BioControl

, Volume 62, Issue 3, pp 373–384 | Cite as

Determining the effects of life stage, shared prey density and host plant on intraguild predation of a native lacewing (Chrysoperla carnea) by an invasive coccinellid (Harmonia axyridis)

  • P. M. Wells
  • J. Baverstock
  • S. J. Clark
  • F. M. Jiggins
  • H. E. Roy
  • J. K. Pell
Article

Abstract

Negative impacts of non-native Harmonia axyridis (Pallas) on members of the native aphid enemy guild have been widely hypothesised but mainly only assessed with other coccinellid species, and mostly in small experimental arenas. Here we investigated the interactions between H. axyridis and Chrysoperla carnea Stephens larvae. In small-scale (Petri dish) arenas 2nd-instar C. carnea were at risk of predation from larval (2nd and 4th-instar) and adult (male and female) H. axyridis while 3rd-instar C. carnea were only at minimal risk from 4th-instar and adult female H. axyridis. Plant species, aphid species and aphid density did not affect intraguild predation of 2nd-instar C. carnea by 4th-instar and adult H. axyridis in mesocosm experiments. Chrysoperla carnea consumed similar numbers of Megoura viciae Buckton, Aphis fabae Scop. and Acyrthosiphon pisum Harris aphids while H. axyridis consumed fewer M. viciae than the other two species. The greatest suppression of A. pisum was achieved in treatments with both C. carnea and H. axyridis. Life stage and the sex of H. axyridis as well as the life stage of C. carnea are important variables affecting intraguild predation and these attributes should be considered when assessing the potential threat of other potentially invasive alien predators.

Keywords

Coleoptera Coccinellidae Neuroptera Chrysopidae Intraguild predation 

Introduction

The vast majority of non-native species do not threaten biodiversity in their introduced environment, a small number do and are termed invasive. Negative effects of invasive non-native arthropods can be especially far reaching if they are generalist predators with a wide prey range. One such example is Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), a generalist predator native to eastern Asia. Harmonia axyridis spread from its native range as a result of intentional releases as a biocontrol agent and unintentional transportation (Roy et al. 2016). This coccinellid now occupies an extensive non-native range encompassing areas of North America, Canada, South America, Europe, Africa (Koch et al. 2006; Brown et al. 2008) and more recently New Zealand (http://naturewatch.org.nz/taxa/48484-Harmonia-axyridis). The presence of H. axyridis has been correlated with declines in native species of Coccinellidae (Colunga-Garcia and Gage 1998; Michaud 2002; Majerus et al. 2006; Brown et al. 2011; Roy et al. 2012, 2016). It has been widely hypothesised that these declines are, at least in part, a result of intraguild interactions. Indeed, there are many examples of H. axyridis acting as an asymmetric intraguild predator of native coccinellid species (e.g. Ware and Majerus 2008; Mirande et al. 2015). In addition, numerous small-scale laboratory studies have demonstrated the potential for H. axyridis to act as an intraguild predator of non-coccinellid species ranging from aphidophagous Neuroptera to entomopathogenic fungi (Gardiner and Landis 2007; Wells 2011; Ingels and De Clercq 2011). Using the risk assessment framework outlined in van Lenteren et al. (2003) which uses biological attributes including direct effects on non-target herbivores and intraguild predation, H. axyridis was deemed to be a ‘high-risk’ invasive non-native species and a major threat to biodiversity in its non-native range, both indirectly through resource competition and directly as an intraguild predator (Majerus et al. 2006).

