Discussion
Our study identified strong direct and indirect effects of active,
seeking predators (weasels) on arboreal rodent presence, activity, and
survival at nest platforms. Arboreal rodents, primarily tree voles, were
killed most frequently by weasels and their activity several weeks post
weasel-detection remained depressed. Secondary nest predators, thrushes
and jays, probed and dug out nests in apparent pursuit of invertebrates
in discarded and decaying nest materials of tree voles, and were
positively correlated with flying squirrel presence, perhaps indicating
that flying squirrels were attracted to nest disturbances (Forsman &
Swingle, 2007).
Predator foraging mode can strongly influence the timing and location
where prey are killed. In our study, weasels (i.e., active, seeking
predator) were the strongest nest predators whereas owls and flying
squirrels exhibited comparatively weak effects at prey nest sites. Owls
were detected at similar rates as weasels but may simply be ineffective
nest predators, unable to reliably enter or drive tree voles from their
nests. Our inferences were limited to nest platforms in young forests
and did not extend to foraging tree voles or to the old forests in which
strong relationships between tree voles and one of their main predators,
the northern spotted owl (Strix occidentalis caurina ), have been
established (Forsman, Anthony, Meslow, et al., 2004). Nonetheless, our
results provide evidence that tree voles face strong pressure from
weasels at nests and owls while tree voles are foraging (Forsman, 1974;
Swingle et al., 2010).
Although foraging mode may have differed, diel activity patterns of
predators broadly overlapped those of tree voles except for diurnally
active digging birds. Weasels can be active throughout the day (Linnell,
Epps, Forsman, & Zielinski, 2017) but appeared to be more effective at
capturing tree voles in the morning hours (Fig. 3b), a pattern similar
to least weasels (M. nivalis nivalis ) which were more active at
sunset but captured most Microtus field voles in the morning
(Sundell, Norrdahl, Korpimäki, & Hanski, 2000). Determining if this
reflects a temporal vulnerability of prey will require additional
studies, including where and how weasels use cues to locate arboreal
prey.
Weasels can cue into rodent scent when hunting, and scent can accumulate
at or near small rodent nests and is hypothesized to increase predation
risk (Sharpe & Millar, 1990; Ylönen, Sundell, Tiilikainen, Eccard, &
Horne, 2003). Female tree voles may be especially at risk of nest-site
mortality because they have high fidelity (typically only one nest used
per month) to nests that they invest substantial effort into building,
resulting in extensive structures (0.06 m3) (Swingle
2005; Sharpe and Millar 1990). Large, old tree vole nests typically
contain multiple tunnels and chambers within layers of soil, providing
shelter and escape routes from predators (Maser, 1966). The relative
tradeoffs of long-term habitation with predation risk from predators
cuing into accumulated scent remains unknown but the higher visitation
rates by weasels after year three in our study indicates a response of
these predators to prolonged tree vole occupancy of nests. Whether this
was due to a functional response to environmental cues such as scent or
to numerical response of the predators is unknown, but indicates
predation risk can limit long-term population growth of tree voles
regardless of an increase in resource availability (i.e., new nests).
Homogeneity of nest platform placement could have provided a visual cue
to avian nest predators (Santisteban, Sieving, & Avery, 2002) although
vertical placement within the live tree canopy was broadly
representative of natural nest substrates found in young forests
(Linnell et al., 2018; Swingle, 2005). In contrast, older forests have
much higher heterogeneity in tree height and natural substrates for tree
vole nests vary in type (Lesmeister & Swingle, 2017), location within
the canopy, and may be more numerous (Swingle, 2005). Moreover, higher
nests in a more heterogenous environment may disperse scent, decoupling
cues from terrestrial predators. These characteristics of tree vole
nests in old forest—more numerous nest substrates, varied height,
size, and substrate—may make those nests more difficult to locate for
predators using visual or olfactory cues.
