1870

IntroductionDeer mice (Peromyscus maniculatus) are remarkably flex-

ible in their habitat distribution, ranging from mature coni-ferous forests to grasslands. Red-backed voles (Clethrionomysrutilus) live in a variety of forest and shrubland habitats,frequently coexisting with deer mice. In contrast to the twoprevious species, meadow voles (Microtus pennsylvanicus)occur mainly in open habitats such as meadows, grasslands,abandoned fields, forest edges, and openings. These threegenera dominate rodent communities in nonarid temperatehabitats and often show contiguous populations between"forest species" and "grassland species."

What factors determine the use of habitats by these threespecies? Early observations on islands, where one species oc-cupied a wider range of habitats in the absence of the others(ecological release), stimulated experimental work to test thehypothesis that competitive interactions between species wereresponsible for their habitat distribution (Grant 1972, 1978).However, the evidence accumulated on interactions betweenthese three genera (P eromy scus, M icrotus, and C lethrionomy s)is contradictory (Grant 19721,Redfield et al. 1977; Abramskyet al. 19791, Hallet et al. 1983; but see M'Closkey 1975a,

Habitat use and abundance of deer mice: interactions with meadow voles andred-backed voles

Cnnr-os G¿.r-rNoo nNl CnRnr-es J. KnsssDepartment of Zoology and Institute of Animal Resource Ecology, The University of British Columbia,

2075 Wesbrook Mall, Vancouver, 8.C., Canada V6T lwsReceived December 31. 1984

GnI-INoo, C., and C. J. KREBS. 1985. Habitat use and abundance of deer mice: interactions with meadow voles and red-backedvoles. Can. J.Zoo1.63: 1870-1879.

In this study we investigated the influence ofcompetitive interactions on the use ofhabitats and relative abundance ofdeermice (Peromyscus manicularas). If interspecific competition is influencing the habitat use and relative abundance of deer mice,then removal or introduction of potential competitors will change habitat use and abundance of this species. During the firstfield season we removed meadow voles (Microtus pennsylvanicus) to look at the effect on the contiguous population ofdeermouse. The removal ofone species had no effect on the other species' distribution or demography. In the second field season,meadow voles declined to very low numbers and we used their natural fluctuation as a removal experiment. Deer mousepopulations were not affected even when the natural decline of meadow voles was more effective in maintaining the sedgemeadow free of voles than the previous removal manipulation was. During the 3rd year, meadow voles colonized two areasofforest where deer mice had been alone the previous two field seasons. Red-backed voles (Clethrionomys rutilus), in turn,increased from very low numbers in four grids. Neither meadow voles nor red-backed voles affected the spatial distributionor abundance of deer mice. The results of this study indicate that competitive interactions have no influence on the use ofhabitats and relative abundance of the common species of small mammals in the southwestern Yukon.

GnI-Iuno, C., et C. J. KREBS. 1985. Habitat use and abundance of deer mice: interactions with meadow voles and red-backedvoles. Can. J. Znol. 63: 1870-1879.

L'influence des interactions compétitives sur I'utilisation de I'habitat et sur I'abondance relative des souris sylvestres(Peromyscus maniculatus) a fait I'objet d'une étude. Si la compétition interspécifique a une influence sur ces paramétres, leretrait ou l'introduction de compétiteurs potentiels devrait entrainer des changements dans I'utilisation de I'habitat et la densitéde la population. Au cours de la premiére saison d'étude, les campagnols des champs (Microtus pennsylvanicus) ont été retirésde la région d'étude et les effets de ces retraits sur la population voisine de souris sylvestres ont été examinés. Le retrait d'uneespéce est resté sans effet sur la répartition ou la démographie de I'autre espéce. Au cours de la seconde saison d'étude, lescampagnols des champs ont subi une importante réduction de leur nombre et cette fluctuation naturelle a pu étre utilisée commeexpérience de retrait. Les populations de souris sylvestres n'ont pas été affectées, méme si le déclin naturel de la densité descampagnols diminuait le nombre de campagnols dans la clairiére de laiches plus efficacement que I'expérience précédente. Aucours de la troisiéme année, les campagnols des champs ont colonisé deux régions forestiéres oü les souris sylvestres étaientles seuls habitants durant les deux saisons antérieures. Des campagnols á dos roux (Clethrionomys rutilus) ont aussi connu unerecrudescence de leur population dans quatre territoires oü leur nombre était tr¿s faible auparavant. Ni les campagnols deschamps, ni les campagnols i dos roux n'ont affecté la répartition spatiale ou I'abondance des souris sylvestres. Il semble doncque les interactions compétitives n'aient pas d'influence sur I'utilisation du milieu ou sur I'abondance relative des espécescommunes de petits mammiféres dans le sud-ouest du Yukon.

[Traduit par le journal]

1975b; M'Closkey and Fieldwick 1975; Morris 1983; King1983; Martell 1983).

Alternatively, these temperate rodents have been describedto be strong habitat selectors (M'Closkey 1975a, 1975b;M'Closkey and Fieldwick 1975; Monis 1983).

To test the hypothesis that competition is responsible for thedifferential habitat use (small overlap) and relative abundanceamong these three species, we used artificial and natural fieldexperiments. In the first field season we artificially removedthe meadow vole population from a sedge meadow adjacent tothe forest where deer mice occurred alone. In the 2nd year adecrease in this cyclic population provided us with a naturalremoval experiment: voles were almost completely absent fromthe sedge meadow. The'third summer, meadow voles colo-nized the forest, and red-backed voles, absent the previous 2years, increased in numbers, providing natural introductionexperiments.

