Discussion
We report for the first time that frequency of grazing has effects on
the phylogenetic community structure that are not captured by standard
diversity indexes. Plant communities grazed every other year (i.e. pulse
grazing), but not communities grazed every year (i.e. press grazing)
were more phylogenetically dispersed than lightly grazed communities,
while there was no effect of grazing on species richness, the
Shannon-Wiener index (H’) and community evenness (Evar).
This does not support our predictions that grazing would act as a biotic
filter, resulting in communities that are more phylogenetically
clustered, but rather suggests that pulses of grazing release biological
control and allow more phylogenetically diverse communities.
We observed no effect of grazing on species richness, the Shannon-Wiener
index (H’) and community evenness (Evar). Since the
productivity of our study site is intermediate, these results are in
agreement with previous studies, which show that excluding reindeer
decreases species richness in sites with low productivity, but increases
species richness in productive sites (Proulx and Mazumder 1998, Bernes
et al. 2015, Sundqvist et al. 2019). A neutral effect of reindeer
grazing on species diversity is expected for sites that have
intermediate productivity in this region (Sundqvist et al. 2019).
While we do not observe a change in the overall richness and evenness of
vascular plants across grazing regimes, we do detect an effect of
grazing on the species composition of communities. Plots with pulse and
press grazing both differed in community structure from lightly grazed
plots (Figure 2a) as there was a transition from shrubs to graminoids
that occurred with grazing (Figure 3). These results are fully
consistent with previous studies in Fennoscandia that report the
replacement of dwarf shrubs by graminoids in grazed areas (Olofsson et
al. 2001). Similar effects of grazing on vegetation composition have
also been observed in other systems (McKendrick et al. 1980, Clarke et
al. 1995, Rooney 2009, Begley-Miller et al. 2014, Ferreira et al. 2020).
For example, grazing by sheep in Great Britain has resulted in the
replacement of heather moorlands with graminoids (Clarke et al. 1995),
and grazing by mammalian herbivores in northern Alaska also resulted in
the replacement of tundra heaths by graminoids (McKendrick et al. 1980).
Potential reasons for this shift in vegetation composition include
increased soil nutrient concentrations that favour graminoids
(McKendrick et al. 1980) and an increased ability of graminoids to
outcompete shrubs and ferns in heavily grazed environments due to their
short stature, high shoot densities, and capacity for compensatory
growth (Coughenour 1985). This combination of traits allows graminoids
to be the first plants to colonize following disturbances (Chapin and
Shaver 1981). Interestingly, the shift from shrubs to graminoids was
also observed in plots with several years of pulse grazing (Figure 2a;
Figure 3). This may be explained by the decades of chronic grazing these
plots were exposed to before the temporary fences were established.
Our novel analysis of the effect of reindeer grazing on the phylogenetic
structure of vascular plant communities revealed that communities with
pulse, but not press grazing seem more phylogenetically dispersed than
lightly grazed communities (Figure 4). This is in contrast to our
prediction that, assuming anti-herbivore traits are evolutionarily
conserved (Loiola et al. 2012, Yessoufou et al. 2013, but see Kursar et
al. 2009) and reindeer are generalist herbivores (Baskin and Danell
2003), reindeer grazing would result in communities that are more
phylogenetically clustered compared to lightly-grazed communities
(Cavender-Bares et al. 2009). Other studies examining the effect of
grazing on phylogenetic structure have found conflicting results.
Grazing by white-tailed deer (Odocoileus virginianus ) resulted in
phylogenetic clumping (Begley-Miller et al. 2014), but grazing by large
herbivores in the African savanna resulted in changes in phylogenetic
community structure dependent on the initial community structure:
communities that were initially clumped became more dispersed while
communities that were initially dispersed became more clumped (Yessoufou
et al. 2013). In contrast, grazing by livestock had no effect on the
phylogenetic dispersion of plant communities in Chile (Salgado-Luarte et
al. 2019). One potential explanation for our result is that
anti-herbivore defense traits are actually evolutionarily convergent in
our study region, a situation where grazing by a generalist herbivore
would result in phylogenetic clumping (Cavender-Bares et al. 2009).
However, it should be noted that this predicted effect of grazing on the
phylogenetic structure of plant communities by Cavender-Bares et al.
(2009) is based only on the direct effects of herbivory (i.e. the
physical removal of species) and does not account for the indirect
effects on e.g. productivity, nutrient availability, trampling
disturbance and competitive interactions between species. For example,
if herbivory increases soil nutrient availability and decreases
competition between plant species, this might lead to phylogenetic
clumping, given that both competition between distantly related taxa
(Mayfield and Levine 2010) and limited nutrient availability (Hurteau et
al. 2016) may drive phylogenetic clumping. In this case, the indirect
effects of grazing by herbivores on phylogenetic structure may act in
the opposite direction of direct effects of grazing, and the resulting
phylogenetic structure may depend on the relative strength of the direct
and indirect effects. Given that we found that pulse, but not press,
grazing results in increased phylogenetic dispersion, it is possible
that in our study system, the indirect effects of reindeer grazing are
more important than the direct effects in driving community assembly for
plant communities that are exposed to acute periods of grazing after
decades of chronic grazing.
The results of this study may be relevant to management decisions
involving reindeer in Fennoscandia. While we do not observe any richness
effects of reindeer grazing, we do observe a significant effect of
grazing on vegetation composition and phylogenetic structure. More
specifically, several years of pulse grazing (following over forty years
of chronic grazing) increased the phylogenetic dispersion of vascular
plant communities compared to plots with almost no grazing and plots
with continued press grazing. Changes to the phylogenetic structure of
communities may have important consequences for community function if
phylogenetic diversity captures genetic and functional diversity related
to ecosystem productivity (see, e.g. Cadotte et al. 2009, Flynn et al.
2011). Given the numerous studies that have analyzed the impact of
reindeer herbivory on vegetation composition, there is a potential to
re-analyze existing datasets using the framework of phylogenetic
community ecology as done here. Additionally, future studies considering
variation in productivity and grazing intensity will reveal if general
relationship between grazing and phylogenetic diversity exist in the
same way they do for common diversity measures, or whether the responses
depend on other factors such as the evolutionary history of plants and
herbivores. Direct measurement of ecosystem function in such
experimental communities are also needed to help understand the
mechanisms driving plant community assembly in support of future
management decisions.
Declarations
Ackowledgements: We thank Lauri Oksanen for knowledge of the
study area and design and Oleg Dmytrenko, Jonas Gustafsson, Pirjo
Isotupa, Marisano James, Maciek Koperwas, Nicolai Krichevsky, Anne
Muola, Karin Nilsson, Antti Oksanen, Lotta Ström and Gunnar Öhlund for
help in the field. We also thank James Bodnarchuk and Sara Durkin for
help with the phylogenetic analyses.
Funding: Funding for this study was provided by the Swedish
Research Council (MJM grant number 637-2013-274) and NSERC Canada (AOM).
Data accessibility: Data will be submitted to Dryad upon
acceptance.
Competing interests: The authors declare no competing
interests.