Ecology, 95(1), 2014, pp. 56–67
 2014 by the Ecological Society of America
Predation pressure by avian predators suggests summer limitation
of small-mammal populations in the Canadian Arctic
J.-F. THERRIEN,1,4 G. GAUTHIER,1 E. KORPIMA¨KI,2 AND J. BEˆTY3
1De´partement de biologie and Centre d’e´tudes nordiques, Universite´ Laval, 1045 Avenue de la Me´decine, Que´bec,
QC G1V0A6, Canada
2Section of Ecology, Department of Biology, University of Turku, FIN-20014 Turku, Finland
3De´partement de Biologie and Centre d’E´tudes Nordiques, Universite´ du Que´bec a` Rimouski, Rimouski, QC G5L 3A1, Canada
Abstract. Predation has been suggested to be especially important in simple food webs
and less productive ecosystems such as the arctic tundra, but very few data are available to
evaluate this hypothesis. We examined the hypothesis that avian predators could drive the
population dynamics of two cyclic lemming species in the Canadian Arctic. A dense and
diverse suite of predatory birds, including the Snowy Owl (Bubo scandiacus), the Rough-legged
Hawk (Buteo lagopus), and the Long-tailed Jaeger (Stercorarius longicaudus), inhabits the
arctic tundra and prey on collared (Dicrostonyx groenlandicus) and brown (Lemmus
trimucronatus) lemmings during the snow-free period. We evaluated the predation pressure
exerted by these predators by combining their numerical (variation in breeding and fledgling
numbers) and functional (variation in diet and daily consumption rates) responses to
variations in lemming densities over the 2004–2010 period. Breeding density and number of
fledglings produced by the three main avian predators increased sharply without delay in
response to increasing lemming densities. The proportion of collared lemmings in the diet of
those predators was high at low lemming density (both species) but decreased as lemming
density increased. However, we found little evidence that their daily consumption rates vary in
relation to changes in lemming density. Total consumption rate by avian predators initially
increased more rapidly for collared lemming but eventually leveled off at a much higher value
for brown lemmings, the most abundant species at our site. The combined daily predation rate
of avian predators exceeded the maximum daily potential growth rates of both lemming
species except at the highest recorded densities for brown lemmings. We thus show, for the first
time, that predation pressure exerted without delay by avian predators can limit populations
of coexisting lemming species during the snow-free period, and thus, that predation could play
a role in the cyclic dynamic of these species in the tundra.
Key words: functional response; lemmings; Long-tailed Jaeger; numerical response; population
limitation; predation; Rough-legged Hawk; Snowy Owl; tundra.
INTRODUCTION
Predation pressure by second-order consumers has the
potential to regulate vertebrate communities in several
ecosystems (Krebs et al. 1995, Korpima¨ki and Norrdahl
1998, Ripple et al. 2001, Korpima¨ki et al. 2002, Schmitz
2006). This force has been hypothesized to be especially
important in simple food webs characterized by a low
primary productivity such as the boreal forest or the
arctic tundra (Strong 1992, Korpima¨ki and Krebs 1996).
However, according to an alternative view, the tundra
food web could be primarily controlled from the
bottom-up (i.e., by food resources; Oksanen and
Oksanen 2000). Assessing the relative strength of top-
down vs. bottom-up forces in an ecosystem is essential
to understand the food web functioning and to predict
impacts of anticipated environmental changes.
In the tundra, small mammals such as lemmings
(Dicrostonyx and Lemmus spp.) are often the dominant
herbivores (Krebs et al. 2003). Those herbivores show
tremendous variations in numbers from year to year and
exhibit population cycles in most circumpolar regions
(Elton 1924, Stenseth 1999, Predavec et al. 2001, Gilg
2002). The potential causes of those fluctuations have
been studied for a long time but still remain unclear
(e.g., Gauthier et al. 2009, Oksanen et al. 2009, Krebs
2011), although in several systems high predation rates
have been reported, especially during the summer
(Korpima¨ki and Norrdahl 1991a, Reid et al. 1995,
Korpima¨ki and Krebs 1996, Wilson et al. 1999, Hanski
et al. 2001, Gilg et al. 2003, Korpima¨ki et al. 2004, Ims
et al. 2011). Very few studies, however, have quantified
the numerical and functional responses of arctic
predators to fluctuations in small-mammal abundance
and their combined impact on prey populations (but see
4 Present address: Acopian Center for Conservation
Learning, Hawk Mountain Sanctuary, 410 Summer Valley
Road, Orwigsburg, Pennsylvania 17961 USA.
E-mail: jean-francois.therrien.3@ulaval.ca
56
Pitelka et al. 1955, Gilg et al. 2006), an essential
prerequisite to evaluate the role of predation in the
control of food webs (Korpima¨ki and Krebs 1996).
Moreover, among-year variation in daily consumption
rates of small mammals by avian predators has rarely
been investigated, but is essential to determine their
functional response.
