Response of an invasive liana to simulated herbivory: implications for its biological control

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Original article

Response of an invasive liana to simulated herbivory: implications for its biological control S. Raghu a,b,*, K. Dhileepan a,b, M. Treviño b a

Cooperative Research Centre for Australian Weed Management, Queensland Department of Natural Resources, Mines and Energy, PO Box 36, Sherwood, Queensland 4075, Australia b Alan Fletcher Research Station, Queensland Department of Natural Resources, Mines and Energy, PO Box 36, Sherwood, Queensland 4075, Australia

A R T I C L E

I N F O

Article history: Received 29 July 2005 Accepted 14 December 2005 Available online 14 February 2006 Keywords: Cat’s claw creeper Macfadyena unguis-cati Herbivory Tolerance Compensation Biological control Agent selection and prioritisation Invasive species management Insect–plant interactions

A B S T R A C T

Pre-release evaluation of the efficacy of biological control agents is often not possible in the case of many invasive species targeted for biocontrol. In such circumstances simulating herbivory could yield significant insights into plant response to damage, thereby improving the efficiency of agent prioritisation, increasing the chances of regulating the performance of invasive plants through herbivory and minimising potential risks posed by release of multiple herbivores. We adopted this approach to understand the weaknesses herbivores could exploit, to manage the invasive liana, Macfadyena unguis-cati. We simulated herbivory by damaging the leaves, stem, root and tuber of the plant, in isolation and in combination. We also applied these treatments at multiple frequencies. Plant response in terms of biomass allocation showed that at least two severe defoliation treatments were required to diminish this liana’s climbing habit and reduce its allocation to belowground tuber reserves. Belowground damage appears to have negligible effect on the plant’s biomass production and tuber damage appears to trigger a compensatory response. Plant response to combinations of different types of damage did not differ significantly to that from leaf damage. This suggests that specialist herbivores in the leaf-feeding guild capable of removing over 50% of the leaf tissue may be desirable in the biological control of this invasive species. © 2006 Elsevier SAS. All rights reserved.

1.

Introduction

A significant factor considered responsible for the invasiveness of introduced plant species is the loss of associated herbivores (enemy release hypothesis) during its translocation from its native geographic range into novel habitats (Maron and Vila, 2001; Keane and Crawley, 2002; DeWalt et al., 2004). This release from herbivory in the introduced range could re-

* Corresponding author. Present address: Centre for Ecological Entomology, Illinois Natural History Survey and University of Illinois, Champaign, IL 61820, USA. Tel.: +1 217 333 7028; fax: +1 217 265 5110. E-mail address: [email protected] (S. Raghu).

sult in competitive superiority over native plants resulting in invasive spread (Blossey and Notzold, 1995; Rogers and Siemann, 2002; Shea and Chesson, 2002) and associated ecological and economic impacts (Pimentel, 2002). The enemy release hypothesis therefore predicts that re-establishing the trophic link between an introduced plant and its endemic herbivores could limit its invasiveness (growth and/or spread) (McEvoy et al., 1991; Maron and Vila, 2001). This is the objective of the applied science of weed biological control (McEvoy, 2002). Though biological control is widely regarded as a safer and more sustainable alternative to other forms of invasive species management (Ehler, 1998; McFadyen, 1998; Thomas

1146-609X/$ - see front matter © 2006 Elsevier SAS. All rights reserved. doi:10.1016/j.actao.2005.12.003

