letters to nature
Correspondence and requests for materials should be addressed to J.D.C.
(e-mail: jcoates@micro.siu.edu). GenBank accession numbers for strains RCB and JJ are
AY032610 and AY032611, respectively.
.................................................................
Life-history traits of voles in a
¯uctuating population respond to
the immediate environment
D
21/20 20/10
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C
b 21
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D
A
B
13/28
9/0
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18/14
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10 km
B
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200 A
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10 A
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50 A
16
A
c
A B C D
Site
A
S
S
A
S
A
S
A
S
B
A
S
S
S
A
D
10 C
1997
Acknowledgements
This work was supported in part by funding to J.D.C. by the US Of®ce of Naval Research.
Funding to J.D.C. and L.A.A. was also from the US Department of Defense SERDP
Program.
C
Body mass (g)
a
Density (voles ha–1)
20. Coates, J. D., Phillips, E. J. P., Lonergan, D. J., Jenter, H. & Lovley, D. R. Isolation of Geobacter
species from a variety of sedimentary environments. Appl. Environ. Microbiol. 62, 1531±1536
(1996).
21. Vogel, T. M. & Grbic-Galic, D. Incorporation of oxygen from water into toluene and benzene during
anaerobic fermentative transformation. Appl. Environ. Microbiol. 52, 200±202 (1986).
22. Rooney-Varga, J. N., Anderson, R. T. & Fraga, J. L. Microbial communities associated with anaerobic
benzene degradation in a petroleum-contaminated aquifer. Appl. Environ. Microbiol. 65, 3056±3063
(1999).
23. Bruce, R. A., Achenbach, L. A. & Coates, J. D. Reduction of (per)chlorate by a novel organism isolated
from a paper mill waste. Environ. Microbiol. 1, 319±331 (1999).
24. Coates, J. D. et al. The ubiquity and diversity of dissimilatory (per)chlorate-reducing bacteria. Appl.
Environ. Microbiol. 65, 5234±5241 (1999).
25. Coates, J. D., Bruce, R. A., Patrick, J. A. & Achenbach, L. A. Hydrocarbon bioremediative potential of
(per)chlorate-reducing bacteria. Bioremed. J. 3, 323±334 (1999).
26. Lovley, D. R., Fraga, J. L., Coates, J. D. & Blunt-Harris, E. L. Humics as an electron donor for anaerobic
respiration. Environ. Microbiol. 1, 89±98 (1999).
27. Achenbach, L. A., Bruce, R. A., Michaelidou, U. & Coates, J. D. Dechloromonas agitata N. N. gen., sp.
nov. and Dechlorosoma suillum N. N. gen., sp. nov. two novel environmentally dominant (per)chlorate-reducing bacteria and their phylogenetic position. Int. J. Syst. Evol. Microbiol. 51, 527±533
(2001).
28. Achenbach, L. A. & Coates, J. D. Disparity between bacterial phylogeny and physiology. ASM News 66,
714±716 (2000).
29. Anderson, R. T. & Lovley, D. R. Anaerobic bioremediation of benzene under sulfate-reducing
conditions in a petroleum contaminated aquifer. Environ. Sci. Technol. 34, 2261±2266 (2000).
30. Coates, J. D., Bruce, R. A. & Haddock, J. D. Anoxic bioremediation of hydrocarbons. Nature 396, 730
(1998).
1998
1999
1997
1998
1999
Year
Figure 1 Design of the study. a, Groups of voles were swapped between half-sides of four
1-ha unfenced trapping grids in early winter (November/December). Arrows, pairs of
transplanted groups. A second transplant was done between two of the sites (B and D) in
February because few voles settled in some groups. Numbers in the boxes show number
of males/females that were successfully transplanted between grids and captured at least
once during the spring. b, Average body mass (6s.e.) at the time of transplant in
November/December among animals that had not previously bred. Open circles, females;
®lled circles, males. c, Density trajectories at the four sites plotted on a log10 scale.
Density estimates denoted by S (spring) and A (autumn) are based on vole sign indices21.
Estimates plotted as ®lled circles are obtained by the robust design model27 of capture±
mark±recapture data. Vertical lines show the time of transplant. Density trajectories in
neighbouring control areas showed similar patterns (see Supplementary Information).