Birds present high diversity of predators compared to
mammals in the tundra. Snowy Owls (Bubo scandiacus),
Rough-legged Hawks (Buteo lagopus), Long-tailed and
Parasitic Jaegers (Stercorarius longicaudus, S. parasit-
icus), Peregrine Falcons (Falco peregrinus), and Glau-
cous Gulls (Larus hyperboreus) all dwell in the tundra
during the snow-free period. Diet has been previously
described individually for those predators in different
regions of the Arctic (reviewed in Birds of North
America accounts: Glaucous Gull, Gilchrist 2001;
Long-tailed Jaeger, Wiley and Lee 1998; Parasitic
Jaeger, Wiley and Lee 1999; Peregrine Falcon, White
et al. 2002; Rough-legged Hawk, Bechard and Swem
2002; Snowy Owl, Parmelee 1992) and showed that the
primary prey for most of them are small mammals.
However, there have been very few studies that
simultaneously investigated their breeding numbers,
diet, and consumption rates when these predators occur
in sympatry during contrasting years of lemming
abundance.
The response of Snowy Owls and Long-tailed Jaegers
to varying abundance of lemmings has been studied in
northern Greenland by Gilg et al. (2003, 2006). They
found that density-dependent predation by these two
species could induce summer decline in lemming
populations. However, the food web at this site is
simpler than at most other tundra sites. Indeed, whereas
only one species of lemming and two species of avian
predators breed in Greenland, much of the circumpolar
tundra is inhabited by at least two species of small
mammals and four or more competing species of avian
predators. Therefore, competition for scarce resources
among these multiple predators could be high in the
relatively unproductive tundra ecosystem. As suggested
by Reid et al. (1995) and Wilson et al. (1999), we
anticipated that avian predators could have a significant
impact on small-mammal numbers, and thus, on the
food web functioning.
Our aim was to assess the predation pressure of
sympatric avian predators by simultaneously determin-
ing variations in numbers (numerical response) and in
diet and consumption rates (functional response) to
varying lemming density. Arctic avian predators are
predominantly migrants and predation on lemmings
mostly occurs when snow cover is absent (typically from
early June to early October). These predators are highly
mobile and have the potential to track small-mammal
outbreaks over large geographic areas (Korpima¨ki and
Norrdahl 1991b, Norrdahl and Korpima¨ki 1996). We
thus hypothesized that (1) lemming-eating avian pred-
ators of the tundra would exhibit strong numerical
responses without any time lag to local variations in
lemming abundance, (2) consumption rate of lemmings
by avian predators would increase in response to an
increase in lemming abundance, and (3) the combined
predation pressure by avian predators would be
sufficient to limit the summer growth of lemming
populations during the snow-free period and cause
population declines. Here we present a unique and
detailed evaluation of the numerical, functional, and
total responses of avian predators in order to provide
further insights into the trophic control of arctic
terrestrial food webs.
MATERIALS AND METHODS
Study area
The 100-km2 study area was located on Bylot Island
(Nunavut, Canada; 738 N, 808 W) and field work
occurred during summers 2004 to 2010. The study area
is dominated by rolling hills and low-elevation plateaus
interspersed by streams and rivers that created numer-
ous valleys ranging in size from narrow gullies to wide
and relatively flat valley bottoms. Mesic tundra (dom-
inated by prostrate shrubs and a sparse forb and
graminoid cover) was most common in the hilly
landscape, whereas flat areas had a mosaic of mesic
and wet tundra (the latter habitat being dominated by
graminoid plants growing through a ground moss cover;
see Gauthier et al. 2011).
Brown (L. trimucronatus) and collared (D. groenland-
icus) lemmings have a widespread distribution across
most of the Canadian tundra and are the sole small
mammals present on Bylot Island. Both species exhibit
three-to-four year cyclic fluctuations in abundance, but
the amplitude of fluctuations is much larger in the
brown lemming (Gruyer et al. 2008). Breeding predatory
birds are dominated by the Snowy Owl, the Rough-
legged Hawk, the Long-tailed Jaeger, the Glaucous
Gull, the Peregrine Falcon, and the Parasitic Jaeger. No
nesting Raven (Corvus corax) or Gyrfalcon (F. rustico-
lus) was found during the study, although the former
species is also present in small numbers. Other major
predators present include the arctic fox (Vulpes lagopus)
and the stoat (Mustela erminea). Bylot Island has a large
Snow Goose (Chen caerulescens) breeding colony
situated roughly 30 km to the south of the study area,
which can be an alternative prey for some predators.
Other alternative prey include passerines (Calcarius and
Plectrophenax spp.), shorebirds (Charadrii spp.), the
Rock Ptarmigan (Lagopus mutus), ducks (Somateria and
Clangula spp.), as well as many arthropods taxa (such as
Arachnidae, Tipulidae, Muscidae).
