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\begin{document}

\title{Dynamic effects of insect herbivory and climate on tundra shrub growth:
roles of browsing and ramet age}



\author[1]{Risto Virtanen}%
\author[2]{Adam Clark}%
\author[3]{Michael den Herder}%
\author[4]{Heikki Roininen}%
\affil[1]{University of Oulu}%
\affil[2]{German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig}%
\affil[3]{European Forest Institute}%
\affil[4]{University of Eastern Finland}%


\vspace{-1em}



  
  \date{June 18, 2024}


\begingroup
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\selectlanguage{english}
\begin{abstract}
To predict plant responses under climate change, we need to understand
how thermal conditions and herbivory contribute to shoot growth. Here,
we used empirical dynamic modelling (EDM) to analyse an 18-year time
series from an experimental system at the forest-tundra ecotone to
identify relationships between growth, climate, insect herbivores,
browsers and ramet age. We found that negative effects of insect
herbivory on willow shoot growth are intensified during warmer years.
Moreover, the negative effect of insect herbivores was moderated by
ramet age, but this moderation was only realized in the absence of
vertebrate herbivores -- under browsing by both ptarmigans and reindeer,
the positive effects of ramet age were eliminated. Jointly, these
results demonstrate the context-dependent and dynamic effects of climate
and multiple herbivores on shoot growth, and improve our ability to
predict effects of climatic warming in arctic environments.%
\end{abstract}%



\sloppy


\textbf{Introduction}

Climatic constraints limit annual growth of woody plants in cold
high-latitude environments (Havstr\selectlanguage{ngerman}öm \emph{et al} . 1993;
Myers-Smith\emph{et al} . 2015; Weijers \emph{et al} . 2018). The growth
of tundra shrubs positively correlates with warmer summer thermal
conditions (Pajunen 2009; Forbes \emph{et al} . 2010; Li \emph{et al} .
2016; Ackerman \emph{et al} . 2018), implying that under warming
conditions shrub growth will increase (Myers-Smith \emph{et al} . 2015).
On the other hand, broad-scale insect outbreaks causing defoliations of
most deciduous woody plants are becoming more frequent (Jepsen \emph{et
al} . 2008; Tenow \emph{et al} . 2004; Lund \emph{et al} . 2017;
Svensson\emph{et al} . 2018). Defoliations have been associated with
reductions in growth (Crawley 1983, 1989; Hoogesteger \& Karlsson 1992;
Takahashi \& Huntly 2010; Wilmking \emph{et al} . 2012). The browsing of
vertebrate herbivores also reduces woody plant growth in various
environments (Post \& Pedersen 2008; Newton \emph{et al} . 2014,
Vuorinen \emph{et al} . 2020). At high latitudes, reindeer browsing has
been found to reduce flowering and survival of entire ramets (i.e. a
clonal colony or a group of genetically identical plants) or their parts
(den Herder \emph{et al} . 2004; Hakkarainen \emph{et al} . 2007;
Ravolainen \emph{et al} . 2014) and long-term browsing reduces the
abundance of willows (Pajunen\emph{et al} . 2008, 2012, Kitti \emph{et
al} . 2009; Ravolainen \emph{et al} . 2011). In addition, browsing by
willow ptarmigan has been found to increase shoot dieback and constrain
ramet growth (Hakkarainen \emph{et al} . 2007; den Herder \emph{et al} .
2008; Tape \emph{et al} . 2010; Christie \emph{et al} . 2014).

The effects of climatic factors and herbivory on growth dynamics of
tundra shrubs is of growing research interest (Christie \emph{et al} .
2015; Martin \emph{et al} . 2017). Here a key unresolved question
concerns teasing apart dynamic effects of herbivory and warming climate
on willow growth. While there is experimental and observational evidence
that warmer conditions are associated with higher levels of herbivory
(Roy \emph{et al} . 2004; Birkemoe \emph{et al} . 2016; Barrio \emph{et
al} . 2017; Lehmann \emph{et al} . 2020), it is infrequently documented
that herbivory can counteract positive climate effects on plant growth
(but see O'Connor 2009; Vuorinen \emph{et al} . 2020). Such possible
antagonistic effects of climate warming and herbivory on plant growth
are further complicated by the moderating effects of plant age or
browsing pressure affecting meristem activity and growth (Wijk 1986;
Massad 2013). Thus, it is important when investigating the dynamic
effects of insect herbivores and climate on plant growth, it is also
necessary to consider plant age and browsing pressure.

