Geographic variation and temporal changes in plant–herbivore interaction: Case studies with Solidago altissima in native and introduced ranges

Plants are subjected to environmental gradients and may encounter various herbivores, leading to geographic variation in defensive traits. The present review highlights that biological invasions are remarkable natural experiments for studying geographic variation in plant–herbivore interaction and tracking temporal dynamics in plant defense in response to environmental changes. Studies from this viewpoint can challenge various general topics in plant ecology, including the evolution of plant defense and indirect interactions among plants. First, I provide a brief overview on how the introduction of exotic herbivores drives rapid evolution after the establishment of exotic plants and its impacts on native plants. Second, I present a series of case studies investigating the patterns and mechanisms of geographic variation in the interaction between Solidago altissima and Corythucha marmorata (lace bug) in the native range in the United States and the introduced range in Japan. By combining biogeographical and experimental approaches, my collaborators and I unraveled the temporal dynamics of S. altissima's resistance to lace bugs and explored the drivers of differentiation in resistance between native and introduced ranges. These studies provide new insight into the geographic variation in exotic plant–herbivore interaction by unraveling the mechanisms and the temporal scale that cause the variation. These findings are vital not only for predicting invasiveness of exotic plants but also for understanding the evolution of plant–herbivore interaction in community contexts and under climate change.     

Environmentally triggered variability in the genetic variance–covariance of herbivory resistance of an exotic plant Solidago altissima

The variability in the genetic variance–covariance (G‐matrix) in plant resistance and its role in the evolution of invasive plants have been long overlooked. We conducted an additional analysis of the data of a reciprocal transplant experiment with tall goldenrod, Solidago altissima, in multiple garden sites within its native range (USA) and introduced range (Japan). We explored the differences in G‐matrix of resistance to two types of foliar herbivores: (a) a lace bug that is native to the USA and recently introduced to Japan, (b) and other herbivorous insects in response to plant origins and environments. A negative genetic covariance was found between plant resistances to lace bugs and other herbivorous insects, in all combinations of garden locations and plant origins except for US plants planted in US gardens. The G‐matrix of the resistance indices did not differ between US and Japanese plants either in US or Japanese gardens, while it differed between US and Japanese gardens in both US and Japanese plants. Our results suggested that the G‐matrix of the plant resistance may have changed in response to novel environmental differences including herbivore communities and/or other biotic and abiotic factors in the introduced range. This may have revealed a hidden trade‐off between resistances, masked by the environmental factors in the origin range. These results suggest that the stability of the genetic covariance during invasion, and the environmentally triggered variability in the G‐matrices of plant resistance may help to protect the plant against multiple herbivore species without changing its genetic architecture and that this may lead to a rapid adaptation of resistance in exotic plants. Local environments of the plant also have a critical effect on plant resistance and should be considered in order to understand trait evolution in exotic plants.     

Community structure of insect herbivores on introduced and native Solidago plants in Japan

We compared community composition, density, and species richness of herbivorous insects on the introduced plant Solidago altissima L. (Asteraceae) and the related native species Solidago virgaurea L. in Japan. We found large differences in community composition on the two Solidago species. Five hemipteran sap feeders were found only on S. altissima. Two of them, the aphid Uroleucon nigrotuberculatum Olive (Hemiptera: Aphididae) and the scale insect Parasaissetia nigra Nietner (Hemiptera: Coccidae), were exotic species, accounting for 62% of the total individuals on S. altissima. These exotic sap feeders mostly determined the difference of community composition on the two plant species. In contrast, the herbivore community on S. virgaurea consisted predominately of five native insects: two lepidopteran leaf chewers and three dipteran leaf miners. Overall species richness did not differ between the plants because the increased species richness of sap feeders was offset by the decreased richness of leaf chewers and leaf miners on S. altissima. The overall density of herbivorous insects was higher on S. altissima than on S. virgaurea, because of the high density of the two exotic sap feeding species on S. altissima. We discuss the importance of analyzing community composition in terms of feeding guilds of insect herbivores for understanding how communities of insect herbivores are organized on introduced plants in novel habitats.     