Small-mammal density
We measured small-mammal density throughout the
snow-free period each year by live-trapping them on two
trapping grids (11 ha each) spaced by 2 km. We set up
trapping grids in areas representative of the typical
habitat; one grid was located in hill side dominated by
January 2014 57AVIAN PREDATION IN THE TUNDRA
mesic tundra and one grid in a valley bottom dominated
by wet habitat. Each trapping grid had 144 Longworth
live traps that were opened over three or four
consecutive days at each trapping period, and checked
at 12-h intervals. We conducted three (sometimes four)
trapping sessions each summer (mid-June, mid-July, and
mid-August). We individually marked all animals with
passive integrated transponder (PIT) tags before release
(see Gruyer et al. 2010 for details). We estimated
densities of each species at each trapping session using
capture–mark–recapture (CMR) techniques with the
Program DENSITY 4 (Efford et al. 2004, Efford
2009). When the number of captured individuals was
too low for analysis in DENSITY (i.e., ,4 individuals),
we used the minimum number known to be alive (MNA)
divided by the effective trapping area (see Bilodeau et al.
2013b). Given that both wet and mesic habitats are
present in similar proportions in the study area, we
averaged densities of each species between the two grids
for each corresponding trapping session.
Avian predators
Numerical responses.—We conducted systematic
searches for nests of predatory birds during June and
early July. Over hilly terrain, we followed ridges and
scanned the surrounding landscape from vantage
points. Nests of most avian predators are conspicuous
and typically located on elevated mounds. Moreover,
nesting predators often reveal their presence from a
relatively long distance through alarm calls and
behavioral displays. For jaegers that prefer lowland
habitats and exhibit less conspicuous nests, we
conducted systematic searches by walking parallel
transects 250 m apart over a 30-km2 area suitable
for nesting. Because a portion of the whole study area
(;30%) was unsuitable for jaegers (mostly steep hills),
we multiplied the density measured over the 30-km2
search area by 0.7 to determine jaeger nesting density
over the whole study area. Although we did not assess
the nest detection probability, we are confident that it
was very high for all avian predator species in this
open landscape. However, any possible bias related to
detection probability would result in an underestima-
tion of nest density, and hence, predation pressure on
lemmings. Nonbreeding, resident adults were seldom
encountered in any species. We divided the number of
nests of each species by the area searched annually to
obtain nesting density. We assessed the numerical
responses of avian predators by plotting their annual
nesting densities separately against the density of
lemming (both species combined) measured during
the first two trapping season (June and July, thereafter
called: early summer period). We determined fledgling
numbers by revisiting nests on a weekly basis. We
considered chicks able to sustain flight as fledglings.
This number should be considered a minimum
estimate as young avian predators sometimes disperse
over large areas and are difficult to find away from the
nest.
Functional responses.—We used methods similar to
Gilg et al. (2006) to assess functional responses. We
measured the relative proportions of collared and brown
lemming in the diet of Snowy Owls, Rough-legged
Hawks, and Long-tailed Jaegers with pellet analyses
(Errington 1930, Lewis et al. 2004) collected throughout
the breeding season annually. Nests were visited weekly
and all pellets found in its surrounding (,20 m) were
collected. We later analyzed pellets in the laboratory to
identify ingested prey using hair, bones, and feather
remains. We determined the minimal number of prey
ingested by counting the number of jaws and skulls
found in pellets. Overall, we collected and analyzed
1668, 28, and 147 pellets for Snowy Owls (25 nests),
Rough-legged Hawks (9 nests) and Long-tailed Jaegers
(30 nests), respectively. We plotted the annual propor-
tion of collared lemmings in the diet of the three main
predators in relation to the density of both lemming
species on the study area and compared it to the
proportion of collared lemmings in the overall lemming
population.
We used direct observations to assess the number of
prey consumed daily by the three major avian predators
from 2007 to 2010. We set up blinds ;150 m from focal
nests and conducted behavioral observations during 3-h
to 8-h bouts using a spotting scope. Observations
covered the 24-h period to account for any possible
circadian variation in predator activity despite the 24-h
daylight during the summer. We conducted observations
from the mid-incubation (20 June) through the chick-
rearing period (until 15 August). We conducted a total
of 50, 50, and 80 h of direct visual observations on
Snowy Owls (7 nests), Rough-legged Hawks (4 nests),
and Long-tailed Jaegers (8 nests) respectively. We also
set automatic-triggered cameras at;5 m from 11 Snowy
Owl and 5 Rough-legged Hawk nests to monitor food
delivery over periods of two to seven days. We
programmed the motion-sensitive cameras to take
pictures every time a movement was detected and under
fixed intervals (ranging from 1 to 20 s). Cameras worked
well for Snowy Owls and Rough-legged Hawks, but not
for jaegers because the chicks leave the nest one or two
days after hatching and cannot be followed by a fixed
camera. We recorded a total of 3876 and 314 h of
observations with cameras on Snowy Owl and Rough-
legged Hawk nests, respectively. Since identification of
lemmings to the species level by both observational
techniques was difficult, we used the proportion of each
lemming species found in the pellets to split overall
lemming consumption rates of predators among the two
species.
