Experimental Studies of Competitive Interaction in a Two-Species System

Experimental Studies of Competitive Interaction in a Two-Species SystemAuthor(s): P. R. GrantSource: Journal of Animal Ecology, Vol. 40, No. 2 (Jun., 1971), pp. 323-350Published by: British Ecological SocietyStable URL: http://www.jstor.org/stable/3249 .

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323

EXPERIMENTAL STUDIES OF COMPETITIVE INTERACTION IN A TWO-SPECIES SYSTEM

III. MICROTUS AND PEROMYSCUS SPECIES IN ENCLOSURES

BY P. R. GRANT

Biology Department, McGill University, Montreal, P. Q., Canada

INTRODUCTION

A knowledge of the distribution of Microtus and Clethrionomys species on mainland and islands has given rise to an hypothesis of competitive interaction between species of the two genera (Cameron 1958, 1964; Clough 1964; Corbet 1964; Morris 1969; Ota & Jameson 1961). The hypothesis is that competitive interaction between the species tends to restrict each to its preferred (and different) habitat. The hypothesis has been tested experimentally with North American species, and has been supported by the results of the test (Grant 1969); the woodland species C. gapperi gapperi (Vigors) entered grassland significantly less frequently in an enclosure containing Microtus pennsylvanicus pennsylvanicus (Ord) in the grassland than in another enclosure which had no resident Microtus.

A more critical test can be performed in this two-species two-habitat system by introducing Microtus to grassland which, in the previous absence of Microtus, has been occupied by Clethrionomys. The hypothesis is falsified if Clethrionomys remain distributed in the grassland as previously, and supported if they return to the woodland. Unfortunately this second test could not be performed in the following year because of the almost complete absence of Clethrionomys at Mont St Hilaire, the source area for that species in the first experiment. Instead it was decided to substitute the woodland species Pero- myscus maniculatus gracilis (Wagner) for Clethrionomys gapperi, and to test the hypothesis that competitive interaction between this species and Microtus pennsylvanicus tends to restrict each to its preferred habitat.

It is reasonable to anticipate that Peromyscus would enter grassland and respond to Microtus in a manner similar to that of Clethrionomys. The movement of Peromyscus species into atypical habitat (shrubs, grassland, etc.) has been reported several times, on islands (Cameron 1958; Fall, Jackson & Carpenter 1968; Ozoga & Phillips 1964; Sheppe 1965) and mainland in both natural (Brown 1964; Gentry 1966; McCabe & Blanchard 1950; McCarley 1963) and manipulated situations (Caldwell 1964; Caldwell & Gentry 1965; Sheppe 1967). In almost all instances such movements have been associated with the absence or rarity of those species which usually occupy this habitat.

This paper reports the results of two experiments carried out in successive years and designed to perform the two tests outlined above. The results of experiment 1 determined the nature and design of experiment 2. The results are presented in such a way as to emphasize (a) the reasons for the movement of Peromyscus from woodland to grassland, and (b) the influence of Microtus upon Peromyscus in the grassland.

EXPERIMENTAL DESIGN AND TEST CRITERIA

Three 1-ac (0 4 ha) enclosures were used, each containing half woodland (deciduous)



324 Competition between species of Microtus and Peromyscus

and half grassland (Fig. 1). Peromyscus were introduced to the woodland of each enclosure and Microtus were introduced to the grassland of just one. This arrangement allowed Peromyscus to enter grassland with and without Microtus. The movement of Peromyscus from woodland to grassland was assessed by regular weekly live-trapping in both habitats. The influence of Microtus upon Peromyscus was assessed, indirectly, by comparing the distribution of captures of Peromyscus in enclosures with and without Microtus. The assumption underlying both methods of measurement is that the data obtained from trapping truly reflect the distribution of activity of the animals. Its correctness can be determined only by making, in addition, more direct measures of animal activity (see, e.g. Kikkawa 1964). These were not made in the present study. Two of the most obvious possible trapping biases which could render the assumption invalid are not likely to have operated. These are too few traps for the number of animals present, and tripping mech- anisms of the traps substantially more difficult to release in the traps in one habitat or enclosure than in another (cf. Grant 1970a).

I :E 1 1 23 . 4 .

2

3 .Woodland

4

5

6

7

8 Grassland

9

10

50 Yd

FiG, 1. The enclosures. The broken line indicates the boundary of woodland and grassland. The trapping positions are indicated in enclosure L. In each enclosure there are five trap

columns and ten trap rows.

METHODS AND MATERIALS

The experimental site, method and procedure are described in detail in the preceding paper (Grant 1969) and will be only summarized here. The site is situated at the edge of the Morgan Arboretum of Macdonald College (McGill University) at Ste Anne de Bellevue, Quebec. The walls of the enclosures are metal, 12-18 in. (30-45 cm) below ground and 30-36 in. (75-90 cm) above ground. An electric wire was placed - I in. (2-5 cm) above the outer walls to keep out raccoons (Procyon lotor Linnaeus). Twelve-inch (30 cm) widths of metal window screening were placed continuously against and at right angles to the walls 9-12 in. (22'5-30 cm) below the ground in an attempt to prevent animals from burrowing beneath the walls, and 'aprons' of thick vinyl acetate sheet were nailed about 6 ft (I 80 cm)



P. R. GRANT 325

above ground to the trunks of those trees close to the walls to prevent Peromyscus from escaping by trees. This plastic is smooth and, in such a position, impossible for the mice to cross.

Animals to be used in the experiments were trapped at the McGill University Field Station at Mont St Hilaire, Quebec. The choice of Peromyscus individuals was made with care. Wrigley (1969) has found in this area that animals trapped at the edge of the woodland, close to an orchard, often resemble the phenotype of P. leucopus more than P. maniculatus. The former species is occasionally found in the grassy edges of woodland in western Quebec. Therefore, only those Peromyscus trapped at least a mile from the edge of the woodland, and exhibiting a P. maniculatus phenotype (Peterson 1966), were used. All animals were toe-clipped with individual codes.

Details of experiment I now follow, and those methods specific to experiment 2 are presented later (p. 335). Experiment 1, designed to perform the first test, was started on 10 July 1967 with the introduction of three pairs of Peromyscus to the woodland of each of the three enclosures, and four pairs of Microtus to the grassland of enclosure II. These initial densities are similar to those under natural conditions at that time of year. Just prior to week 6, two adult male and one adult female Peromyscus were added to the woodland of each enclosure, numbers present having declined up to this point. In an attempt to perform the second test, four pairs of new adult Microtus were introduced to the grassland of enclosures III just prior to week 1 1. In weeks 11 and 12 all Microtus were removed from enclosure II. These manipulations are summarized in Table 1. Experiment 1 was concluded at week 16 (end of October) and the animals were allowed to remain in the enclosures.

Table 1. The animals used in Experiment 1; indicated also are the addition (+) and removal (-) of animals

Enclosures

I II III Start 6 Peromyscus 6 Peromyscus 6 Peromyscus

8 Microtus Week 6 + 3 Peromyscus + 3 Peromyscus + 3 Peromyscus Week 11 }-All Microtus +8 Microtus Week 12f Week 16 End End End

To determine animal numbers and distribution the procedure was to trap for three consecutive nights each week, using Longworth live-traps supplied with food and nest material and distributed in a regular grid pattern throughout the enclosure (partly illustrated in Fig. 1). Traps were set in the late afternoon and checked early the following morning. Animals trapped were identified and released, and their trapping positions recorded. Traps in the grassland were disassembled at this time to prevent animals being captured and held in the heat of the day. Water-repelling terylene fiberfill (Radvanyi 1964) was substituted for the paper as nest material in cold weather (October). Twenty- five supplementary traps, five per original trap row, were used to aid the removal of Microtus from the grassland of enclosure II. Another twenty-five supplementary traps were used in the grassland of enclosure III, when both species were present there, to avoid the possibility of all traps visited by Peromyscus being occupied by Microtus.