Community‐wide impact of an exotic aphid on introduced tall goldenrod

1. The aphid Uroleucon nigrotuberculatum Olive, which is specialised to the tall goldenrod, Solidago altissima L., in its native range, has become a dominant species on the introduced tall goldenrod in Japan. How this exotic aphid influenced arthropod communities on the introduced tall goldenrod in aphid‐present (spring) and aphid‐absent (autumn) seasons was examined, using an aphid removal experiment. 2. In spring, aphid presence increased ant abundance because aphid honeydew attracted foraging ant workers. A significant negative correlation was found between the numbers of ants and herbivorous insects other than aphids on the aphid‐exposed plants, but no significant correlation was detected on the aphid‐free plants. Thus, the aphid presence was likely to decrease the abundance of co‐occurring herbivorous insects through removal behaviour of the aphid‐tending ants. There were no significant differences in plant traits between the aphid‐exposed and aphid‐free plants. 3. In autumn, the numbers of lateral shoots and leaves, and the leaf nitrogen content were increased in response to the aphid infestation in spring. Because of the improvement of plant traits by aphid feeding, the abundance of leaf chewers increased on aphid‐exposed plants. In contrast, the abundance of sap feeders decreased on the aphid‐exposed plants. In particular, the dominant scale insect among sap feeders, Parasaissetia nigra Nietner, decreased, followed by a decrease in the abundance of ants attending P. nigra. Thus, aphid feeding may have attenuated the negative impacts of the tending ants on leaf chewers. 4. Aphid presence did not change herbivore species richness but changed the relative density of dominant herbivores, resulting in community‐wide effects on co‐occurring herbivores through ant‐mediated indirect effects, and on temporally separated herbivores through plant‐ and ant‐mediated indirect effects. The aphid also altered predator community composition by increasing and decreasing the relative abundance of aphid‐tending ants in the spring and autumn, respectively.     

Top-down effects of insect herbivores during early succession: influence on biomass and plant dominance

We tested the hypothesis that phytophagous insects would have a strong top-down effect on early successional plant communities and would thus alter the course of succession. To test this hypothesis, we suppressed above-ground insects at regular intervals with a broad-spectrum insecticide through the first 3 years of old-field succession at three widely scattered locations in central New York State. Insect herbivory substantially reduced total plant biomass to a similar degree at all three sites by reducing the abundance of meadow goldenrod, Solidago altissima. As a result, Euthamia graminifolia dominated control plots whereas S. altissima dominated insecticide-treated plots by the third year of succession. S. altissima is the dominant old-field herbaceous species in this region but typically requires at least 5 years to become dominant. Past explanations for this delay have implicated colonization limitation whereas our data demonstrate that insect herbivory is a likely alternative explanation. A widespread, highly polyphagous insect, the xylem-tapping spittlebug, Philaenus spumarius, appeared to be the herbivore responsible for the reduction in standing crop biomass at all three sites. Insect herbivory typically caused little direct leaf tissue loss for the ten plant species we examined, including S. altissima. Consequently, the amount of leaf area removed was not a reliable indicator of the influence of insect herbivory on standing crop biomass or on early succession. Overall, we found a strong top-down effect of insect herbivores on biomass at several sites, so our results may be broadly applicable. These findings run counter to generalizations that top-down effects of herbivores, particularly insects, are weak in terrestrial systems. These generalizations may not apply to insects, such as spittlebugs, that can potentially mount an effective defense (i.e., spittle) against predators and subsequently reach relatively high abundance on common plant species. Our results suggest that insect herbivory may play an important but often overlooked role during early old-field succession. Received: 26 December 1998 / Accepted: 3 April 1999     

Coexistence between native and exotic species is facilitated by asymmetries in competitive ability and susceptibility to herbivores

Differences between native and exotic species in competitive ability and susceptibility to herbivores are hypothesized to facilitate coexistence. However, little fieldwork has been conducted to determine whether these differences are present in invaded communities. Here, we experimentally examined whether asymmetries exist between native and exotic plants in a community invaded for over 200 years and whether removing competitors or herbivores influences coexistence. We found that natives and exotics exhibit pronounced asymmetries, as exotics are competitively superior to natives, but are more significantly impacted by herbivores. We also found that herbivore removal mediated the outcome of competitive interactions and altered patterns of dominance across our field sites. Collectively, these findings suggest that asymmetric biotic interactions between native and exotic plants can help to facilitate coexistence in invaded communities.     