We assessed the functional response of the three main
avian predators by plotting their mean daily consump-
tion rates (DCR; individual lemmings consumed per
day) in relation to mean daily lemming density on the
study area. We calculated the lemming density associ-
J.-F. THERRIEN ET AL.58 Ecology, Vol. 95, No. 1
ated with each DCR estimate by assuming a linear
change in density between the two closest trapping
sessions. We assessed consumption rates on a nest rather
than an individual basis and we averaged repeated
measures for each nest. Since the two techniques (direct
observations and cameras) were directed toward the
nest, they could not assess prey consumed away from the
nest by adults. This was especially true for Snowy Owls
and Rough-legged Hawks, which nest in territories with
topographical features that prevent observers from
monitoring provisioning adults away from the nest. In
those cases, the measured consumption at the nest
applies only to the incubating/brooding adult and the
growing chicks. We thus assigned the consumption level
recorded during incubation to the other adult. Any
possible bias resulting from this estimation would likely
tend to underestimate consumption rates because the
energetic needs of an incubating adult is expected to be
lower than that of a foraging one. Long-tailed Jaegers,
on the other hand, nest in flatter landscape and were
seldom foraging out of view during observations. We are
therefore confident that almost all feeding events were
recorded, whether close to the nest or further away in
the territory.
Total responses.—We obtained the total response or
predation rate (the number of lemmings eaten/day 3
km2) by multiplying the numerical (number of nests/
km2) and functional (number of lemming consumed
daily per nest) responses of individual predators. We
plotted the total response in relation to the density
(individuals/km2) and summer growth rate of each
lemming species. We compared the estimated daily
predation rates to the maximum daily potential growth
rates of lemming populations as estimated in other
studies. Maximum growth rate was estimated at 1.97%
for brown lemmings (Batzli et al. 1980) and 2.27% for
collared lemmings (Gilg 2002). According to Stenseth
and Ims’ (1993) review of lemming demography, if we
assume that they suffer no mortality, that each adult
female produces seven offspring per month with a sex
ratio of 1:1, and that young females become mature at
about one month old (the most extreme values),
maximum potential growth rate of lemmings could be
as high as 2.44% per day (finite rate of increase for one
year: r¼ 8.88, assuming constant reproductive rate year
round). Although such extreme values probably never
occur in the wild, we used these three estimates to assess
if our conclusions were robust to the estimate chosen.
We examined if the summer lemming population
change was related to the annual percentage of
lemmings consumed daily by predators. For each year,
we calculated the percentage of population change for
both species using the density measured in early summer
and late summer (mid-August).
Statistical analyses
We used sigmoid functions (Eq. 1) to fit the numerical
responses (breeding densities expressed as BD and
number of fledglings produced per square kilometer
expressed as NFP) as provided by Gilg et al. (2006):
BDðor NFPÞ ¼ aN2=ðb2 þ N2Þ ð1Þ
where a is the asymptotic value of the curve, b is
lemming density at the inflexion point of the curve, and
N is lemming density per square kilometer in early
summer. We then fitted the same equations with the
lemming density measured at year t  1 to test if the
model would better fit the data with a time lag of one
year.
We used simple regressions to assess the relationship
between the proportion of collared lemmings in the diet
of the three main predators and the combined density of
both lemming species. We could not simultaneously
examine the effect of the abundance of each lemming
species separately because their early summer densities
were strongly correlated (Pearson correlation, r¼0.77, P
¼ 0.04, df ¼ 6; Fig. 1).
For the functional response, given that the main
avian predators were absent from the site at low prey
density, Type III curves did not improve the fit than the
simpler Type II curves (in terms of R2). We thus
present functional response curves (daily consumption
rates, expressed as DCR) with the Type II equation
(i.e., the simplest model; Eq. 2) provided by Gilg et al.
(2006):
DCR ¼ cN 0=ðd þ N 0Þ ð2Þ
where c is the asymptotic value of the curve, N0 is
lemming density per square kilometer, and d is the half-
saturation constant (i.e., the N0 value when DCR¼ c/2).
We estimated all parameters (a, b, c, and d ) by fitting
curves where the least-square residuals were minimized
iteratively. We performed analyses with the ‘‘nlin’’
procedure using the Gauss-Newton algorithm in SAS
release 9.2 (SAS Institute 2008). The ‘‘nlin’’ procedure in
SAS allows using a grid of starting values to avoid local
minima; therefore, the starting values for the estimated
parameters were a¼ 0.1 to 1 by 0.1 increments, b¼ 1 to
10 by 1.0 increments, c¼1 to 10 by 1.0 increments, and d
¼ 1 to 10 by 1.0 increments. We calculated a pseudo-R2
for nonlinear models as: 1  sum of square (residual)/
sum of square (corrected total). Results are presented as
mean 6 SE unless otherwise stated. The log scale has
only been used for graphical purposes.
