year, body mass-foodrelationships were analysed per season. There was noincrease of spring body mass with larger seed-crops theprevious autumn in either sex (Fig. 5). However,autumn body mass of both males (p00.058) andfemales (p00.028) was positively correlated with thesize of the autumn seed-crop, although only 15%

BOR

(a)

CED COG OGA

AREA

RHE VAL

200

250

300

350 B o d y m a s s ( g )

(b)

200

250

300

350 B o d y

m a s s ( g )

(c)Season*sex

200

250

300

350 B o d y m a s s ( g )

(d)

2 0 0 0 2 0

0 1 2 0

0 2 2 0

0 3 2 0

0 4

Year 2 0

0 0 2 0

0 1 2 0

0 2 2 0

0 3 2 0

0 4

Year 2 0

0 0 2 0

0 1 2 0

0 2 2 0

0 3 2 0

0 4

Year 2 0

0 0 2 0

0 1 2 0

0 2 2 0

0 3 2 0

0 4

Year 2 0

0 0 2 0

0 1 2 0

0 2 2 0

0 3 2 0

0 4

Year 2 0

0 0 2 0

0 1 2 0

0 2 2 0

0 3 2 0

0 4

Year

200

250

300

350 B o d y m a s s ( g )

Fig. 4. Body mass as a function of study area, year, season and sex: (a) spring mass of males, (b) autumn mass of males, (c) spring mass of females, (d) autumn mass of females.

58



(males) to 19% (females) of variation in mean autumnbody mass was explained by variation in food abun-dance (Fig. 5).

Reproduction

Body mass among adult females increased with footlength (F1,11808.67, p00.0039, slope 4.8891.66)and differed with reproductive status (F2,11808.91,p00.0002), but did not differ between study areas.

Anoestrus females (n027, mean9SD0308916 g)weighed less than oestrus (n070, 324929 g) orlactating females (n025, 337923 g) (DLSM: anoes-trus-oestrus t11803.19, p00.0018, anoestrus-lactating t11804.10, pB0.0001). Lactating females tended tobe heavier than oestrus females, but the difference wasnot significant (DLSM t11801.74, p00.085).

Examining the probability of reproduction over theentire study period with logistic regression, heavierfemale squirrels were more likely to reproduce thanfemales of lower body mass (Wald x

2031.3, DF01,

pB0.0001), and probability of producing offspring differed between areas and years (area-effect Wald x

20

17.0, DF05, p00.0045, year-effect Wald x2010.9,

DF04, p00.028, Fig. 6a, b). For example, in 2004 a female that weighed 300 g had a probability to produceoffspring of only 0.53 at CED against 0.68 at BOR, butfemales of the same mass were more likely to have a litter at COG (0.82) and RHE (0.89, Fig. 6a). For

heavier females of 340 g these probabilities increased to,respectively, 0.84, 0.91, 0.95 and 0.97 (Fig. 6a). But,within each study area, females with a certain body masshad a much lower probability of producing offspring in2000 than in 2004 (Fig. 6a). Another example showedthat probabilities of producing a litter increased from2001 to 2002 and further in 2003, but that they werealways lower at CED than at RHE (Fig. 6b). Adding season (Wald x

201.74, DF02, p00.42), or foot

length (Wald x200.51, DF01, p00.48) did not

improve the fit of the model.

Settling success and length of residency

Of 341 dispersing subadult and adult red squirrels, 167(49%) settled and 174 (51%) were transients. Heaviersquirrels were more likely to settle within the study areas than animals of lower body mass (Wald x

2014.4,

DF01, pB0.0001), and probability of settling washigher for spring and summer immigrants than foranimals that immigrated in autumn (season-effect Waldx2012.7, DF02, p00.0018, Fig. 7a). Adding a

0.0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

0.9

1.0

Probabil

ity

produ

ce

offspring

COG 2000RHE 2000OGA 2000CED 2000COG 2004RHE 2004VAL 2004BOR 2004OGA 2004CED 2004

260 280 300 320 340 360Body mass(g)

0.0

0.1

0.2

0.30.4

0.5

0.6

0.7

0.8

0.9

1.0

Probability

produ

ce

offspring

RHE 2003VAL 2003CED 2003RHE 2002VAL 2002CED 2002RHE 2001CED 2001

(a)

(b)

Fig. 6. Logistic curves representing the increased probability of producing offspring as a function of body mass for adultfemale red squirrels. Different curves show changes inprobability of offspring production as functions of differentstudy area )year combinations.

