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Keywords:

  • Exotic plant invasion;
  • host range expansion;
  • native herbivore;
  • plant–insect novel association

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information
  1. The impact of plant invaders on the fitness of native insects has received increasing attention, but it remains unclear how native insects that have a taxonomic conservatism in host–plant use respond to novel hosts.
  2. In this study, an experimental approach was taken to this issue by comparing the preference and performance of a native beetle, Cassida piperata Hope, on native hosts Chenopodium album and Alternanthera sessilis, and non-coevolved exotic hosts Alternanthera spinosus and Alternanthera philoxeroides of varying invasion history with choice and cross-rearing experiments.
  3. In host choice experiments, adult beetles preferred to oviposit on the older invader A. spinosus to the same degree as it did the native hosts, but generally avoided the newer invader A. philoxeroides. However, in rearing experiments, larval beetles developed more slowly on the two exotic hosts than on the native hosts.
  4. The varying responses of adult beetles to invaders might be explained by their differing invasive history, and suggest that the beetle has adapted to the older invader behaviourally. However, the slower development of the beetle on the two invaders suggests that the beetle has failed to adapt physiologically to either species of invasive plant.
  5. These results offer insights into the temporal dynamics of a native insect adapting to plant invaders, and suggest that when testing the impact of exotic plant invasion on native insect fitness, it is necessary to consider the duration of novel association between the insect and the novel plant species.

Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

The success of alien species in their new range has often been viewed as a result of escaping from their co-evolved natural enemies (the enemy release hypothesis) (Keane & Crawley, 2002). Nonetheless, there is growing evidence that some native insects have expanded their host range and formed novel associations with alien invasive plants (Strauss et al., 2006; Carroll & Fox, 2007). Although many studies have examined the effects of native herbivores on exotic plant invasion, the effects of exotic plant invasion on the fitness of novel-associated native herbivores have received little attention (Bertheau et al., 2010). A few authors have compared the performance of insects on their novel and ancestral hosts and found that, in general, insects perform more poorly on novel hosts than on their ancestral hosts (Bertheau et al., 2010), although in some cases insects perform better on novel hosts than on their ancestral hosts due to the novel hosts' lack of defences (Gandhi & Herms, 2010; Desurmont et al., 2011). However, almost all of these studies only compared the performance of native herbivores on pairs of native and exotic hosts (Trowbridge & Todd, 2001; Keeler & Chew, 2008; Cogni, 2010), and the duration of these novel associations has not been considered.

As most phytophagous insects larvae are immobile, and thus grow and develop on the hosts chosen by the adults for oviposition, the relationship between adult oviposition preference and larval performance is fundamental to understanding many aspects of insect host plant use (Thompson, 1988). Accordingly, any host range expansion of phytophagous insects is initiated by plastic or evolutionary changes in adult host choice behaviour, followed by evolution in physiology and morphology in response to the selection imposed by novel hosts (Jaenike, 1990). In response to novel invasive plants, especially those with native relatives, adults of some native insects may recognise them as suitable hosts for oviposition. However, without a co-evolutionary history, the exotic hosts may be of lower quality or even toxic for native insects and result in a reduction of insect fitness, thus serving as ecological traps (Schlaepfer et al., 2005). In such cases, plastic or evolutionary adaptive changes are critical for mitigating the negative impacts of novel hosts on insect fitness and maintaining a population's demographic stability. Adaptive changes in behaviour, physiology and life history have been reported in several native insects, such as soapberry bugs (Jadera, Leptocoris spp.) (Strauss et al., 2006). However, how quickly native herbivores can adapt to invasive plants remains unclear.