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and Willis, 1998; Pemberton, 2000), concerns and perceptions about the risks posed by some organisms introduced for biological control (Simberloff and Stiling, 1996; Louda et al., 1997; Louda et al., 2003b) has resulted in decision making that is risk-averse (Louda et al., 2003a; Sheppard et al., 2003). Part of the reason for this risk-averse attitude towards biological control is the realisation that only a small proportion of all agents released for biological control for any given weed actually contribute to its control (Myers, 1985; Myers et al., 1989; McEvoy and Coombs, 1999; Denoth et al., 2002). While the contemporary practice of repeated release of different agents (albeit with a narrow host range) in anticipation that one or a combination will be successful (termed the ‘lottery approach’ by Myers, 1985) has yielded positive results, the addition of herbivores into a community can be seen to result in the accumulation of ecological risk towards non-target species (McEvoy and Coombs, 1999; Denoth et al., 2002; Louda et al., 2003b; Sheppard, 2003). Therefore ecological approaches, such as pre-release evaluation of potential impact of herbivory on plants (e.g. Colpetzer et al., 2004; Goolsby et al., 2004), that minimise the chances of releasing ineffective agents may facilitate successful biological control while simultaneously reducing ecological risk (McEvoy and Coombs, 1999; Louda et al., 2003b; Balciunas, 2004). Pre-release evaluation of the efficacy of biological control agents is often not possible in the case of many neotropical weeds. Logistic difficulties in the native range and difficulties of evaluating impact in restricted quarantine facilities, makes assessments of potential efficacy of agents difficult. An alternate option for assessing the potential for biological control consists of simulating herbivore damage through mechanical damage to different plant modules and studying plant response. Though artificial (see Baldwin, 1990; Walling, 2000; Hjalten, 2004; Lehtilä and Boalt, 2004, for potential uses and shortcomings of simulating herbivory), such an approach offers significant insights into the ecological response of plants to herbivory (Marquis, 1992; Welter, 1991; Hjalten et al., 1993; Welter and Steggall, 1993; McLaren, 1996; Gavloski and Lamb, 2000; Marquis, 1992; Tiffin and Inouye, 2000; Rogers and Siemann, 2002; Sullivan, 2003; Hjalten, 2004; Lehtilä and Boalt, 2004; Van Kleunen et al., 2004). In the context of biological control such an approach facilitates the prioritisation of potential guilds of herbivores (candidate biological control agents) based on their impact on plant productivity and growth rates, thereby narrowing the prospective list of biological control agents and helping to prioritise agents in relation to management expectations (Ehler, 1998). At the very least, such studies generate hypotheses of the potential efficacy of the different guilds of herbivores (providing an explicit a priori basis for selection of particular agents) that can be tested against the performance of biological control agents during quarantine testing, and after approval for release (Winder and van Emden, 1980; Welter, 1991; Broughton, 2003; Sullivan, 2003; Balciunas, 2004; Van Kleunen et al., 2004). In this study we investigate the response of the invasive tropical liana Macfadyena unguis-cati (L.) Gentry to simulated herbivory, to assess its susceptibility to biological control and to generate a priori predictions for potential perfor-

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mance of different guilds of herbivores selected as biological control agents.

2.

Materials and methods

2.1.

Study species

M. unguis-cati (Bignoniaceae: Scrophulariales, cat’s claw creeper) is a common forest liana with a wide native range from Mexico through Central America to tropical South America and Trinidad and Tobago (Gentry, 1974; Gentry, 1983; Sparks, 1999). It is a high climbing woody vine, with stems up to 6 cm in diameter and roots becoming elongated and tuberous with age. Branches and runners can develop adventitious roots. The leaves are have three-forked claw-like tendril that enables the plant to attach itself to tree trunks, other vegetation and other artificial structures (e.g. fences). The plant can be propagated from seed, and vegetatively from belowground tubers. Stems trailing along the ground are also capable of producing roots at the nodes. Seeds are dispersed by wind and water and the species does not have a persistent seedbank, suggesting that while its mechanism of spread is through seeds, its mechanism of persistence is through the tuber bank (Vivian-Smith and Panetta, 2004). Cat’s claw creeper is reported to be invasive in Australia, India, Mauritius, New Caledonia, South Africa and in the United States of America (Holm et al., 1991; Csurhes and Edwards, 1998; Sparks, 1999; Meyer, 2000). In Australia, it occurs in coastal and sub-coastal Queensland and New South Wales (Csurhes and Edwards, 1998; Batianoff and Butler, 2002; Harden et al., 2004). It is skototropic and grows towards tree trunks and other dark silhouettes (Lee and Richards, 1991). It exhibits within-plant variation in light response, with the shoot tip being positively phototropic and the tendrils (claws) being skototropic. This combination of traits facilitates the climbing habit of this liana (Lee and Richards, 1991) which coupled with its capacity for sexual and asexual reproduction enables it success as an invader. M. unguis-cati is a serious threat to biodiversity in riparian and rainforest communities in eastern Australia (Csurhes and Edwards, 1998; Harden et al., 2004). It thrives in full sun or partial shade and in a wide variety of soils, and the stolons and root tubers produce dense mats on the forest floor. It climbs over standing trees in vine scrubs, gallery forests, rainforests, closed forests and open forests, thus competing for light. Trees can be crushed by the weight of vines, allowing further light to enter the forest and promoting invasion by more light-demanding species. Furthermore, cat’s claw creeper infestations may cause an inward collapse of the forest margin, as individual trees are colonised and killed (Csurhes and Edwards, 1998; Harden et al., 2004). Given the considerable ecological impact of this plant, it is regarded as a ‘structural parasite’ (sensu Stevens, 1987) and a ‘transformer species’ (sensu Richardson et al., 2000). Chemical control is difficult given the sensitive habitats (riparian and rainforest edges) invaded by this plant and the large belowground tuber reserves, and mechanical control of vines is not cost-effective (e.g. Pérez-Salicrup et al., 2001).

