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

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

References
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Journal ArticleDOI
TL;DR: The post-introduction evolution of a trade-off between resistance to and tolerance of herbivory of Brassica nigra is explored, contributing to an emerging pattern of both increasing resistance and growth in invasive populations contrary to the predictions of earlier theories of resistance-growth trade-offs.
Abstract: Summary •Rapid post-introduction evolution has been found in many invasive plant species, and includes changes in defence (resistance and tolerance) and competitive ability traits. Here, we explored the post-introduction evolution of a trade-off between resistance to and tolerance of herbivory, which has received little attention. •In a common garden experiment in a native range, nine invasive and 16 native populations of Brassica nigra were compared for growth and defence traits. •Invasive populations had higher resistance to, but lower tolerance of, herbivore damage than native populations. Invasive populations survived better and produced more seeds than native ones when released from herbivores; but fitness was equivalent between the regions under ambient herbivory. The invasive populations grew taller, and produced more biomass and lighter seeds than natives, irrespective of insecticide treatment. •In addition to supporting the idea of post-introduction rapid evolution of plant traits, our results also contribute to an emerging pattern of both increasing resistance and growth in invasive populations, contrary to the predictions of earlier theories of resistance–growth trade-offs.

67 citations

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TL;DR: It appears that the moss Physcomitrella patens can respond to auxin and contains key elements of the auxin signalling pathway, although there is some doubt as to whether it shows a fully developed rapid auxin response.
Abstract: The plant growth hormones auxin, gibberellins (GAs) and brassinosteroids (BRs) are major determinants of plant growth and development. Recently, key signalling components for these hormones have been identified in vascular plants and, at least for the GAs and BRs, biosynthetic pathways have been clarified. The genome sequencing of a range of species, including a few non-flowering plants, has allowed insight into the evolution of the hormone systems. It appears that the moss Physcomitrella patens can respond to auxin and contains key elements of the auxin signalling pathway, although there is some doubt as to whether it shows a fully developed rapid auxin response. On the other hand, P. patens does not show a GA response, even though it contains genes for components of GA signalling. The GA response system appears to be more advanced in the lycophyte Selaginella moellendorffii than in P. patens. Signalling systems for BRs probably arose after the evolutionary divergence of the mosses and vascular plants, although detailed information is limited. Certainly, the processes affected by the growth hormones (e.g. GAs) can differ in the different plant groups, and there is evidence that with the evolution of the angiosperms, the hormone systems have become more complex at the gene level. The intermediate nature of mosses in terms of overall hormone biology allows us to speculate about the possible relationship between the evolution of plant growth hormones and the evolution of terrestrial vascular plants in general.

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Journal ArticleDOI
TL;DR: Results are consistent with a hormonal antagonism model rather than a resource-cost model to explain the negative relationship between herbivory-induced defenses, leaf energy reserves and growth.
Abstract: Plants respond to herbivory by reconfiguring hormonal networks, increasing secondary metabolite production and decreasing growth Furthermore, some plants display a decrease in leaf energy reserves in the form of soluble sugars and starch, leading to the hypothesis that herbivory-induced secondary metabolite production and growth reduction may be linked through a carbohydrate-based resource trade-off In order to test the above hypothesis, we measured leaf carbohydrates and plant growth in seven genetically engineered Nicotiana attenuata genotypes that are deficient in one or several major herbivore-induced, jasmonate-dependent defensive secondary metabolites and proteins Furthermore, we manipulated gibberellin and jasmonate signaling, and quantified the impact of these phytohormones on secondary metabolite production, sugar accumulation and growth Simulated herbivore attack by Manduca sexta specifically reduced leaf sugar concentrations and growth in a jasmonate-dependent manner These effects were similar or even stronger in defenseless genotypes with intact jasmonate signaling Gibberellin complementation rescued carbohydrate accumulation and growth in induced plants without impairing the induction of defensive secondary metabolites These results are consistent with a hormonal antagonism model rather than a resource-cost model to explain the negative relationship between herbivory-induced defenses, leaf energy reserves and growth

64 citations

Journal ArticleDOI
TL;DR: The current results indicate that certain populations of native plant species could potentially adapt evolutionarily to invasive plant species, but the ecological and evolutionary mechanisms that probably underlie such evolutionary responses remain unexplored and should be the focus of future studies.
Abstract: Strong competition from invasive plant species often leads to declines in abundances and may, in certain cases, cause localized extinctions of native plant species. Nevertheless, studies have shown that certain populations of native plant species can co-exist with invasive plant species,suggesting the possibility of adaptive evolutionary responses of those populations to the invasive plants. Empirical inference of evolutionary responses of the native plant species to invasive plants has involved experiments comparing two conspecific groups of native plants for differences in expression of growth/reproductive traits: populations that have experienced competition from the invasive plant species (i.e. experienced natives) versus populations with no known history of interactions with the invasive plant species (i.e. naive natives). Here, I employ a meta-analysis to obtain a general pattern of inferred evolutionary responses of native plant species from 53 such studies. In general, the experienced natives had significantly higher growth/reproductive performances than naive natives, when grown with or without competition from invasive plants.While the current results indicate that certain populations of native plant species could potentially adapt evolutionarily to invasive plant species, the ecological and evolutionary mechanisms that probably underlie such evolutionary responses remain unexplored and should be the focus of future studies.

64 citations

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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.