Discussion
Our results based on EDM modelling provide several new insights on joint
effects of insect herbivory and climate as drivers of annual willow
growth. First, our results support the prediction that negative effects
of insect herbivory on shoot growth intensify along with effects of
warmer conditions of growing season. However, contrary to our
expectation, the effects of warming summer conditions on annual shoot
growth were generally, on net, negative, although effects tended to
become either less negative or weakly positive under warmer conditions,
especially in experimental treatments that included vertebrate
herbivores. Second, supporting our expectations, dynamic effects of
insect herbivory and climate on shoot growth depend on vertebrate
browsing and ramet age. In particular, the negative impact of insect
herbivory is weaker on young ramets, while vertebrate browsing tended to
enhance insect herbivory effects. Jointly, these results from a
long-term experiment and EDM markedly advance our understanding of
context-dependent effects of climate and herbivory on shrub growth at
forest-tundra ecotones.
The finding that the negative effect of insect herbivory on shoot growth
becomes more intense under warmer climates provides support for earlier
studies suggesting that at more northerly latitudes, higher summer
temperatures extend the summer season and increase the thermal budget
for growth and reproduction insect herbivores, and it could result in
increasing herbivory (Bale et al . 2002; see also Lehmann et
al . 2020). It is also compatible with findings from an experimental
system, in which O’Connor (2009) found that increasing temperature
increased per capita interaction strength between macroalgae and their
grazers, and reversed positive effects of temperature on plant growth.
Barrio et al . (2016), however, found that a cold-adapted
caterpillar performed worse under warmer conditions in the tundra.
Therefore, it is still uncertain how insect herbivory levels will change
under climatic warming as well as to what extent insect herbivory can
modify climate-growth relationships.
Our finding of negative effects of warming on shoot growth, at least
under cooler conditions, although somewhat counter-intuitive, could
potentially be a result of the net balance between increasing
respiration costs vs. faster overall growth and photosynthetic rates.
Although photosynthesis rates generally increase faster than tissue
growth rates – leading to an overall positive increase in growth with
temperature – these changes depend strongly on the timing of the
warming and the physiology of the plant (Grace et al . 2002). For
example, in cropping systems, increased night time temperatures can have
strong negative impacts on growth and yield due to a disproportionally
large increase in respiration rates (Mohammed & Tarpley 2008). Similar
imbalances would explain why growth under the herbivory treatments was
generally bolstered by warming (where growth was presumably focused on
edible tissues such as leaves and buds, which also contribute to
photosynthesis), whereas warming effects were more strongly negative in
the rejuvenation treatments (where growth presumably also included large
amounts of structural tissue). Additionally, it is possible that in the
coldest soils, root systems have strongly limited nutrient uptake
activity (Havraneck 1972; Day et al . 1989) and cold conditions
further decrease sink strength (Hoch & Körner 2003).
Importantly, our EDM analyses of long-term time series data on shoot
growth reveal that growth dynamics are not a simple function of summer
thermal conditions, but rather are highly context dependent, and vary as
a function of herbivory and plant age. Our results are generally
compatible with results of the meta-analysis of Arft et al .
(1999) who found that deciduous shrubs exhibited weak growth responses
to short-term experimental warming. They proposed that deciduous shrubs
such as Salix may have a tight control of meristem activity,
which may limit their response or ability to respond quickly to warming.
Based on our results, we find it likely that vertebrate browsers change
meristem activity of buds, and thus either stimulate or inhibit shoot
growth and thus influence shoot growth-climate relationships. We find
further evidence that young and old ramets differ in their inherent
growth dynamics (see also Wijk 1986). In other studies, Vuorinenet al . (2020) found that pine growth reduced at high browsing
pressure and warm climate conditions and Marshall et al . (2014)
reported that woody vegetation responses to shifts in browsing pressure
can depend on plant age. Also, the continuum ontogenetic response model
(Massad 2013) predicts that plant herbivore responses can vary depending
on plant age. Therefore, there is a growing body of empirical and
theoretical evidence pointing out that climate and insect herbivory
effects on tundra shrub growth dynamics will necessitate jointly
considering both browsing level and age.
Our results have two main implications to current understanding of
plant-herbivore interactions under climatic warming. First, these
findings seem to challenge a common perspective that temperature is a
dominant factor controlling shrub growth at their range edges
(Myers-Smith et al . 2015). As our study system is at the edge of
the common occurrence of the studied Salix species, we find it
possible that effects of herbivory are at strongest at range edges and
limit growth of established shrubs. We suspect that this phenomenon is
wide-spread but remains rarely documented due to lack of long-term data
and dynamic modelling that can link growth and growth regulating
drivers. See, however Trotter et al . (2002) and comparable
results of Wilmking et al . (2018) reporting Eurois occultaoutbreak effects on Alnus viridis in Greenland and Vuorinenet al . (2020) reporting negative warming effects on pine growth
at high deer browsing levels. Second, as has been suggested with regard
to vertebrate browsers (Christie et al . 2015) we find it possible
that potentially intensifying effects of insect herbivores and their
outbreaks (Seidl et al . 2017; Ren et al . 2020), the
expansion of deciduous shrub genets is markedly slowed down, while newly
established genets and their ramets in warmer and sufficiently enemy
free circumstances play the greatest role in the observed tundra shrub
expansion.