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Therefore biological control is regarded as the only prospect for long-term management of this invasive liana in locations where this weed is widespread.

2.2.

Experimental design

Plants that had a single tuber (tuberlings) were collected in December 2002 from a large infestation along the Kolan River (24°42′45′′S, 151°41′49′′E) in Central Queensland, Australia. It was not possible to determine whether they had grown from seed or from tubers that had detached from other plants. They were grown for 6 weeks in the greenhouse before use in the experiments.

2.2.1.

Simulated herbivory

This experiment was done between January and June 2003. Tuberlings were randomly allocated to one of 10 simulated herbivory treatments. Treatments comprised of defoliation (D = removal of 100% of the leaves of the plant), shoot damage (S = D + 1/3 of the shoot), root damage (R = removal of 1/3 of the root) and tuber damage (T = removal of 25% of the tuber volume) and combinations of these treatments, including D + R, D + R + T, D + T, R + T, S + R, and S + T. The level of biomass removal was dictated by the limited information available on the feeding habits of candidate biological control agents (Sparks, 1999). However, the tuber damage levels were arbitrarily selected as no tuber herbivores have been recorded thus far. Plants allocated to these treatments received the simulated damage either one, two or three times over an 18-week period at 6-week intervals. The 6-week interval was selected as it corresponded to the generation time of a defoliating agent Charidotis auroguttata (Dhileepan et al., 2005). Stem damage could not be done without leaf removal and therefore effect of shoot damage on its own cannot be inferred from this study. Therefore, when plant response is similar between S and D, this can be attributed to the effect of defoliation. Eight plants were allocated to each simulated herbivory × frequency combination. Twenty-six plants were allocated as Control (C) for each of the treatment frequencies. Following the application of each treatment all plants were subjected to the same stresses of washing and replanting into pots to ensure that the only difference among the plants was the simulated damage and the damage frequency. To prevent pathogen infection following simulated herbivory treatments, all plants were immersed in a fungicide solution (Benlate 50 WP, DuPont Australia Ltd., Active ingredient 500 g kg–1 Benomyl, Concentration of solution used = 1. 42 g l–1) prior to potting. Plants were distributed randomly in a glasshouse. The aboveground stem height, belowground root length, wet weight of the plant, the number of belowground tubers per plant (tuber abundance) and the diameter of each tuber were measured before the application of treatments at the start of the experiment, at 6-week intervals, and at the end of the experiment (24 weeks). The dry weight of each of the plant modules was measured at the end of the experiment. A random sample of 20 tuberlings not used in the study, indicated that there was a strong relationship (y = 0. 0568e1.6959x; R2 = 0.95) between the tuber diameter (x) and its

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dry weight (y). This relationship was used to estimate the initial tuber biomass of plants used in the study. The relative growth rate (RGR) of the tuber was calculated the formula RGR = (ln(final) – ln(initial))/Δ time (McGraw and Garbutt, 1990; Hoffmann and Poorter, 2002), using the final tuber dry weight that was directly measured and estimated initial tuber dry weight.

2.2.2.

Simulated defoliation

This experiment was done between September and December 2003. To quantify the response of tuberlings to different levels of defoliation, 10 field-collected tuberlings were randomly allocated to each of four levels (25%, 50%, 75% and 100%) of simulated defoliation. In addition, 10 plants were allocated as control (0% defoliation). These treatments were applied twice, 6 weeks apart. As in the simulated herbivory experiment, all plants were distributed randomly among glasshouse benches and were subjected to the same stresses to ensure that the only difference among them was the simulated level of defoliation. The aboveground stem height, belowground root length, wet weight of the plant and tuber abundance were measured at the beginning and at the end of the experiment. RGR for tuber biomass was calculated as in the simulated herbivory experiment.