There was no evidence of Microtus leaving or entering the enclosures from outside, or moving from one enclosure to another, either in experiment 1 or in experiment 2, but five adult Peromyscus were known to have escaped to the outside in experiment 1 because they were trapped there (and replaced inside). As the experimental animals (from Mont St Hilaire) could be distinguished from local animals by the colour of the hairs on the tarsus, it is known that strange Peromyscus did not enter the enclosures from the outside. Several Peromyscus moved from one enclosure to another and were trapped in the 'wrong' enclosure; these were replaced in the correct one. The only other small mammal species encountered in the enclosures in the two experiments was Sorex cinereus: four were trapped in experiment 1, two were trapped in experiment 2, and all these were removed.

EXPERIMENT 1: RESULTS

Demographic features (1) Microtus

(a) Recruitment. By recruitment is meant the addition of young to the trappable population. The first young were trapped in week 8, and by the end of week 10 a total of ten young had been trapped. Removal of animals from enclosure II started in week 11. All eight original adults and eleven young were removed on the first day, and by the end of week 12 the last of twenty-seven young had been trapped and removed. The eight Microtus introduced to enclosure III just prior to week 11 did not breed there.

(b) Losses. An adult male was found dead in a trap on the first day of trapping in week 1 and was replaced by another male. Eleven weeks later, at the time of removal, all eight were present. All ten young recruited in weeks 8, 9 and 10 were captured and removed in week 11. Therefore survival had been complete.

Of the eight adults placed in enclosure III, two were not captured and two appeared only once; one of the latter was found dead in a disassembled trap the next day. Since they constituted 50 % of the starting population these four animals were replaced in week 12 by four young animals from enclosure II. Thereafter two animals were found dead in traps at the end of week 13, and were not replaced, and one was last trapped in that week. The remaining five survived to the end of week 16.

(c) Daily numbers. An integration -of the estimates of the time when individuals entered the population and when they left gives daily estimates of the numbers composing the population. Entries and departures were estimated on the basis of first and last dates of capture. The numbers in enclosure II varied from eight at the start of the experiment to 19 at the beginning of removal (Fig. 2). The numbers in enclosure III varied from four to eight.

(2) Peromyscus (a) Recruitment. The pattern of recruitment varied among the enclosures. In enclosure

III it began at week 5, in enclosure I at week 6 and enclosure II at week 8. As new young were captured in the enclosure I and II populations in the last 2 weeks of the experiment, it is quite likely that recruitment had not ceased at the close of the experiment. This is reinforced by the fact that three females first captured in week 6 in enclosure I were all pregnant in week 10, yet only one new young animal was trapped in that enclosure in the last two weeks of the experiment. Others may have been trapped if the experiment had been prolonged. The numbers of young recruited to the three populations were 7 (I), 9 (II) and 15 (III), comprising a minimum of two, two and three litters respectively.



P. R. GRANT 327

(b) Losses. No animals died in traps. Nevertheless the persistence of animals (i.e. remaining alive in the enclosures) was poor from the start, necessitating the addition of animals prior to week 6 as explained in the section on Methods. Of the eighteen original adults, only two, both of enclosure II, persisted to the end of the experiment. Of the

20

151 . *1

- o VI E 10 v~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~ z _ _ _ _ _ - . 1 '7'

5 _

11 18 25 1 8 15 22 29 5 12 19 26 3 10 17 24 31

July August September October

FIG. 2. The numbers of Microtus. The arrow indicates the addition of four animals in

replacement of four dead.

12 x

lo *\ il n, I l o r 10 1 X @-"~

X- I '\ 8 0x- --

-0 6 x_

4 t i9jJ- 2

.. 1 ." _...

11 18 25 1 8 15 22 29 5 12 19 26 3 10 17 24 31

July August September October

FIG. 3. The numbers of Peromyscus. The arrow indicates the time at which additional adults were introduced.

nine animals added after week 5, again only two were present at the end. Persistence of the young was considerably better. Only one young from each of enclosures I and II was estimated to have left the populations before the end of week 16. However, nine of the enclosure III recruits were estimated to have left by this time.



ot' 00

Table 2. Total number of Peromyscus captures per week (Microtus were present in enclosure II up to and including week 12, and in enclosure IIIfrom week 11 onwards)

Enclosures

I III III Totals m

8 A, l / ,~~- , X5

Week Woodland Grassland Woodland Grassland Woodland Grassland Woodland Grassland Grand totals 1 10 0 8 0 12 0 30 0 30 2 5 0 8 0 3 0 16 0 16 3 8 0 6 0 9 1 23 1 24 4 10 0 3 0 9 0 22 0 22 5 8 0 9 0 8 1 25 1 26 6 6 0 6 0 19 0 31 0 31 7 12 0 12 0 12 2 36 2 38 8 12 3 12 0 14 2 38 5 43 0 9 21 3 12 1 12 7 45 11 56

10 18 3 7 1 9 5 34 9 43 11 17 4 9 1 7 4 33 9 42 12 13 5 12 1 6 4 31 10 41 13 18 3 7 3 5 7 30 13 43 14 5 9 8 5 3 6 16 20 36 o 15 5 11 4 9 2 10 11 30 41 16 8 10 5 10 6 10 19 30 49



P. R. GRANT 329

Losses from the populations definitely involved escapes from the enclosures. Five animals, all adults, were trapped on the outside of the enclosures on several occasions, and were then replaced inside. Rarely did this result in the animals staying inside. The only recruit known to have escaped (from enclosure III) was found dead on the outside close to enclosure I, where it had probably been killed by a raccoon.

(c) Daily numbers. The daily numbers varied from two to eleven in enclosure I, four to eleven in enclosure II and two to twelve in enclosure III (Fig. 3). The ranges of variation are therefore similar, but the pattern of variation among the three enclosures differs, according principally to the time at which recruitment took place. A consistent feature is a loss of one or more animals within a few days of each recruitment. Nevertheless, all three enclosures had more animals at the end of the experiment than at the start.

12

10 > I'tXO

E ~~~~~~~~~~~$x

8 /// /N

/*\ ~ ~ ~ * ,9/i / / xxx x

z 4

//

0 2 4 6 8 10 12 14 16

Wee ks FIG. 4. The weekly occurrence of Peromyscus in the grassland. The arrows indicate the times at which adult Peromyscus were added and Microtus were transferred to enclosure

III, respectively.

The distribution of animals within their unusual habitat

(1) Microtus: occurrence in the woodland Only once was an animal trapped in the woodland; immediately after animals were put

into enclosure III, a male was trapped in row 5 and thereafter was never trapped again.

(2) Peromyscus: occurrence in the grassland (a) The temporal distribution of animals in the grassland, and the influence of Microtus.

The weekly trapping data are shown in detail in Table 2 and graphically in Fig. 4. Up to the end of week 5 only two animals had entered the grassland, both in enclosure III and in different weeks. In week 6, immediately following the addition of adults, no animals were trapped in the grassland. However, from week 7 onwards animals were trapped each week in the grassland of III, from week 8 onwards in the grassland of I and from week 9 onwards in the grassland of II. In each enclosure grassland trapping records rose more or less gradually to a maximum; but in the last 2-4 weeks they rose somewhat sharply, and there occurred a concomitant decline in woodland records (Table 2).




If we ignore weekly records of one grassland occurrence only per enclosure, then we find that in enclosures I and III animals start being trapped in the grassland approximately 2 weeks after initial recruitment to each of the populations (i.e. 2 weeks after the first young were captured). Regular weekly records of one occurrence in the grassland of enclosure II start 1 week after initial recruitment in that enclosure. This relationship suggests that the introduction of new adults, which occurred before initial recruitment, had little to do with the onset of grassland exploration. Movement between enclosures, in itself, probably had little influence on exploration of the grassland also; it occurred principally from wxeeks 3 to 8, involved the original adults of enclosure II almost entirely, and was nearly completely restricted to the woodland habitat (Table 3).