The relationship between the summer population
change and consumption rate by predators was exam-
ined with a Pearson correlation coefficient. A problem
arose, however, in years where lemming density was
estimated by the minimum number alive (years of very
low abundance; two years for the collared and three
years for the brown lemmings) because summer popu-
lation change is likely to be poorly estimated in those
situations. We thus present the analysis with all years
and with only those where population density was
estimated with robust CMR methods.
January 2014 59AVIAN PREDATION IN THE TUNDRA
RESULTS
Small-mammal density
Both lemming species exhibited strong, rather syn-
chronized variations in density from one year to the
next, although the amplitude of fluctuations was much
greater in the brown lemming (Fig. 1). That species
reached peak densities in 2004, 2008, and 2010.
Numerical responses
We recorded a total of 30 Snowy Owl, 21 Rough-
legged Hawk, 98 Long-tailed Jaeger, 64 Glaucous Gull,
3 Peregrine Falcon, and 3 Parasitic Jaeger nests over the
seven years of the study. The breeding density of some
predators changed considerably in response to variation
in lemming density at time t, but not all of them (Fig. 2).
We observed strong numerical responses in the Snowy
Owl (a ¼ 0.13, b ¼ 224.2, F2,5 ¼ 41.2, P , 0.01) and
Rough-legged Hawk (a¼ 0.11, b¼ 29.9, F2,2¼ 18.4, P¼
0.05). The Long-tailed Jaeger also showed a strong
numerical response to variations in lemming density (a¼
0.92, b ¼ 46.1, F2,5 ¼ 34.5, P , 0.01) and reached the
highest densities among all avian predator species (0.92
nests/km2). Adding a time lag of one year to the
response to lemming density provided a much poorer fit
for all the relations described in this paragraph (all F ,
0.6, all P . 0.63). The other avian predators exhibited
no detectable response to an increase in lemming density
at time t or t  1 (Fig. 2).
With an increase in lemming density, the number of
fledglings produced per square kilometer increased
sharply in Snowy Owls (a ¼ 0.43, b ¼ 278.5, F2,5 ¼
38.4, P, 0.01), Rough-legged Hawks (a¼0.38, b¼27.8,
F2,2¼ 13.7, P¼ 0.07), Long-tailed Jaegers (a¼ 1.42, b¼
254.9, F2,5¼ 186.6, P , 0.01), and Glaucous Gulls (a¼
0.22, b ¼ 13.7, F2,2 ¼ 62.0, P ¼ 0.02), but remained
constant in Peregrine Falcons and Parasitic Jaegers (Fig.
3). Overall, for species exhibiting the strongest responses
in breeding numbers (Snowy Owl, Rough-legged Hawk,
and Long-tailed Jaeger), there was an average of 3.0 6
0.3 (n ¼ 18), 3.0 6 0.7 (n ¼ 5), and 1.0 6 0.1 (n ¼ 71)
young fledged per nest at the highest recorded lemming
density, respectively.
Functional responses
The proportion of collared lemming in the diet of all
three predators tended to vary with the overall lemming
density (for Snowy Owls, F1,42 ¼ 3.7, P ¼ 0.06; Rough-
legged Hawks, F1,9 ¼ 5.6, P ¼ 0.05; and Long-tailed
Jaegers, F1,29 ¼ 3.8, P ¼ 0.06; Fig. 4). Given the large
difference in lemming density (and most probably
availability) between the two species in years of peak
abundance (brown lemmings averaged three times the
density of collared lemmings), the proportion of collared
lemmings in the diet decreased sharply in those years.
Nonetheless, the proportion of collared lemmings in the
diet of all three predators remained higher than its
proportion in the overall lemming population at all
densities (Fig. 4). At low lemming density, collared
lemmings represented 82%, 61%, and 83% of the diet of
Snowy Owls, Rough-legged Hawks, and Long-tailed
Jaegers, respectively, whereas at high lemming density,
those proportions fell to 24%, 13%, and 8%.
We did not detect any increase in the daily consump-
tion rate of collared lemmings by Snowy Owls, Rough-
legged Hawks, and Long-tailed Jaegers with increasing
collared lemming density (all F , 6.2, P . 0.1; no
equation could be fitted to owls due to a decreasing
trend; Fig. 5). Average daily consumption of collared
lemmings by a breeding pair was 6.7 6 0.7 individuals (n
¼ 13) for Snowy Owl, 2.86 0.3 (n¼ 6) for Rough-legged
Hawk, and 2.1 6 0.8 (n¼ 8) for Long-tailed Jaeger (Fig.