Responses of a native beetle to novel exotic plant species with varying invasion history

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Geographic variations in phenotypic traits of the exotic herb Solidago altissima and abundance of recent established exotic herbivorous insects

Abstract

Many invasive plants increase aggressiveness after introduction. Since evolutionary forces such as herbivore pressure may change over different time scales, understanding the changes in biotic interactions in invasive plants through time can clarify the mechanism of their evolution in aggressiveness. In this study, we examined the geographic variation in phenotypic traits of Solidago altissima and the abundance of two exotic herbivorous insect species (the aphid, Uroleucon nigrotuberculatum and the lacebug, Corythucha marmorata), which are recently expanding their habitat on S. altissima populations over Japan. The two exotic insects were present at high density on S. altissima throughout their range. No differences in growth traits (plant height and number of leaves) were found among populations, and all plants examined appear to be exclusively hexaploid. Future studies on population genetics and common garden experiments are necessary to evaluate the potential evolutionary dynamics of the S. altissima after introduction.     

Heterospecific pollen transfer from an exotic plant to native plants: assessing reproductive consequences in an Andean grassland

Background: The presence of exotic plants increases the heterospecific pollen (HP hereafter) received by native plants and reduces their reproductive output.

Aims: We assessed whether the exotic herb Echium vulgare (Boraginaceae) increased HP and reduced seed output of the native plants Phacelia secunda (Boraginaceae) and Stachys albicaulis (Lamiaceae) in an Andean locality, central Chile.

Methods: The presence of HP was studied in native plants growing with and without co-existence with the exotic E. vulgare. A complementary hand pollination experiment was carried out to assess whether E. vulgare pollen reduced the reproductive success of native plants.

Results: In the presence of E. vulgare, 17.3% and 3.7% of P. secunda and S. albicaulis individuals that coexisted with the exotic species received HP. For P. secunda, the number of conspecific pollen grains decreased in invaded patches compared with non-invaded patches; no differences were observed for S. albicaulis. The pollen of E. vulgare negatively affected the reproductive success of S. albicaulis but not that of P. secunda.

Conclusions: The presence of HP cannot be predicted from the presence of exotic plants alone, and other factors, such as flower morphology, could explain the greater HP transfer in P. secunda (actinomorphic flowers) than in S. albicaulis (zygomorphic flowers). A higher negative effect of E. vulgare pollen on P. secunda versus S. albicaulis could be related to the phylogenetic resemblance between the exotic donor and native recipient plant because pollen-stigma compatibility may be evolutionary conserved through common lineages.     

Urban landscape and forest vegetation regulate the range expansion of an exotic lace bug Corythucha marmorata (Hemiptera: Tingidae)

Landscapes and vegetation are critical factors in dispersion of exotic insects and expansion of their range. However, few studies have addressed how the surrounding landscape affects the establishment of exotic insects. We assessed the relationship between establishment of an exotic lace bug Corythucha marmorata (Uhler) and the surrounding landscape in the northern edge of the lace bug's expanded range. We found that the lace bugs showed variability in their density among populations. Urban areas had a positive effect, while the natural forest vegetation had a negative effect on lace bug density, with a buffer range of 1–2 km. Moreover, their abundance decreased with distance from the source population. Our results suggest that natural forest landscapes in urban areas may inhibit the range expansion of invasive insects that feed on exotic plants growing in human‐disturbed habitats.     

Feeding preferences of Melanoplus femurrubrum grasshoppers on native and exotic grasses: behavioral and molecular approaches

Generalist insect herbivores, such as grasshoppers, may either avoid feeding on exotic plants, potentially enabling these plants to become invasive in the introduced range, or insects may incorporate exotic plants into their diet, contributing to the biotic resistance of native communities and potentially preventing plant invasions. Accurate determination of insect diet preferences with regard to native and exotic plants can be challenging, but this information is critical for understanding the interaction between native herbivores and exotic plants, and ultimately the mechanisms underlying plant invasions. To address this, we combined behavioral and molecular approaches to accurately compare food consumption of the polyphagous red‐legged grasshopper, Melanoplus femurrubrum (De Geer) (Orthoptera: Acrididae), on native [Andropogon gerardii Vitman and Bouteloua curtipendula (Michx.) Torr.] and exotic, potentially invasive grasses [Miscanthus sinensis Andersson and Bothriochloa ischaemum (L.) Keng] (all Poaceae). We found that M. femurrubrum grasshoppers demonstrated strong feeding preferences toward exotic grasses in experiments with intact plants under both field and greenhouse conditions, but they showed no preference in experiments with clipped leaves. Additionally, we sampled the gut contents of M. femurrubrum collected in the field and identified the ingested plant species based on DNA sequences for the non‐coding region of the chloroplast trnL (UAA) gene. We found that exotic plants were prevalent in the gut contents of grasshoppers collected at study sites in Ohio and Maryland, USA. These results suggest that the generalist herbivore M. femurrubrum does not avoid feeding on exotic grasses with which they do not share coevolutionary history. In addition, by demonstrating greater food consumption of exotic plants, these grasshoppers potentially provide biotic resistance should these grasses escape cultivation and become invasive in the introduced range.     