Initially Microtus were present in the grassland of enclosure II. Peromyscus started to enter the grassland of this enclosure later than in the other enclosures, apparently because recruitment occurred last in this enclosure. But, in addition, the frequency of occurrence of Peromyscus in the grassland of enclosure II was unusually low once the movements had started (Fig. 4). This can be attributed to the presence of Microtus.

Table 3. Number of captures of Peromyscus in the three enclosures

Enclosures

I II InI A. Enclosure I animals in Woodland 144 1 1

Grassland 50 1 0 B. Enclosure II animals in Woodland 22 127 28

Grassland 1 29 1 C. Enclosure III animals in Woodland 0 3 113

Grassland 0 0 60

The difference between the occurrence of Peromyscus in the grassland of enclosure II and in the grassland of the other two enclosures is calculated as follows. First, the total number of Peromyscus captures in the grassland of enclosure II is determined from the week after initial recruitment to the week in which the last Microtus were removed from enclosure II. Four captures of Peromyscus were made in the grassland in these 4 weeks (9-12). The figure of four captures is now compared with the number of captures in the grassland of the other two enclosures during the 4 weeks following initial Peromyscus recruitment in those enclosures. The captures number nine in enclosure I grassland (weeks 7-10) and eleven in enclosure III grassland (weeks 6-9). Thus, for these comparable time periods, the frequency of occurrence of Peromyscus in the grassland of enclosure II is one half to one third what it is in the other enclosures. All these values are small, but the reality of the differences between enclosures is apparent when we consider them in relation to the cumulative number of Peromyscus individuals (i.e. number of individuals x trapping nights) in the three enclosure populations; during those 4 weeks the cumulative number of individuals was higher in the enclosure II population than in the other two. In other words there were generally more Peromyscus present, and available to enter the grassland, in the enclosure II population than in the other two populations. However, the number of captures in grassland expressed as a proportion of the number of captures in the enclosure as a whole is small in each case, and there are no significant differences between enclosures.

The complete removal of Microtus from enclosure II by week 13 coincided with a sharp



P. R. GRANT 331

increase in the frequency of captures of Peromyscus in the grassland there, and from then on the frequency of occurrence continued to increase until the end of the experiment (Fig. 4). This further suggests that Microtus had acted as a deterrent to Peromyscus in the grassland.

The introduction of Microtus to the grassland of enclosure III did not have the effect of restricting Peromyscus to the woodland or of increasing the frequency of capture of Peromyscus in the woodland (Table 2). However, until the end of week 13, when the Microtus numbers dropped sharply from eight to five, the Peromyscus were restricted to trap rows 6 and 7 (the presence of supplementary traps makes a trapping bias extremely unlikely). After week 13, Peromyscus were trapped in rows 8 and 9 once more. This suggests that interactions between the species might have occurred, resulting in partial restriction of Peromyscus activity in the grassland. The data are now analysed by x2, and it is found that the distribution of Peromyscus in the grassland by trap rows when the Microtus population numbered eight differs significantly from that when Microtus numbered five (P < 0 05) and from that in the three weeks preceding the introduction of Microtus (P <0.05). The direction of the difference is the same in the two analyses; trap rows 8, 9 and 10 are under-represented with Peromyscus captures when eight Microtus were present. No such change in distribution of Peromyscus captures occurred in the grassland of enclosure I, which lacked Microtus at all times.

The relationship between movement of Peromyscus into the grassland and population (Peromyscus) and habitat features is now examined by multiple linear regression analysis. The number of weekly occurrences in the grassland of each enclosure (Y) is regressed on the mean number of original adults (XI), added adults (X2) and recruits (X3), of each enclosure population, the mean number of total animals in the three enclosures com- bined (X4) and an index of the woodland habitat (X5). To obtain values for the habitat index, weekly estimates were made of the quantity of fallen leaves accumulated on the ground in the three enclosures and these were transcribed to a uniform interval scale of 0.0 (0-5 % of leaves fallen) to I 0 (> 95 % of leaves fallen). The regression equations are:

YI = 3419+9-55 (X5-0O72) (1)

YI= 1P94+ 8 04 (X5- 072) (2)

fill = 3 69+0 40 (X3-8.67) (3)

Occurrences in the grassland are correlated with the habitat index (X5) in enclosures I and II, but with the number of recruits (X3) in enclosure III. The coefficients of determination are large in each case. Thus percentage contribution values are 86 30 00 for enclosure I, 83-36 00 for enclosure II and 81 900% for enclosure III.

Tracks and faeces were found on the snow in the grassland of each enclosure on 26 December, which shows that use of this habitat persisted well into the winter. However, only two animals were trapped in the following spring, in the woodland of enclosures I and Il.

(b) Contributions of adults and recruits to the movements into the grassland. Original adults, added adults and recruits entered the grassland to a different extent, and differ- ently in the three enclosures. Tables 4, 5 and 6 portray the data. For all three enclosures it may be said that few of the original adults took part in the movements into the grassland. On the other hand almost all the recruits did, with added adults being intermediate (Table 4 and 5).

X2 tests are now applied to the data in Table 6. No significant differences exist among the original adults of the three enclosures. Added adults occurred in the grassland of




enclosures I and II proportionally more frequently than did original adults of those enclosures (P<0 001), but for enclosure II P>01. Recruits occurred in the grassland

Table 4. Number of Peromyscus individuals recorded in the grassland habitat

Original adults Added adults Recruits Total A. Enclosure I animals in I 0 0 7 7

II 0 0 1 0 III 0 0 0 0

Total, as a fraction of those available 0/6 0/3 7/7 7/16

B. Enclosure II animals in I 0 0 1 1 II 1 0 9 10

III 0 1 0 1 Total, as a fraction of those available 1/6 1/3 9/9 11/18

C. Enclosure III animals in I 0 1 0 1 II 0 1 0 1

III 1 2 13 16 Total, as a fraction of those available 1/6 3/3 13/15 17/24

Table 5. Numbers of Peromyscus individuals captured most frequently in woodland or grassland; half values indicate that an individual was captured

with equalfrequency in woodland and grassland

Enclosures

I II III Total Original adults Woodland 6 6 2 18

Grassland 0 0 0 0 Added adults Woodland 4 3 2 9

Grassland 0 0 0 0 Recruits Woodland 6 5 2 7 15-5

Grassland 2-5 5 8 15-5 All animals Woodland 16 5 11 15 42-5

Grassland 2 5 5 8 15-5

Table 6. Number of captures of the three categories of Peromyscus in the three enclosures

Enclosures

I II III Totals Original adults Woodland 57 78 62 197


Grassland 9 1 33 43 Recruits Woodland 77 27 33 137

Grassland 39 27 27 93 All animals Woodland 169 131 141 441

Grassland 48 30 60 138

more frequently than did original adults in each enclosure (P< 0001 in each case), and more than did added adults in enclosures I (P<0 001) and II (P<0 001, but not III



P. R. GRANT 333

(P>01). When living contemporaneously, recruits occurred in the grassland of each enclosure more frequently than did original adults (P <0 001) or added adults (P < 01), and added adults did so more frequently than original adults (P< 0001).

Added adults occurred in the grassland more frequently in enclosure III than in I (P<0 001), and more frequently in I than in II (P<0 001). Recruits occurred in the grassland of enclosures II and III with approximately equal frequency, but relatively less frequently in enclosure I (P<0001). These differences can be at least partly related to differences in sequence of events in the three enclosures. For instance, the original adults were present mainly in the first one-third of the experiment, the added adults in the middle third and the recruits mainly in the last third. Furthermore the original adults, which rarely entered the grassland (Table 6), did not persist equally in the three enclosures, but longest in II and shortest in III. In reciprocal fashion the added adults, which did enter the grassland frequently, persisted longest in III and shortest in II. Persistence of original and added adults in I was intermediate. The cumulative totals of added adults available in the three enclosures show the effects of persistence better: 42 (II), 66 (I), 81 (111). The cumulative totals trapped in the grassland parallel this sequence, although the rate of progression is quite different: 1 (II), 9 (1), 33 (III). Thus the original adults, in apparently affecting the persistence of added adults, influenced the amount of movement of the latter into the grassland, and hence may have been partly responsible for the difference between enclosures.