The predictions for these situations from Grant's hypothesisare the following: (i) A change in resource use. In the absenceof meadow voles in the contiguous habitat (removal experi-ment), deer mice will expand their use of habitats (niche shiftor ecological release), showing a larger niche breadth and a

larger niche overlap. In the presence ofmeadow voles and (or)red-backed voles in the same habitat (introduction experi-ments), deer mice will restrict their use of the habitat, showinga smaller niche breadth and smaller niche overlap. (rr) Achange in numbers. Deer mice will increase in numbers afterthe removal of meadow voles (removal experiment). Thismight happen through higher immigration, lower emigration.higher survival and (or) higher reproduction. Deer mice willdecrease in numbers after the introduction of meadow voles and(or) red-backed voles (introduction experiments).

Study areaThe fieldwork took place at the south corner of Kluane Lake, Yukon

Territory (61" N, 138'W), during the snow-free seasons (May toSeptember) of 1981, 1982, and 1983.

The study was carried out in three different habitats: boreal forest,sedge meadow, and shrubland. The first two habitats have been de-scribed as vegetation zones by Hoefs et al. (1975). Shrubland includessuccessional stages of different ages.

The boreal forest, dominated by white spruce (Picea glauca), oc-cupies the lower valleys from 770 to I100 m. The density of differentspruce stands and the presence of balsam poplar (Populus balsami-fera) andtrembling aspen (Populus tremuloides) in some areas createsa variety of associations of dominant hee species that influence theshrub and herb undergrowth. These associations have been recognizedas different plant communities (Douglas 1914) or habitats (Krebs andWingate 1976).ln this study we defined boreal forest as one habitat.The common species in the understory are soapberry (Shepherdiacanadensis) in the shrub stratum and licorice root (Hedysarumboreale) and bearberry (Arctostaphylos rubra, A. uva-ursi) in theherb stratum.

The sedge meadow is mostly restricted to the margins of the lake.The fine-textured soils of this habitat are water saturated and in someareas flooding occurs during autumn because of the rising level of theunderground water table (determined by rising lake level). A varietyof sedges (Carex spp.), cottongrass (Eriophorum angustifolium),and other monocotyledons (Juncus spp.) are the most conspicuousplants in the meadow. Horsetails (Equisetum palustre) are very abun-dant, and small willow shrubs (up to I m) (Salix glauca) are widelyscattered.

The shrubland habitat is less well defined and encompasses suc-cessional forest stages dominated by tall (l to 3 m) willows (Salrrglauca), balsam poplar, and white spruce in open stands. The shrubsare common in patches and along creeks close to the sedge meadows.Soapberry and licorice root are abundant in the understory.

MethodsPatterns

Since pattems of habitat use (habitat breadth, habitat overlap) andrelative abundance change from year to year (Krebs and Wingate1976), we determined habitat utilization pattems and abundance in-dices during the first field season (1981) by the use of snap-trap lines.Each line consisted of 20 stations with three "museum special" snap-traps per station (Krebs 1964; Krebs and Wingate 1976). Stations werespaced at l0-m intervals. The traps were baited with peanut butter, setfor th¡ee consecutive nights, and checked daily. Throughout thesummer we set 45 snap-trap lines in the following way: 13 in theforest, 14 in the sedge meadow, l0 in the ecotone between forest andmeadow, and 8 in the shrubland habitat.

We used simple measures of niche breadth and niche overlap(Levins 1968; Colwell and Futuyma l97l; Southwood 1978, formulas13.30 and 13.31, pp. 445 and 446).

We used both Cole's (C7) and Hulbert's (C8) coefficients of inter-specific association to indicate the strength of the associations in thecontingency table analysis (Cole 1949; Hurlbert 1969).

We used adjusted G logJikelihood tests (G"¿¡) to analyze the habitat

187 I

TABLE l. Experimental design. During l98l and 1982 the grids occu-pied both rireadow and forest habitats, and removal of meadow volestookplace in the meadow habitat; during 1983 the grids were reduced

to the forest habitat

1982 1983

A Control Removal

-meadow volesControl

-meadow volesControl

Removal

-meadow voles

distribution of captures at both snap-traps and live traps. Captures atlive traps are not completely independent since the same individualsare sampled. To minimize this, we took into account only the firstcapture of every trap session.

Trapping techniqueThe experiments were carried out on livetrapping grids. We used

Longworth live traps spaced at lO-m intervals. We prebaited the trapsfor 5 days and set them for two nights every other week or more often.Whole oats were used as bait and cotton batting as bedding. Afterevery trap session the traps were locked open, allowing the animals tomove in and out freely. Animals captured were ear-tagged with finger-ling fish tags, and we recorded species, tag number, sex, breedingcondition, body weight, and trap location. Breeding condition ofmales was assessed by recording their testes position as either abdom-inal (not breeding) or scrotal (breeding). For females we recordedvaginal status (open or closed), nipple size (small, medium, or large),condition ofthe pubic symphysis (closed, slightly open, or open), andevident pregnancies.

Experimental design I98IDuring 1981 we used two livetrapping grids: an experimental

(B.81) and a control (A.81). Each grid had 120 Longworth live trapsarranged in a rectangular grid of 6 x 20 trap stations, covering an areaof approximately l.2ha. Both grids were located in a similar way atthe ecotone between spruce-poplar forest and sedge meadow. One-third of each grid (rows 14 to 20) was on the forest area while the othertwo{hirds (rows I to 13) were on the sedge meadow. The grids wereparallel to each other and separated by 213 m (700 f0. Some of thesnap-trap lines described above were near the livetrapping grids butnever closer than 150 m (492 ft).