Here, we take an experimental approach to this issue by comparing the preference and performance of a native Chinese beetle on two native hosts and two non-coevolved exotic plant species of the Amaranthaceae family with varying invasion history. Cassida piperata Hope (Coleoptera: Cassididae) is an oligophagous beetle found throughout eastern Asia and Russia (Tang, 1994); it only feeds upon species in the Amaranthaceae and Chenopodiaceae families in China, where it has historically occurred, and mainly on the native species Chemopodium album Linn. and Alternanthera sessilis (L.) DC. (Lin et al., 1990). However, since the invasion of the exotic species Amaranthus spinosus Linn. and Alternanthera philoxeroides (Mart.) Griseb, the beetle has expanded its host range and now mainly occurs on these two exotic species (X. M. Lu, pers. obs.). A. spinosus, native to the tropical Americas, was first introduced into China in the 1830s, while A. philoxeroides, native to South America, was first introduced into China in the 1930s (Li & Xie, 2002). The beetle had no association with either exotic species before they were introduced into China, and has a different exposure history to each one.

In this study we compared the adult oviposition preference and larval performance of the beetle taken from six populations on the two exotic and two native hosts, using caged choice tests and laboratory cross-rearing experiments. In particular, we predicted that: (i) adult beetles would find the two invasive species and the two native plants equally suitable after such a long exposure to the novel hosts; and (ii) larval beetles would develop more slowly on A. philoxeroides than on A. spinosus, as the beetles have associated with A. spinosus for 100 years longer than they have with A. philoxeroides

Materials and methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

Experimental organisms

In China, C. piperata (see Fig. S1A,B) is widely distributed and is present from early May to October. There are four generations per year and the adults overwinter in the soil or under the litter of host plants (Tang, 1994). Both larvae and adults feed exclusively on the leaves of host plants, producing tiny feeding scars, and eggs are laid individually on the undersides of leaves.

Chemopodium album (Fig. S1C) is an annual plant native to China. It reproduces solely by sexual production; it flowers and produces seeds from August to October that germinate early the following April (http://www.cvh.org.cn). Alternanthera sessilis (Fig. S1D), meanwhile, is a native annual or short-lived perennial herb, capable of reproducing both by vegetative means from stem buds or sexually by seeds. It produces small seeds in August–October that can be transported by wind and that germinate the following April in moist soils (http://www.cvh.org.cn).

Amaranthus spinosus (Fig. S1E) is an annual herb that was first introduced into China in the 1830s. It is now widely distributed in more than 20 provinces across southern and northern China (Li & Xie, 2002). It propagates sexually, flowers from May to August, and produces seeds from August to October that germinate in early April the following year.

Alternanthera philoxeroides (Figure S1F) is an herbaceous perennial with horizontal to ascending stems, first introduced into China in the 1930s (Ma, 2001). Since then, it has spread rapidly and now occurs over a large area from 21.5°N to 31.8°N (Lu et al., 2013). In its invasive range, A. philoxeroides rarely sets seeds and reproduces solely by vegetative means from stem and root buds (Sainty et al., 1998).

Material collection

In May 2008, we collected larval beetles from six populations distributed across a large area of China (Shanghai, Yangzhou, Wuhan,Yueyang, Zhengzhou and Xinyang populations) (Fig. S2). The distance between any two populations was at least 100 km. Initially, we planned to sample larval beetles from different host plants, but in the field the beetle was much more common on A. philoxeroides than on other species. So to reduce the possible trans-generational impact of parental hosts on offspring performance, we only sampled larvae from A. philoxeroides. The larvae were taken back to the laboratory and reared on A. philoxeroides, and their offspring were used for the experiments.

All the tested host plants were collected from the Wuhan location. The seeds of A. spinosus and C. album were collected during the fall of 2007 in a suburb of Wuhan. The seeds were sown in pots filled with topsoil in early March 2008 and placed in an unheated greenhouse without artificial light. Most of the seeds germinated in early April, and the seedlings were allowed to grow for another month. In May 2008, the seedlings were transplanted into pots (25 cm in diameter) filled with topsoil at the density of two seedlings per pot and placed in the same greenhouse to await use in the experiment. Both A. philoxeroides and A. sessilis were propagated clonally from cut stems. In early May, cut stems (5–7 cm long) of A. philoxeroides and A. sessilis were collected in a suburb of Wuhan and planted vertically into pots (25 cm in diameter) filled with topsoil and placed in the same greenhouse to await use in the experiment. As there are differences in morphology among the four host species, A. philoxeroides and A. sessilis were planted at a density of four seedlings per pot instead of two, as was done for A. spinosus and C. album, in order to attain a similar amount of host plant mass in every pot during the trial.