50

,40 x o x 4-

30 0 \ (

1 20 3 4 5 6

0 ~~~- E R0 '10 z X

1 2 3 4 5 6 7 8 9 10 Trap Rows

Woodland Grassland

FIG. 5. The distribution by trap rows of Peromyscus trapping records.

The difference in movements between the recruits of enclosures II and III on the one hand and enclosure I on the other is related to the time recruitment took place and to persistence of the recruits. Persistence was equal in enclosures I and II, but recruitment began much earlier in I than in II, when movements into the grassland were on a small scale, hence records in the grassland of enclosure I are relatively under-represented. In enclosure III recruitment occurred earliest, but persistence of recruits was poorest, and the majority of the recruits were produced late in the experiment as in enclosure II but not in enclosure I (Fig. 3).

(c) The spatial distribution of animals in the grassland. The trapping records were distributed in a significantly aggregated fashion in all three enclosures, with a minimum




Coefficient of Dispersion s2/g of 3-06 in enclosure II. Departures from an expected uniform distribution in trap rows were significant in all three enclosures (P< 0-05). The over- represented rows were 7 (I), 6 and 7 (II) and 6 (III), closest to the habitat interface, and the under-represented rows were 10 (I), 8 and 9 (II) and 9 and 10 (III), furthest from the interface (see also Fig. 5).

CONCLUSIONS

Peromyscus entered the grassland in all three enclosures, thereby providing the necessary conditions for the performance of the first test of the competition hypothesis. Conforming to the expectation of the hypothesis, Peromyscus were trapped less frequently in the grassland of one enclosure (II) which had a Microtus population than in the other two which did not, although the differences were not statistically significant. After Microtus had been completely removed from the grassland of enclosure II the frequency of capture of Peromyscus there increased markedly. In contrast, the frequency of capture of Pero- myscus in the grassland of enclosure I, which lacked Microtus throughout the experiment, did not increase at this time. This result is also in agreement with the hypothesis. It cannot be accounted for solely by changes in the structure of the woodland, with which the weekly number of occurrences of Peromyscus in the grassland of enclosures I and II were significantly correlated, because leaf-fall progressed at the same rate in the two enclosures. Furthermore, in the previous experiment with Clethrionomys, Microtus were not removed from the grassland of enclosure IT, and the occurrence there of Clethrionomys remained at a low frequency throughout that experiment.

The results of the second test also support the hypothesis. Microtus were introduced to the grassland of enclosure III where Peromyscus had been occurring frequently. Although Peromyscus did not return to and remain in the woodland, captures of this species in the grassland were significantly restricted to the area closest to the woodland, at least while the Microtus population numbered eight. No such restriction was evident in enclosure I without Microtus.

The experiment also provides evidence that movement of Peromyscus into grassland is influenced by both population and habitat features.* The weekly number of Peromyscus captures in the grassland was correlated with an index of the woodland habitat in two enclosures and with the number of recruits in the other enclosure. The importance of recruits is further indicated by (a) the high proportion of recruits captured at least once in the grassland, (b) the high proportion of recruits captured more frequently in the grassland than in the woodland, and (c) the high total number of captures of recruits in the grassland. However, it is not easy to distinguish between the relative contribution of population and habitat features to the movements because first recruitment occurred only shortly before the onset of leaf-fall in the woodland.

The correlation with the leaf-fall index is probably not spurious. After leaf-fall started the behaviour of Peromyscus when released from a trap was observed to change. Animals no longer ran away immediately, but walked carefully over the leaves until they reached a log or fallen branch, whereu pon they ran. Since movement, particularly running, over recently fallen leaves is noisy, these observations suggest that animals might attract the

* Movement of Peromyscus into the grassland is not a simple consequence of confining the animals in enclosures. In September 1970, nearly a year after the enclosure walls in the grassland had been taken down, two animals were captured in the now unenclosed grassland in trap rows 10 ('enclosure' I) and 7 ('enclosure' II). Trapping was conducted on only six nights. The animals were born probably no later than July.



P. R. GRANT 335

attention of predators when moving over the litter more at this time of year than earlier. In this way the woodland appears to be less suitable for Peromyscus at the time of leaf- fall than before; there may be other ways in which it is less suitable, e.g. easier detection of Peromyscus by bird predators due to greater visibility in the woodland, etc.

EXPERIMENT 2

Introduction

The results of experiment 1 constitute evidence that Microtus deter Peromyscus from using the grassland, and that the degree of influence of Microtus upon Peromyscus is a function of Microtus density. Therefore it is to be expected that Microtus, at a density considerably greater than those prevailing in experiment 1, would entirely restrict the movements of Peromyscus to the woodland. Experiment 2 was designed to test this prediction by first allowing Peromyscus to establish regular movements into a Microtus- free grassland, and by then introducing Microtus there at high density.

Experiment 2 was begun in the next year 5 weeks earlier than experiment 1. This was done to gain additional information on the influence of habitat changes (leaf-fall) and population changes (recruitment) upon movement of Peromyscus into the grassland. It was hoped that, by starting experiment 2 early, recruitment would be brought forward distinctly more in advance of leaf-fall than was the case in experiment 1. The data presented in the Results are pertinent to both the movement of Peromyscus into the grassland and the influence of Microtus upon Peromyscus.

Table 7. The animals used in experiment 2; indicated also are the addition (?) and removal (-) of animals

Enclosures

I II III Start 4 Peromyscus 4 Peromyscus 4 Peromyscus

8 Microtus Week 4 -8 Microtus + 8 Microtus Week 5 + 4 Peromyscus + 2 Peromyscus + 6 Peromnyscus Week 8 + 5 Microtus Week 14 +25 Microtus -All Microtus Week 21 End End End

METHODS

All animals from experiment 1 were removed and experiment 2 was started on 4 June 1968 with the introduction of two pairs of Peromyscus to the woodland of each of the three enclosures. The choice of which enclosure to use for the introduction of Microtus at high density had to be delayed until it was known which grassland(s) Peromyscus entered with high frequency. In the meantime a Microtus population was allowed to increase from four pairs introduced to the grassland of enclosure I at the start of the experiment.

Manipulations of the populations of the two species are summarized in Table 7. The initial rate of loss of Peromyscus due to death or escape was high, and to compensate for it additional pairs were added to enclosures I (2 pairs), II (1 pair) and III (3 pairs), immediately prior to week 5. From early on it was apparent that Peromyscus were avoiding enclosure III because the animals introduced there were captured more frequently in enclosure IT, and since the first object of the experiment was to get Peromyscus




to enter the grassland, the Microtus were transferred from enclosure I to enclosure III prior to week 4. The population of Microtus in enclosure III was reduced to three on 9 July (week 6) when a raccoon entered the enclosure early in the evening, perhaps before the electric fence was switched on, so five more Microtus were added to enclosure III to make the total eight. The final manipulation was made just prior to week 14, when all Microtus in enclosure III (eight adults and four recruits) were trapped and put into the grassland of enclosure II, together with an additional six males and seven females. This was done to see if the Peromyscus, which had been occurring regularly in the grassland of enclosure II, would be prevented by the Microtus from doing so further. When the Microtus were transferred twenty-five supplementary traps were added to the grassland of enclosure II so that there would be many more traps than animals.

The same trapping procedure was adopted as in experiment 1, and the experiment was concluded at week 21 (late October). As in experiment 1 Microtus did not move from

25 * _ _

20

15

1: \.; 1

E) 10.- .

