Discussion
Our results demonstrate that an intraspecific competitive environment
alters the effect of the ubiquitous plant-fungi mutualism on
plant-herbivore interactions. Arbuscular mycorrhizae decreased plant
resistance to herbivores when the plants were grown without competition,
but not when they were grown in competition. We found that arbuscular
mycorrhizae decreased plant nutritional quality when grown in
competition and induced with jasmonic and this correlated with increased
resistance to herbivores. While most studies on mycorrhizae find
positive or neutral effects on plant quality, mycorrhizae conferred
benefits are highly conditional. Our results are in agreement with the
work of Gange and West (1998) and Wurst et al. (2004) who found that,
under certain conditions, mycorrhizae can reduce plant resistance to
herbivores. Furthermore, we found that mycorrhizae suppress induction of
jasmonic acid pathway based defensive protease inhibitors. This supports
a number of studies which have found that mycorrhizal do not always
benefit plant growth (Ryan and Angus 2003; Bennett and Bever 2007) but
can still have effects on plant resistance to herbivores.
Our results support the vast body of literature ((Zimdahl 1980; Weiner
1990; Casper and Jackson 1997; Schwinning and Weiner 1998;
Getman-Pickering et al. 2018 among many) showing that competition
reduces plant growth. However, our results show no effect of mycorrhizae
on size dimorphism in competing plants contradicting the findings by
Weremijewicz and Janos (2012), and Ayers, Gange and Aplin who found that
mycorrhizae increased size dimorphism in Andropogon gerardii and
decreased size dimorphism in Plantago lanceolater espectively. However, both studies do not use entangled root
systems, which may account for the difference.
Mycorrhizae suppressed induction of defensive protease inhibitors. These
results support the growing body of work that shows that the
relationship between arbuscular mycorrhizae and plants can be
antagonistic, especially in tri-trophic frameworks. Arbuscular
mycorrhizae have been shown to suppress defensive compounds and increase
susceptibility of their hosts to a variety of insect herbivores,
including garden tiger moths, chrysanthemum leaf-miners and garden
buckeyes (Gernns et al. 2001; Gange et al. 2003; Bennett and Bever 2007;
Hartley and Gange 2009; Gehring and Bennett 2009). Similar effects have
been shown in mycorrhizae-plant-pathogen studies (Volpin et al. 1995;
Shaul et al. 1999; Gernns et al. 2001). In our study and others, a
suppression of defenses did not necessarily mean a decrease in overall
growth. The decrease in induction and the fact that mycorrhizae did not
increase growth suggest a more parasitic relationship between the plant
and fungus in this experiment.
The fact that arbuscular mycorrhizae did not alter the plant’s
constitutive defenses but did suppress induced defenses supports
previous research that finds that the formation of the association
between plants and arbuscular mycorrhizae alters defensive hormone
signaling in the plant. As protease inhibitors are known to be regulated
by the jasmonate pathway in tomato plants, it is not surprising that
protease inhibitor induction was altered by arbuscular mycorrhizae.
However, while overall trends in protease inhibitor activity matched the
treatment effects on cabbage looper caterpillars, protease
inhibitor activity in each individual plant was not correlated with
caterpillar weight or the leaf area they consumed. This result implies
that while arbuscular mycorrhizae are altering expression of the
jasmonic acid pathway, the protease inhibitors are not the primary
chemicals responsible for the effect on cabbage loopers.
The presence of mycorrhizae and competition alter the way that plants
induce changes in nitrogen levels and subsequently the C/N ratio. While
carbon levels independently didn’t impact herbivory, high ratios of
carbon to nitrogen decreased cabbage looper feeding. As herbivores are
frequently nitrogen limited, increased C/N ratios in foliage can be an
effective defense strategy for deterring herbivory. Plants associated
with mycorrhizae may have lower nutritional levels due to competition
between the two organisms for limited nutrients in the soil media (Kaye
and Hart 1997). This novel demonstration that mycorrhizae can suppress
leaf nutrient content following herbivory provides a new mechanism for
the effects of mycorrhizae on plant nutrition and resistance. It is
particularly interesting that mycorrhizae can affect constitutive and
induced defenses quite differently.
In our study, competition had no effect on induction of protease
inhibitors or leaf area consumed. This supports the growing body of
literature that fails to find support for the competition-defense
tradeoff (Viola et al. 2010). While our study only addressed
intraspecific competition, chosen because it is common in agricultural
settings, weeds and intercropping systems can result in interspecific
competition for the target crop. We predict that in interspecific
competitive situations, the effects of arbuscular mycorrhizae on
herbivory might not be suppressed for both partners as we found in this
study. Rather, the stronger partner might continue to see a strong
effect of arbuscular mycorrhizae on herbivory, while the weaker partner
will not, depending on the strength of the interaction as mycorrhizae
often preferentially give nutrients to one partner over another (Marler
et al. 1999b).
Our results, along with the many papers cited above, show that
tri-trophic effects of arbuscular mycorrhizae are context dependent, and
while previous studies have shown that the species of insect and
arbuscular mycorrhizae can alter the outcome of interactions, our work
shows that the presence of competition can change the direction of the
interaction between plant and mutualist. Due to the challenges of
working with mycorrhizae, the vast majority of studies on mycorrhizae
and herbivory have been conducted in greenhouse experiments where the
plants are grown individually (Riedel et al. 2008; Bennett et al. 2009;
Tomczak et al. 2016), although a few have studied this phenomenon in
field settings (Gehring & Whitham, 1991; Gange & West, 1994; Gangeet al. , 2005). As plants mostly exist in competition, either with
conspecifics or other species, it is important that future tests of the
effect of mycorrhizae-conferred resistance to herbivores account for the
role of competition.