Adult oviposition preference experiment

To test the feeding and oviposition preferences of adult beetles among the four host species, we conducted a choice test from June to July 2008. For this experiment, 48 nylon cages (1 m × 1 m × 1 m) were placed on a lawn and four pots (one each of the four plant species) were randomly placed in each cage. Two pairs of newly mated adult beetles were released in each cage that had been reared on A. philoxeroides in the laboratory for one generation. Each insect population (from the six field collection sites) was replicated eight times. The number of eggs laid on each host plant in each cage was recorded every 3 days, over a 24-day period.

Larval rearing experiment

To compare the performance of larvae on exotic versus native hosts, we conducted a rearing experiment. We evaluated larval and pupal development time (days from egg hatch to emergence) and pupal weight, which are predictive of larval survival from predator attack (Haggstrom & Larsson, 1995) and adult fecundity (Butler & Walker, 1992) in other systems. Offspring of the second generation reared on A. philoxeroides in the laboratory were used for this experiment. In this and following experiments, we reared larvae on fresh leaf discs instead of whole plants. Mated second-generation females were allowed to lay eggs on leaves of the four host plant species. Then the leaf discs (with eggs) of each host plant species were transferred into individual Petri dishes lined with moist filter paper. The Petri dishes were held at 28 °C with a natural light/dark photoperiod (about LD 14:10 h). Each treatment was repeated 10–12 times, and a total of 278 larval beetles were used. Throughout the experiment, the filter papers were kept moist and fresh leaves were provided when necessary (leaves were changed daily after hatching). Only a few larvae died during the experiment. Following pupation, we weighed all pupae individually, recorded the date of their emergence, and calculated larval and pupal development times.

Cross-rearing experiment

To distinguish between the impacts of parental and rearing hosts on the performance of the larvae, we conducted a cross-rearing experiment under the same conditions and in the same laboratory as the larval survival experiment. The offspring of the third generation of beetles reared on A. philoxeroides in the laboratory were used for this experiment. Newly hatched larvae were transferred to leaves of the four host species planted in 25-cm-diameter pots and caged separately with nylon cages and reared for one generation. The newly hatched offspring from each host plant were then divided into four groups that had their offspring raised on leaves of the four host species in Petri dishes. These offspring were cultured in Petri dishes individually with leaves of their chosen host species. The Petri dishes were lined with moist filter paper and inspected every day until adult emergence, during which time the leaves were changed daily. Each treatment was repeated 10–12 times and a total of 1078 larval beetles were used. The period from newly hatched larva to moulting to the next life stage was recorded to calculate the larval and pupal development times, and pupae were weighed individually.

Data analyses

We used the Statistical Analysis System (SAS version 8.1, SAS Institute, Cary, North Carolina) to conduct all data analyses. Before analysis, data on the number of eggs in the choice experiments were square-root-transformed to achieve normality.

We used mixed anovas to test the dependence of the number of eggs, pupal weight, and larval and pupal development times on host species in the oviposition, feeding choice and rearing experiments. The models included host species as a fixed factor and insect population as a random factor. We performed additional mixed anovas to test the dependence of pupal weight, larval and pupal development time on parental host, rearing host and their interactions in the cross-rearing experiment. The models included parental host and rearing host as fixed factors and insect population as a random factor. When significant interactive effects occurred, we examined differences among treatment combinations using adjusted means partial difference tests (P < 0.05).

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

The number of eggs laid by adult beetles varied significantly among host plant species (F3,159 = 23.31, P < 0.0001). Adults laid most eggs on the native host C. album, followed by A. sessilis and the invasive plant A. spinosu, and laid the least on A. philoxeroides (Fig. 1a). This result indicates that C. piperata has accepted A. spinosu as a suitable host, equivalent to its native hosts, while it avoids A. philoxeroides.

image

Figure 1. The number of eggs (a), pupal weight (b) and larval and pupal developmental times (c) of Cassida piperata on different host species in the host choice and rearing experiments (means ± 1 SE). Columns with different letters are significantly different (P < 0.05).