S 12 19 26 3 10 17 24 31 7 14 21 28 4 11 18 25 2 9 16 23 30

June July August September October

FIG. 6. The numbers of Microtus. The arrows indicate the times at which animals were transferred from enclosure I to II, when animals were added to replace those killed by a

raccoon and when animals were transferred from enclosure III to Il.

one enclosure to another, whereas Peromyscus did. In recognition of the impossibility of constraining the Peromyscus, no attempt was made to return them from a new to their original enclosure. Therefore the Peromyscus in the three enclosures are considered to constitute not three populations but one.

RESULTS

Demographic features (1) Microtus

(a) Recruitment. Owing partly to the transpositions of the population and partly to raccoon predation on one occasion, several litters did not develop sufficiently to add recruits to the population. The only recruitment occurred just prior to and in week 14, when a litter of seven made their appearance. The four recruits trapped just prior to week 14, together with the adults, were placed in enclosure II at this time, while the remaining three recruits were removed in week 14. Litters were born after the animals were placed in enclosure II, but this did not result in recruitment before the end of the experiment.



P. R. GRANT 337

(b) Losses. Animals did not survive as well as in the previous experiments, even after allowance is made for the predation. A steady decline in numbers occurred after the trans- fer to enclosure II (Fig. 6). Several animals died in the traps, and on one occasion (5 October) four animals died in traps during one night. None of these was replaced. Two of the recruits died during the experiment. Only one of the original adults survived throughout.

(c) Daily numbers. The pattern of temporal variation in numbers is illustrated in Fig. 6. The decline in numbers in enclosure II is well shown, but the recruitment in enclosure III is not shown because it occurred at the time animals were removed from this enclosure.

(2) Peromyscus (a) Recruitment. This occurred at sufficiently discrete times to permit an estimate to

be made of the number and size of the litters. The first litter, of six animals, to appear as

25 l V

20

L. 15 4)15 1X.._!ll-. -o E .

Z 10 I

5

5 12 19 26 3 10 17 24 31 7 14 21 28 4 11 18 25 2 9 16 23 30

June July August September October

FIG. 7. The numbers of Peromyscus. The arrow indicates the time at which additional adults were introduced.

recruits did so in week 10 in enclosure II. Thereafter litters of four (week 11), seven (week 13) and seven (week 14) entered the population. None of the female recruits became pregnant. In this feature and in the early termination of breeding the experiment differed from the last one.

Almost all of the recruits were trapped first in enclosure II; two of the litter of four were trapped first in enclosure I. The mothers of all litters were trapped most frequently in enclosure II, with the exception of the mother of the litter of four, which was nevertheless trapped frequently in enclosure II. This strongly suggests that three, and possibly all four, litters were born and raised in enclosure II.

(b) Losses. Despite the fact that the starting density was lower in this experiment than in the previous one, the total numbers dropped rapidly to seven, necessitating the addition of more animals just prior to week 5 (Fig. 7). The initial rate of loss of added adults was even greater than that of original adults, but after week 6 both groups declined more slowly. No animal of either group persisted to the end of the experiment. The last added adult disappeared before the last original adult. Persistence of the recruits was poor, if anything worse than that of original and added adults. By the end of the experi-



00

Table 8. Total number of Peromyscus captures per week

Enclosures

I II III Totals A - ,- - - - - - - A ,- -, , -A ,

Period* Week Woodland Grassland Woodland Grassland Woodland Grassland Woodland Grassland Grand total

A 1 8 0 11 0 8 0 27 0 27 ;> 2 6 0 8 0 0 0 14 0 14 3 3 0 10 0 0 0 13 0 13 4 5 0 13 0 0 0 18 0 18

B 5 12 0 19 0 6 1 37 1 38 6 13 0 13 1 2 0 28 1 29 7 16 0 9 1 2 0 27 1 28 8 11 0 9 2 4 0 24 2 26 9 12 1 15 0 0 0 27 1 28

10 10 0 16 7 1 0 27 7 34 11 11 1 14 8 3 0 28 9 37 12 7 1 16 7 2 0 25 8 33 C 13 11 2 12 7 4 0 27 9 36

C 14 10 1 11 3 1 0 22 4 26 15 7 3 19 3 3 0 29 6 35 16 7 1 19 0 4 0 30 1 31 17 4 1 9 0 6 0 19 1 20 18 2 1 7 0 1 2 10 3 13 19 0 0 8 0 0 1 8 1 9 20 0 1 5 0 0 1 5 2 7 21 0 2 1 4 0 1 1 7 8

*A, Microtus in enclosure I; B, Microtus in enclosure III; C, Microtus in enclosure II.



P. R. GRANT 339

ment no animal from the first two litters was present, and only three and two of the last two were present.

Losses from the population definitely included escapes from the enclosures. No attempt was made to capture and replace the escapees inside the enclosures as this procedure did not result in the animals staying inside in experiment 1. Furthermore disturbance of traps by raccoons made trapping outside the enclosures precarious.

(c) Daily numbers. These varied from six to twenty-two (Fig. 7). The maximum is lower than in experiment 1.

The distribution of animals within their unusual habitat

(1) Microtus: occurrence in the woodland In this experiment, as in the previous two, an individual Microtus was trapped in the

12

10

8 (A ~~~~~~~~0 0-

s 6 o/\oo

z 4 o

0-Z I 2 / \

7\ N /O 0 1 . O -. O -

\.. 0 /

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20-21

Weeks

FIG. 8. The weekly occurrence of Peromyscus in the grassland of enclosures I and II. The arrow indicates the time at which Microtus were placed in the grassland of enclosure IL

woodland once. Immediately after animals were put into enclosure II a new female was trapped once in row 3; thereafter, until the end of the experiment, it was trapped in the grassland.

(2) Peromyscus: occurrence in the grassland (a) The temporal distribution of animals in the grassland, and the influence of Microtus.

The weekly trapping data are shown in detail in Table 8 and graphically in Fig. 8. No animals were trapped in the grassland in the first 4 weeks. Adults were then added to the woodland of each enclosure before the fifth week. From weeks 5 to 9 inclusive one or two captures in the grassland were made each week, all three enclosures being involved; all but two of the animals were added adults. For the next 4 weeks (10-13) the frequency of occurrence in the grassland of enclosure II was consistently high. The increase in frequency coincided with recruitment in this enclosure. Microtus were then placed in the grassland of enclosure II before week 14, and there occurred a concomitant drop in Peromyscus records there. After week 15 no Peromyscus were trapped in the grassland of enclosure II until the last week of the experiment.




In the 4 weeks following recruitment, and prior to the introduction of Microtus (weeks 10-13), Peromyscus were recorded in the grassland of enclosure II twenty-nine times. In the first 4 weeks following the introduction of Microtus (weeks 14-17), Peromyscus were recorded there only six times. This is a highly significant drop (P<0 001). Signi- ficance would be even greater if allowance was made for the fact that frequency of occurrence in the grassland should be increasing at this time (see Fig. 9). The drop cannot be explained by a decline in numbers of Peromyscus available in enclosure II during the latter 4 weeks because there were more available, on average, than in the preceding 4 weeks. In the same period of 8 weeks no Peromyscus were recorded in the grassland of enclosure III. In the grassland of enclosure I there was a slight, but not significant (P >0' 1), increase in Peromyscus records in the latter 4 weeks-certainly no decrease

12

, vx 10 1

l 8 0

B U' ~~ ~~~~~~0 0-0/

E Z

4 0

2 0 A0

o 0.-OV-0.-0. -0.- *---OO_

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21

Weeks

FIG. 9. A comparison of the weekly occurrence of Peromyscus in the grassland under three conditions: A, No Peromyscus recruitment, no Microtus present (1,1968); B, Peromyscus recruitment, no Microtus present (1,1967); C, Peromyscus recruitment, Microtus present

after time indicated by the arrow (11,1968).

running parallel to that in enclosure It. It thus seems clear that the decline in frequency of occurrence of Peromyscus in the grassland of enclosure II is due to the manipulated variable, the Microtus population.

