Introduction
Herbivores have important effects on elemental cycling in terrestrial
ecosystems (Bardgett and Wardle 2003, Schmitz et al. 2018). Most
attention has been given to vertebrates, but insect herbivores can exert
a similar or even stronger control on ecosystem functioning than mammals
(Risch et al. 2018, Kristensen et al. 2020), particularly in forest
ecosystems, where their impact is likely to intensify substantially with
global change (e.g. Logan et al. 2003).
Studies on insect herbivory in high-latitude forests have hitherto
emphasised the importance of outbreaks (e.g. Jepsen et al. 2013, Sandén
et al. 2020), especially as some species are increasing their ranges
into new areas with climate warming (Jepsen et al. 2008, 2011). However,
non-outbreak, low-intensity rates of insect herbivory, termed background
insect herbivory (BIH), has attracted increasing attention in recent
years (Kozlov and Zvereva 2017). Although BIH at high latitudes is
generally low - 1-2 % of the leaf area (Barrio et al. 2017) compared to
the global average of ~8% (Kozlov et al. 2015) - the
rate will likely increase at high latitudes with global warming (Kozlov
et al. 2015), despite the observation that insect predation and
parasitism also increase with temperature (Virtanen and Neuvonen 1999,
Roslin et al. 2017). It has been argued that BIH, despite the small
annual contribution, may be more important for long-term ecosystem
functioning in a wide range of globally important ecosystems, including
tropical (Metcalfe et al. 2014), boreal (Zvereva et al. 2012, Metcalfe
et al. 2016), and arctic systems (Barrio et al. 2017).
The fact that most of the global terrestrial soil C is stored at high
latitudes (Hugelius et al. 2014), where global warming is most
pronounced (ACIA 2004), makes it particularly important to understand
perturbations in this region. While low productivity ecosystems dominate
at high latitudes (Higgins et al. 2016), subarctic birch forests
constitute a relatively productive ecosystem (Sjögersten and Wookey
2009). Therefore, perturbations in birch forests may exert
disproportionately large impacts on regional biogeochemical cycling. The
end consequences of herbivory, by primarily the geometrid mothsEpirrita autumnata and Operophtera brumata, have been
demonstrated in terms of plant traits (Haukioja 2003; Karlsson et al.
2004), plant (Jepsen et al. 2013, Sandén et al. 2020) and soil community
composition (Saravesi et al. 2015, Parker et al. 2016, Kristensen et al.
2018), soil nutrient and carbon (C) turnover (Kaukonen et al. 2013,
Parker et al. 2016, Kristensen et al. 2018, Sandén et al. 2020), and
photosynthetic C-fixation (Heliasz et al. 2011, Bjerke et al. 2014), but
quantification of the key mechanism driving these changes - canopy to
soil fluxes of C, N and P through insect deposits - is still lacking.
Elements channelled through insects are not a novel element input to the
ecosystem, but rather an alternative pathway of transferring high
quality organic matter from the canopy to the soil in the early growing
season rather than the usual transfer of senesced litter by the end of
the season. Most studies indicate that N is the main plant
growth-limiting nutrient in most forest systems (e.g. LeBauer and
Treseder 2008), but an increasing body of literature suggests that P is
co-limiting plant growth (Vitousek et al. 2010, Sundqvist et al. 2014).
Further, nutrient limitation will become even more widespread in the
future due to warming and CO2-fertilisation, which may
weaken the terrestrial ecosystem C-sink (Fisher et al. 2012, Wieder et
al. 2015). Therefore, it is relevant to assess the amounts of both N and
P channelled through labile insect deposits and recalcitrant litter
respectively. Insect deposits contain much larger amounts of nutrients
compared to senesced litter (e.g. Kristensen et al. 2018) because
insects feed on green leaves before the highly conservative Subarctic
birches resorb up to ~70 % of their nutrients during
senescence (Nordell and Karlsson 1995). Thus, the balance of elemental
transfer between the litter and insect pathways regulate the timing and
quality of soil substrate inputs, which can in turn lead to both
increased and reduced soil C and nutrient turnover (Parker et al. 2016,
Kristensen et al. 2018, Sandén et al. 2020).