0 3000 6000 9000

Food abundance (103

kJ/ha)

250

270

290

310

330

350

Meanbody

mass(g)

Females, autumn

Females, spring

Males, autumn

Males, spring

f

m

Fig. 5. Relationship between mean body mass in spring (yeart) and mean seed-crop size of the previous year (year t Á 1) and

mean body mass in autumn (year t) and mean seed-crop sizeof the same year (year t) over all study areas for male andfemale red squirrels. Regression lines are provided forrelationships of food with autumn body mass of males (m)and with autumn body mass of females (f).

59



body mass by season interaction (Wald x204.52,

DF02, p00.10), or foot length (Wald x201.24,

DF01, p00.27) did not improve the fit of the model.The other factors tested, sex, age, area and year, or theirinteractions with body mass, were not related withprobability of settling (all p0.10). Average residency was 16911 months (skewness 1.28, kurtosis 2.29,SE00.82), with a minimum of 3 and a maximum of 51 months. Length of residency increased with body mass (Fig. 7b), and body mass together with study area explained 15% of the variation in length of residency

among individual red squirrels (Table 3). Local survivalwas higher at OGA than at RHE, COG, and BOR (Tukey test). There was no relationship between footlength and residency (Table 3). Effects of sex, age, ortheir interactions with body mass were not significant

(Table 3).

Discussion

We found differences in body size and body mass of Eurasian red squirrels among nearby populations andaverage body mass in the different populationsfluctuated between years. Significant area by yearinteractions showed that patterns of changes in body mass were complex. Differences in size and massbetween populations were partially explained by

habitat-related differences in body size and foodavailability, but variation in seed crop-size corre-sponded only weakly with variation in autumn body mass. There was no sexual dimorphism in body size,but patterns of seasonal variation in body massdiffered between the sexes. In spring and summerfemales tended to be slightly heavier than males, dueto pregnancy and/or a mass gain during early lacta-tion. There was no evidence of autumn fattening (Wauters and Dhondt 1989b, Lurz and Lloyd 2000,

Wauters et al. 2001a) in these alpine populations.Finally, we found several positive effects of having a relatively high body mass on fitness components:heavier females were more likely to reproduce; and,within each population, having a relatively high body mass positively affected male and female settlementsuccess and length of residency. Hence, our resultssuggest that in temporally variable environments thatdiffer in overall amount of food resources, individualvariation in body mass is related to habitat type, andthat having a relatively high body mass is advanta-geous, increasing both reproductive success and localsurvival.

Table 3. General linear model investigating effects of bodymass, study area, age, sex, and their interactions with bodymass, and foot length as co-variate, on variation in length of residency (ln-transformed) of red squirrels.

Parameter Statistics

Body mass by study area F5,17600.68, p00.64Body mass by sex F1,18101.67, p00.20Body mass by age F2,18201.53, p00.22

Foot length F1,18400.32, p00.57Sex F1,18500.50, p00.48Age F2,18601.64, p00.20Study area F5,18803.30, p00.007Body mass F1,188012.95, p00.0004R2 selected model00.15 F6,18805.65, pB0.0001

250 270 290 310 330 350

Body mass(g)

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

Probabilitytosettle

Autumn

Summer

Spring

250 300 350 400

Average individual body mass(g)

0

10

20

30

40

50

60

Reside

ncytime(months)

COG

RHE

VAL

BOR

OGA

CED

(a)

(b)

Fig. 7. (a) Logistic curves representing the increased prob-ability of settling as a function of body mass for subadult andadult red squirrels. Different curves show changes in prob-ability of settling in relation with immigration period(season). (b) Relationship between mean body mass of individual red squirrels and length of residency: differentsymbols present the different study areas.

60



Sexual size dimorphism

Patterns of sexual size dimorphism differ betweenspecies of sciurids. In some species of chipmunks (e.g.yellow-pine chipmunk Tamias amoenus ) females are ca 4% larger (body size) and 10 Á 20% heavier than males(Levenson 1990, Schulte-Hostedde et al. 2001), whileadult males of territorial North American red squirrelsTamiasciurus hudsonicus are on average ca 10 Á 30 g heavier than adult females (Boutin and Larsen 1993). Inthis species, post-weaning growth and survival were notcorrelated and sexual dimorphism was less pronouncedin years of abundant food (Boutin and Larsen 1993).

