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Increase in nutrient availability promotes success of invasive plants through increasing growth and decreasing anti-herbivory defenses

Liping Shan1, Ayub M. O. Oduor2, Wei Huang1, Yanjie Liu1•
Chinese Academy of Sciences1, Technical University of Kenya2
19 Oct 2021-bioRxiv (Cold Spring Harbor Laboratory)-
TL;DR: In this article, a greenhouse experiment with simulated herbivory (clipping vs. no-clipping) and competition (alone vs. competition) was conducted to investigate the effect of nutrient enrichment on the growth and defense of invasive plants.
Abstract: Invasive plant species often exhibit greater growth and lower anti-herbivory defense than native plant species. However, it remains unclear how nutrient enrichment of invaded habitats may interact with competition from resident native plants to affect growth and defense of invasive plants. In a greenhouse experiment, we grew five congeneric pairs of invasive and native plant species under two levels of nutrient availability (low vs. high) that were fully crossed with simulated herbivory (clipping vs. no-clipping) and competition (alone vs. competition). Invasive plants produced more gibberellic acid, and grew larger than native species. Nutrient enrichment caused a greater increase in total biomass of invasive plants than of native plants, especially in the absence of competition or without simulated herbivory treatment. Nutrient enrichment decreased leaf flavonoid contents of invasive plants under both simulated herbivory conditions, but increased flavonoid of native plants under simulated herbivory condition. Nutrient enrichment only decreased tannins production of invasive species under competition. For native species, it enhanced their tannins production under competition, but decreased the chemicals when growing alone. The results indicate that the higher biomass production and lower flavonoids production in response to nutrient addition may lead to competitive advantage of invasive species than native species.
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1
Increase in nutrient availability promotes success of invasive plants through increasing 1
growth and decreasing anti-herbivory defenses 2
Liping Shan
1
, Ayub M.O. Oduor
1,2
, Wei Huang
3,4
, Yanjie Liu
1*
3
1
Key Laboratory of Wetland Ecology and Environment, Northeast Institute of Geography and 4
Agroecology, Chinese Academy of Sciences, Changchun, 130102, P.R. China 5
2
Department of Applied Biology, Technical University of Kenya, P. O. Box 52428
00200, 6
Nairobi, Kenya 7
3
CAS Key Laboratory of Aquatic Botany and Watershed Ecology, Wuhan Botanical Garden, 8
Chinese Academy of Sciences, Wuhan, Hubei, China 9
4
Center of Conservation Biology, Core Botanical Gardens, Chinese Academy of Sciences, 10
Wuhan, Hubei, China 11
12
*
Corresponding author: Yanjie Liu, liuyanjie@iga.ac.cn, +86-431-82536096. 13
14
Total word count for the main body: 4426 words 15
Word count for introduction: 732 words 16
Word count for materials and methods: 1389 words 17
Word count for results: 558 words 18
Word count for discussion: 1556 words 19
Word count for conclusion: 86 words 20
Number of figures: 3 21
Number of tables: 1 22
Supporting information: 4 (2 tables and 2 figures) 23
24
.CC-BY-NC 4.0 International licenseavailable under a
(which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
The copyright holder for this preprintthis version posted October 19, 2021. ; https://doi.org/10.1101/2021.10.18.464765doi: bioRxiv preprint
2
Summary: 25
Invasive plant species often exhibit greater growth and lower anti-herbivory defense than 26
native plant species. However, it remains unclear how nutrient enrichment of invaded habitats 27
may interact with competition from resident native plants to affect growth and defense of 28
invasive plants. 29
In a greenhouse experiment, we grew five congeneric pairs of invasive and native plant 30
species under two levels of nutrient availability (low vs. high) that were fully crossed with 31
simulated herbivory (clipping vs. no-clipping) and competition (alone vs. competition). 32
Invasive plants produced more gibberellic acid, and grew larger than native species. Nutrient 33
enrichment caused a greater increase in total biomass of invasive plants than of native plants, 34
especially in the absence of competition or without simulated herbivory treatment. Nutrient 35
enrichment decreased leaf flavonoid contents of invasive plants under both simulated 36
herbivory conditions, but increased flavonoid of native plants under simulated herbivory 37
condition. Nutrient enrichment only decreased tannins production of invasive species under 38
competition. For native species, it enhanced their tannins production under competition, but 39
decreased the chemicals when growing alone. 40
The results indicate that the higher biomass production and lower flavonoids production in 41
response to nutrient addition may lead to competitive advantage of invasive species than 42
native species. 43
44
Key words: competition, exotic, interactions, nutrient, phytohormone, secondary metabolites 45
46
.CC-BY-NC 4.0 International licenseavailable under a