Beginning on the second trap session we removed all meadow volescaught at the experimental grid (8.81) every other week or more often.The aim of this manipulation was to reduce their population to observethe effects of such reduction on the contiguous population of deermice.

Experimental de sign I 982During 1982 we set four livetrapping grids. The two former grids

were used in the same way as in the previous year, but the treatmentswere reversed. The control grid (A.81) in l98l became the removalgrid in 1982 and vice versa. We added a new grid (E.82) of similarsize to the previous and situated also at the ecotone between the twohabitats (Table l).

This year, however, the population of meadow voles had becomevery scarce and stayed low throughout the summer. Therefore, thethree grids are considered natural removal experiments. The onlydifference between the afificial removal treatment (A.82) and the

GALINDO AND KREBS

1981Grid

B

CDE

G

H

Removal

-meadow volesIntroduction

*meadow volesControlControlIntroduction

*meadow voles*red-backed voles

Introduction*red-backed voles

Introduction*red-backed voles

1872

4

Number 3of

lndiv¡dualscaught

per 1OO

frap 2

Nights

cAN. J. ZOOL. VOL.63, 1985

MEADOW ECOTONE FOREST SHRUBLAND

Hc. l. Density indices for deer mice and meadow voles in dif-ferent habitats for May to September 1981.

Observed

Expected

DEER MICE

Numberof

Captures

600MEADOW VOLES

Number 4ooof

CaDtures' 200

FOREST MEi

Flc. 2. Microhabitat use by deer mice and meadow voles on thecontrol grid during 198 I . Each species used one habitat and was rarelycaught in the contiguous habitat.

other grids is that on the former we removed the few animals livingthere, reducing this population even further and keeping the habitatempty of Microtus.

The control grid (C.82) was located further away from the meadowsin an advanced successional stage dominated by tall willows and a fewspruce trees. It was a rectangular 4 x l0 grid occupying an area

similar in size to the forest part of the removal grids. We trapped thisgrid froÍn July to September.

Experimental design 1983During the field season of 1983 we used six livetrapping grids. We

reduced them to about one-third of their former size, leaving only thetraps in the forest habitat. Their sizes ranged from 0.42ha to 0.54 ha,and the number of raps ranged from42 to 60. Two grids (B.83, E.83)were colonized by meadow voles. Three grids were colonized byred-backed voles (E.83, G.83, H.83). The other two grids (C.83,D.83) had very low numbers ofred-backed voles and were considered

MEADOWVOLES

MinimumNumber '

Al¡ve

FIc. 3. Effect of the removal treatment on numbers of meadowvoles. The natural decline during 1982 made the removal treatmentsmore effective in reducing vole densities.

controls. However, we made comparisons with grids in previous years

also (Table 1).

Results

Patterns of habitat use

Habitat useThe captures from snap-trapping lines (8040 trap-nights)

indicated broad patterns of habitat use by both species duringthe summer of 1981. We caught nearly equal numbers of deermice and meadow voles but in different habitats. Deer mice(¿ : 105) were caught mainly in the forest (47Vo) and sec-ondarily in the shrubland (25Vo) and ecotone (24Vo) habitats.Very few (4Vo) were caught in the sedge meadow. In contrast,meadow voles (n : 108) were highly restricted to the sedgemeadow (78Vo). Some were caught in the ecotone (l8Vo) andfewer (4Vo) in the shrubland habitat, none was caught in theforest (Fig. l).

A resource matrix analysis using these four habitats as differ-ent resource states indicates a larger habitat niche breadth fordeer mice (B : 3.06) than for meadow voles (B : 1.76). Theirhabitat niche overlap is small (C : 0.313).

Microhabitat useThe habitat that showed the maximum overlap of both

species was the ecotone. A closer analysis of the microdistri-bution in this area revealed prominent differences. To analyzethis microdistribution we used the control livetrapping grid thatwas set perpendicular to the boundary between forest andmeadow. Each habitat had a different proportion of live traps.The distribution of both species in these habitats was verydifferent from that expected if the animals were using thehabitats proportionally to the number of traps set in each. Deermice were almost confined to the forest habitat (G"¿¡ : 130.71,p < 0.005) while meadow voles were nearly confined to themeadow habitat (G¡:: 465.31, p < 0.005). Both speciesrarely used the shrubland habitat and were nearly absent fromthe habitat occupied by the other species (Fig. 2).

In summary, deer mice and meadow voles used distincthabitats and showed contiguous populations with small overlap

o:a A.81 coNrRoL a? g.gt EXPERIMENTAL /o< 8.82 coNrRoL ^/? ,¡.az ExpERtMeNr^L

Za=ao'.ao.z

///

FORESf MEADOW

4.81 8.81 8.82 4.82 E.82

GALINDO AND KREBS 1873

't4

DEEB MICE 12

Capturesper 'l O0

Trap Nights

FOREST

MEADOW

Hc. 4. Habitat use by deer mice. Deer mice were mainly confinedto the forest habitat of the five livetrapping grids in spite of the absence

of meadow voles.

when their habitats come into contact. Deer mice used a widerrange of habitats. They were mainly found in the forest butused shrubland habitat too. Meadow voles, on the other hand,were mainly confined to the meadow habitat.

Removal experimentsWe used four removal grids. During the first summer we

used grid B.8l as an artificial removal grid. The natural declineof the meadow vole population during the second summerproduced natural removal experiments in A.82, B.82, andE.82. Grid A.82 was subjected to an additional artificialremoval to lower the population of meadow voles even further.