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The pupal weight (F3,269 = 8.89, P < 0.0001) and larval and pupal developmental times (F3,269 = 26.89, P < 0.0001) also varied among host species. Pupae reared on C. album and A. spinosu were heavier than those reared on A. sessilis and A. philoxeroides (Fig. 1b). Meanwhile, beetle larvae and pupae developed more slowly on the exotic than on the native hosts, resulting in a longer developmental time on exotic species (Fig. 1c). The number of eggs and larval and pupal developmental times all varied significantly among insect populations (for both P < 0.0001), but pupal weight (F5,269 = 1.26, P = 0.2818) did not vary among insect populations.

The effect of parental and rearing host species on larval performance

Parental and rearing hosts interactively affected pupal weight and beetle developmental time (Table 1). Pupae were lighter on A. philoxeroides than on native hosts (Fig. 2a). When the beetle was parentally fed with a native host, their pupal weight was similar on A. spinosu and the two native species, but when they were parentally fed with invasive hosts, pupal weight was less on A. spinosu than on native hosts (Fig. 2a). In general, larvae and pupae developed more slowly on exotic hosts than on the native hosts regardless of their parental host species (Fig. 2b).

Table 1. anova results for the effects of parental and rearing hosts, and population on larval and pupal development time and pupa weight in the cross-rearing experiment
Source of variationd.f.Pupal weightLarval and pupal development times
FPFP
  1. Significant effects are shown in bold.

Parental host (PH)3  2.29  0.0769    5.98  0.0005
Rearing host (RH)348.76<0.0001274.29<0.0001
PH × RH9  1.96  0.0410    8.75<0.0001
Insect population5  3.17  0.0076  17.40<0.0001
Error1057
image

Figure 2. Pupal weight (a) and larval and pupal developmental times (b) of Cassida piperata on different host species after being reared on varying host species for one generation in the cross-rearing experiment. Values are means ± 1SE. Columns with different letters are significantly different (P < 0.05).

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Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

A phytophagous insect is generally expected to preferentially accept novel hosts that are phylogenetically close to its ancestral hosts and that are therefore likely to share certain chemical traits (Ødegaard et al., 2005; Bertheau et al., 2010). The ancestral hosts of C. piperata include Amaranthus ascendens and A. sessilis (www.biol.uni.wroc.pl), which share genera with the novel hosts A. spinosu and A. philoxeroides, respectively. Thus it is reasonable to assume that the beetle would be pre-adapted to the two novel hosts, at least behaviourally. However, while adult beetles accepted A. spinosu for oviposition, they avoided A. philoxeroides in the choice experiment. The quality (e.g. nitrogen content), morphology of a plant, other than its chemical traits, may also influence adult host preference (Jaenike, 1990). The performance of larval beetles on the two novel hosts in the rearing experiment indicated that the two exotic hosts are of the same quality to the beetle. Furthermore, the adults showed no preference in feeding and oviposition between morphologically different hosts A. spinosu and A. sessilis, suggesting that morphological differences between the two exotic species may not directly lead to the detected preference.

The observed difference in preference of adult beetles to the two novel hosts may reflect a temporal dynamic response of an insect to novel exotic species. The host range expansion or shift of a phytophagous insect to novel hosts is initiated by changes in host choice behaviour that impose new environmental pressures on individuals and thus facilitate evolutionary diversification (Oppenheim & Gould, 2002; Sol et al., 2005) . As A. spinosu was introduced into China about 100 years earlier than A. philoxeroides, a maximum of 400 more generations of the beetle could have been exposed to A. spinosu than to A. philoxeroides. Such a duration has been shown to be sufficient for evolutionary changes to occur in the behaviour, or even physiology, of insects towards non-coevolved novel plants (Strauss et al., 2006). Although the non-genetic maternal effect, the effect of maternal environment on offspring, is reported to influence insect host preference (Liu et al., 2005; Amarillo-Suarez & Fox, 2006), it is less likely to occur in this case because adult beetles avoid feeding and ovipositing on A. philoxeroides even when the beetle has been reared on that host for two generations in the choice experiments.