(which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
The copyright holder for this preprintthis version posted October 19, 2021. ; https://doi.org/10.1101/2021.10.18.464765doi: bioRxiv preprint
3
1. Introduction 47
Understanding the physiological and ecological processes underlying invasion success of 48
alien plant species is an important topic in ecology (Jia et al., 2016; Reilly et al., 2020). 49
Invasive plants commonly experience herbivory in their native ranges (Keane & Crawley, 50
2002; Wolfe, 2002), but because plant defense against herbivory incurs significant 51
physiological and ecological costs (Cipollini et al., 2014), plants often have to trade off 52
defense against growth and reproduction (Herms & Mattson, 1992). Therefore, theory 53
predicts that alien plants that become successful invaders are those that have escaped from 54
their own herbivores and re-allocated limited resources into greater growth and reproduction 55
at the expense of defense (Keane & Crawley, 2002). In support it, several studies have 56
reported that invasive plants interact with fewer herbivore species, and thus exhibit less 57
defense and greater growth in the exotic range than in the native range (Colautti et al., 2004; 58
Oduor et al., 2011; Meijer et al., 2016; Zhang et al., 2018). Therefore, alien plant species that 59
become successful invaders may trade-off high growth and reproductive output with low 60
investments in anti-herbivory defenses. 61
Observational studies have found that low-resource environments are generally less 62
prone to invasion (Chytrý et al., 2008). Experimental studies also suggest that increased 63
availability of resources for plant growth can confer invasive species with growth advantage 64
over native species (D'Antonio & Vitousek, 1992; Bobbink et al., 1998; Davis et al., 2000; 65
Tilman et al., 2001), becasue many native plant species are adapted to conditions of soil 66
low-nutrient and water availability in their natural habitats (Bobbink et al., 1998; Dukes & 67
Mooney, 1999). In fact, meta-analyses have found that nutrient enrichment is more beneficial 68
to growth of invasive plant species than of native plant species (González et al., 2010; Liu et 69
al., 2017). Following this logic, nutrient enrichment might also affect defense differently 70
between invasive plant species and native plant species due to the trade-off between plant 71
.CC-BY-NC 4.0 International licenseavailable under a
(which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
The copyright holder for this preprintthis version posted October 19, 2021. ; https://doi.org/10.1101/2021.10.18.464765doi: bioRxiv preprint
4
growth and defense (Herms & Mattson, 1992). However, how nutrient availability impacts 72
growth-defense trade-offs of invasive and native plants remains little tested empirically. 73
Competition is important to determine plant invasion success (Levine et al., 2004; 74
Petruzzella et al., 2020). On the one hand, strong competition from invasive plants often 75
reduces diversity of native plant species, and results in mono-specific stands of invaders 76
(Gaertner et al., 2009). Invasive plants exert strong competitive effects on native plants 77
because invasive plants often have disproportionately higher demand for resources (Leishman 78
& Thomson, 2005; Funk, 2013). Consequently, nutrient enrichment could confer invasive 79
plants greater competitive advantage relative to native plants in communities (Seabloom et al., 80
2015). On the other hand, given that competition from other plants could create stressful 81
environments, costs of plant defense against herbivory in such environment may also increase 82
when competition is present (Herms & Mattson, 1992; Siemens et al., 2002). In other words, 83
competition may amplify the growth-defense trade-offs of plants. However, it remains 84
unclear whether competition affect trade-offs of invasive and native plants differently. 85
Therefore, studies testing effects of tests of whether nutrient availability enrichment on 86
growth-defense trade-offs of invasive and native plants, should also consider whether the 87
plants grow alone or with competition. 88
Plant growth and defense are generally regulated by different types of hormones. For 89
example, as the major hormones that stimulate plant growth and development (Ross & Reid, 90
2010), gibberellic acids (GA) stimulate seed germination, trigger stem elongation, leaf 91
expansion, flowering and seed development (Yang et al., 2012; Gupta & Chakrabarty, 2013). 92
However, expression of defense hormones can suppress expression of plant 93
growth-promoting hormones, because these two type hormones often have negative 94
cross-talks within the plants (Ross & Reid, 2010; Yang et al., 2012; Vos et al., 2015). For 95
example, herbivory-induced production of a defense-regulating hormone jasmonic acid (JA) 96
.CC-BY-NC 4.0 International licenseavailable under a
(which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
The copyright holder for this preprintthis version posted October 19, 2021. ; https://doi.org/10.1101/2021.10.18.464765doi: bioRxiv preprint
5