As with many other invasive non-native species, the information used to determine the risk status of H. axyridis was derived in part from studies carried out using simple laboratory arenas such as Petri dishes (Lucas 2005; Pell et al. 2008). Nedvěd et al. (2013) collated information from studies assessing intraguild predation between H. axyridis and 27 aphidophagous species and examined the symmetry of the interaction. In all cases, H. axyridis had the potential to be an intraguild predator of the other species but nine of the other species were shown to be intraguild predators of H. axyridis to some extent. While these experiments may predict worst-case scenarios, the limited number of life stages assessed, and the simplicity of the experimental arenas used, inevitably means that they are not truly representative of what occurs under field conditions (Nedvěd et al. 2013). There have been many studies examining the effects of prey density on intraguild predation (IGP) (e.g. Lucas et al. 1998) including those involving H. axyridis as the intraguild predator which have shown that IGP is reduced with the addition of shared aphid prey (e.g. Kajita et al. 2000; Nóia et al. 2008; Ingels and De Clercq 2011; Gagnon and Brodeur 2014; Mirande et al. 2015). Here we increased the complexity of the study system by using mesocosms and explored the effects of life stage, shared prey density and host plant on intraguild interactions between H. axyridis and C. carnea. The overarching aim of this research was, therefore, to determine whether IGP of native by H. axyridis has the potential to occur to the same extent when assessed under more natural conditions. Previous studies have shown 2nd-instar larvae of the lacewing Chrysoperla carnea Stephens to be asymmetric intraguild prey of adult H. axyridis (Gardiner and Landis 2007). However, Nedvěd et al. (2013) found that predation between 2nd-instars of both these species was symmetrical, and between larger instar pairings H. axyridis was the intraguild prey but these experiments were conducted in the absence of other prey in simple Petri dish arenas. IGP of C. carnea larvae by H. axyridis was therefore used as the model system in the experiments described here. We first determined the outcome of this interaction under small-scale controlled conditions using multiple life stages of both the lacewing and the coccinellid and then we used mesocosms to create complex environments where the effects of plant morphology and shared prey on IGP could be assessed.

Materials and methods

Plant and insect cultures

Dwarf broad bean plants (Vicia faba L., cv. The Sutton), Chinese cabbage (Brassica chinensis L., cv. Wong Bok), barley (Hordeum vulgare L., cv. Saffron) and stinging nettle (Urtica dioica L.) were grown in glasshouses under ambient conditions. These plants were selected to represent three common crop types (bean, cabbage and barley) and a common field margin plant (nettle). The four plant species vary in architecture and are host to different aphid species.

All insect cultures were maintained at 18 °C (L:D 16:8) within the insectary at Rothamsted Research, UK. Cultures of the pea aphid (Acyrthosiphon pisum Harris), the black bean aphid (Aphis fabae Scop.) and the vetch aphid (Megoura viciae Buckton), were maintained on V. faba plants and sub-cultured onto new plants when necessary. Chrysoperla carnea larvae were purchased from Just Green (Crouch, UK) or Koppert UK Ltd. (Haverhill, UK) and maintained within 90 mm triple-vented Petri dishes and allowed to feed ad libitum on A. pisum until required. A stock colony of H. axyridis was replenished with wild stock from Rothamsted Farm, maintained in Perspex insectary cages (43 × 43 × 70 cm) on V. faba plants infested with A. pisum and allowed to reproduce. Parent stock were replenished from wild stock on Rothamsted Farm to ensure that experimental stock were within eight generations of wild populations. The larvae produced were transferred to triple-vented Petri dishes (seven larvae per dish) and allowed to feed ad libitum on A. pisum until required for bioassays, or until they pupated after which time they were placed in insectary cages containing V. faba plants infested with A. pisum. Only H. axyridis larvae that had undergone ecdysis in the previous 24 h were used in experiments, while adults were used within eight weeks of eclosion. Harmonia axyridis used in bioassays were never more than three generations from field collected individuals.