Although bigger mothers might provide more and/orbetter maternal care (Wauters et al. 1993, Dobson andMichener 1995, Wauters and Dhondt 1995), it is stilluncertain how natural selection has favoured femalesgrowing larger than males in some species, since they allhave promiscuous mating-systems where larger orheavier males tend to be dominant over lighter (orsmaller) males during mating chases, and, consequently,obtain a higher mating success (Wauters et al. 1990,Koprowski 1993a, b, 1998, but see Farentinos 1980).In contrast, lack of sexual size or mass dimorphismseems to be the rule for most holarctic tree squirrels of the genus Sciurus (Wiltafsky 1973, Nash and Seaman1977, Koprowski 1994a, b). In Eurasian red squirrelsthere are no differences in body mass between the sexesthroughout most of its range (Wauters and Dhondt1989a, Lurz 1995, Munch 2000). In Belgium, malesand females did not differ in body size measurementsand had similar body mass in late autumn and winter,when females did not invest extra energy in lactation(Wauters and Dhondt 1989a, b). During months whenmany females were pregnant or in early lactation they weighed more than males (Wauters and Dhondt1989b). In this study on alpine populations, using average body mass over all years and seasons, femaleswere 3.6% heavier than males, a small but statistically significant difference. In our data set, however, somefemales were in reproductive condition (pregnant orlactating) in all seasons, which might cause an upwardmass bias in adult females (Wauters and Dhondt1989b, 1995, Humphries and Boutin 1996, 2000).The significant sex by season interaction, indicating different seasonal patterns of body mass changes formales and females, and small differences between maleand female body mass in autumn (males, 307926 g,females, 312929 g), when only a small proportion of females is still lactating, agree with this hypothesis.Finally, females averaged 10 g heavier than males inonly one population, VAL. This population has only been monitored for ca 2 yr and further data will begathered to examine possible sexual dimorphism inbody mass.

Habitat type and annual and seasonal variation inbody mass

The size of conifer seed crops varied strongly over yearsin some study areas (e.g. CED and RHE) but remainedrather constant in others (e.g. OGA). This is theconsequence of patterns of seed production of thedominant tree species. Norway spruce and silver fir

show masting (high and synchronized, episodic seedproduction, Smith 1970, Silvertown 1980), thus inspruce and spruce-fir forests, years of rich seed-cropsalternate with poor to medium seed production, withseed-crop failure occurring about every 5 yr (Mencuc-cini et al. 1995, Wauters et al. 2005). Scots pine, incontrast, produces rather stable seed-crops in most years(Wauters and Lens 1995, Castro et al. 1999) and totalseed-energy production varied little throughout thestudy period. Our results showed that this variation inseed-production affected between-population differ-ences and fluctuations in average body mass of red

squirrels over years. Autumn condition was weakly butpositively correlated with autumn seed-crop size. This isprobably directly related with higher feeding ratescausing a more positive energy-balance in autumnswith high seed abundance and lower foraging costs.

Also in squirrel populations in Belgium, good tree seed-crops positively affected autumn-winter body mass of red squirrels, thereby increasing immigration success of subadults and winter survival of subadults and adults(Wauters and Dhondt 1989a, b, 1993, Wauters andLens 1995, Wauters et al. 2004b). Why was the food Á body mass relationship in different alpine populations

rather weak? We suggest this is related to between-sitedifferences in body size and in temporal variation in theavailability of the major seed species. At OGA, redsquirrels were heavier than expected on the basis of absolute seed-energy production, but the dominant treespecies, Scots pine, had relatively stable seed-crops overyears. This might help squirrels to use relatively smallhome ranges linked with low costs of moving (Wautersand Dhondt 1992), and have activity patterns thatallow them to maintain higher body mass than in morevariable spruce-larch forests. At CED squirrels wereheavier than in other populations in most years, but

they were also larger in structural size. Finally, inspruce-larch forests, body mass might be only poorly related to available food supplies because squirrelsshowed a time-lag in responding to changes in seedabundance, still using large home ranges, and thereforehaving high energy-costs of locomotion, in the autumnwith a medium to good seed-crop when it followed a seed-crop failure (Wauters et al. 2005)

Contrary to expectation, there were no relationshipsbetween spring condition of squirrels and tree-seedcrops produced the previous autumn. There might beseveral explanations for this. In spring, seed-crops of the

61



previous year become gradually depleted, because coneshave dispersed most of their seeds (Norway spruce,Scots pine, larch), or because all cones have beenharvested from the trees and their seeds cached (Arolla pine). Therefore, a squirrel’s condition might depend of the amount of stored (cached) food within its homerange, and thus within-home-range food availability,which was not measured here, might affect body mass ata fine-grained level (Wauters et al. 2001b). Analternative, but not mutually exclusive hypothesis isthat secondary food resources, such as fungi (Moller1983, Wauters and Dhondt 1987, Bertolino et al.2004), buds, shoots, and male flowers of conifersconstitute an important part of the diet and affectbody-mass variation. Finally, each sex might beoptimizing its daily food-intake to ‘‘face’’ the currentor future costs of reproduction. Breeding females tendto increase daily energy-intake and thus become heavierduring pregnancy and early lactation (see below),whereas males might try to maximize body mass to

improve their competitive ability in intrasexual en-counters during mating chases (Wauters et al. 1990,Koprowski 1998).