土著昆虫素毒蛾在本地植物芦苇与入侵植物互花米草上的生活史

互花米草(Spartina alterniflora)入侵盐沼生态系统导致了土著广食性昆虫素毒蛾(Laelia coenosa)发生宿主转移。但是, 目前对素毒蛾在互花米草和芦苇(Phragmites australis)上的生活史规律的比较尚未见报道, 而此信息对评价素毒蛾能否持续利用互花米草具有重要的参考价值。为了明确素毒蛾在其原始宿主芦苇和外来新宿主互花米草上的生活史动态, 我们在上海崇明长江口盐沼湿地中, 对素毒蛾在芦苇和互花米草生境中的发生情况进行了系统调查。结果显示, 虽然素毒蛾在芦苇和互花米草上均一年发生3代, 并都以幼虫越冬, 但在互花米草生境中, 越冬代幼虫开始越冬的时间要比芦苇中晚20 d左右, 其他世代中的多个虫态在互花米草上持续出现的时间也比芦苇上延迟了约10 d。这些结果表明, 互花米草入侵后素毒蛾在外来植物上出现的持续时间虽然发生了延长, 但其年世代数未变化。我们推测素毒蛾在互花米草和芦苇上生长发育规律的差异可能受生境的资源可利用性及两种植物的营养与防御水平调控。     

Habitat expansion of an exotic lace bug, Corythucha marmorata (Uhler) (Hemiptera: Tingidae), on the Kii Peninsula and Shikoku Island in western Japan

Habitat expansion of an exotic lace bug Corythucha marmorata (Uhler) was observed on the Kii Peninsula in 2003–2004, and on Shikoku Island between 2004 and 2007. The bug was first sighted in Nishinomiya City in Hyogo Prefecture in 2000, and then further south in central Kii Peninsula in 2003 before reaching the southern tip of the peninsula by 2004. The bug was first observed in the Tokushima and Ehime Prefectures of Shikoku Island in 2004, after which the range expanded and extended across the entire island by 2007. In this study, six wild Asteraceae species were identified as the host plants to the lace bug.     

入侵与本地植物对气候变暖和氮沉降交互效应的动态响应

入侵与本地植物对气候变暖和氮沉降交互效应的动态响应 在全球气候变暖背景下,对入侵物种扩张的预测往往并未考虑到同时出现的氮沉降变化。因此,气候变暖和氮沉降的复杂交互将如何改变入侵物种和本地物种的生长动态尚需进一步探索。在此,本研究假设氮沉降和温度的同时增加可能对入侵植物的生长促进效应大于本地植物。本研究在模拟气候变暖、氮沉降及其交互处理下,对入侵植物加拿大一枝黄花(Solidago canadensis L.)及其本地共存物种艾草(Artemisia argyi Levl. et Van)的生长响应进行温室对照试验。结果表明：由于氮沉降对物种生长的显著促进效应,温度升高和氮沉降的交互作用导致入侵物种和本地物种的生长适应性显著提高,即温氮交互可能使区域微生境更加有利于植物生长。然而,在生物量、高度和直径等生态适应特征方面,入侵物种加拿大一枝黄花的相对增加幅度显著低于本地物种艾草,这表明入侵物种加拿大一枝黄花相对于本地物种艾草的生长优势会在未来气候变暖与氮沉降持续增强的背景下逐渐减弱。因此,纳入氮沉降因素可能会缓解入侵物种加拿大一枝黄花在气候变暖条件下的入侵扩张。     