The current pressing questions concern shrub growth under climatic and
non-climatic drivers (Myers-Smith \emph{et al} . 2015). In this study we
conduct a model-based analysis of long-term shoot growth of a tundra
willow, and test how it is linked to variation in thermal conditions,
insect herbivory, vertebrate browsing and plant age. In particular, we
hypothesized that higher temperatures in the growing season would
promote shoot growth, while intensifying insect herbivory would
counteract the effects of warming conditions on shoot growth. We further
expected that plant age and vertebrate browsing could moderate both
climatic and insect herbivore effects on shoot growth. We quantified the
joint dynamic effects of insect herbivory and thermal conditions on
shoot growth using empirical dynamic modelling (EDM), a recently
developed method which can quantify the strength and direction of
interactions in observational time series data, even when these
interactions vary through time. Using these techniques, we succeeded in
identifying dynamic effects of climate and herbivory on plant shoot
growth in an 18-year time-series data from a browser-exclusion
experiment in NW Finnish Lapland. Moreover, our analyses reveal that
plant-herbivore interactions vary greatly with ecological context,
including differences among experimental treatments manipulating
browsing pressure (fences) and plant age (rejuvenation by pruning
treatment).

\textbf{Material and methods}

The study area is located in NW Finnish Lapland at a transitional area
between boreal mountain birch forests and treeless oroarctic and arctic
tundra heaths at higher elevations (Virtanen \emph{et al} . 2016). The
study site lies at an elevation of 550--570 m a.s.l. (68.92° N, 20.97°
E). In this landscape, tundra-like vegetation occurs also in valleys
with frost-hummocky dwarf birch (\emph{Betula nana} ) heath with some
willows and mountain birch (\emph{Betula pubescens}
ssp.\emph{czerepanovii} ), and moss and lichen dominated ground-layer.
In the study area, tea-leaved willow (\emph{Salix phylicifolia} ) is a
common shrub that is generally regarded as palatable, and is browsed by
several vertebrate species. Willow ptarmigan (\emph{Lagopus lagopus} )
browses willows primarily in winter when willow shoots and buds reach
above snow level. Reindeer (\emph{Rangifer tarandus} ) browse willow by
ripping leaves and shoots primarily in early summer. In the study area,
reindeer are semi-domesticated and have had relatively high stocking
rates of c. 10 ind/km\textsuperscript{2}. The study area was a summer
reindeer range until 2008, after which reindeer were moved to another
area for the summer season. Therefore, in 2008--2018 only solitary
reindeer were seen in the area in summer-time. Mountain hare
(\emph{Lepus timidus} ) browsing has been very infrequent in the study
area, as well as that of Norway lemmings (\emph{Lemmus lemmus} ) and
voles (\emph{Microtus oeconomus} , \emph{Myodes rufocanus} . Peaks of
vole and lemming populations occurred in 2009--2010 and 2014--2015. In
our study area we have observed two main folivorous insect herbivores
that defoliate leaves partly or completely. One is autumnal moth
(\emph{Epirrita autumnata} ) that feeds on the willow during population
outbreaks and can cause complete defoliation of willows. Outbreaks of
autumnal moth defoliating willows occurred in 2003--2005 and
2011--2013. The other are folivorous beetles (mainly \emph{Gonioctena}
spp.; Chrysomelidae) that have been observed in most years.

Experimental design

Eighty willow genets in two forest-tundra ecotone sites were selected
for the experiment in 1997. In these sites, the genets were selected
within areas of c. 50 × 200 m and 50 × 250 m. Genets were 30--50 cm tall
and consisted of 10--25 ramets each. All genets were initially
accessible to both reindeer and ptarmigan. The genets were then assigned
into blocks of four genets. In 1997--1998, two random genets within each
block were rejuvenated by pruning ramets five cm above the ground level.
The pruned genets produced sprouts that initially grew vigorously for
1--3 years and within a few years reached the size of unpruned genets.
Thus, each block consisted of two old genets and two rejuvenated genets.
Within each block one of the old and rejuvenated genets were protected
by reindeer fences (2×2 m area). In 2000, reindeer fences were replaced
by ptarmigan proof fences in half of the blocks, selected at random. The
experimental design from 2000 onwards included treatment combinations of
reindeer exclusion and reindeer+ptarmigan exclusion on both old and
rejuvenated genets (see Table 1, Supporting Information).