can constrain plant growth by antagonizing production of GA (Machado et al., 2017). 97
Therefore, invasive plants that escape intense herbivores may produce high concentrations of 98
growth-promoting hormones (e.g., GAs) and low concentrations of hormones that regulate 99
anti-herbivore defenses (Liu et al., 2021). However, this prediction has not been tested 100
empirically. 101
Here, we conducted a greenhouse experiment with five congeneric pairs of invasive and 102
native plant species to test the following hypotheses: (i) Nutrient enrichment induces invasive 103
plants to produce greater total biomass and lower concentrations of anti-herbivore defense 104
compounds than native plants; (ii) Invasive plants express a lower concentration of a defense 105
hormone JA and a higher concentration of a growth-promoting hormone GA. 106
2. Methods 107
2.1 Plant species 108
We used five congeneric pairs of native and invasive clonal plant species from three families 109
that co-occur naturally in the field in China (Table S1). We raised plantlets/seedlings of the 110
test plant species using seeds and asexual reproductive organs that were collected in the field 111
(Table S1). For asexual species, we first selected intact rhizomes and stolons and cut them 112
into single-node/bud fragments, and then cultivated the fragments in trays. For the sexually 113
reproducing species, we directly sowed seeds in trays filled with potting soil (Pindstrup Plus, 114
Pindstrup Mosebrug A/S, Denmark). The resultant plantlets/seedlings were then raised under 115
uniform conditions for one month in a greenhouse (temperature: 22-28
; natural lighting 116
with an intensity of c. 75% of the light outdoors; and c. 60% relative humidity). We then 117
selected similar-sized plantlets /seedlings of each species for use in the experiment described 118
below. 119
2.2 Experimental set up 120
To test whether native and invasive plants differed in their responses to competition and 121
.CC-BY-NC 4.0 International licenseavailable under a
(which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
The copyright holder for this preprintthis version posted October 19, 2021. ; https://doi.org/10.1101/2021.10.18.464765doi: bioRxiv preprint
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TL;DR: Data support the notion that hormonal crosstalk in plants during multi-attacker interactions allows plants to prioritize their defenses, while limiting the fitness costs associated with induction of defenses.
Abstract: The hormone salicylic acid (SA) generally induces plant defenses against biotrophic pathogens. Jasmonic acid (JA) and its oxylipin derivatives together with ethylene (ET) are generally important hormonal regulators of induced plant defenses against necrotrophic pathogens, whereas JAs together with abscisic acid (ABA) are implicated in induced plant defenses against herbivorous insects. Hormonal crosstalk between the different plant defense pathways has often been hypothesized to be a cost-saving strategy that has evolved as a means of the plant to reduce allocation costs by repression of unnecessary defenses, thereby minimizing trade-offs between plant defense and growth. However, proof for this hypothesis has not been demonstrated yet. In this study the impact of hormonal crosstalk on disease resistance and fitness of Arabidopsis thaliana when under multi-species attack was investigated. Induction of SA- or JA/ABA-dependent defense responses by the biotrophic pathogen Hyaloperonospora arabidopsidis or the herbivorous insect Pieris rapae, respectively, was shown to reduce the level of induced JA/ET-dependent defense against subsequent infection with the necrotrophic pathogen Botrytis cinerea. However, despite the enhanced susceptibility to this second attacker, no additional long-term negative effects were observed on plant fitness when plants had been challenged by multiple attackers. Similarly, when plants were grown in dense competition stands to enlarge fitness effects of induced defenses, treatment with a combination of SA and MeJA did not cause additional negative effects on plant fitness in comparison to the single MeJA treatment. Together, these data support the notion that hormonal crosstalk in plants during multi-attacker interactions allows plants to prioritize their defenses, while limiting the fitness costs associated with induction of defenses.

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Madalin Parepa1, Markus Fischer1, Oliver Bossdorf1•
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Ragan M. Callaway1, Beth A. Newingham1, Cathy A. Zabinski1, Bruce E. Mahall2•
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University of Bern1, University of Konstanz2, Spanish National Research Council3, University of Fribourg4
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Frequently Asked Questions (1)
Q1. What are the contributions in "Increase in nutrient availability promotes success of invasive plants through increasing growth and decreasing anti-herbivory defenses" ?

For example, Zhang et al. this paper found that high growth and reproductive output with low investments in anti-herbivory defenses may amplify the growth-defense trade-offs of plants.