The reappearance of Peromyscus in the grassland of enclosure II in the last week coincided with a drop in Microtus numbers to seven. This is about the same level of density (i.e. eight) at which, in enclosure III in experiment 1, Peromyscus movements into the grassland were restricted but not entirely inhibited. This supports the view that the density of Microtus influences the density of Peromyscus in the grassland. However, the change in suitability of the woodland at this time might also be expected to produce an increase in the movements of Peromyscus into the grassland. Therefore either one or both factors may have been responsible for the observed increase.

In experiment 1, the first week in which Peromyscus were recorded in the grassland of an enclosure three or more times was week 8, whereas in the present experiment it was week 10 (Fig. 8). But the present experiment was begun 5 weeks earlier in the summer, so regular movement into the grassland occurred 3 weeks earlier than in experiment 1. In both experiments the onset of regular movements was associated with initial recruit-



P. R. GRANT 341

ment. In experiment 1 there was a lag period, in experiment 2 there was not, perhaps because a larger number of young entered the trappable population simultaneously in experiment 2 than in experiment 1.

The relationship between frequency of occurrence in the grassland and population and habitat features is now examined by multiple linear regression analysis. The number of weekly occurrences in the grassland of each enclosure (Y) is regressed on the weekly mean number of all original adults (X1), added adults (X2), recruits (X3), total animals (X4) and an index of the woodland habitat (X5). The regression equations are:

?I = 0 7+0-12 (X3-4X81) (4)

l = 2 6+0-59 (X3-2*52) (5)

-ill = 0 3 + 1P18 (X5-O081) (6) In enclosures I and II the frequencies of occurrence in the grassland are correlated with number of recruits available in the population (for enclosure II, only those data from the period preceding the introduction of Microtus have been used). Contributions of this variable to variations in Y are 51 21 % and 44 07% respectively. In enclosure III the correlation is with the index of woodland habitat, for which the coefficient of determination is 48.660%.

Table 9. Number of Peromyscus individuals recorded in the grassland habitat

Enclosures Total as a fraction of

I II I those available Original adults 1 1 0 2/12 Added adults 1 1 1 3/12 Recruits 4 9 2 13/24 Total 6 11 3 18/48

Table 10. Number of captures of the three categories of Peromyscus in the three enclosures

Enclosures

I 1I III Totals Original adults Woodland 85 132 14 231


Grassland 1 15 1 17 Recruits Woodland 11 79 21 111

Grassland 9 20 5 34 Total Woodland 152 241 45 438

Grassland 16 41 6 63

(b) Contributions of adults and recruits to the movements into the grassland. The types of animals contributing to the movements into the grassland are, in order of importance, recruits, added adults and original adults (Table 9), as was found in experiment 1. Table 10, more than Table 9, shows the importance of added adults. In enclosure II, the proportion of added adult captures in the grassland was higher than that of original adults (P< 0001). The difference between added adults and recruits is not significant (P> 0 1). Possibly this was because most added adults were present before the introduction of Microtus to the grassland of enclosure II, whereas recruits were present mainly




afterwards; and, as was seen above, following the Microtus introduction, the frequency *of occurrence of all Peromyscus in the grassland dropped sharply. When living contemporaneously, recruits occurred proportionally more frequently in the grassland than did original adults (P<0 001), as did added adults (P<0 001). In contrast to experiment 1, added adults occurred in the grassland more frequently than contemporaneous recruits (P < 005), possibly for the reason involving Microtus given above.

A comparison of animals in the three enclosures reveals some interesting differences. The proportion of occurrences in the grassland of original adults in each of the three enclosures is, statistically, the same. A significantly higher proportion of added adult trapping records occurred in the grassland of II than in the grassland of I (P<0O001) and III (P<0001). The highest proportion of recruit records in the grassland occurred in enclosure I, although this is not significantly different from the other two enclosures (P > 0 1). The highest number of recruit records in the grassland occurred in enclosure II, where most of the recruits are considered to have been raised. The fact that enclosure II did not have the highest proportion of recruit records in the grassland is, once again, probably due to the introduction of Microtus.

80 O

- 60 ///'\

,@ ~~~~~~~~~~~~/

U40\XI

E 20 x x Z . 0 X ---0

0 0

o -- s0., - .x 1 2 3 4 5 6 7 8 9 10

Trap Rows

Woodland Grassland

FIG. 10. The distribution by trap rows of Peromyscus trapping records.

(c) The spatial distribution of animals in the grassland. Only the distributions in enclosures I and II have been analysed, because there are insufficient data from enclosure III (Table 10). The enclosure II data are taken from the period up to the introduction of Microtus (and supplementary traps). In both enclosures the distributions are aggregated (P<0O001), with Coefficients of Dispersion of 2-48 (I) and 2-53 (II). Analysed by trap rows the distributions in the two enclosures exhibit departures from unifo'rm, and in both enclosures row 6 is over-represented with captures (Fig. 10). In addition row 7 is over- represented and row 9 is under-represented in enclosure II (P< 005 in each case).

The movement of Peromyscus between enclosures The movement of animals between enclosures is pertinent to the movements from

woodland to grassland. Since animals moved frequently from one enclosure to another in this experiment these movements are reported in some detail.

In experiment 1, when Peromyscus were trapped in an enclosure to which they had migrated, they were replaced in their correct enclosure. As a consequence, only 11 % of all



P. R. GRANT 343

trapping records involved animals in the wrong enclosures. In the present experiment animals were not put back when captured in a wrong enclosure, and animals in wrong enclosures accounted for 32% of all trapping records. The difference between years is found by x2 to be highly significant (P<0001). In both experiments original adults comprised 6400 of the migrant records.

The data for adults in the present experiment are shown in Table 11. Proportionally fewer added adult records came from the wrong enclosures than did original adult records (P<0 05). Recruit data are not strictly comparable with adult data because of the uncertainty about where the recruits were born. In the absence of knowledge of the movements of recruits before they were trapped for the first time, it is assumed that they were first trapped in the enclosure in which they were born. By this criterion only 8 % of recruit trapping records were in wrong enclosures. If the recruit data are now compared with added adult data, it is found that wrong enclosure records occurred in a significantly smaller proportion among recruits than among added adults (P< 0005), hence also than among original adults.

Table 11. The movements of adults between enclosures, as shown by the cumulative number of captures

Original adults Added adults Enclosure I animals

(a) Right enclosure 74 43 (b) Wrong enclosures 30 6

Enclosure II animals (a) Right enclosure 76 36 (b) Wrong enclosures 7 8

Enclosure lII animals (a) Right enclosure 13 10 (b) Wrong enclosures 41 10

Totals (a) Right enclosure 163 89 (b) Wrong enclosures 80 23

There are thus differences among the three components of the population. There are also differences among the enclosures. Enclosure III adults moved the most frequently. Original adults from this enclosure were trapped in other enclosures more frequently than were the original adults of I and II (P<0'001 in each case). Original adults introduced to I migrated more than original adults introduced to II (P< 0.001). Added adults of III changed enclosures more frequently than did those of I and II (P<0 01 in each case), and these migrated to approximately the same extent.

Thus enclosure II animals stayed put and enclosure III animals, and to a much lesser extent enclosure I animals, tended to move into II. In experiment 1 the prevailing movement was in the opposite direction, from II into the others. At least part of the reason for this difference between experiments is presumably that the animals were allowed to re-distribute themselves in the present experiment, unhindered by the investigator, whereas in the previous one migrants were replaced in the correct enclosures. Another contributing factor is the pattern of persistence. In experiment 1, the persistence of original adults was greatest in enclosure II, hence, during the time that the movements were principally occurring, adult density tended to be highest in this enclosure. In the present experiment the persistence of original adults was greatest in enclosure 1, and the lowest

C J.A.E.




in enclosure III, where only two males persisted after the first week. The movements of these two males from a low density area may have been impelled by reproductive needs (cf. Lowe 1969).