Table 1. The experimental design of the long-term browsing experiment.
Reindeer exclusion (--) consists of experimental units with reindeer
fence, whereas ptarmigan and reindeer browsing exclusion treatments (--)
have fences with 3.5 cm mesh size. Rejuvenated (+) treatments were
initially pruned above ground level.\selectlanguage{english}
\begin{longtable}[]{@{}lllll@{}}
\toprule
Treatment & Reindeer & Willow ptarmigan & Rejuvenation &
Abbreviation\tabularnewline
\midrule
\endhead
Reindeer + ptarmigan browsing + rejuvenation & + & + & + &
RPJ\tabularnewline
Reindeer + ptarmigan browsing & + & + & -- & RP\tabularnewline
Ptarmigan browsing + rejuvenation & -- & + & + & PJ\tabularnewline
Ptarmigan browsing & -- & + & -- & P\tabularnewline
Rejuvenation & -- & -- & + & J\tabularnewline
None & -- & -- & -- & N\tabularnewline
\bottomrule
\end{longtable}

In summer 2001, four willow ramets of each genet were tagged with basal
plastic slips. The shoot growth of tagged ramets was monitored every
year. The shoot lengths of each tagged willow ramet were measured in
early August (at the end of the active growing season) to an accuracy of
0.5 cm. In cases where an individual ramets died, a new ramet of the
same genet were tagged. Initially, 320 ramets were tagged in 2001, while
the total number of individual ramets tagged was 626. In addition, the
level of insect herbivory was estimated using the following defoliation
classes: 0 no observable insect herbivory, 1 (0--1\%), 2 (1--5 \%), 3
(6--25 \%), 4 (25--100\%) or 5 (leaves totally defoliated) (den
Herder\emph{et al} . 2004). Herbivory shows remarkable among-year
variation in 2001--2018, but no trend (Supporting Information).

Climate data were obtained from the nearest Finnish Meteorological
Institute weather station (Kilpisj\selectlanguage{ngerman}ärvi Kyläkeskus) located 10 km from
the experimental site (480 m a.s.l.). The weather station provides daily
records on mean temperature. These climatic station data were used to
calculate thermal sum for the season, when shoot growth takes place.
Therefore, daily mean temperatures exceeding + 5 °C in May--July were
summed up to produce a ``growing degree days - GDD'' index, hereafter
denoted as \emph{Climate} . Thermal sum shows remarkable among-year
variation in 2001--2018, but no clear trend (Supporting Information).
Note that although there are many other potential climate-related
variables that we could have considered (e.g. length of growing season,
growing degree days with different threshold, mean July temperature),
these all correlated with the thermal sum as described above -- we
therefore chose to only consider this commonly used variable in our
analyses.

Empirical dynamic modelling

We used EDM to model the relationships between willow shoot growth,
climate and herbivory. EDM is a recently developed technique that
combines two tools (Deyle \emph{et al} . 2016) -- convergent cross
mapping (CCM) and sequential locally weighted global linear maps
(S-mapping). CCM is a nonparametric method for tracking information flow
among variables, and is a powerful tool for identifying causal links in
systems with complex dynamics (Sugihara \emph{et al} . 2012;
Clark\emph{et al} . 2015). Because the direction of information flow is
directional in causal interactions (i.e. ``forcing'' processes impart
information onto ``response'' processes, whereas the reverse is not
true), CCM is also often successful at identifying the direction of
causal interactions based on observational data. S-mapping is a related
technique that can be used to extract information about the strength and
direction of these relationships (Sugihara 1994). These methods are
particularly useful for our purposes, as they can be applied
without\emph{a priori} knowledge of the functional form of the
relationship governing interactions and apply even for highly complex or
chaotic dynamics. They also provide two major advantages over more
classic methods, such as mixed-effects linear models or GLM's. First, in
complex ecological systems, results from CCM tend to be more closely
aligned with actual causal forcing than is true for regression
(Sugihara\emph{et al} . 2012; Clark \emph{et al} . 2015). This feature
allows us to generate putative interaction networks among species based
on observational data. Second, S-mapping captures effects of dynamic,
nonlinear relationships among variables. Thus, S-mapping allows us to
analyse the strength and direction of interactions among species even
when they are complex, time-varying, and context dependent. The analyses
were employed using rEDM package and EDMhelper packages in R (Ye\emph{et
al} . 2018; Karakoç \emph{et al} . 2020).