Effectiveness of removal manipulationsA major difficulty in using and interpreting the results of

removal experiments is that animals living in surrounding areascontinuously immigrate after the resident individuals have beenremoved. This immigration into the vacant area was stronglyreduced during the second field season (1982) when the volepopulation decreased naturally. We used two ways to evaluatehow effective the removal treatments (8.81, 8.82, A'.82) wereat keeping the areas without voles. (i) By comparing theintensity of use (number of trap stations used per trappingsession) in these treatments with that in the control. The meannumber of trap stations used by Microtus per trapping sessionwas 15 at B.81, 3 atB.82, and2 at A.82. This translates intoa reduction of use by Microtus of 53Vo,9l%o, and 94Vo, re-spectively, in relation to the control grid in 1981, where 32 fiapstations per trapping session were used on average. (tt) Bycomparing the intensity of use with the availability of trapstations in the meadow. The reduction is even more dramaticin relation to the number of traps available in the meadow. Onthe control grid, an average of 397o of the meadow traps wereusedby Microlrrs per trap session while only 22Vo , 4Vo , and 2Vo

were used at B.81, B.82, and A.82, respectively.A further indication of the effectiveness of the removal treat-

ments is given by the number of individuals removed withintrapping sessions. Voles were caught and subsequently re-moved either during the first or the second night of every trapsession. In both grids (B.81, 4.82) from which voles wereartificially removed, most were removed on the first night andvery few on the second. At 8.81 the mean number of volesremoved per trap session was 10.44, from which an average of8.9 were removed on the first night, whereas only an averageof 1.54 were removed on the second. At A.82, 3.44 individuals

TABLE 2. Results of G logJikelihood testfrom comparisons of habitat use by deer

mice in 1981 and 1982

Grid comparisons Forest Meadow10

I

6

4

B.8l vs. A.8lA.82 vs. A.8lB.82 vs. A.81A,.82 vs. B.82B.82 vs. B.8l

. A.82 vs. B.8lE.82 vs. A.8l8.82 vs. A'.828.82 vs. B.81E.82 vs. B.82

l.oE 5.50*0.54 0.540.04 I .181.20 0.220.77 1.570.08 I . 18

o.2t 2.260.18 0.962.83 0.340.68 0.30

NorE: Expected values were obtained using trappingintensity (trapnights). Only I out of 20 comparisonswas significant. Habitat use by deer mice was similar inthe grids regrdless of the absence of meadow voles.

14

12

DEER MICE

MinimumNumberAlive

'1412

DEER MICE 10

Minimum INumberAlive 6

4

2

MJJASFrc. 5. Changes in minimum number alive of deer mice during

l98l and 1982 in both experimental and control grids.

were removed every session on average. The average was 2.54and 0.9 for the first and second night, respectively. This de-cline of animals removed within trapping sessions indicatesthat the area was almost free of voles after each session.

In summary, the removal treatments were highly effective inreducing vole densities. This was more so during the secondfield season (1982), when the natural decline in vole numbersoccurred. Figure 3 shows the effect of the removal treatmentson numbers.

Spatial distibutionDid deer mice change their habitat use after the removal of

nieadow voles? Deer mice used mainly the forest habitat in the

10

8

6

4

2

a-aA-82 ExPERTMENTAL

o-o 8.82 coNrRoL o..i

., i9'... .p"o ii'olt'?

\ / oo..,., \/ oo

1874 cAN. J. ZOOL. VOL. 63, 1985

Tenm 3. Deer mouse reproductive data, l98l and 1982

B.8lA.8l (artificial

(control) removal)

8.82C.82 (natural

(control) removal)

4.828..82 (natural +

(natural artificialremoval) removal)

Juveniles firsttrapped

End of malebreeding season*

End of femalebreeding season*

No. of litters(No. of females)f

No. of juvenilesrecruited*

Juvenile productivity

Jul. 3

Jun. 18

Aug. I

2 (r)

Jul. 3

Jul. 3

Aug. I

2 (2)

Jul. 10

Jul. 29

I (l)

Jun.29

Jun. l7

Aug. ll

5 (5)

Jul. 8

Jul. l4

Jul. l4

6 (4)

264.3

Jul. 8

Jul. l4

Aug. ll

s (4)

1l2.2

l53

t212

22ll

20l0

*Last individual breeding.iAdult females caught in two or more trapping sessions.

fJuveniles tagged in the grid.

Te¡le 4. Deer mouse survival data, l98l and 1982 (minimum 2-week survival rates averaged overthe spring and summer for adults and over the summer for juveniles, sexes pooled)

B.8lA.8l (artificial C.82

(control) removal) (control)

4.828.82 E.82 (natural *

(natural (natural artificialremoval) removal) removal)

Adult survivalSpring

Summer

Juvenile survivalSummer

0.66(4)

0.3(l)

0.5(2t)

0.92(4)

0.8(4)

0.67(24)

1.0(2)

0.66(le)

0.'76(8)

0.73(4)

0.61(17)

0.7(6)

0.37(3)

0.61(2e)

0.9(10)o.'16(5)

0.36(t7)

NorE: Sample size (number of individuals) is given in parentheses.

grids (4, B, E) both years (1981, 1982) regardless of theabsence of meadow voles (Fig. 4). Only a small percentage ofthe total number of captures was recorded in the meadowhabitat. From 20 comparisons (5 grids, 2 habitats), the onlystatistically significant difference appeared in their use of themeadow habitat at B.8l (Gu¿j : 5.50, p < 0.025) (Table 2).Several elements indicate that this difference was not related tothe treatments. (l) The difference occuffed in the grid wherethe removal of voles was least severe. Grids A.82 and B.82 hadalmost no voles present but there was no change in the habitatdistribution of deer mice in these grids. (ii ) The trap stationsused in the meadow habitat at B.8l were located very close tothe forest afea. (iii) The same trap stations or others in the closevicinity were used during the second season (B.82) when therewas no significant difference. (ív) Individuals that used mea-dow trap stations did not remain there. They were caught onlyonce or twice and subsequently were recorded back in theforest. (v) Most of these individuals were juveniles probablyattempting dispersal movements.