Torbjùrn Ergon*, Xavier Lambin² & Nils Chr. Stenseth*
..............................................................................................................................................
Life-history traits relating to growth and reproduction vary
greatly among species and populations1,2 and among individuals
within populations3. In vole populations, body size and age at
maturation may vary considerably among locations and among
years within the same location4±8. Individuals in increasing
populations are typically larger and start reproduction earlier in
the spring than those in declining populations6±8. The cause of
such life-history variation within populations has been subject of
much discussion7,9,10. Much of the controversy concerns whether
the memory of past conditions, leading to delayed effects on lifehistory traits, resides in the environment (for example,
predators11,12, pathogens13 or food14,15) or intrinsically within
populations or individuals (age distribution16,17, physiological
state3, genetic18 or maternal effects19,20). Here we report from an
extensive ®eld transplant experiment in which voles were moved
before the breeding season between sites that differed in average
overwintering body mass. Transplanted voles did not retain the
characteristics of their source population, and we demonstrate an
over-riding role of the immediate environment in shaping lifehistory traits of small rodents.
NATURE | VOL 411 | 28 JUNE 2001 | www.nature.com
Change in body mass of transplants (g)
Females
* Division of Zoology, Department of Biology, University of Oslo,
PO Box 1050 Blindern, 0316 Oslo, Norway
² Department of Zoology, University of Aberdeen, Tillydrone Avenue,
Aberdeen AB24 2TZ, UK
Males
5
CtoD
AtoD
4
AtoB
BtoD
3
DtoB
DtoC
AtoD
2
CtoB
CtoD
CtoB
DtoB
1
0
DtoC
BtoC
BtoD
BtoA
DtoA
BtoA
BtoC
DtoA
–1
–2
–1
0
1
2
3
–1 0
1
2
3
4
5
6
Site difference in body mass (g)
Figure 2 Average (6s.e.) individual change in body mass of transplanted voles
recaptured in January/February during the ®rst session after transplanting plotted against
difference in average body mass at the sites. The site differences in body mass are
calculated as average body mass in the target population during the ®rst trapping session
after the transplant minus average body mass of transplants at capture during the
transplantation. Voles in the transplant group are excluded from the target population
when calculating the site differences. Hence, measurements are independent. Line is the
unity slope through the origin, indicating perfect convergence. Plotted labels denote
`source-to-target' transplant groups. See Supplementary Information.
© 2001 Macmillan Magazines Ltd
1043
letters to nature
Females
Within A
40 source ×
session **
Males
From A
site × t NS
Within A
source × session NS
From A
site × t ***
From B
site × t2***
Within B
source ×
session *
From B
site × t2***
Within C
From C
site × t *
site × t2**
Within C
source × session NS
From C
site × t *
Within D
From D
site × t ***
site × t2***
Within D
source ×
session NS
From D
site × t **
Body mass (g) mean ± 2s.e.
30
20
Within B
40 source ×
30
session NS
20
40 source × session NS
30
20
40 source × session NS
30
20
Feb. Mar. Apr. May
Feb. Mar. Apr. May
Feb. Mar. Apr. May
Feb. Mar. Apr. May
Date
This ®eld experiment was carried out in the Kielder Forest region,
northern England, where ¯uctuating populations of ®eld voles
(Microtus agrestis L.) inhabit distinct `clear-cuts' showing asynchronous dynamics within the region21,22. We successfully transplanted
266 voles between four clear-cuts in the forest system (Fig. 1a). At
the time of transplant, average body mass at the site with the
heaviest voles was 18% greater than at the site with the smallest voles
(Fig. 1b). Although an estimated 98% of residents were removed
before the release of the transplanted voles, 281 non-transplanted
voles (mostly immigrants) were recorded in the ®rst trapping
session 2±3 months after the transplant (in January and February).
A further 287 overwintering voles entered the trapping grids at some
time during the spring.