Biological soil crusts determine the germination and growth of two exotic plants

In arid and semiarid ecosystems, the potential threats of exotic invasive species are enhanced due to increasing human activities. Biological soil crusts (BSCs), acting as arid ecosystem engineers, may play an important role in preventing the establishment of exotic invasive plants. Our goal was to examine whether BSCs could inhibit the establishment of probable exotic plant species originating from adjacent grasslands located along the southeast edge of the Tengger Desert. In our study, we investigated the effects of three BSC types (cyanobacteria, lichen, and moss crusts) under two disturbance conditions (intact and disturbed) on the establishment of two exotic plant species (Ceratoides latens and Setaria viridis) using indoor experiments. We found both negative and positive effects of BSCs on the establishment of the two exotic plant species. Compared with the disturbed BSCs, the germination percentages of C. latens and S. viridis were reduced by 54% to 87% and 89% to 93%, respectively, in intact BSCs. In contrast, BSCs significantly promoted the height growth and aboveground biomass of the two exotic plant species (p < .05) by enhancing the soil water and nutrient availability for the exotic plants. Our results confirm that BSCs strongly suppress the rapid expansion of exotic plant populations by inhibiting germination of seed with big size or appendages and have a weak inhibitory effect on exotic plant with small and smooth seeds. This may decrease the threat of propagation of exotic species. In the meantime, BSCs promote the growth of a few successful engraftment seedlings, which increased the beta diversity. Our work suggests that better understanding the two opposing effects of BSCs on the establishment of exotic plant species in different growth stages (germination and growth) is important for maintaining the health and stability of revegetated regions.     

Climate warming affects biological invasions by shifting interactions of plants and herbivores

Plants and herbivorous insects can each be dramatically affected by temperature. Climate warming may impact plant invasion success directly but also indirectly through changes in their natural enemies. To date, however, there are no tests of how climate warming shifts the interactions among invasive plants and their natural enemies to affect invasion success. Field surveys covering the full latitudinal range of invasive Alternanthera philoxeroides in China showed that a beetle introduced for biocontrol was rare or absent at higher latitudes. In contrast, plant cover and mass increased with latitude. In a 2‐year field experiment near the northern limit of beetle distribution, we found the beetle sustained populations across years under elevated temperature, dramatically decreasing A. philoxeroides growth, but it failed to overwinter in ambient temperature. Together, these results suggest that warming will allow the natural enemy to expand its range, potentially benefiting biocontrol in regions that are currently too cold for the natural enemy. However, the invader may also expand its range further north in response to warming. In such cases where plants tolerate cold better than their natural enemies, the geographical gap between plant and herbivorous insect ranges may not disappear but will shift to higher latitudes, leading to a new zone of enemy release. Therefore, warming will not only affect plant invasions directly but also drive either enemy release or increase that will result in contrasting effects on invasive plants. The findings are also critical for future management of invasive species under climate change.     

Impacts of a native parasitic plant on an introduced and a native host species: implications for the control of an invasive weed

Background and Aims: While invasive species may escape from natural enemies in thenew range, the establishment of novel biotic interactions withspecies native to the invaded range can determine their success.Biological control of plant populations can be achieved by manipulationof a species' enemies in the invaded range. Interactions weretherefore investigated between a native parasitic plant andan invasive legume in Mediterranean-type woodlands of SouthAustralia. Methods: The effects of the native stem parasite, Cassytha pubescens,on the introduced host, Cytisus scoparius, and a co-occurringnative host, Leptospermum myrsinoides, were compared. The hypothesisthat the parasitic plant would have a greater impact on theintroduced host than the native host was tested. In a fieldstudy, photosynthesis, growth and survival of hosts and parasitewere examined. Key Results: As predicted, Cassytha had greater impacts on the introducedhost than the native host. Dead Cytisus were associated withdense Cassytha infections but mortality of Leptospermum wasnot correlated with parasite infection. Cassytha infection reducedthe photosynthetic rates of both hosts. Infected Cytisus showedslower recovery of photosystem II efficiency, lower transpirationrates and reduced photosynthetic biomass in comparison withuninfected plants. Parasite photosynthetic rates and growthrates were higher when growing on the introduced host Cytisus,than on Leptospermum. Conclusions: Infection by a native parasitic plant had strong negative effectson the physiology and above-ground biomass allocation of anintroduced species and was correlated with increased plant mortality.The greater impact of the parasite on the introduced host maybe due to either the greater resources that this host providesor increased resistance to infection by the native host. Thisdisparity of effects between introduced host and native hostindicates the potential for Cassytha to be exploited as a controltool.