2.3.

Data analysis

The simulated herbivory experiment was analysed with a fixed-factor two-way ANOVA with simulated herbivory (11 levels = control and 10 treatments) and damage frequency (three levels = three frequencies) as factors. Aboveground biomass, belowground biomass, tuber abundance, tuber RGR were used as dependent variables. The simulated defoliation experiment was analysed using a fixed-factor one-way ANOVA with percent defoliation (five levels) as the factor and aboveground biomass, belowground biomass, stem height at harvest and RGRs tuber biomass as the dependent variables. All analyses were done using SAS 8e (SAS Institute Inc., Cary, NC, USA). For both experiments, when the raw data did not conform to the ANOVA assumptions (homogeneity of variances and normal distribution of residuals), they were suitably transformed prior to analysis. Significant interaction effects were explored using the SLICE option within the PROC GLM procedure of SAS. When significant treatment effects were detected, post-hoc pairwise comparisons of means were made using the Ryan–Einot–Gabriel–Welsch (REGWQ) multiple range test (Yandell, 1997). Where data transformation was unable to overcome violations of assumptions of parametric analyses, the equivalent non-parametric test was used. Data were back transformed for presentation in graphs.

3.

Results

3.1.

Simulated herbivory

The main effect of herbivory type and frequency was significant for all plant productivity measures (Table 1), but the sig-

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nificance of the interaction term in all analyses indicated that the effect of herbivory was not consistent across all treatment frequencies (Table 1).

3.1.1.

Aboveground biomass

There was no difference in aboveground biomass among the different herbivory treatments when they were inflicted just once over the course of the study (Fig. 1a). When the simulated herbivory treatments were applied twice, belowground damage (i.e. R, R + T and T) did not significantly differ from control plants in terms of aboveground biomass produced (Fig. 1b, c). All other treatments resulted in a comparatively similar reduction in aboveground biomass relative to control plants (Fig. 1b, c). Comparison among damage frequencies within treatments revealed that treatments that exclusively simulated belowground herbivory (i.e. R, R + T and T) did not have any evident impact on aboveground biomass at any frequency (Fig. 1). All other treatments resulted in a significant reduction in aboveground biomass when applied more than once (Fig. 1). However, there was no difference in aboveground biomass between treatments applied twice or thrice over the course of the study (Fig. 1b, c).

3.1.2.

Belowground biomass

As in the case of aboveground biomass, there was no difference in belowground biomass among the different herbivory treatments when they were applied just once over the course of the study (Fig. 2a). When the simulated herbivory treatments were applied twice or thrice, the greatest reductions in belowground biomass were found in plants that had received leaf or stem herbivory treatments (in isolation or in combination) (Fig. 2b, c). Notably, tuber damage did not result in a decline in belowground biomass relative to control even at multiple frequencies (Fig. 2b, c). Comparisons among frequencies within treatment showed that that treatments that exclusively simulated belowground herbivory (i.e. R, R + T and T) did not have any impact on belowground biomass at any frequency (Fig. 2). All other treatments resulted in a significant reduction in belowground biomass when applied more than once (Fig. 2), with little difference in belowground biomass between treatments applied twice or thrice over the course of the study (Fig. 2b, c).

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3.1.3.

Stem height

Post-hoc analyses revealed that the effect of a single frequency of simulated herbivory did not significantly influence stem height relative to control (Fig. 3a). However, some multiple herbivory treatments lowered the growth rates of stems compared to control (Fig. 3b, c). When the treatments were imposed twice and thrice, the greatest reduction was achieved through a combination of shoot and root herbivory (S + R), and shoot herbivory (S), respectively, while belowground treatments (R, R + T and T) had a negligible impact on the growth of stems (Fig. 3b, c). Comparison of stem height among frequencies within treatment showed that multiple treatments were required in most cases to reduce growth rate. However even multiple applications of some herbivory treatments (D + R, D + T, R, R + T, S, S + T and T) did not reduce the stem height relative to a single application (Fig. 4).

3.1.4.

Tuber abundance

None of simulated herbivory treatments had any effect on tuber abundance when inflicted either once or twice over the course of the experiment (Fig. 4a, b). However, when the herbivory treatments were imposed thrice, plants that received tuber damage in isolation or in combination with root damage (T and R + T) had a significantly higher number of tubers at harvest than those receiving other treatments (Fig. 4c). Comparisons among frequencies within treatment revealed that when imposed thrice, tuber damage and tuber and root damage combined resulted in an increased number of tubers at harvest (Fig. 4).