Based on a time-delayed application of Convergent Cross Mapping (CCM)
(Fig. 1), we chose to quantify effects of climate (\emph{Climate} ) and
insect herbivory (\emph{Herbivory} ) on mean shoot length of topmost
part of the ramets (\emph{Shoot} ). In CCM analysis, causal forcing is
indicated when predictive skill increases significantly with the total
number of historical observations used to make predictions (i.e.
``library length''). We identified significant forcing of ramet dynamics
by both climate and herbivory (Fig 1). Because multi-trophic
interactions often involve time-delayed effects, we tested for both
immediate and lagged effects. Analyses suggested that effects of insect
herbivores on shoot growth were immediate (i.e. time-lag = 0), whereas
climate was best represented by a time-lagged effect (time-lag = -1).
All variables were standardised to zero mean and unit standard deviation
before analysis, to better allow for comparison of effect sizes among
variables. Note that although ``best practices'' dictate that 30--40
sequential observations are usually necessary for CCM and, to a lesser
extent, S-mapping, this limit can be met either by single long time
series, or using composites that have been stitched together from
multiple shorter time series (Hsieh \emph{et al} . 2008; Clark \emph{et
al} . 2015). For all analyses presented here, within each treatment,
time-series from all ramets and replicates were stitched together,
resulting in time series of \textgreater{} 640 measurements for each
treatment.\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/image1/image1}

\end{center}
\end{figure}

\textbf{Figure 1.} CCM results of mean shoot length vs. growing degree
days (measured May -- July) and insect herbivory. Prediction skill is
measured as Pearson's correlation coefficient. Significant causal
forcing is indicated in cases where prediction skill increases
significantly with library length. P-values indicate significant
increase in prediction skill for the longest library length tested
relative to the shortest library length tested at lag = 0 and lag = 1,
respectively, as well as a comparison of the predictive skills for lag =
0 vs. lag = 1.

Using this information, we found that the best embeddings (i.e.
predictive models) of system dynamics were achieved using four
time-lagged dimensions, and a tuning parameter that indicated moderately
nonlinear dynamics (\selectlanguage{greek}\emph{θ} \selectlanguage{english}= 0.75). To construct a predictive model of
willow shoot growth dynamics as a function of the full set of causally
related variables, we therefore used two lagged dimensions of willow
shoot lengths, one lagged dimension of climate, and one non-lagged
dimension of insect herbivory. These relationships yielded a model of
the form:

\emph{mean\_shoot} (\emph{t} +1) =\selectlanguage{greek}\emph{β} \selectlanguage{english}\textsubscript{0}+\selectlanguage{greek}\emph{β}
\selectlanguage{english}\textsubscript{1}\emph{Shoot} (\emph{t} )+\selectlanguage{greek}\emph{β}
\selectlanguage{english}\textsubscript{2}\emph{Shoot} (\emph{t} --1)+\selectlanguage{greek}\emph{β}
\selectlanguage{english}\textsubscript{3}\emph{Climate} (\emph{t} --1)+\selectlanguage{greek}\emph{β}
\selectlanguage{english}\textsubscript{4}\emph{Herbivory} (\emph{t} )

where \selectlanguage{greek}\emph{β\textsubscript{i}}\selectlanguage{english} indicates fitted values, which are
allowed to vary through state-space based on historical dynamics. For
example, \selectlanguage{greek}\emph{β} \selectlanguage{english}\textsubscript{1} might be high for low values
of\emph{mean\_shoot} (\emph{t} ), indicating that increases in shoot
biomass also lead to increases in growth, whereas it might be low for
larger values of \emph{mean\_shoot} (\emph{t} ), indicating
self-limitation.