Population dynamicsInterspecific interactions may affect not only the spatial dis-

tribution (habitat use) of the species but also their local pop-ulation density. Release from a negative interaction mayresult in higher reproductive rate, higher immigration, lowermortality rate or lower emigration, or a combination of these

parameters. In fact, the populations of Peromysczs remarkablywere similar in both l98l and 1982 (Fig. 5).

NumbersIn general, populations of deer mice in the study area have

a very low density in the spring, from 2 to 16 overwinteredadults per hectare. Adult females have one or two litters. Thefirst litter is born in mid-June and becomes trappable in lateJune or early July, whereas the second litter is born in mid-Julyand joins the trappable population in early August. The popu-lation increases through June and July and reaches its peak of24 to 3O animals/ha in August. Little is known about thedemography in winter, but there is never winter breeding.

During the lst year, deer mouse populations on the control(A.81) and experimental (B.81) grids behaved very similarly.Both started with very low numbers in the spring and increasedto a peak in August, then declined in the fall (Fig. 5). Thepopulation on the removal grid reached a slightly higher peakthan that on the control and declined proportionally.

During the second field season the population of deer miceon B.82 behaved like that in the former year, increasingsteadily through June and July to a peak in early August anddeclining subsequently. On the other hand, on A.82 numbersstayed very stable at an average of 14 per hectare throughoutthe summer (Fig. 5). In spite of the dramatic reduction ofmeadow voles in 1982, both populations of deer mice were

GALINDO AND KREBS 1875

slightly lower in 1982 than 1981.

ReproductionThe demographic machinery might be affected through

changes in reproduction. Table 3 presents a comparison ofthereproductive attributes between deer mice on experimental andcontrol grids.

In early May when trapping began, all overwintered individ-uals had reached sexual maturity and were in breeding condition. Therefore we used the date when juveniles were firstcaught to compare the onset of breeding season on differentgrids. The populations bred synchronously, andjuveniles werefirst caught during early July.

To estimate the end of the breeding season we recorded thelast adult individual that showed signs of breeding condition.For males we recorded the testis in scrotal position and forfemales signs of lactation. The population sizes are too smallto use 507o of the population breeding as a limit as other studieshave done. Most adult males disappeared from the grids duringmid-June to early July; thus the male breeding season was over.There was little overlap between adults males and juveniles.By the time juveniles became trappable, adult males had disap-peared. The breeding season of females extended to late Julyand early August, when they stopped lactating.

By following the breeding condition of individual females,we estimated a minimum number of litters produced. Preg-nancies were determined either by the size and shape of thefemales or by evidence of lactation. All adult females presenthad at least one litter and some had two.

Juvenile recruitment, the number of juveniles tagged forthe first time on a grid, was very similar among grids in l98l.The second surnmer juvenile recruitment was lower evenwhen more adult females were present and more litters wereproduced.

Juvenile productivity, the number of juveniles recruited perpregnant female, was similar on both grids during the first fieldseason. In the second season, production ofjuveniles was lowon the three experimental grids and high on the control. Con-sidering both years, there seems to be a negative intraspecificrelation between juvenile productivity and the number ofbreeding females (Table 3).

In summary, the grids were similar in their reproductiveattributes. They were almost identical during the first summer.The second field season there was more variation but no consis-tent trend. Only juvenile productivity seems to show a consis-tent trend. It was low on the experimental grids. However, thefact that these three grids had the higher number of breedingfemales makes the result unclear.

SurvivalPopulations may be affected through changes in the rate of

disappearance of individuals. Disappearance may be due eitherto mortality or emigration. In the following analysis these twosources are indistinguishable and are included in the survivalrate.

Survival rate of adults was divided into two periods, spring(May and June) and summer (July. August, and Septem-ber),when juveniles were also present. Juvenile survival was notdivided into periods. Table 4 shows minimum 2-week survivalrates averaged for adults and juveniles.

In 1981, survival rates were higher in the experimental grid,for adults both during spring and summer, and for juveniles.During 1982, spring adult survival was slightly higher than in

T,qsI-e 5. Use of trap stations by pairs of species

Grid Species

Fager'sFisher's index of

exact test, p affinity, z

8.83 Peromyscus vs. MicrotusE.83 Peromyscus vs. MicrotusE.83 Peromyscus vs. ClethrionomysG.83 Peromyscus vs. ClethrionomysH.83 Peromyscus vs. Clethrionomys

0.617*0.699*0.4840.632*0.852*

NoTE: In all chses, species use trap stations independently (Fisher's exact probabilitytest). However, Fager's index of affinity shows that in four out of the five compuisons,trap stations re used by both species more often than by either alone. *, significant iflarger thm 0.5 (according to Fager 1957).

the previous year. Summer adult survival was lower on theexperimental grids than on the control, and juvenile survivalwas similar on all grids.