We used capture±recapture data collected at two-week intervals
throughout the spring to investigate differences in patterns of body
mass development and onset of maturation between the different
groups of voles. Trapping two to three months after the transplant
showed that individual body mass during midwinter changed
towards the mean body mass at the site to which the voles were
moved (Fig. 2). Voles in the sites with the highest midwinter body
mass also grew faster and reached higher body mass by the end of
the study than those in the sites with low midwinter body mass
(Fig. 3). Individuals originating from different sites before the
transplant but living in the same site showed no clear differences
in body mass trajectories through the spring. However, there was
large variation in individual growth rates between sites during the
spring: voles originating from the same site but transplanted to
different sites showed up to 60% higher body mass in one site than
at another at the same dates. Hence, individuals adjusted their
midwinter body size and spring growth rate according to their
immediate environment.
The change in proportion of matured animals in different groups
through the spring reveals a difference of around three weeks in
onset of spring reproduction between sites (Fig. 4). There was no
signi®cant effect of source population on timing of maturation, but
1044
Within/from D
2
effects of both time (t ) and t were included. This gave homogenous residuals that
appeared normally distributed. A categorical time variable (trapping session) was used
when growth patterns within sites were compared. Because there are missing
combinations of `site' and `source', the population effects were examined with separate
analysis for each group of `site' and `source'. Asterisks represent signi®cance levels of the
interaction effect of population and time (triple asterisk; P , 0.001, double asterisk;
0.001 , P , 0.01, single asterisk, 0.01 , P , 0.05). NS, not selected by the lowest
AIC. Effects of whether the voles had been transplanted or immigrated to the sites were
not signi®cant at the 10% level.
1.0
Proportion
perforate
Figure 3 Average body mass (62s.e.) over the spring after the transplant. Each line
represents a group of animals that were living in the same site and were coming from the
same site before transplant. Left column, time trends are grouped according to the site the
animals were living in; right column, the same time trends are grouped according to site of
origin. The data were analysed with a repeated-measures analysis with individuals as
random subjects (SAS Proc MIXED28). An unstructured covariance matrix (UN(3)28) was
selected by the lowest AIC. When studying the `source' effect, a continuous time variable
(t, number of days since the ®rst trapping session) was used because sites were not
trapped on the same dates. To account for the exponential pattern in the growth curves,
Within/from C
D
C
0.5
B
A
0
1.0
Proportion
lactating
Within/from B
0.5
0
1.0
Proportion
scrotal
Within/from A
0.5
0
1 March
1 April
Date
1 May
Figure 4 Onset of spring reproduction measured as proportions of perforate and lactating
females (top and middle panels) and proportion of males with scrotal testes (bottom
panel). The Figure shows ®ts from the logistic regression models (see Methods and Table
1). Effects of whether the voles were transplanted or immigrated and effects of source
population were not signi®cant (see Table 1) and hence not accounted for.
the site effect was highly signi®cant (Table 1). There was a one-toone correspondence of the sites ranked according to onset of spring
reproduction and ranks of average overwinter body mass and spring
growth. Reproduction started earlier in the sites with higher body
mass. The onset of spring reproduction may contribute profoundly
to the variation in population growth rate, and is generally
© 2001 Macmillan Magazines Ltd
NATURE | VOL 411 | 28 JUNE 2001 | www.nature.com
letters to nature
Table 1 Test statistics for logistic regression of proportion of matured voles in the trapping sessions
Sex (no. individuals)
Response
Factor
F
d.f.*
P
Deviance of model
...................................................................................................................................................................................................................................................................................................................................................................
Females
(n = 121)
Proportion with
perforate vagina
Proportion lactating
Males
(n = 145)
Proportion with
scrotal testis
Site
Source
Site ´ date
Source ´ date
Site
Source
-6
11.31
3,113
1.5 ´ 10
1.36
2.76
1.11
10.03
3,113
3,107
3,107
3,137
0.26
0.046²
0.35
5.1 ´ 10-6
0.70
3,137
0.55
107.2
84.7
111.2
...................................................................................................................................................................................................................................................................................................................................................................
All models include a `date' effect. Models with either parallel or different slopes (`group ´ date' interactions) are chosen on the basis of the models' AIC26. Because of imbalanced replication, `site' is tested
assuming an effect of `source' and vice versa. Only voles that have been transplanted (that is, no immigrants) are included in the analysis.
*Degrees of freedom re¯ect number of individuals, not observations (see Methods).