In general, the fitted parameters \selectlanguage{greek}\emph{β} \selectlanguage{english}\textsubscript{3} and\selectlanguage{greek}\emph{β}
\selectlanguage{english}\textsubscript{4} can be interpreted as partial derivatives describing
the effect of thermal climate and insect herbivory on shoot growth (i.e.
[?]\emph{Shoot} /[?]\emph{Climate} and [?]\emph{Shoot} /[?]\emph{Herbivory} ,
respectively). Positive values indicate that shoot growth increases as a
function of warmer climate or higher insect herbivory. Negative values
indicate that growth declines with warming, or declines with increased
insect herbivory. Note that these can be interpreted identically to
slopes in a standard linear regression (e.g. where the slope term
describes the partial derivative of response variable \emph{y} relative
to explanatory variable \emph{x} , [?]\emph{y} /[?]\emph{x} ).

\textbf{Results}

When considered across all experimental treatments (Fig. 2), we find
evidence for negative effects of insect herbivory on willow shoot
growth, and for a mix of negative and positive effects of climate (Fig.
2a). These climate effects generally became more positive with warming,
such that at cool climate conditions (low GDD), warming climate
conditions were associated with declines in shoot growth, whereas under
warmer conditions, further warming had either no effect, or weakly
positive effects (Fig. 2b). The joint outcome of these patterns was that
under cooler climate conditions, insect herbivores had relatively weak
effects on willow shoot growth, whereas under warmer conditions, the
negative effects of insect herbivory on shoot growth became more
pronounced (Fig. 2c).

\textbf{Hosted file}

\verb`image2.emf`  available at \url{https://authorea.com/users/308015/articles/439003-dynamic-effects-of-insect-herbivory-and-climate-on-tundra-shrub-growth-roles-of-browsing-and-ramet-age}

\textbf{Figure 2.} Estimated interaction strengths from S-mapping
analysis, based on pooled data including all experimental treatments.
Points show results for individual time steps, whereas lines show mean \selectlanguage{ngerman}±
one standard deviation. Recall that partial derivatives can be
interpreted in the same way as the slope of a linear regression -- i.e.
\selectlanguage{english}[?]\emph{y} /\selectlanguage{english}[?]\emph{x} describes the slope of a regression of \emph{y} as
a function of \emph{x} . \textbf{(A)} Estimated effect of herbivory on
shoot growth, vs. estimated effect of climate on shoot growth for a time
lag of -1. Note that cases with more positive effects of climate are
associated with more negative effects of insect herbivory.
\textbf{(B)}Estimated effect of climate on shoot growth, vs. time-lagged
climate (GDD). Note that warmer years are associated with a more
positive effect of climate on shoot length. \textbf{(C)} Estimated
effect of insect herbivory on shoot growth, vs. time-lagged climate
(GDD). Note that in warmer years, negative effect of insect herbivory is
intensified.\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/image3/image3}

\end{center}
\end{figure}

\textbf{Figure 3.} Relationship between climate effects on willow shoot
growth, and effects of insect herbivores on shoot growth. Tests are the
same as those in Fig. 2a, except that analyses are run separately for
each of the experimental treatments. Abbreviations indicate: no
vertebrate herbivores (\emph{N} ); only herbivory by ptarmigans
(\emph{P} ), herbivory by ptarmigans and reindeer (\emph{RP} ), and the
interaction of each of these treatments with ``rejuvenation'' (i.e.
pruning of shoots in year 1 of the experiment) (\emph{J} , \emph{PJ} ,
and\emph{RPJ} , respectively) (Table 1).

When separated by browsing and rejuvenation treatments, we found that
the general pattern of responses of willow shoot growth to climate and
insect herbivores was similar to that in our pooled analysis (Fig. 3,
compare to Fig. 2a). However, the test revealed that the treatments
differ and that relationships within treatments were not uniform. Recall
that there are six different experimental treatments: neither vertebrate
herbivores (\emph{N} ); only herbivory by ptarmigans (\emph{P} ),
herbivory by ptarmigans and reindeer (\emph{RP} ), rejuvenation (i.e.
pruning of shoots at the initiation of the experiment) (\emph{J} ),
rejuvenation plus browsing by ptarmigans (\emph{PJ} ), and rejuvenation
plus browsing by ptarmigans and reindeer (\emph{RPJ} ). For most
treatments, there was still a negative relationship between the effects
of climate and the effects of insect herbivory, except in the case of
rejuvenation treatments, for which the relationship reversed (J, PJ
treatments in Fig. 3). Additionally, the treatments that included
vertebrate herbivores tended to experience more positive effects of
climate on shoot growth, while for treatments that included
rejuvenation, herbivory effects were generally less negative (compare
treatments P vs. PJ, RP vs. RPJ in Fig. 3).\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/image4/image4}