Although adult beetles responded differently to the two exotic hosts, their larvae and pupae developed more slowly on both of the exotic hosts than on the native hosts. Such poor performance of insects on novel hosts compared with ancestral hosts was also found by Bertheau et al. (2010) in a meta-analysis. The poorer performance on novel hosts than on ancestral hosts may have resulted from evolutionary non-adaption in physiology to the novel hosts, regardless of changes in adults' preference. Such non-adaptation in physiology to novel hosts has also been reported in the soapberry bugs Jadera haematoloma, Ophraella notulata and Baltimore checkerspot Euphydryas phaeton, even though their adults have shown changes in host choice behaviour (Bowers et al., 1992; Carroll & Fox, 2007).

The non-genetic maternal effect also affected larval performance on the novel hosts in our study. The hosts on which the parental generation have been reared can affect the offsprings' developmental rate, egg size, and phenology and thus may influence the direction and pace of their evolution (Fox et al., 1995; Amarillo-Suarez & Fox, 2006). In the cross experiments, beetle pupal weight was similar between the exotic host A. spinosu and the two native hosts when the beetles were parentally reared on native hosts, but smaller on A. spinosu when the beetles were parentally reared on exotic hosts. While it has been shown that the maternal effect can be found in both herbivores and plants in hetero-environments, it may result in large time lags in an evolutionary response to natural selection (Roach & Wulff, 1987; Lande & Kirkpatrick, 1990). This might explain why, while C. piperata has adapted to A. spinosu behaviourally, it failed to adapt to A. spinosu physiologically nearly 200 years after the plant's introduction.

Even though exotic plant invasion has been proposed to be the second biggest threat to biodiversity (D'Antonio & Kark, 2002), how plant invasions affect native insect species has remained largely unstudied. While our experiments indicated that exotic plant invasion may harm individual native beetles, whether this will translate into population decline needs further study. Given that invasive plant species often form dense monocultures over large areas (Gurevitch et al., 2011) and provide native insects with a new range of enemy-free habitat (Bowers et al., 1992; Chaplin-Kramer et al., 2011), they may facilitate local and geographic range expansion, save host searching time and promote population growth of native insects that prove able to exploit novel hosts. Furthermore, the detected genetic variation and non-genetic maternal effects could also buffer the negative effects of plant invasion on the native beetle.

The impacts of exotic plants on native insect species have received increasing attention. However, most studies have only compared the performance of native insects on native and invasive plants, while overlooking the invasion history. With this study, we have shown that native species responded differently to invaders with different invasion histories, although larvae developed more slowly on both invaders than on native hosts. The varying invasion history of target plants might be at least partially responsible for such variation, as native herbivores need time to accept and adapt to novel hosts, though other differing traits (e.g. chemical composition) between the two invaders may also lead to such variation. Likewise, field experiments have demonstrated that native herbivores accumulate on exotic species over time (Siemann et al., 2006). Therefore, further studies testing the impacts of invasive plants on native insects should carefully consider the duration of the novel association between native insects and plant invaders.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

We would like to thank Shunliang Feng and Wenfeng Guo for their field and laboratory assistance, and also Tony Grice, Matthew Purcell and Roy van Driesche for valuable suggestions and edits for improving the manuscript. This work was funded by the Knowledge Innovation Program of the Chinese Academy of Sciences and the National Science Foundation of China (30871650 & 31100302).

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  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information
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Supporting Information

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information
FilenameFormatSizeDescription
een12072-sup-0001-FigureS1.tifTIFF image5780KFigure S1. The insect and plant species used in this study. (A–F) Adult (A) and larva (B) of Cassida piperata, Chemopodium album Linn. (C), Alternanthera sessilis (L.) DC. (D), Amaranthus spinosus Linn. (E) and Alternanthera philoxeroides (Mart.) Griseb (F).
een12072-sup-0002-FigureS2.tifTIFF image22918KFigure S2. Locations of the sites where we collected Cassida piperata across China for this study.

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