CONCLUSIONS TO EXPERIMENT 2 AND GENERAL DISCUSSION (1) Interspecific interaction in the grassland

Taken together, the results of these two experiments with Peromyscus and of the previous one with Clethrionomys demonstrate that Microtus tend to exclude these woodland species from the grassland. Clethrionomys occurred in a Microtus-free grassland (I) significantly more frequently than in another grassland (II) occupied by Microtus (Grant 1969). The same result was obtained, though not demonstrated statistically, when Peromyscus were used instead of Clethrionomys (experiment 1). There is nothing peculiar to enclosure II which prevents woodland animals from entering the grassland. In experiment 2 the grassland of enclosure II was initially without Microtus, and Peromyscus were trapped there frequently immediately following recruitment.

If Microtus tend to exclude woodland animals from the grassland then the removal of Microtus should lead to more frequent use of the grassland by these woodland animals. Exactly this happened in experiment 1. When Microtus were eventually removed from the grassland of enclosure II, the frequency of occurrence there of Peromyscus increased sharply, and within a few weeks it reached the level in the other two enclosures.

The conclusive evidence for the influence of Microtus upon a woodland species in the grassland is obtained by the opposite manipulation, that of introducing Microtus to a grassland where the woodland species is occurring frequently. This manipulation was performed in both experiments 1 and 2, the results differing in degree only. In experiment 1, following the introduction of Microtus at low density, Peromyscus were restricted in the grassland to the area closest to the woodland. This contrasts with lack of such restriction before the introduction of Microtus and after the Microtus density had fallen in that enclosure. No such restriction was manifest in the Microtus-free grassland of enclosure I. In experiment 2, following the introduction of Microtus at high density, the frequency of occurrence of Peromyscus in the grassland dropped to zero in the first 3 weeks, and remained there for the next 4 weeks despite the presence of many Peromyscus in the woodland. This contrasts with the increase in frequency of occurrence in the grassland of the same enclosure and at approximately the same time of year following the removal of Microtus in experiment 1.

Thus at low density Microtus either partially excludes or restricts the Peromyscus in the grassland, while at high density Microtus excludes Peromyscus from the grassland altogether. The hypothesis of competitive interaction between species is supported by the results of all the tests performed.

Other studies have provided evidence, mainly circumstantial, that Microtus species interact competitively with other species. Wirtz & Pearson (1960) inferred, from reciprocal changes in numbers and distribution, that M. pennsylvanicus at high density excluded Peromyscus leucopus. Chitty & Phipps (1966) found large numbers of Clethrionomys glareolus in grassland only when the adult male Microtus agrestis had disappeared from most of the study area, which may indicate that the Clethrionomys were kept out of the grassland earlier by the male Microtus; the Clethrionomys were considered to have immigrated from surrounding woodland and scrub. Brown (1954, 1956) observed that Apodemus sylvaticus (L.) entered grassland from neighbouring woodland when the



P. R. GRANT 345

numbers of Microtus agrestis were low, and returned to the woodland when the numbers of M. agrestis increased. Apodemus sylvaticus may have returned to the woodland anyway (Bergstedt 1966 Kikkawa 1964; Zejda 1965), regardless of the density of Microtus agrestis. Nevertheless it is reasonable to conclude, as did Brown, that Apodemus sylvaticus competes successfully with Microtus agrestis for space in the grassland only when the numbers of the latter are low.

The theory that animals occupy more habitats on islands than on mainland because of the absence of competitor species on islands is supported by the results of these experiments (Grant 1970b). The exclusion of Peromyscus from the grassland by Microtus is the result of competition for space. The reverse exclusion, that of Microtus from the woodland by Peromyscus, did not occur in the experiments because Microtus did not enter the woodland, according to the trapping results, even in the near-absence of Pero- myscus; only when a much higher density of Microtus in the grassland is reached do some of them enter the woodland (Grant 1971). However, in Saskatchewan, Morris (1969) has studied Microtus populations which regularly enter woodland, and has evidence that Clethrionomys tend to exclude Microtus from the woodland. Thus competition, tending to competitive exclusion, operates between small mammal species in both woodland and grassland. Evidence of competitive interaction between other species of rodents, not necessarily a woodland and a grassland species, has been provided for the species M. pennsylvanicus and M. montanus (Koplin & Hoffman 1968), M. pennsylvanicus and M. ochrogaster (Krebs, Keller & Tamarin 1969), M. oeconomus and M. agrestis (Tast 1966, 1968a, b), Peromyscus polionotus and Mus musculus (Caldwell 1964; Caldwell & Gentry 1965) and Peromyscus maniculatus and P. oreas (Sheppe 1967) (see also Miller 1967).

The behaviour of Microtus and Peromyscus individuals in the field experiments was not observed, so it is not known how Microtus exclude Peromyscus from the grassland. However, the behaviour of the two species when placed together in a laboratory arena has been investigated, and it was found that members of the two species interacted aggressively, with the result that a dominance relationship was established between them (Grant 1970c). Individuals of each species were more restricted to segments of their usual habitat in the presence of the other species than in the presence of a conspecific. This leads me to suggest that the dispersion of the species, in both field and laboratory, is a consequence of interspecific aggressive behaviour (see also Christian 1970; Collias 1944). The laboratory experiments were not designed to reveal unequivocally the exact cause of dispersion. It is possible that each species is influenced by other factors as well as direct contact, such as the odour or noise produced by the other species. Previously it was suggested (Grant 1969) that Microtus and Clethrionomys interacted aggressively in the field experiment, and that signs of the presence of Microtus, rather than the presence itself, might have been sufficient to deter Clethrionomys from further exploration of the grassland, at least for a time. The same suggestion may be offered for the Microtus-Peromyscus interaction.

(2) The causes of movement of Peromyscus into the grassland Undoubtedly there are many factors which determine whether an animal will leave its

usual habitat and enter another, and whether it will do so repeatedly or not. The two experiments provide some evidence that both habitat and population factors are involved in the determination of these between-habitat movements.

The onset of regular movements of Peromyscus into the grassland appears to have been



346 Comnpetition between species of Microtus and Peromyscus

determined by recruitment, since Peromyscus were regularly captured in the grassland only after initial recruitment had occurred. Changes in the woodland associated with leaf- fall are not likely to have been important determinants because, although regular movements began in 1967 (experiment 1) just before leaf-fall started, they began several weeks earlier in 1968 (experiment 2). The onset of regular movements could have been influenced by habitat changes only if inconspicuous changes in the structure and food composition of the woodland occurred several weeks earlier in 1968 than in 1967. This seems unlikely, mainly for the reason that conspicuous changes in the woodland leaf-fall, which might be expected to vary concordantly with inconspicuous changes, occurred not early but later in 1968 than in 1967.

The frequency of occurrence of Peromyscus in the grassland appears to have been determined by both the number of recruits present and changes in the woodland habitat. In experiment 1 the weekly number of occurrences of Peromyscus in the grassland was correlated with the number of recruits present (enclosure III) and the woodland index (enclosure I and II). In experiment 2, begun earlier in the year in an attempt to distinguish between the importance of recruitment and habitat changes, the weekly number was correlated with the woodland index in enclosure III and with the number of recruits in the other two enclosures. As there was no recruitment in enclosure III in this experiment, and generally poor persistence there, it is concluded that the frequency of occurrence in the grassland was determined mainly by population, rather than woodland habitat, factors.