I ntro duction exp e rime nt s

During 1983, two forest grids adjacent to the meadow habitat(B.83, E.83) were colonized by meadow voles, providing anintroduction experiment with both year-to-year controls as wellas contemporaneous controls. Similarly, red-backed voles in-creased from being nearly absent in the previous years. Wecompared the demographic parameters in four grids, two wherered-backed voles and deer mice were about equally abundant(G.83, H.83) and two where red-backed voles were very scarce(no more than two individuals) (C.83, D.83).

Spatial distributionDid the increase in numbers of meadow voles and (or) red-

backed voles influence the distribution of deer mice? Neithermeadow voles nor red-backed voles influenced the spatial dis-tribution of deer mice. The distribution of these species wasindependent on all grids (Table 5). There were no negativeassociations as expected if interspecific interactions were in-fluencing their distribution. Furthermore, Fager's index ofaffinity, which eliminates cell D (both species absent) from thecontingency tables (Fager 1957), showed that voles and deermice tended to use the same trap stations in four out of fivegrids. There were more trap stations used jointly than used byeither species alone.

Population dynamics

NumbersIn two forest grids adjacent to the meadows (B.83, 8.83)

voles (Microtus pennsylvanicus) appeared during mid-Mayand early June 1983. They had been completely absent or invery low numbers in previous years. From very few indi-viduals, they increased throughout the summer to a high peakin the fall, and became more abundant than deer mice. Deermice, in turn, increased as in former years throughout thesummer but did not decline in the fall. At the end of thetrapping program deer mice were 1.5 to 3.5 times higher thanin earlier years (Fig. 6). The colonization by meadow voles didnot affect deer mice populations. This is further confirmed bycomparing deer mice populations within the same year. Thepopulations on grids where the colonization occurred (8.83,E.83) are very similar to those on the controls (C.83, D.83).

In a similar way, red-backed voles (Clethrionomys rutilus)colonized three grids (C.83, D.83, G.83), during early July1983. At grid H.83, they were present from the beginning ofthe trapping program. The firsts two grids (C.83, D.83) never

0.530.090.570. l80.87

t876 cAN. J. ZOOL. VOL. 63, 1985

J1 982

24

20MinimumNumber 16Alive

M¡nimum 16NumberAlive 12

I

4

24

Minimum 20NumberAlive

16

12

8

4

Frc. 7. Changes in minimum number alive of deer mice and red-backed voles in 1983. The populations of deer mice are very similarin the four grids regardless of the number of red-backed voles present.

supported more than two individuals. The third grid (G.83)maintained a medium to low density of 6 individuals (12/ha).The fourth grid (H.83) had a resident population of red-backedvoles that grew parallel to the coexisting deer mouse populationuntil July. Then it maintained an ayerage of I I individuals

JA1 983

through the summer.Deer mouse numbers on these four grids were much the same

regardless ofhow many red-backed voles were present (Fig. 7).

Repro/uctionIf there is a negative interaction between these species, re-

production in deer mice might be affected by the presence ofmeadow voles and (or) red-backed voles in different ways.Deer mice might show a reduction in length of breeding season,number of breeding females, number of litters, litter size, orjuvenile productivity. Table 6 compares the reproductiveattributes measured between control and experimental grids.

The beginning of the breeding season was not documented,since both males and females were already breeding in earlyMay when trapping started. The first juveniles were trappedfrom mid-June to late July. Two of the grids where red-backedvoles were present had late recruitment of juveniles. Malesended breeding synchronously on most grids. Females, on theother hand, were more variable. The end of lactation rangedfrom mid-June to mid-August, with no consistent trend. Thenumber of breeding females, number of litters, and juvenilesrecruited were higher where voles were present. Juvenile pro-ductivity, however, was more variable. The highest produc-tivity was obtained at E.83, where both species of voles werepresent. This grid, however, was also being used for a deermouse female removal experiment where adult females wereremoved after the first litter had been recruited-

SurvivalThe rate of disappearance of individuals might be affected

directly, through behavioral interactions leading to emigration,or indirectly, through increased mortality. Table 7 shows min-imum 2-week survival rates averaged for adults and juveniles.

Adult survival was divided into two periods: spring, when

32

12

24

M¡nimumNumber -^Alive t ¿

MJJASMJJASMJJAS1981 1982 1983

Frc. 6. Changes in minimum number alive of deer mice and meadow voles. The colonization of these two grids by meadow voles had noeffect on deer mice numbers.

20

16

8

4

24

20

9;:::' ;ó

E.83 iJO

. 9/la\ i I,.- il/ -i¡

a.vo o_.j/ ,'oI:/o.;liOa ,.'

^ a\.-.Eo /\ Io

^^^^J -*4

o-o Peromyscus '

o. o MicrotusH Qlslh¡is¡s¡yg

8.82

J-i/ !.l^ \/?/o"i at.',t-.-.rÉ 9^ oo

IB,eg .r

i'.u

9oj/\9/.

o/:1Q iooj '. i/\/aa-o a

.o -''o-¡'o.,6oo .oooci

o-o Peromyscuso-o Microtus B'a 1

,/v. ¡*4t.l t.\

D.a 3

a

a

.'o'o--o--o-..o

./'oal\./I

i¿

/t't.'t'

II

a-aaI

\ oo.ooooMJJAS

a-a Peromyscus G'ag

O..O Cl€thrionoñys

./'\lr't \aa\

l..,rf -,e-o'o"""o-o

MJJA

":"

/\/'

. /t'/-. o

?oo F"q--..oo'

.r'.tEJ.ooo

MJJASM

GALINDO AND KREBS

TnsI-e 6. Deer mouse reproductive data, 1983

t877

IntroductionsControls

c.83 D.83E.83,

M.p.*C.r.G.83, H.83,C.r. C.r.