3.1.5.

Tuber biomass–RGR

When the simulated herbivory treatments were imposed once, defoliation resulted in a markedly higher rate of increase in tuber biomass than all other treatments (Fig. 5a). When the treatments were inflicted twice, plants receiving leaf, root and tuber damage (D + R + T) demonstrated the greatest reduction in growth rate of tuber biomass, while most other treatments resulted in little reduction in this (Fig. 5b). When the treatments were imposed three times, belowground herbivory treatments (R, R + T and T) resulted in little reduction in tuber biomass growth rate, unless they were imposed in combination with leaf or stem damage treatments (e.g. D + R + T, D + T, S + R, S + T) (Fig. 5c).

Table 1 – Summary of ANOVA results with type of simulated herbivory (SIM) and frequency of simulated herbivory (FREQ) as factors and plant productivity parameters as dependent variables. Type III sums of squares were used

Source

df

Aboveground biomass (logtransformed) (R2 = 0.63) F

Among cells 32 15.37 SIM 10 22.40 FREQ 2 92.03 SIM*FREQ 20 5.89 Error 285 P < 0.0001 for all F statistics presented.

Belowground biomass (log-transformed) (R2 = 0.62) F

Tuber abundance (R2 = 0.40)

Stem height (logtransformed) (R2 = 0.46)

F

F

Tuber biomass RGR (log-transformed) (R2 = 72) F

14.64 19.77 98.13 5.60

5.92 9.70 19.90 3.32

7.64 12.90 31.34 3.50

22.81 35.36 134.25 8.64

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Fig. 1 – Aboveground biomass (mean + 1 S.E.) of plants experiencing different frequencies and types of simulated herbivory over an 18-week period. Bars with same letters adjacent to them are not significantly different as tested by the REGWQ multiple range test. Capital letters represent between frequency comparisons of a particular type of simulated herbivory and lower case letters represent comparisons between simulated herbivory treatments with a given frequency. Simulated herbivory treatments: D = defoliation; R = root damage; S = shoot damage; T = tuber damage. All other treatments are combinations of these basic treatments (see text for descriptions of these treatments). For each frequency, N = 26 for control plants and N = 8 for each of the other treatments.

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Fig. 2 – Belowground biomass (mean + 1 S.E.) of plants experiencing different frequencies and types of simulated herbivory over an 18-week period. Post-hoc tests, x-axis legend and replication are same as in Fig. 1.

Comparison within treatments among frequencies revealed that multiple defoliation treatments were required to have any impact on tuber biomass growth rates (Fig. 5). Again there was little difference in the effect of belowground herbivory (R, R + T and T) on tuber biomass at any frequency (Fig. 5).

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Fig. 3 – Tuber abundance (mean + 1 S.E.) of plants experiencing different frequencies and types of simulated herbivory over an 18-week period. Post-hoc tests, x-axis legend and replication are same as in Fig. 1.

3.2.

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Fig. 4 – Stem height (mean + 1 S.E.) of plants experiencing different frequencies and types of simulated herbivory over an 18-week period. Post-hoc tests, x-axis legend and replication are same as in Fig. 1.

Simulated defoliation

The greatest reduction in aboveground and belowground biomass at harvest was observed when plants received 75–100% defoliation, and most defoliation resulted in a reduction in biomass relative to control plants (0% defoliation) (Fig. 6a).

There was no effect of level of defoliation on tuber abundance (Kruskal–Wallis H = 5.56, df = 4, P = 0.4898). Reduction in stem height growth rate was greatest in plants that received between 75% and 100% defoliation

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Fig. 5 – Tuber biomass RGR (mean + 1 S.E.) of plants experiencing different frequencies and types of simulated herbivory over an 18-week period. Post-hoc tests, x-axis legend and replication are same as in Fig. 1.

(Fig. 6b). In terms of total biomass growth rates, the greatest reductions were achieved through 50–100% defoliation (Fig. 6b). The rate of accumulation of tuber biomass was significantly lower in plants receiving 75–100% defoliation than in other simulated defoliation treatments (Fig. 6b) Table 2.

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4.

Discussion

4.1.