5). Similarly, daily consumption rate of brown lemmings
did not vary according to its density in both Snowy Owls
and Long-tailed Jaegers (all F , 2.1, P . 0.21). Snowy
Owls consumed an average of 11.0 6 2.1 (n ¼ 13)
individual brown lemmings per pair per day, whereas
Long-tailed Jaegers consumed 6.5 6 2.1 (n ¼ 8)
lemmings. Daily consumption rate of brown lemmings
by Rough-legged Hawk breeding pairs increased grad-
ually with prey density and reached 9.5 individuals per
FIG. 1. Annual collared (Dicrostonyx groen-
landicus) and brown (Lemmus trimucronatus)
lemming density measured in early summer
(June/July) on Bylot Island, Canada (2004–
2010). The insert shows the linear relationship
between the two species.
J.-F. THERRIEN ET AL.60 Ecology, Vol. 95, No. 1
pair/d when brown lemming density reached 500
individuals/km2 (c ¼ 10.2, d ¼ 39.6, F2,6 ¼ 41.6, P ,
0.01; Fig. 5).
Total responses
Total consumption of collared lemmings by the three
main avian predators gradually increased as their
density increased and tended to stabilize around 3.0
individuals consumed daily/km2 above 100 individuals/
km2 (Fig. 6). Total consumption of brown lemming also
increased gradually with their density to level off around
8.2 individuals consumed daily/km2 above 500 individ-
uals/km2 (Fig. 6). It is noteworthy that the Long-tailed
Jaeger showed the highest consumption rate per square
kilometer of all avian predators for both lemming
species (consumption by the Snowy Owl, Rough-legged
Hawk, and Long-tailed Jaeger was 0.6, 0.3, and 1.9
collared lemmings/km2 at 100 collared lemmings/km2
and 1.2, 1.0, and 6.0 brown lemmings/km2 at 500 brown
lemmings/km2, respectively). This was mainly due to the
higher breeding densities of jaegers compared to the two
other species.
All three avian predators consumed a high proportion
of the summer lemming populations on Bylot Island.
Their combined daily predation rate exceeded the
maximum daily potential growth rates of both lemming
FIG. 2. Breeding density of avian predators (Snowy Owl [Bubo scandiacus], Rough-legged Hawk [Buteo lagopus], Long-tailed
and Parasitic Jaegers [Stercorarius longicaudus, S. parasiticus], Peregrine Falcon [Falco peregrinus], and Glaucous Gull [Larus
hyperboreus]) in relation to pooled lemming density (both species combined) in early summer on Bylot Island, Canada (2004–2010).
Significant relationships are shown.
January 2014 61AVIAN PREDATION IN THE TUNDRA
species over a wide range of recorded densities,
suggesting a control of those species by predation (Fig.
7). The shapes of the curves were similar between the
two lemming species, as predation rate increased to
reach a peak value at intermediate prey densities and fell
at higher densities. However, predation rate peaked at
lower density and reached a higher maximum value for
collared than brown lemming. Total daily predation rate
fell below the maximum potential growth rate of
lemmings only at around 125–135 and 325–410 individ-
uals /km2 for collared and brown lemmings, respective-
ly. Such values were not reached in collared lemming,
although it was encountered twice in brown lemming
during the study period.
Average summer population change was 0.5% 6
0.5% for collared lemmings and 0.8% 6 0.4% for brown
lemmings over the seven years of the study (when using
only population estimates based on CMR, these values
were 0.8% 6 0.7% and 0.1% 6 0.4%, respectively).
Summer lemming population change was negatively
associated with the estimated daily predation rate by
avian predators, although not significantly (for collared
lemming, r¼0.41, P¼ 0.37, df¼ 5; brown lemming, r¼
0.44, P ¼ 0.32, df ¼ 5; Fig. 8). The association was
stronger when using only data points derived from
CMR, although still not significant (for collared
lemming, r ¼0.74, P ¼ 0.16, df ¼ 3; brown lemming,
r¼0.63, P ¼ 0.37, df¼ 2; Fig. 8).
FIG. 3. Reproductive success (number of fledglings produced) of avian predators in relation to pooled lemming density (both
species combined) in early summer on Bylot Island, Canada (2004–2010). Significant relationships are shown.
J.-F. THERRIEN ET AL.62 Ecology, Vol. 95, No. 1
DISCUSSION
As expected, the main avian predators (Snowy Owl,
Rough-legged Hawk, and Long-tailed Jaeger) responded
to local variations in lemming density by exhibiting
strong numerical responses without any obvious time
lag. In contrast with our second hypothesis, we did not
detect any clear increase in consumption rates of brown
or collared lemmings by the three main predator species
with an increase of each respective prey density, except
for consumption of brown lemmings by Rough-legged
Hawk in response to variations in this prey species. Our
ability to detect a functional response by these predators
was, however, limited by the relatively narrow range of
prey density over which consumption rate could be
measured in the field. Nevertheless, measured predation
pressure by the dominant avian predators, Snowy Owls,
Rough-legged Hawks, and especially Long-tailed Jae-
gers, suggests that it has the potential to limit lemming
populations during the snow-free period on Bylot
Island, which supports our third hypothesis. These
observations are in accordance with previous studies
FIG. 4. Proportion of collared lemmings in the diet of the
three main avian predators (solid circles and solid lines) and
proportion of collared lemming in the overall lemming
population (open circles and dashed lines) in relation to the
density of lemming (both species combined) in early summer on
Bylot Island, Canada (2004–2010).
