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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
References
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Journal Article•DOI•
Cost of defense in the context of plant competition: brassica rapa may grow and defend

[...]

David H. Siemens1, Shannon H. Garner1, Thomas Mitchell-Olds1, Ragan M. Callaway1•
University of Montana1
01 Feb 2002-Ecology
TL;DR: The breakdown products of the glucosinolate-myrosinase reaction appeared to function as allelopathic agents, which may benefit B. rapa plants in competition, thereby reducing net costs of chemical defense.
Abstract: Theory on costs of plant defense against herbivory in stressful environments predicts that costs should increase when competition is intense. This amplifies a fundamental dilemma that plants are thought to face: allocate limited resources to grow fast enough to compete, or invest these resources in secondary metabolites to maintain defense. We studied costs associated with genetic and environmental variation in secondary metabolite pro- duction of Brassica rapa in the presence and absence of the generalist competitor Lolium perenne. We used experimental quantitative genetics (artificial selection) to manipulate genetic variation, and herbivore-induction treatments to produce environmental variation in myrosinase and glucosinolate concentrations and resistance. Glucosinolates, and their byproducts after breakdown by myrosinase, are known to affect herbivory on plants in the Brassicaceae family. Defense costs were significant in the absence of competitors, but in contrast to theoretical predictions, costs of constitutive defense (measured as growth rates) were not detectable and the cost of induced defense remained the same in the competitive environment. To understand what factors made constitutive defense costs not detectable under competition we conducted several experiments to assess the effects of limited re- sources and allelopathy on costs and benefits of the defense chemicals. None of the ex- periments involving nutrient supply and weak competition supported the hypothesis that the lack of defense costs in competitive environments was due to limited resources. Instead, the breakdown products of the glucosinolate-myrosinase reaction appeared to function as allelopathic agents, which may benefit B. rapa plants in competition, thereby reducing net costs of chemical defense. We found that: (1) the effects of exogenous glucosinolates on Lolium root length depended on the presence of myrosinase. (2) In the absence of nutrients, Lolium root lengths were shorter when seeds germinated with B. rapa. (3) Genetic increases in glucosinolate concentration negatively affected Lolium seedling growth only when there were simultaneous genetic increases in myrosinase concentration. Activated carbon treat- ments designed to neutralize allelopathic effects and restore costs in the competitive en- vironments were, however, not statistically significant. When plant defenses also function to benefit plants in competitive interactions, plants may evolve to compete and defend.

230 citations

Journal Article•DOI•
Experimental evidence for the effects of additional water, nutrients and physical disturbance on invasive plants in low fertility Hawkesbury Sandstone soils, Sydney, Australia

[...]

Michelle R. Leishman1, Vivien P. Thomson1•
Macquarie University1
01 Feb 2005-Journal of Ecology
TL;DR: It would appear that on relatively infertile sites, invasive species cannot take advantage of additional resources provided by physical disturbance or water addition due to overwhelming nutrient-limitation.
Abstract: Summary 1 The environmental conditions of a site are thought to influence its invasibility by exotic plants. We tested the effects of physical disturbance, water and nutrient addition on growth and survival of a total of 28 plant species from urban bushland remnants on low fertility Hawkesbury Sandstone soils in Sydney, Australia. Species were classified as native (to Australia, including the local community) or exotic (from outside Australia) and as non-invasive or invasive. 2 In a glasshouse experiment the treatments were control (natural soil), added water, added nutrients and added water and nutrients. We found significant differences in response of the plant types to additional nutrients but not to water. Under additional nutrients, exotic invasive species had better survival than all other plant types. There were strong biomass responses to added nutrients for all plant types except native non-invasives. In contrast, the survival and growth of all plant types were similar under control and additional water treatments. 3 In a field experiment the factors were site (high and low nutrient soils) and physical disturbance but survival differed between plant types only in relation to site. Exotic species had much better survival than native species at the high nutrient site only. Exotic invasive species had the strongest biomass responses to the high nutrient site while native and exotic non-invasive species showed relatively smaller growth responses. 4 Differences between invasive and non-invasive plants were not consistent between exotic and native species. Exotic invasives had greater survival than exotic non-invasives under high nutrient conditions in both experiments, and only exotic invasives showed consistently strong biomass responses to nutrient addition. For native species, there were no differences between invasives and non-invasives in survival in high nutrient conditions in the glasshouse or field; however, only invasive species showed a positive growth response to high nutrient conditions. 5 This study provides clear evidence that the success of exotic invasive species in this low fertility vegetation community is facilitated by the addition of nutrients. It would appear that on relatively infertile (particularly phosphorus-limited) sites, invasive species cannot take advantage of additional resources provided by physical disturbance or water addition due to overwhelming nutrient-limitation. We suggest that a combination of the environmental conditions (nutrient-enrichment) and invading species having traits that allow high survival and faster growth in response to nutrients, may allow successful invasion in Hawkesbury Sandstone communities.

206 citations

Journal Article•DOI•
The physiology of invasive plants in low-resource environments

[...]