N is also the growth-limiting nutrient for the moths in our study system
(Metcalfe et al. 2019). The foliar content of N is therefore expected to
be an important driver of moth success, hence BIH level. In order to
conserve nutrients from herbivores, host plants may increase the level
of foliar chemical defence compounds (Haukioja 2005, Fürstenberg-Hägg et
al. 2013). For example, the leaf content of bioactive specialised
compounds, such as condensed tannins (CT), has been found to increase in
leaves subjected to herbivory (Fürstenberg-Hägg et al. 2013). Yet, the
relationship between herbivory and plant defence compounds is not simple
in natural systems. In fact, geometrid moth species in subarctic birch
forests are rather tolerant to the birch chemical defence compounds
(Haukioja 2003, 2005). Therefore, it is only relevant for the birch to
pursue this defence strategy when the growth-limiting nutrient level in
the leaves is so low that the insects have to eat large amounts of
foliage to compensate for low nutrient concentrations (Haukioja 2003).
Thus, a negative relationship between the foliar content of the moth
growth-limiting nutrients and foliar defence compounds should be
expected at ecosystem scale.
Apart from the links to foliar chemistry, BIH also varies with climate,
with an expected increase with warmer temperatures in mid-high latitude
systems (Kozlov et al. 2015, Barrio et al. 2017, Galmán et al. 2018).
Nonetheless, moth outbreaks most often appear close to the treeline in
birch forests across subarctic Scandinavia rather than in valley
bottoms, probably due to the higher likelihood of winter temperatures
below their egg survival limit (< -35-37 °C) along the valley
bottom due to thermal inversion of air masses during winter (Ruohomäki
et al. 1997, Hagen et al. 2007), and/or higher parasitism during the
summer (Virtanen and Neuvonen 1999). Yet, such decrease in top-down
controls on herbivory at higher local elevation may be confounded by
decreasing bottom-up controls. For example, the food quality (leaf N
content) is also expected to increase with elevation (Körner 1989, Read
et al. 2014). Nonetheless, no systematic increase in BIH with the local
elevation above the valley bottom has been found previously (Virtanen
and Neuvonen 1999), and such an increase would oppose the overall
elevational decrease in herbivory at the global scale (Galmán et al.
2018).
In this study, we quantified BIH on the mountain birch (Betula
pubescens ssp. czerepanovii (Orlova) Hämet-Ahti) along 9
elevation gradients in Subarctic birch forests spanning a considerable
portion of the environmental variation in the Fennoscandian mountain
birch forests. We estimated the canopy-to-soil fluxes of C, N and P per
unit ground area in litter and insect deposits and compared them to
other relevant sources of soil input of the same elements. We also
evaluated the dependence of BIH and the resulting elemental fluxes on
leaf chemistry, climate, elevation and relative position over the valley
bottom to identify potential abiotic and biotic drivers. Our setup with
multiple gradients spanning a larger regional elevational gradient
allowed us to test the universality of relationships between elevation
and foliar loss to herbivory. We hypothesised that:
(H1) Elemental fluxes : The BIH levels in
subarctic birch forests are minor compared to lower latitude systems,
and consequently the annual contribution of nutrients to the soil
through this channel is much smaller than other internal (i.e. recycling
from litter) and external sources (i.e. fixation, deposition,
weathering).
(H2) Biotic controls : The BIH level increases
with concentration of leaf N, which is the growth-limiting nutrient in
the system. Consequently, we expected no strong relationship with leaf
condensed tannin concentration, as this only play a role as a defence
compound at low N-levels, where we already expected low foliar loss to
herbivory. Moreover, we hypothesised that the importance of insect
herbivores for channelling nutrients from the canopy to the soil would
increase with stronger foliar nutrient resorption, as this would
decrease the transfer of nutrients through senesced litter on annual
basis.
(H3) Abiotic controls : We expected a local scale
increase in BIH with the relative position above the valley bottom along
each transect towards the treeline, due to decreasing likelihood of
extreme winter cold and summer parasitism, which are both strongest in
the valley bottom. Yet, we also expected an overall BIH level increase
with site temperature, as insect herbivory levels are generally higher
in warmer mid-latitude systems, but this effect may be substantially
weakened by the expected local elevational increase in BIH.