Seasonal body mass variation in alpine populations(on averageB3% of summer mass) was much smallerthan in populations in west and central Europe(Wauters and Dhondt 1989a, b, Munch 2000), anddaily changes (difference between subsequent measure-ments within a single trapping session) were of the samemagnitude (see our preliminary analyses). In contrastwith other populations, there was no evidence for alpinesquirrels fattening in autumn (September Á October). A

similar lack in autumn mass increase was also found fornative red and introduced grey squirrels in coniferplantations (with several exotic conifer species) innorthern England (Lurz and Lloyd 2000). Theseauthors suggested that fat accumulation was lesspronounced or even absent in conifer habitats whereautumn and winter food supplies are more predictable,and manoeuvrability to feed on cones in the canopy isimportant.

Size differences between populations

The average body mass of adult red squirrels fromalpine populations was 315925 g (range 240 Á 400 g).This was less than mean adult body mass frompopulations living in high-quality woodlands withstable food supplies, and high squirrel densities inBelgium (mean9SE033097.1 g, t04.14, pB0.0001, Wauters and Dhondt 1989a, b). Variance inbody mass was similar in both countries (from 270 to380 g in Belgium). Adult squirrels from alpine forestswere also smaller than conspecifics in Belgium (averagehind foot length: Italy 58.091.5 mm, Belgium 59.99

0.25 mm, t02.13, pB0.0001). Subadults were smal-ler and weighed less than adults in all populations andyears, as found in other habitats throughout thesquirrel’s range (Wauters and Dhondt 1989a, Lurz1995, Munch 2000).

Among populations from the southern Alps, meanhind foot length did not differ between male (57.891.5 mm) and female squirrels (57.791.5 mm), butsquirrels were larger at CED and smaller at RHE thanat the other 4 sites. This could be the result of differential selection in populations at CED and RHE(Garant et al. 2005). CED is part of large contiguousforests of the Orobic Alps in Valtellina that changefrom deciduous woods dominated by chestnuts Casta- nea sativa at submontane elevations, over mixedmontane forests of beech Fagus sylvatica , silver fir andNorway spruce (in the study area), to subalpine spruce Á larch forests at elevations above 1800 m a.s.l. Hence,many animals in this population have access to largenuts (sweet chestnuts, hazelnuts, and beechnuts) that

allow higher rates of energy intake than foraging onsmall-seeded conifers (Wauters et al. 2001a, Steele et al.2005). Larger squirrels might be advantaged oversmaller ones in handling these large nuts (Weigl et al.1998). RHE, in contrast, is part of an extensivesubalpine conifer forest dominated by Norway sprucewith patches of larch that increase at higher elevations(Wauters et al. 2004a, 2005). Here, squirrels only haveaccess to small conifer seeds that are difficult to extractfrom closed cones. Therefore, squirrels are likely toneed more time to fulfil their daily energy demands andnatural selection might favour smaller individuals with

lower absolute energy requirements. Although thissuggestion is speculative, recent studies on birds andclosely related tree squirrels have shown that there isstrong selection on traits of body size and that non-random dispersal might reinforce population differen-tiation and adaptation at small spatial-scale (McAdamand Boutin 2003a, b, Haughland and Larsen 2004,Garant et al. 2005).

Body mass and reproduction

Body mass among adult females differed with repro-ductive status, independent of foot length. Anoestrusfemales weighed ca 5% less than females in oestrus andca 9% less than lactating females. We found thatheavier female squirrels were more likely to reproducethan females of lower body mass, but probability of producing offspring also differed between study areasand years. These results agree with earlier studies onEurasian red squirrels in Belgium (Wauters andDhondt 1989a, 1995) and eastern chipmunks Tamias striatus . However, as Humphries and Boutin (1999)pointed out, the differences found in these cases may be