Plant response to simulated herbivory

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M. unguis-cati plants are able to tolerate a single event of herbivory as indicated by a lack of difference in above and belowground biomass relative to control plants (Figs. 1, 2a). This may be because plants are able to recover, possibly buffered by the presence of storage reserves (Belsky, 1986; Welter and Steggall, 1993). Herbivory needed to be applied at least twice over the duration of the study to have a negative effect on plant productivity. Even at these higher frequencies, belowground treatments only had an effect when imposed in conjunction with defoliation (Figs. 1–4). However, given that the effects of these treatment combinations did not differ from defoliation, the observed plant response can be attributed to the effects of defoliation. The loss of photosynthetic tissue may result in a reduction in the assimilate available for supporting compensatory growth (Andersen, 1987). Tuber damage on its own, or in combination with root damage appears to result in compensation and vigorous regrowth as indicated by a greater number of tubers produced at harvest by such plants than control plants (Fig. 4c). Since tubers serve as resource sinks, the apparent compensation to tuber damage may have activated other sinks (Julien et al., 1987; Honkanen et al., 1994; Honkanen et al., 1999), resulting in the production of additional tubers. This may be a contributing factor to its invasiveness along riparian corridors where mechanical disturbance to soil may be frequent (Bazzaz, 1991). Since M. unguis-cati propagates vegetatively from the tuber this may be construed as being adaptive. However plants in this study were grown under ideal nutrient and water regimes. Examination of plant response under more natural field conditions in the native range of this liana may shed light on whether this is an adaptive response to herbivory or disturbance, or an artefact of the growing conditions in this study (Belsky, 1986; Belsky et al., 1993). When the plant was defoliated once, the rate of tuber biomass production increased significantly (Fig. 5). This may be a plant response to divert resources away from damaged components and into the storage organs, enhancing its tolerance to herbivory (Andersen, 1987). However, frequent damage results in a depletion of tuber reserves and a decline in the rate of allocation to storage tissues (Fig. 5) suggesting that the plants are allocating these reserves to repair/restore damaged photosynthetic tissues (Jameson, 1963; Honkanen et al., 1994). One potential interpretation of our results is that the patterns of biomass allocation observed at harvest are an artefact of the treatment imposed. However, there was no correlation between the biomass removed as a part of the treatment and the biomass at harvest, indicating that the patterns observed are due to plant response to loss of specific tissues.

4.2.

Implications for biological control

Given the economic and ecological constraints of chemical and mechanical methods of control, regulation of this inva-

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Fig. 6 – (a) Biomass (mean + 1 S.E.) of plants experiencing different levels of simulated defoliation over a 12-week period. (b) Tuber growth rate (g g−1 day−1) and stem height (cm) (mean + 1 S.E.) of plants experiencing different levels of simulated defoliation over a 12-week period. Bars within a given response variable with same letters adjacent to them are not significantly different as tested by the REGWQ multiple range test. N = 10 plants for each treatment.

sive plant through herbivory (biological control) may be vital in the management of this species.

Table 2 – Summary of ANOVA results with level of simulated defoliation as the factor and plant productivity parameters as dependent variables. Type III sums of squares were used Dependent variable

F4,

P

R2

Aboveground biomass Belowground biomass (logtransformed) Stem height at harvest Tuber biomass–RGR (log-transformed)

9.64 3.92

< 0.0001 0.0082

0.46 0.26

8.48 3.01

< 0.0001 0.0277

0.43 0.46

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Insect herbivores from different feeding guilds have been recorded on this species in its native range (Sparks, 1999). Agent selection needs to be made in light of the type of damage the plant is most likely to succumb to. Any inference for biological control from this study, needs to take into account the fact that this study was done on the tuberling stage of the plant and plant response to simulated and actual herbivory may vary depending on the plant age and/or life-stage (Hjalten, 2004). Since M. unguis-cati is a structural parasite, management of this liana will need to target its climbing habit. Its primary mechanism of persistence is through subterranean tubers (Vivian-Smith and Panetta, 2004). Therefore depletion of the tuber bank and stored reserves may be critical in its manage-

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Table 3 – Summary of responses of M. unguis-cati to different types of simulated herbivory in relation to different management objectivesa Management objective

Damage typeb (frequency)