8.83,M.p.

Juveniles firsttrapped

End of malebreeding season*

End of femalebreeding season*

No. of litters(No. of females)f

No. ofjuvenilesrecruitedt

Juvenile productivity

Jun. 19

Jul. 19

Jun. 19

2 (r)

Jll. 2

Jul. 2l

Aug. 15

2 (r)

l89.0

Jun.30

Jul. l9

Jlun. 23

3 (2)

Jun. 23

Ju.n.23

Jlun.23

3 (2)

3411.3

Jul. 28

Jul. l9

Jul. 9

Jul. 19

Aug. 13 Jul. 9

6 (3) 3 (2\

l36.5

22 18

3.6 6.0237.6

NorE: Mp., Microtus pennsylvanicus, C.r., Clethrionor.trys mtilus.*Last individual breeding.tAdult females caught in one or more trapping sessions.

*Juveniles tagged on the grid.

TABLE 7. Deer mouse survival data, 1983 (minimum 2-week survivalrates averaged over the spring and summer for adults, and over the

suÍlmer for juveniles, sexes are pooled)

IntroductionsControls

c.83 D.83

TABLE 8. Summary of the effects of removal of meadow voles (M¿. )and introduction of meadow and red-backed voles (C.r.) on popu-

lation parameters of deer mice(A) Removals

B.83, 8.83,M.p. M.p.-tC.r.

G.83, H.83,C.r. C.r.

Adult survivalSpring 0.66 0.'79(e) (e)Summer 0.92 0.68

(1) (7)Juvenile survival

Summer 0.91 0.74(2e) (27)

0.82(7)

0.02*(6)

0.79(38)

0.74 0.94(8) (10)0.81 0.91(s) (8)

0.63 0.76(24) (24)

NoTE: M?., Microtus pennsylvanicus; C.r., Clethyrionomys rutilus. Sample size(number of individuals) is given in parentheses.

+[¡w value due to an experimental adult female rcmoval.

only overwintered adults were present, and summer, whenjuveniles had been recruited. Adult survival was very similarboth during spring and summer in all the grids regardless of thepresence of voles. Compared with that in previous years(Tables 4 and 7), spring adult survival was similar whereassummer adult survival was higher in the years when voles werepresent. Juvenile survival, in turn, was slightly lower at thegrids where red-backed voles were present, but higher than informer years when deer mice were alone.

Discussion

Populations of deer mice were not affected by the removal ofmeadow voles from adjacent habitat. Neither the artificial re-moval of Microtus during l98l nor their natural decline innumbers in 1982 influenced deer mouse spatial distribution ordemography. Furthermore, neither the colonization of foresthabitat by meadow voles nor the increase in numbers of red-backed voles during 1983 had negative consequences on thespatial distribution or population attributes of deer mice.

In contrast, populations ofdeer mice seem to perform betterwhen another species is present. During 1982 when the declineof meadow voles occurred, deer mouse numbers were slightlylower. Conversely, in both forest grids colonized by meadow

B.8l 8.82(artificial (naturalremoval) removal)

4.82(natural * 8.82artificial (naturalremoval) removal)

Habitat usePopulation densityReproduction

(uvenileproductivity)

SurvivalAdult

SpringSummer

Juvenile(summer)

++

(B) Introductions

B.83, E.83,M.p. M.p.+C.r.

G.83, H.83,C.r. C.r.

Habitat usePopulation densityReproduction

(uvenileproductivity)

SurvivalAdult

SpringSummer

Juvenile(summer)

0+

0+

+*

NoTE: +, higher thm control; 0, similar to control; -, lower thm control.*No adults present.

voles during 1983, deer mice reached higher numbers than inthe previous year. Similarly, the grid that held the highestdensity of red-backed voles also supported the highest densityof deer mice (Table 8). This suggests that these species mightbe affected by a common environmental factor.

0.54(e)

0.8(1)

0.84(2e)

+0

++

00

++

00

00

00

00

00

0+

+0

0

0

0

1878

The results of this study are in agreement with the suggestionfrom observational studies that competitive interactions be-tween Peromyscus, Clethrionomys, and Microtus have littleinfluence in their habitat use and relative abundance(M'Closkey 1975a, 1975b; M'Closkey and Fieldwick l9'15;Morris 1983; King 1983). On the other hand, the results con-trast with early findings in enclosure experiments (Grant 1969,1970, 19'71, 1972:'Morcis 1969; Monis and Grant 1972) andremoval experiments (Redfield et al. 19'17; Abramsky et al.1979).

Three possibilities may explain the disagreement betweenthese results and other findings. First, competitive interactionsamong species of these three genera may be contingent on a

number ofdifferent factors that change locally. Second, earlierstudies may have interpreted their findings as competitionwhen some other processes were responsible for the results.Third, competitive interactions may affect the populations ofsmall mammals in our study area, but the manipulations and

natural experiments were unable to detect them. We willdiscuss these three possibilities in turn.

First, interactions among species of these genera mightbe contingent on a number of local factors. The degree ofsimilarity among resources utilized (food, habitat, nest sites),population densities in relation to resource availability, theirspecies-specific aggressive behavior (level of tolerance and

specificity) may all influence the relative importance ofcompetition.