62



due to reproductive females increasing their daily rate of food-energy intake gaining more mass to meet thegrowing energy-demands of lactation (Cuthill andHouston 1997). In Tamiasciurus hudsonicus , massgain during early lactation (indicating changes inbody fat levels) was positively related to litter size andfemales that gained most mass had the highest levels of

juvenile survival to emergence (Humphries and Boutin1996). Hence, in female North American red squirrelsearly lactation mass gain is an important component of parental investment under favourable conditions(Humphries and Boutin 1996). Because of highly asynchronous breeding in alpine red squirrel popula-tions, our spring data were taken during the prepartumperiod for part of the animals and during early postpartum for others. Since lactating females tendedto be heavier than oestrus females and both were heavierthan those that did not reproduce, our data suggest thatboth mechanisms occur. On the one hand, reproduc-tion is mass-dependent, with a minimum threshold of

body condition (mass corrected for size) that must bereached before a female enters oestrus (Wauters andDhondt 1989b, Lurz 1995, Wauters and Lens 1995).On the other hand, successfully reproducing femalesincrease body mass, independent of size, during early lactation, suggesting that they supplement their energy reserves in preparation for pronounced increases inenergy requirements during late lactation (Gittlemanand Thompson 1988, Wauters and Dhondt 1989b,Humphries and Boutin 1999).

Interestingly, the probability of reproducing among alpine female red squirrels of a given body mass varied

strongly between habitats and, to a lesser extent,between years. The between-year differences wererelated to variation in tree seed production, andprobability of reproducing increased when seed abun-dance was high. However, in a given year (e.g. 2004)females of 280 Á 290 g at RHE and COG had a similarprobability (975%) to reproduce than conspecificsweighing 310 Á 315 g at BOR and VAL, and females of 320 Á 325 g at OGA and CED. Since in 2004 goodseed-crops were produced at all sites, these between-habitat differences suggest variation in life-history strategies, linked with variation in body size/mass

among red squirrel populations occurring in differentforest types at a small spatial scale. In North Americanred squirrels, probability of (first) reproduction wascorrelated with cone crop size and further constrainedby foraging and cone-handling efficiency that mightdiffer between primiparous and multiparous females,but also between forest types (Becker et al. 1998).Variation in feeding efficiency (rate of energy-intake perunit time) while processing cones from different treespecies are likely to exist also in Eurasian red squirrels,where cone size, ratio of protective cone mass on totalseed mass (Molinari et al. 2006) and, probably,

concentrations of secondary compounds (resins, tan-nins) differ between conifer tree species.

Finally, body mass in alpine red squirrel populationsalso positively affected probability of settlement andlength of residency, a measure of local survival. This wasalso the case in high-density populations in mixedconifer and broadleaf woods in Belgium, where body mass was positively related with immigration success andwith longevity (Wauters and Dhondt 1989a, 1993).

We conclude that in temporally variable environ-ments that differ in overall quantity of food resources,individual variation in body mass of Eurasian redsquirrels is high and body mass, in particular itscondition component, positively affects male andfemale settlement success and local survival, and femalereproductive success. Overall, this confirms results fromother populations that live at higher densities in habitatswith larger and more stable food supplies (Wauters andDhondt 1989b, 1993, 1995). However, significantdifferences existed in both size (hind foot length) and

mass between alpine populations, that could beexplained, at least partly, by habitat-related differencesin total size and degree of (annual) variation of seed-crops of the dominant conifer species. This suggestsdifferential selection for smaller red squirrels in spruce-larch forests (RHE, COG, VAL), against larger andheavier animals in mixed conifers with some nut-bearing broadleaves (CED) or in Scots pine dominatedforests (OGA). In North American red squirrels,direction and strength of selection on growth ratesvaried with age, but also with cohort (young born inrich food-years against young born in poor food-years,

McAdam and Boutin 2003a, b). In populations of Eurasian red squirrels in high-quality habitats inBelgium, there was no cohort effect on any of thecomponents affecting lifetime reproductive success of females (Wauters and Dhondt 1995). However, inalpine squirrel populations occurring in habitats with a high degree of temporal variation in resource abun-dance (availability), cohort effects may exist. The data presented in this paper are still on too short a time-scaleto explore this hypothesis in more depth.

Acknowledgements Á We wish to thank G. Airoldi, P. Lurz, and

M. Zaninetti for assistance with fieldwork, and D. Preatoni forpreparing figures. Comments by Petit D. Kelt helped toimprove the ms. The study was part of the ASPER (AlpineSquirrel Population Ecology Research) project, carried out by Univ. of Insubria, Varese and Istituto Oikos NGO, Milan.Financial support was provided by the Wildlife Service of theProvince of Sondrio, the Parco Regionale Orobie Valtellinese,and grants awarded to L.A.W. and S.B. from the Gran ParadisoNational Park, Italy (DGE 25 Á 2000), and the Committee forResearch and Exploration of the National Geographic Society,

Washington DC, USA (grant no. 6997-01). Additionalfinancial support was obtained from MIUR (Ministerodell’Istruzione, dell’Universita ` della Ricerca, project COFIN

63



2003, number 2003053710-006) to Insubria Univ., andlogistic support was provided by the Stelvio National Park.

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