FIG. 5. Daily consumption rate by breeding pairs of the
main avian predators in relation to daily density of brown and
collared lemmings on Bylot Island, Canada (2007–2010). Open
circles represent collared lemmings, whereas solid circles and
the solid line represent brown lemmings. Significant relation-
ships are shown.
January 2014 63AVIAN PREDATION IN THE TUNDRA
conducted in the central Canadian Arctic where the
collared lemming was apparently continuously main-
tained at low density by predators during summer time
(Reid et al. 1995, 1997).
Even though up to six avian predators may occur at
our study site, our analysis focused primarily on the
three most abundant species. Peregrine Falcons, Glau-
cous Gulls, and Parasitic Jaegers are additional preda-
tors known to prey upon lemmings to some extent
during the breeding season (Pitelka et al. 1955, Gilchrist
2001, White et al. 2002, Legagneux et al. 2012), but none
of them showed any aggregative numerical response to
lemming densities and their densities were relatively low,
except for the Glaucous Gull (Figs. 2 and 3). Failure to
include these species in our estimation of the overall
predation rate should not have changed much our
conclusions on predation patterns. Nonetheless, it
probably rendered our evaluation of the impact of
predators on lemming populations somewhat conserva-
tive.
Despite the very high potential growth rate of the
species, lemming populations remained fairly stable or
decreased during the summer in most years, which is
consistent with the high predation pressure recorded at
our study site. Although the small sample size and the
methods used to estimate population size at low density
limited our ability to detect statistically significant
relationships, the summer population change of both
lemming species appeared negatively associated with the
estimated predation intensity by avian predators.
However, several other factors may contribute to the
variability in summer population change, and longer
time series would be needed to confirm such trends.
Spatial heterogeneity in predation pressure and popula-
tion growth rate at the landscape scale may contribute to
variation in lemming population change. Moreover,
predation rate by other predators (especially arctic fox
and stoat) can be a major source of annual variation in
summer population change because these species also
have the potential to strongly influence lemming
population dynamics (Gilg et al. 2006, Bilodeau 2013).
A combination of factors may contribute to the high
lemming predation rates by avian predators that we
observed during the snow-free period. First, the open
landscape and scant cover characteristic of the tundra
environment may provide few refuges for small mam-
mals during the snow-free period, thereby increasing
their vulnerability to predation (Ims and Andreassen
2000). Second, the diverse suite of predators present on
the tundra and their associated diverse hunting behav-
iors may further increase the vulnerability of lemmings.
Finally, subsidies acquired from adjacent ecosystems or
the presence of alternative prey species (Henden et al.
2010, Gauthier et al. 2011, Therrien et al. 2011, Giroux
et al. 2012) may help to maintain the populations of
some predators at higher levels than autochthonous
resources would allow in this relatively low productivity
environment. However, the latter phenomenon is not
unique to Bylot Island and may actually be widespread
across the Arctic, especially in North America (Gauthier
et al. 2011).
Overall, the collared lemming suffered a higher
predation rate than the brown lemming and its
population generally declined during the summer (i.e.,
negative growth rate). Proportion of collared lemmings
in the diet of the three main avian predators decreased
when lemming density increased, most likely because in
years of high abundance, the brown greatly outnum-
bered the collared lemming. Nonetheless, the collared
lemming was most often consumed in a greater
FIG. 6. Total daily lemming consumption by the three main
avian predators in relation to the density of each lemming
species in early summer on Bylot Island, Canada (dashed line
represents collared lemmings while solid line represents brown
lemmings; 2004–2010).
FIG. 7. Daily predation rate (percentage of the lemming
population consumed) by avian predators in relation to the
density of each lemming species in early summer on Bylot
Island, Canada (dashed thick line represents collared lemmings,
while solid thick line represents brown lemmings; 2004–2010).
The horizontal lines represent various estimates of maximum
daily potential growth rate of collared lemming (dashed thin
line ¼ 2.27%), brown lemming (solid thin line ¼ 1.97%), and
lemming spp. (dotted line¼ 2.44%; see Materials and methods:
Total responses).
