Herbivory mediated canopy-to-soil fluxes and their controls
Our results showed that BIH constitute a minor fraction
(~1.6 %) of the annual soil input of organic matter
from the birch canopies, in line with our hypothesis
(H1). These rates are similar to the estimates of insect
herbivory in dwarf shrub tundra (Barrio et al. 2017), but lower than
ecosystems at lower latitudes (Kozlov et al. 2015, Galmán et al. 2018).
Despite the relatively short recurrence interval of insect population
peaks of about 10 years (Jepsen et al. 2008), major outbreaks only
return to the same site every ~50-100 year (Tenow and
Bylund 2000). Thus, the low contributions to fluxes at low insect
densities may cumulatively recycle similar or larger amounts of elements
than the major outbreaks, where most of the leaf area is lost, but it is
much less disruptive to the ecosystem. Further, as background densities
may increase with future climate warming (Kozlov et al. 2015, Galmán et
al. 2018), BIH may increase in overall importance for nutrient cycling.
The variation in insect herbivory level across our sites was
considerable, with leaf area loss at some sites of up to 7%. When the
nutrient resorption during leaf senescence (~55% N,
~30% P) was accounted for, the average
herbivore-mediated fraction of the annual soil input was slightly higher
than for C (~3.5% N and ~2.5% P), yet
still a relatively small contribution. Nonetheless, at the sites with
the highest herbivory levels, this corresponded to ~14%
and ~9% of annual N and P fluxes, respectively. These
estimates of herbivory mediated fluxes may be in the low end, as our
estimated mean N resorption efficiency of 55% was lower than what has
previously been found in these forests (~70 %, Nordell
and Karlsson 1995). This suggests an even larger gap between the
substrate quality of litter and insect deposits. The higher substrate
quality (availability to soil decomposer microbes) of insect deposits
compared to litter (Kristensen et al. 2018) may trigger increased soil N
and C-turnover early in the season. Yet, these belowground responses to
BIH are most likely within the ranges of what the soil biota can take up
and keep within the ecosystem, and so are unlikely to cause nutrient
losses, in contrast to outbreaks which can cause substantial nutrient
losses from the soil (Lovett et al. 2002, Kristensen et al. 2020).
The positive relationship between herbivory and leaf N-concentration in
the green leaves was in line with our expectations (H2),
suggesting that leaves of higher nutritive quality suffer greater
herbivore damage, with no apparent effect of foliar condensed tannin
concentration. Moreover, the strong negative relationship between leaf N
content and condensed tannins (linear regression w. CT:C
log-transformed, p<0.001) corroborates the theory of Haukioja
(2003) predicting that it is only beneficial for the plants to increase
the content of defence compounds when the nutritive quality of the
leaves is low. Only under such conditions will the insects eat large
enough amounts of the leaves to encounter a negative effect from the
tannins. We note that our measurements of leaf condensed tannin content
were quite low compared to some other literature observations from
similar trees and ecosystems (Paaso et al. 2017; Stark et al. 2007).
This may be partly due to large variation between sampling years,
genotypes, and responses to other regulators than herbivory, such as
soil nutrient content and photochemical conditions (Madritch and
Lindroth 2015, Rubert-Nason et al. 2015).
The significant increase in insect herbivory with relative position
above the valley bottom, i.e. towards the treeline, was in line with our
expectations (H3) derived from the patterns found for
outbreaks (Hagen et al. 2007), and previous indications from studies of
non-outbreak conditions in subarctic Finland (Virtanen and Neuvonen
1999). Yet, this is, to our knowledge, the first time a significant
effect has been shown for background herbivore densities. Nonethless,
the mechanisms remain unclear. The proposed drivers of the patterns –
higher parasitism in valley bottoms during the summer and eggs being
killed by extremely cold air masses creeping into valley bottoms during
the winter (e.g. Virtanen and Neuvonen 1999) – are confounded by the
consistent increase in leaf N content with local elevation. Yet, if
foliar chemistry was the paramount driver of BIH across scales, the N
concentration should show a neutral-negative trend with elevation at the
regional scale. In contrast, the leaf N content also increase with
elevation at the regional scale, although the relationship is weaker
than at the local scale as should be expected (Read et al. 2014). Thus,
abiotic drivers, e.g. climate, are likely moderating the biotic
relationships at the regional scale.
The local increase in herbivory with elevation found here contrasts with
the more general decrease with elevation along individual transects
across the World’s woody species (Galmán et al. 2018). This suggests
that the proposed responsible mechanisms in subarctic mountain birch
landscapes may only apply to high-latitude systems. Thus, our study
serves as a great example of how global generalisations may lead to
wrong assumptions in certain ecosystems highly important for the global
climate. Interestingly, we found no significant relationship between BIH
and the most commonly studied climate variables, temperature and
humidity, nor with a commonly used climate proxy, absolute elevation
(Table 2). Instead, solar radiation was a marginally significant
positive predictor of BIH, which may suggest that this is in fact a
better integrator of relevant abiotic conditions, when working in
mountainous landscapes. This should be particularly relevant to consider
at high latitudes, where sun-angles are low, yielding a particularly
marked difference in solar energy input between north- and south-facing
slopes in steep-sided valleys (~50 % higher annual
solar radiation on south-facing slopes in our dataset, e.g. N8 compared
to N7, Figure 1). Hence, our data point to the potential value of
including solar radiation as an abiotic predictor of ecological
characteristics in other landscapes with complex topography.