\end{center}
\end{figure}

\textbf{Figure 4.} Relationship between climate effects on willow shoot
growth, and lagged climate. Tests are the same as those shown in Fig.
2b, except that analyses are run separately for each of the experimental
treatments. Abbreviations are as described in the legend to Fig. 3 and
in Table 1.

The effects of climate on shoot growth were also similar across
treatments, generally with a positive relationship between climate
effects and growing degree days (Fig. 4). Recall that negative climate
effects suggest that warming will have a negative impact on shoot
growth, whereas positive effects suggest that warming leads to increases
in shoot growth -- our results therefore suggest that at low
temperatures, warming will have an overall negative effect on growth,
whereas at higher temperatures, warming will have an overall positive
effect. Interestingly, treatments that included vertebrate herbivores
and no rejuvenation (\emph{P} , \emph{RP} ) tended to experience more
positive effects of climate, such that the effect was consistent over a
range of previous year thermal conditions. In contrast, rejuvenation
treatments tended to suppress the positive relationship between climate
and climate effects, such that there was a fixed, negative effect of
climate regardless of growing degree days. However, for the treatment
that included both vertebrate herbivores and rejuvenation, the positive
relationship returned, and the overall pattern was similar to that for
shoot growth in conditions without browsers (\emph{N} ).\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/image5/image5}

\end{center}
\end{figure}

\textbf{Figure 5.} Relationship between insect herbivore effects on
willow shoot growth, and lagged climate. Tests are the same as those in
Fig. 2c, except that analyses are run separately for each of the
experimental treatments. Abbreviations are as described in the legend to
Fig. 3 and Table 1.

The joint outcome of these patterns again led to negative relationships
between effects of insect herbivory and climate, such that insects had
more strongly negative effects in warmer years. Interestingly, while
vertebrate herbivory alone had little impact on this trend (i.e.\emph{P}
, \emph{RP} ), negative effects of herbivory appeared to be buffered by
rejuvenation treatments, such that the overall effect of insect
herbivores was smaller (e.g. \emph{J} , \emph{PJ} ) (Fig. 5). Again,
however, this buffering appeared to be nullified by vertebrate
herbivory, such that the treatment that included both vertebrate
herbivores and rejuvenation (\emph{RPJ} ) showed a response that was
roughly identical to that in the untreated experimental unit (\emph{N}
).

\textbf{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 \emph{et al} . 2002; see also Lehmann
\emph{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 \emph{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 \emph{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 \emph{et al} . 1989) and cold conditions
further decrease sink strength (Hoch \& K\selectlanguage{ngerman}örner 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 \emph{et al} .
(1999) who found that deciduous shrubs exhibited weak growth responses
to short-term experimental warming. They proposed that deciduous shrubs
such as \emph{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, Vuorinen\emph{et
al} . (2020) found that pine growth reduced at high browsing pressure
and warm climate conditions and Marshall \emph{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 \emph{et al} . 2015). As our study system is at the edge of
the common occurrence of the studied \emph{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 \emph{et al} . (2002) and comparable
results of Wilmking \emph{et al} . (2018) reporting \emph{Eurois
occulta}outbreak effects on \emph{Alnus viridis} in Greenland and
Vuorinen\emph{et 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 \emph{et al} . 2015) we find it
possible that potentially intensifying effects of insect herbivores and
their outbreaks (Seidl \emph{et al} . 2017; Ren \emph{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.

\textbf{Acknowledgements}

This research has been supported by grants of Academy of Finland
(project \#259072), Maj and Tor Nessling Foundation, and University of
Oulu Arctic Interactions funding. We thank Matt Ayres for useful
comments on the manuscript. We also thank Helena Hakkarainen for
assistance in the growth measurements in 2004, and the Metsähallitus and
Kilpisjärvi Biological Station for providing logistic support during
field work.

\textbf{Data availability statement}

Data will be made publicly available through open access Dryad Digital
Repository.

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