² Main effects in a parallel slopes model: site, F3,113 = 12.3, P = 5.0 ´ 10-7; source, F3,113 = 0.61, P = 0.6; deviance, 101.0.
described as varying consistently between the phases in rodent
¯uctuations5,7. Even though the variation in life-history traits
documented here is correlated with the variation in population
growth rate in the spring, there is no indication that this variation
re¯ects present or past densities (Fig. 1c).
Our results show strong plasticity in life-history traits of voles.
Individuals do not perform according to past environmental conditions. Instead, the environmental conditions during the winter
and spring directly give rise to large differences in body mass and
timing of maturation between sites. Thus, there is no need to invoke
intrinsic mechanisms16,17,23 to explain the conspicuous variation in
M
these life-history traits within vole populations.
Methods
Transplanting voles
The transplant took place in November/December, when the voles were non-reproductive.
Each 1-ha trapping grid was divided into two sides, and voles were swapped between halfsides of two different grids at a time (Fig. 1). Trapping continued for 5 d until an estimated
98% of the resident animals were captured. Voles were transferred between sites in wooden
boxes containing hay, sawdust, carrots and whole wheat (two individuals in each box).
After the last day of trapping, the boxes were opened but left in the ®eld for at least one
week. In total, 761 individually marked animals were swapped between the four locations.
Of these, 266 individuals were recaptured during the following spring. Although voles that
had not previously reproduced (91% of the transplanted voles) had a higher probability of
being recaptured after transplant (odds ratio = 1.4, x1 = 4.84, P = 0.03), re¯ecting similar
effects on natural mortality, there was no signi®cant difference in the effects of body mass
and reproductive history on transplant success between the groups de®ned by `target
population', `source population' and `target ´ source group' (all interactions tested in
logistic regression models selected by the lowest Akaike Information Criterion26 (AIC); all
P . 0.1). Thus, there is no reason to believe that differential transplant success will
substantially bias our results. A detailed presentation on the analysis of transplant success
is available as Supplementary Information.
Population monitoring
The populations at the four sites were monitored by capture±mark±recapture
methods24,25. At each site, 196 traps at 7-m intervals were pre-baited with carrots 2 d before
the traps were set (baited with carrots and ¯aked barley). Food was removed from the traps
after each session. The ®rst trapping session after the transplant took place in January/
February. Each site was thereafter visited every two weeks (except for the ®rst interval;
which varied in length between sites). In the autumn before the transplant, traps were
checked every 6 h and not left set overnight. After the transplant, traps were set in the
evening and checked at sunrise and sunset for the three consecutive sessions.
Comparing onset of reproduction
At each capture occasion, we recorded whether females had perforated vagina and whether
they were lactating. Males were classi®ed as mature when they had scrotal testes with
visible caput epididymis. Effects on the timing of maturation were analysed by logistic
regression of the proportion of matured animals on sampling date (recapture probability
was ,0.9 and not signi®cantly different between sites or source populations). As each
individual will necessarily be recorded as matured on every subsequent capture after
having reached maturity, the saturated model (zero deviance) is a model with individual
speci®c intercepts and a common slope. Hence, we calculated the test statistic as
F = ((DevH0 - DevHA)/d.f.1)/(DevHA/d.f.2) with d.f.1 being the difference in number of
parameters in the two models (H0 and HA) and d.f.2 being the number of individuals
minus the number of parameters in HA, and compared this with the Fisher distribution
with d.f.1 and d.f.2 degrees of freedom.
Received 12 December 2000; accepted 3 April 2001.
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Acknowledgements
The project was funded by grants from the Norwegian Research Council to T.E. and by
the Natural Environment Research Council (UK) to X.L. We thank the Forestry
Commission for support; C. Grif®n and J. Aars for assistance during the transplant;
and R. Boonstra, L. Crespin, K. E. Hodges, R. A. Ims, R. Julliard, T. Klemola,
P. Thompson, E. Tkadlec, H. Viljugrein and N. G. Yoccoz for constructive comments
and advice.
Correspondence and requests for materials should be addressed to N.C.S
(e-mail: n.c.stenseth@bio.uio.no) and X.L. (e-mail: x.lambin@abdn.ac.uk).
© 2001 Macmillan Magazines Ltd
1045