J.-F. THERRIEN ET AL.64 Ecology, Vol. 95, No. 1
proportion than their relative availability in the overall
lemming population, suggesting a selection toward this
species. Those differential predation rates may be a key
factor explaining the divergent population dynamic
observed in these two species when they occur in
sympatry (Gruyer et al. 2010, Krebs et al. 2011). Indeed,
on Bylot Island, the collared lemming seldom reaches
densities higher than 125 individuals/km2 in contrast to
Greenland, where it is the only lemming species present
and where densities can be as high as 1000 individuals/
km2 in a peak year (Gilg 2002, Gilg et al. 2003). Our
results suggest that the two lemming species are
influencing the other population, either through direct
competition (Morris et al. 2000), or perhaps more likely
indirectly via apparent competition due to shared
predators (Holt 1977), with the collared lemming
apparently being more vulnerable to avian predation.
By attracting large densities of avian predators during
population outbreaks, the brown lemming would
contribute to further depress collared lemmings and
keep their populations at relatively low densities.
Our conclusions are limited to the range of lemming
densities encountered during the study period. A
legitimate question to ask is whether lemmings could
escape from this apparent regulation by avian predators
at low to intermediate density and become limited by
other factors like food resources, as suggested in other
studies (Pitelka and Batzli 2007). The numerical
aggregative responses that we recorded for the main
avian predators eventually leveled out, as evidenced by
the asymptotic curves observed in most species, possibly
due to territoriality. Because lemming reproduction
starts under the snow and predation by birds is likely
to be weak when the snow cover is present, lemmings
could reach densities in early summer that are already
beyond the range over which limitation by avian
predators could occur. This is apparently not the case
in collared lemmings as densities have never exceeded
;125 individuals/km2 at our study site. However, brown
lemmings densities up to 1000 individuals/km2 or more
have previously been recorded at our study site
(Bilodeau et al. 2013a), which is beyond the value up
to which limitation by avian predators occurred in this
study (up to 325–410 individuals/km2). If brown
lemming density exceeds such threshold in early summer
in some years, this could allow them to maintain positive
population growth during the summer despite the high
consumption rate of avian predators. Therefore, the role
of avian predation in the regulation of lemming
population dynamic could be modulated by factors
influencing their population growth rate during the long
winter period from October to May (e.g., quality of
snow cover; Bilodeau et al. 2013a). On the other hand, it
is also possible that avian predators could still increase
their numerical reproductive responses, and hence, their
predation pressure if resource levels were higher. Indeed,
over the range of lemming density recorded during the
study period, the three main avian predators apparently
did not reach their maximum reproductive capacity and
the average fledgling numbers per nest that we recorded
during years of high lemming abundance were lower
than the maximum reported for those species (Parmelee
1992, Bechard and Swem 2002, Wiley and Lee 1998).
Finally, mammalian predation was not taken into
account and any lemmings consumed by predators such
as the arctic fox and the stoat should be additive to those
taken by avian species. Using a mass balance model,
Legagneux et al. (2012) recently showed that the
combined consumption rate of avian and mammalian
predators was sufficient to limit at low density the
annual population of collared lemming at our study site.
In conclusion, the combined predation pressure
exerted without delay by avian predators is likely
sufficient to limit lemming populations at low levels
during the snow-free period over a wide range of
densities in the Canadian Arctic. This situation may
thus be similar to the ones previously reported for
collared lemmings in Greenland (Gilg et al. 2006) and
FIG. 8. Relationship between summer population change
and estimated predation rate (percentage of the lemming
population consumed daily) by avian predators for (a) collared
lemmings and (b) brown lemmings on Bylot Island, Canada
(2004–2010). Open circles represent estimates using minimum
number alive (MNA), and solid circles represent estimates using
capture–mark–recapture (CMR; see Materials and methods).
January 2014 65AVIAN PREDATION IN THE TUNDRA
voles in the boreal forest (Korpima¨ki 1985, Korpima¨ki
and Norrdahl 1989, 1991a, Ims and Andreassen 2000).
Our study adds to the growing evidence that mobile
avian predators, in combination to resident mammalian
predators, may drive the population dynamics of small
mammals in many parts of the tundra (Reid et al. 1997,
Gilg et al. 2003, Ims et al. 2011, Legagneux et al. 2012).
ACKNOWLEDGMENTS
We are grateful to the many people who helped us with field
work, especially V. Lamarre, G. Ouellet-Cauchon, M. Sirois,
and J. Tremblay. F. Barraquand, C. Cloutier, F. Doyle, O.
Gilg, C. J. Krebs, D. Reid, and J. P. Tremblay provided
constructive comments on earlier versions of the manuscript.
We also thank the community of Pond Inlet, the Joint Park
Management Committee of Sirmilik National Park, and Parks
Canada’s staff for their assistance. This study was funded by the
International Polar Year program of the Government of
Canada, the Natural Sciences and Engineering Research
Council of Canada (NSERC), the Fond Que´be´cois de
Recherche sur la Nature et les Technologies (FQRNT), the
Garfield-Weston Foundation, the Network of Centre of
Excellence ArcticNet, and the Polar Continental Shelf Program.
This is Hawk Mountain Sanctuary contribution to Conserva-
tion Science number 225.
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