Are the species in this community utilizing similar re-sources? In relation to food resources, there is no strong basisto classify these genera as potential competitors, since theirfood habits are very distinct. Deer mice feed mainly on arthro-pods and seeds (Martell and Macaulay l98l); red-backed volesfeed on lichens, fungi, and seeds (Martell 1981); and meadowvoles feed on green parts of grasses and sedges (Banfield1974). If we consider the possibility that their diet varies lo-cally and that food overlap could be greater in the Kluane studyarea, then the colonization of forest habitat by meadow volesor the density increase by red-backed voles should affect thedemography of deer mice, since populations of the last speciesin the area are limited by food supply (Gilbert and Krebs 1981).Nevertheless, as described above, Peromyscus populationswere unaffected or else changed in the opposite direction to thatpredicted by the competition hypothesis.

Another potential resource that could be involved is nestsites. However, little is known about nest site requirements andspecificity by these genera or the availability of this resource.

Most authors who claim that competitive interactions be-tween these genera are important emphasize competition forspace mediated through agonistic interactions (Grant 1972,1978; Hawes 1976; Tumer et al. 1975; Iverson and Turner1972).In this study, however, both colonization of forest byMicrotus and population increase by Clethrionomys took placeduring the breeding season, when the aggressive behavior ofthese species would have had the strongest effect. Never-theless, the spatial distribution of deer mice did not change inthe presence of coexisting species. Studies comparing islandand mainland situations have documented differences in thefrequency of aggressive behavior among populations of thesethree genera (Halpin 1981). If interspecific agonistic inter-actions are a proximate mechanism influencing the distributionof these genera, then such local variations in behavior wouldaffect the intensity of interactions among them.

Douglass (1976) suggested that factors influencing habitat

use and overlap between meadow voles and montane voles maychange from place to place. In areas where the habitats ofthesevoles are similar, behavioral interactions would be likely tooperate, whereas in ardas where the habitats are dissimilar,their distribution would reflect habitat preferences. If we incor-porate the fact that some populations of voles show multiannualfluctuations, then influencing factors would change from timeto time too. During years of low abundance, populations wouldbe restricted to optimal habitats and at peak years a variety ofhabitats would be occupied, making interspecific interactionsmore likely to occur. The strong negative interaction betweenTownsend's voles and deer mice documented by Redfield er al.(1977) may be one extreme of this density gradient, since thesevoles sustain the highest average densities of any Microtus inNorth America (Taitt and Krebs 1985).

The second explanation for the inconsistency of findings isthat other authors might have interpreted their results incor-rectly. Earlier studies that provided support for the importanceof competition, not only among these rodents but in communityecology in general (Grant 1969,19'10,1971; Morris and Grant1972), exhlbit a number of drawbacks. They were carried outin enclosures that were small in relation to the rodents' homeranges. The movements of the individuals introduced wererestricted. The areas were trapped out, and animals from else-where were introduced after spending some time in captivity.Once inside the enclosure they encountered a novel en-vironment and foreign conspecifics. In one case, the species(red-backed vole) introduced was not found in the study siteprevious to its introduction. This may indicate that the habitatwas not suitable in the first place. Since the responses docu-mented are the result of the behavior of the animals, the con-clusions may not represent the natural situation faithfully.Furthermore, one of the experiments had no conúemporarycontrol (Morris and Grant 1912) and none were replicated. Inspite ofall these drawbacks, the conclusions from these studieshave never been questioned and are probably the most widelyquoted evidence for competition among rodents.

In relation to removal experiments carried out in more natu-ral situations, both studies that show a clear negative re-lationship between Microtus and Peromyscus (Rredfield et al.1977; Abramsky et al. 1979) underlined their uncertaiirty aboutthe mechanism of the interaction.

The last possibility is that competitive interactions areimportant in the study area, but these experiments were unableto detect them. If the relative importance of competitionchanges with density, then the densities we found in the areaduring the last 3 years may not have been high enough to causecompetition.

Deer mouse populations in the area change little from yearto year and are limited by food (Gilbert and Krebs 1981); evenwhen densities are low most available habitat is completelyutilized because home ranges are large. There is enough intra-specific pressure for juveniles to leave the bitth place andcolonize the adjacent vacant habitat, but insteadjuveniles dis-perse long distances to other shrubby and forested habitatswithout making use of the closer meadow habitat. We thinkthis is because these two habitats, forest and meadow, do notgradually merge into each other, but the ecotone is sharplydiscontinuous. Deer mice born in the forest would have astrong genetic preference for this habitat, reinforced by earlyexperience (Wecker 1963).

In contrast, meadow voles and red-backed voles are muchmore variable in their numbers. This fact restricts the conclu-

cAN. J. ZOOL. VOL. 63, 1985

sions to the densities at which we found them. If they reachhigher population numbers than those attained in this study,then competitive interactions may have a stronger influence.However, previous studies in the area have found densitiessimilar to those recorded in this study (Krebs and Wingate1976; Gilbert and Krebs 1981).

In spite of the number of studies on habitat use and com-petition among rodents, several areas remain obscure. Underwhich circumstances do interspecific interactions have an in-fluence on populations of these small mammals? What is themagnitude of such influence in relation to the action of otherfactors? When interspecific competition does occur, what arethe mechanisms of interaction? If we are to understand thedynamics of small mammal communities, the early generali-zation that competition for space among different species ofrodents is a widegpread phenomenon (Grant 1972,1978) oughtto be placed among a number of working hypotheses.

Acknowledgements

We thank the Natural Sciences and Engineering ResearchCouncil of Canada, Consejo Nacional de Ciencia y Tecnologiade Mexico, the Arctic Institute of North America, and theDepartment of Indian Affairs and Nofhern Development forfinancial support. We thank Henrick Aspheldt, Stan Boutin,Jean Carey, John Krebs, and Scott Gilbert for their assistanceduring fieldwork.

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GALINDO AND KREBS