Jennifer L. Funk1•
Chapman University1
01 Jan 2013-Conservation Physiology
TL;DR: This review examines physiological and morphological traits of native and invasive species occurring in environments characterized by low nutrient, water and light availability in species invading low-resource environments.
Abstract: While invasive plant species primarily occur in disturbed, high-resource environments, many species have invaded ecosystems characterized by low nutrient, water, and light availability. Species adapted to low-resource systems often display traits associated with resource conservation, such as slow growth, high tissue longevity, and resource-use efficiency. This contrasts with our general understanding of invasive species physiology derived primarily from studies in high-resource environments. These studies suggest that invasive species succeed through high resource acquisition. This review examines physiological and morphological traits of native and invasive species in low-resource environments. Existing data support the idea that species invading low-resource environments possess traits associated with resource acquisition, resource conservation or both. Disturbance and climate change are affecting resource availability in many ecosystems, and understanding physiological dif ferences between native and invasive species may suggest ways to restore invaded ecosystems.

204 citations

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Do invasive alien plants benefit more from global environmental change than native plants

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Yanjie Liu1, Yanjie Liu2, Ayub M. O. Oduor1, Ayub M. O. Oduor3, Zhen Zhang4, Anthony Manea5, Ifeanna M. Tooth6, Michelle R. Leishman5, Xingliang Xu2, Mark van Kleunen1 •
University of Konstanz1, Chinese Academy of Sciences2, Technical University of Kenya3, Anhui Agricultural University4, Macquarie University5, Royal Botanic Gardens6
01 Aug 2017-Global Change Biology
TL;DR: Elevated temperature and CO2 enrichment increased performance of invasive alien plants more strongly than was the case for native plants, and increases in the four other components of global environmental change considered, particularly global warming and atmosphericCO2 enrichment, may further increase the spread of invasive plants in the future.
Abstract: Invasive alien plant species threaten native biodiversity, disrupt ecosystem functions and can cause large economic damage. Plant invasions have been predicted to further increase under ongoing global environmental change. Numerous case studies have compared the performance of invasive and native plant species in response to global environmental change components (i.e. changes in mean levels of precipitation, temperature, atmospheric CO2 concentration or nitrogen deposition). Individually, these studies usually involve low numbers of species and therefore the results cannot be generalized. Therefore, we performed a phylogenetically controlled meta-analysis to assess whether there is a general pattern of differences in invasive and native plant performance under each component of global environmental change. We compiled a database of studies that reported performance measures for 74 invasive alien plant species and 117 native plant species in response to one of the above-mentioned global environmental change components. We found that elevated temperature and CO2 enrichment increased the performance of invasive alien plants more strongly than was the case for native plants. Invasive alien plants tended to also have a slightly stronger positive response to increased N deposition and increased precipitation than native plants, but these differences were not significant (N deposition: P = 0.051; increased precipitation: P = 0.679). Invasive alien plants tended to have a slightly stronger negative response to decreased precipitation than native plants, although this difference was also not significant (P = 0.060). So while drought could potentially reduce plant invasion, increases in the four other components of global environmental change considered, particularly global warming and atmospheric CO2 enrichment, may further increase the spread of invasive plants in the future.

186 citations

Journal Article•DOI•
Can ecological stoichiometry help explain patterns of biological invasions

[...]

Angélica L. González1, John S. Kominoski1, Michael Danger1, Seiji Ishida1, Noriko Iwai1, Anja Rubach1 •
Pontifical Catholic University of Chile1
01 May 2010-Oikos
TL;DR: A conceptual model that integrates hypotheses of biological invasions within a framework structured by fundamental principles of ecological stoichiometry provides a framework that can help explain how chemical elements and energy constrain key physiological and ecological processes, which can ultimately determine the success of invasive organisms.
Abstract: Several mechanisms for biological invasions have been proposed, yet to date there is no common framework that can broadly explain patterns of invasion success among ecosystems with different resource availabilities. Ecological stoichiometry (ES) is the study of the balance of energy and elements in ecological interactions. This framework uses a multi-nutrient approach to mass-balance models, linking the biochemical composition of organisms to their growth and reproduction, which consequently influences ecosystem structure and functioning. We proposed a conceptual model that integrates hypotheses of biological invasions within a framework structured by fundamental principles of ES. We then performed meta-analyses to compare the growth and production performances of native and invasive organisms under low- and high-nutrient conditions in terrestrial and aquatic ecosystems. Growth and production rates of invasive organisms (plants and invertebrates) under both low- and high-nutrient availability were generally larger than those of natives. Nevertheless, native plants outperformed invasives in aquatic ecosystems under low-nutrient conditions. We suggest several distinct stoichiometry-based mechanisms to explain invasion success in low- versus high-nutrient conditions; low-nutrient conditions: higher resource-use efficiency (RUE; C:nutrient ratios), threshold elemental ratios (TERs), and trait plasticity (e.g. ability of an organism to change its nutrient requirements in response to varying nutrient environmental supply); high-nutrient conditions: higher growth rates and reproductive output related to lower tissue C:nutrient ratios, and increased trait plasticity. Interactions of mechanisms may also yield synergistic effects, whereby nutrient enrichment and enemy release have a disproportionate effect on invasion success. To that end, ES provides a framework that can help explain how chemical elements and energy constrain key physiological and ecological processes, which can ultimately determine the success of invasive organisms.

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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.