Several additional pieces of evidence implicate the role of these population factors (composition and numbers) in causing movement into the grassland. The evidence from experiment 2, comprising persistence and distribution features, may be summarized as follows. Original adults persisted for only moderately long periods and were concentrated mostly in enclosure II. Added adults persisted for shorter periods, on average, and were concentrated more in I than in II, but in II, where the overall density was generally highest, they entered the grassland with high frequency. Recruits were raised mainly if not entirely in enclosure II, and spent most time there. They occurred frequently in the grassland of enclosure II until Microtus were introduced there. They migrated more to enclosure III, where few adults occurred, than to enclosure I, but in the latter, where many adults occurred in the woodland, they entered the grassland with high frequency. The conclusion may be drawn from these results that there is an avoidance of high density conditions by movement (such conditions may lead to death as well) on the part of the new animals (added adults and recruits), either to other parts of the same habitat (other enclosures) or to another habitat. Added adults moving to other enclosures, followed by recruits moving to the other habitat, suggests that all space in the usual habitat is sought first and then, when 'full', space in another habitat is sought. In other words, the state of the population when an animal enters it determines whether the animal moves to another habitat or not. In addition, the added adults and recruits may have differed in the frequency with which they entered the grassland because their experience was different, added adults having spent more time than recruits in the woodland (of the source area) before they entered the population. The more frequent movement of original adults between enclosures than between habitats is consistent with the suggestion that space is first sought in the usual habitat.

There is no fundamental difference between these results and those obtained in experiment 1. Furthermore, the movements of Peromyscus in experiment I differed importantly from the movements of Clethrionomys in the earlier experiment only in the matter of



P. R. GRANT 347

timing. Unlike Peromyscus, the original adult Clethrionomys entered the grassland regularly from the start of the experiment (Fig. 11), and well before the initial recruitment. The two experiments extend over almost identical periods of time. Despite the differences between the species in onset of movements into the grassland, the weekly numbers of captures of the two species in the grassland are positively correlated (rs = + 066, P<0 01). The frequency of occurrence in the grassland of Clethrionomys (either total animals or just original adults) was correlated with the number of recruits available. Therefore I suggest that movements into the grassland in all three experiments were avoidances of high density conditions (in the woodland).

4.0 c

3.0 X I~~~X X-

32.0

z /

1.0/

0_

2 4 6 8 10 12 14 16 18

Weeks

FIG. 11. A comparison of the grassland trapping records of Clethrionomys gapperi (enclosure I) in 1966 and Peromyscus maniculatus (average of I and ILL) in 1967, in terms of captures per trap night per week. The weekly trapping effort was not the same in the two

years.

The regression analyses have shown that the frequency of occurrence of woodland animals in the grassland is associated with both the number of recruits in the population and an index of the woodland habitat. From this it may be deduced that the probability of movement into the grassland does not bear a fixed relationship with density. The relationship will depend upon the suitability of the woodland in terms of food, cover, nest sites, etc.; the 'richer' the habitat the larger the number of individuals supported without emigration induced. The relationship will also depend upon the animals themselves. It will not be the same for populations of the same size comprising 90 0 recruits on the one hand and 10 % recruits on the other, since the behaviour of the components of a population differs. And it will presumably change seasonally for the additional reason that the behaviour of the animals changes from sexual activity, accompanied by dis- persive tendencies, to sexual inactivity, accompanied by aggregative tendencies (Howard 1949; McCabe & Blanchard 1950).

(3) Movements to andfrom the grassland The movements of woodland animals into the grassland, and the reverse movements

when Microtus subsequently occupied the grassland, have been treated separately for the sake of simplicity. In fact they are interrelated. Movement from woodland to grassland has been shown to be at least partly a function of density in the woodland in some instances. There is evidence that movement from grassland back to woodland is a function of the density of the Microtus in the grassland. These facts alone suggest a common




underlying cause of the movements in the two directions. The behaviour experiments in the laboratory show that Peromyscus and Microtus interact aggressively with animals of the same and the other species (Grant 1970c; see also Getz 1962; Healey 1967; Sadleir 1965; Terman 1962; Wirtz & Pearson 1960; Banks & Fox 1968). Therefore the following is offered as an explanation for the movements of woodland animals recorded in the three experiments. The use of the grassland habitat by Clethrionomys and Peromyscus can be interpreted as being due to intraspecific interaction, inducing movement outwards from the woodland, and this tends to be counteracted by interspecific interaction (with Microtus), inducing opposite movement.

ACKNOWLEDGMENTS

For permission to work on the site I thank Dr A. R. C. Jones, Dr J. D. MacArthur and Dr L. G. Johnson. Mr J. W. Pollock and R. J. Watson helped to solve some of the practical problems. D. N. Nettleship, P. G. Wells, U. Fleising and R. Shoofey did a large part of the routine trapping. Colonel P. D. Baird kindly provided working facilities at the Mont St Hilaire Field Station. Dr H. Tyson, H. Nickerson and Miss A. Garai gave considerable help with the regression analyses, which were performed by the McGill University FORTRAN IV G level computer. Dr J. R. Bider offered some useful advice on the interpretation of animal movements, and Dr R. D. Morris and Mr H. N. Southern made many valuable suggestions for the improvement of the manuscript. The study was financed by the National Research Council of Canada (A 2920). I gratefully acknowledge all this help.

SUMMARY

(1) Two experiments were carried out to test an hypothesis of competitive interaction between the woodland species of rodent, Peromyscus maniculatus, and the grassland species Microtus pennsylvanicus. They were designed to permit the movement of Peromyscus from woodland to grassland, and to determine the influence of Microtus upon these movenients. Three 1-ac enclosures, each containing equal portions of woodland and grassland, were used.

(2) The first experiment was carried out for 16 weeks in 1967. Three pairs of Peromyscus were introduced to the woodland of each enclosure. Four pairs of Microtus were introduced to the grassland of one enclosure (II). The fate and distribution of the animals and their offspring were followed by live-trapping.

(3) Peromyscus were trapped in the grassland frequently only after initial recruitment had occurred. The initiation of regular movements into the grassland was not synchron- ous in the three enclosures, but in each enclosure occurred 1-2 weeks after the first recruits appeared. Recruits entered the grassland proportionally more frequently than did adults. The frequency of occurrence of Peromyscus in the grassland was correlated with an index of woodland habitat change in two enclosures and with numbers of recruits in the other enclosure.

(4) Peromyscus were captured rarely in the grassland (II) which contained Microtus, even though recruitment to the enclosure II population of Peromyscus had occurred. Following the removal of Microtus in weeks 11 and 12, the frequency of occurrence of Peromyscus in the grassland of enclosure II rose sharply. Prior to week 1 1, new Microtus were added to the grassland of enclosure III. This did not result in a reduction in the frequency of occurrence of Peromyscus in that grassland, but it did result in a restriction



P. R. GRANT 349

of the captures of Peromyscus in the grassland to the two trap rows adjacent to the habitat interface. It was concluded that Microtus had a small deterring effect upon the use of grassland by Peromyscus.

(5) Based upon the results of experiment 1, it was predicted that Microtus, at a density much higher than those prevailing in the experiment, would exclude Peromyscus altogether from the grassland. To test this prediction the experiment was repeated in the same enclosures in the following year for 21 weeks. Peromyscus were trapped in the grassland of one enclosure (It) with a high frequency immediately following recruitment. After 4 weeks, during which the high frequency was sustained, Microtus were introduced at high density to this grassland. The frequency of occurrence there of Peromyscus immediately declined, and no Peromyscus were trapped there from the third to seventh week after Microtus were introduced. It was concluded that Microtus excluded Peromyscils from the grassland; a mechanism involving aggressive interaction between the species is suggested. The prediction was thus shown to be correct, and the hypothesis supported by the results of this and the previous tests.

(6) In both experiments, factors both intrinsic (e.g. recruitment) and extrinsic (e.g. habitat changes) to the population are considered to have influenced the movements of Peromyscus from woodland to grassland. These movements are believed to have been caused by interactions between Peromyscus individuals similar to the interspecific interactions which occurred in the grassland and which resulted in the opposite movement of Peromyscus.

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(Received 22 January 1970)



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Experimental Studies of Competitive Interaction in a Two-Species System