Predators can effectively reduce resource availability for prey through
non-lethal avoidance and non-lethal effects can be of higher magnitude
than direct consumption, an effect closely tied to prey population
densities (Preisser et al., 2005). In the case of weasels in our study,
we observed potentially lethal effects followed by reduction of activity
(a non-lethal effect) by tree voles for up to several weeks post weasel
detection. Most weasel detections occurred towards the end of our study,
limiting our inferences with regards to longer-term non-lethal effects
of weasel presence on tree vole nest platform occupancy. But given the
limited nest substrate availability in young forests, removal of even
several productive nest substrates through predation followed by
non-lethal avoidance could cause a substantial limit on tree vole
populations. Continued monitoring of nest platforms to assess long-term
lethal and non-lethal effects could provide a measure of the effect nest
predators have on limiting tree vole populations in young forests.
The relative degree of specialization of predators can determine their
functional response to numerical increases in their prey (Sundell et
al., 2000). Least weasels, similar-sized to short-tailed weasels in our
study, show a type II functional response to higher densities of field
voles (rapid initial increased predation rate with prey density) in
boreal ecosystems with a lower diversity of prey available (Sundell et
al., 2000). In temperate forests weasels have access to a higher
diversity of prey but specialization depends on sex and age of weasels
with adult females typically the most specialized (King & Powell,
2007). Weasels seem unlikely to exhibit a type II functional response to
tree voles, particularly because tree voles do not reach sufficiently
high densities to elicit such a response and functional response of
weasels may be more similar to a generalist predator (type III) than a
specialist (type II) with regards to tree voles (Sundell et al. 2000).
We observed a marked difference in model strength and direction at our
finest temporal grain size (1-hour bin-width) compared to coarser
bin-widths (1-day and 1-week), which could dramatically affect
interpretation of the observed species interactions. Weasels clearly
exhibited the strongest indirect (reduction in tree vole activity) and
direct (predation) effects on tree voles but in models using 1-hour
bin-widths these effects were indistinguishable from other species and
the direction of the relationship was negative, opposite that of models
with coarser bin-widths. Using multiple bin-widths provided additional
insights into predator-prey interactions. For example, the lack of
positive correlations of weasels and tree voles at 1-hour bin-widths
indicates that weasels were unlikely to have visually cued into tree
vole activity as they did not overlap directly the exact hours in which
tree voles were detected even though our sampling schedule (1 photo per
minute) should have been more than adequate to detect such overlap. For
the predator-prey interactions that we observed in our study, temporal
grain sizes appeared to have strong effects in interpretation of model
output particularly at the finest temporal grain.
Our models were likely inadequate at detecting weak non-lethal
interactions occurring over longer time periods, such as potential
interference competition between flying squirrels and tree voles. Flying
squirrels were ubiquitous but weak lethal predators of tree voles at
nests killing them at a rate of 0.03% (n = 2 observed
mortalities) compared to the 10% (n = 8 observed mortalities)
predation rate of weasels (Table 1). Nonetheless, the observed weak
decrease in tree vole activity up to several weeks after detection of a
flying squirrel (Fig. 3b) providing circumstantial evidence that flying
squirrels exhibit competition with tree voles, albeit weak and
potentially lagged and further evidence would be needed to corroborate
this observation.
Our technique of artificial marks and visual recaptures using multiple
remote cameras at each site appeared to function well for females, but
this technique may have been less effective for males which have lower
nest fidelity (and conversely, higher local emigration rates; Swingle
2005). Furthermore, our hair clipping technique was effective, but
limited the temporal extent of visual recaptures as fur grew back,
obscuring our marks. This technique, narrowly applied to monitoring
nests of high nest fidelity animals such as female tree voles, may
provide accurate estimates of apparent survival as emigration is
expected to be relatively low and observations of nest predators can
corroborate the fate of marked individuals.
Tree voles responded with strong population growth in 2016 1-year after
addition of nest platforms (Linnell et al., 2018). Herein we
demonstrated that predator activity increased over a 3-year monitoring
period and had strong direct effects on tree voles at nest platforms.
The success or failure of nest-box and nest platform to increase prey
population size may ultimately depend on longer term predator-prey
dynamics inherent to the cover types in which artificial nest substrates
are placed (Sonerud, 1985). Our evidence indicates that predators,
particularly weasels, can exert strong acute effects on tree vole
activity at nests in young forests. Determining whether predators in
young forests represent a substantial limit to tree vole populations as
compared to old forests per se, will require additional monitoring,
ideally of naturally occurring nest substrates or nest platforms (or
both) in old forests.