Plant responsec

Reduce standing aboveground biomass

D, D + R, D + R + T, D + T, S, S + T, S + T Susceptibility R, R + T, T Tolerance Reduce belowground biomass D, D + R, D + R + T, D + T, S, S + T, S + T Susceptibility R, R + T, T Tolerance Reduce abundance of invasive plant part/stage (i.e. tuber) D, D + R, D + R + T, D + T, R, S, S + T, S + T Susceptibility R + T(2), T(2) Tolerance R + T(3), T(3) Compensation Slow the climbing habit of the plant (i.e. reduce stem height) D(3), D + R + T, D + T, S, S + R, S + T Susceptibility D(2), D + R, R, R + T, T Tolerance Slow the accumulation of tuber reserves D(3), D + R(3), D + R + T, D + T, R + T(3), S(3), S + R, S + T Susceptibility D(2), D + R(2), R, R + T(2), S(2), T Tolerance D(1) Compensation a With the exception of rate of tuber biomass production, there was no significant treatment effect on plants receiving single herbivory treatments relative to control plants. Therefore only the outcomes of multiple treatments are presented. Where frequency is not given in brackets, plant response is similar when treatments are applied twice or thrice. b D: defoliation; R: Root damage; S: stem damage; T: tuber damage. c See text for definitions of plant response.

ment. In addition, management objectives also include reducing the biomass accumulation by this liana, as this could result in collapse of its structural host. These management objectives may be achieved through the absolute reduction in biomass and/or through reducing the plant’s growth rate (Table 3). In relation to different parameters of interest, plants may exhibit susceptibility (damaged plant less productive than control plants), tolerance (damaged plant no different to control plants) or compensation (damaged plant more productive than control plants) (Belsky, 1986; Hjalten et al., 1993). Examining plant response to different types of damage can help prioritise different guilds of specialist herbivores. Defoliation on its own, or in combination with other types of damage, results in a decrease in absolute biomass or biomass growth rate while plants tolerate belowground damage (Table 3). Since reducing the tuber bank is an important management objective, belowground damage needs to be avoided, as the plant is either tolerates or counter-productively, vigorously compensates for such damage (Table 3). A similar response has been documented in the case of the aquatic weed Salvinia molesta D.S. Mitchell (Julien et al., 1987; Julien and Bourne, 1988). Similar increases in biomass and reproductive allocation with herbivory have also been documented in other systems (Reichman and Smith, 1991). At least three defoliation treatments are required to slow the climbing habit of the plant. Severe defoliation is required before the rate of tuber biomass accumulation is reduced (Fig. 6 and Table 3). A similar effect of defoliation on belowground tuber reserves was observed in the climbing invasive, Asparagus asparagoides (L.) (Kleinjan et al., 2004). This suggests that defoliating agents may be the most suitable in attaining the management objectives for this invasive liana. Even among defoliation treatments, greater than 50% of the leaves had to be the removed to affect plant performance significantly (Fig. 6). Defoliation also resulted in reduced production of tendrils (claws) (pers. observ.) that facilitate the climbing habit of the plant. This is similar to biomass allocation patterns documented in other climbers in the absence of support structures (Den Dubbelden and Oosterbeek, 1995; Den Dubbelden and Verburg, 1996). However, the effects of biomass removal on other aspects of plant

growth (e.g. nutrient allocation) warrant further investigation. In general, belowground treatments had a negligible impact in this study. This was a counterintuitive result given that attacking primary and ancillary reproductive structures (flowers, seeds and tubers) and roots are regarded as important in biocontrol (Blossey and Hunt-Joshi, 2003). Biocontrol practitioners usually select agents to target multiple plant parts (McFadyen, 1998) to weaken the plant. However, the results of this study show that damaging multiple parts has little more effect on the various plant parameters than targeting certain key plant modules (Table 3). This agrees with Myers’ (1985) and Denoth et al.’s (2002) assessments of that a small proportion of agents selected actually contribute to the management of the target weed. Pre-release evaluation of efficacy of biological control agents is often not possible in the case of many invasive species targeted for biocontrol. In such circumstances simulating herbivory could yield significant insights (despite obvious caveats Hjalten, 2004; Lehtilä and Boalt, 2004) into plant response to damage. This may improve the efficiency of agent prioritisation, increasing the chances of regulating the performance of invasive plants through herbivory, and minimising potential risks posed by adopting the lottery approach.

Acknowledgements We thank Garth Meikle, Leanne Hughes and Jayd McCarthy for technical assistance during this study. Dane Panetta and Gabrielle Vivian-Smith provided helpful comments on this study and on earlier drafts of this manuscript.

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