IGP of C. carnea by H. axyridis in Petri dish arenas

IGP of C. carnea by H. axyridis was assessed in experimental arenas consisting of a 90 mm single-vented Petri dish containing either six C. carnea larvae or six adult A. pisum. A single H. axyridis was then added to each of the dishes. A control treatment containing only C. carnea was also included to assess mortality in the absence of H. axyridis (i.e. through cannibalism). The arenas were arranged in rows, each of which contained a replicate of each treatment following a randomized complete block design. The dishes were maintained at 18 °C (L:D 16:8) and the number of C. carnea surviving in each dish was recorded every 30 min for 3 h. This set-up was used in six experiments to assess the predation of 2nd-instar C. carnea by (i) adult H. axyridis (male and female), (ii) 2nd-instar and (iii) 4th-instar H. axyridis and the predation of 3rd-instar C. carnea by (iv) adult H. axyridis (male and female), (v) 2nd-instar and (vi) 4th-instar H. axyridis. Each experiment was done separately over one to four occasions with replicate numbers per treatment of eight to 11 for H. axyridis larvae and 13–32 for H. axyridis adults (adults comprised 50% of each sex, see supplementary information Table 1). Each experiment was analysed separately using GenStat 13th edition (VSNi 2010). This statistical package was used throughout this study. Generalized Linear Models (poisson distribution, with log link; assuming exponential survival times, allowing for right-censored observations and blocking, and fitted using GenStat’s RSURVIVAL procedure) were used to compare survival times of the prey types (C. carnea or aphid prey) for each of the two H. axyridis larval stages. For adult H. axyridis, the factorial set of treatments represented by the combinations of prey type and coccinellid sex was assessed. For experiments with 3rd-instar C. carnea statistical analysis was only possible for one experiment (with 4th-instar H. axyridis) due to the low incidence of IGP. The logit-transformed proportion of prey eaten after 180 min was analysed using analysis of variance (ANOVA) blocking for row within occasion, and a factorial treatment structure for the adult H. axyridis experiment.

Effect of plant species on IGP

IGP of 2nd-instar C. carnea larvae by either adult female or 4th-instar larval H. axyridis was assessed on four different plant species (V. faba, B. chinensis, H. vulgare and U. dioica) in mesocosms. The size and density of the four plant species was standardised to a surface area of approximately 45 cm2 by selecting plants of a specific age and density. Each mesocosm comprised a clear Perspex cage (43 × 43 × 70 cm) with a horizontal grey acrylic plastic frame supported 12 cm above the base of the cage floor. A 12.5 cm diameter plant pot containing the test plant(s) was placed into a recess in the centre of the plastic frame creating a sealed horizontal surface that was level with the soil. This ensured insects could easily leave the plant if they chose to do so. The soil in the pot was covered with filter paper (Whatman no. 42; 12.5 cm diameter) to allow increased visibility of dead insects. Absorbent matting in the base of each mesocosm was kept wet throughout. Sixteen mesocosms (four per plant species) were prepared and placed in a completely randomized block design in rows of four on the upper and lower shelves of two frames. One adult H. axyridis plus ten C. carnea larvae were added to half of the mesocosms two hours prior to the start of the experiment (to assess IGP) while only ten C. carnea larvae were added to the remaining mesocosms (to assess cannibalism). The mesocosms were maintained at 18 °C (L:D 16:8) for 24 h, after which time the number of C. carnea surviving in each of the mesocosms was determined. The experiment was done on three occasions with seven to nine replicates per treatment (see supplementary information Table 2). The experiment was repeated using H. axyridis larvae over four occasions with five to seven replicates per treatment (see supplementary information Table 2). Data for experiments with adult and larval H. axyridis were analysed separately. For each life stage the effects of plant species and presence of H. axyridis on the logit-transformed proportion of C. carnea surviving to the end of the experiment were assessed using a linear mixed model (LMM) with the random model representing mesocosms within shelves within occasions, and a 2 × 4 factorial fixed model. F-tests associated with the LMM are approximate and may have non-integer estimated denominator degrees of freedom.

The effect of shared prey species on IGP

IGP of 2nd-instar C. carnea by adult H. axyridis in the presence of three aphid species (A. pisum, A. fabae and M. viciae) was assessed on V. faba plants. A single pot containing four V. faba plants infested with a total of 50 one-day-old aphids was added to each mesocosm. The size of the three aphid species differed considerably. Therefore, to ensure that the total quantity of prey resource available was standardised between treatments (equivalent to 0.3 mg of aphids), one-day-old A. pisum and M. viciae were added to the mesocosms one day prior to the start of the experiment while one-day-old A. fabae were added three days prior to the start of the experiment. A total of 14 treatments were tested. Four treatments were prepared for each of the three aphid species: (i) no enemies (control), (ii) ten C. carnea, (iii) one adult female H. axyridis and (iv) ten C. carnea + one adult female H. axyridis. Control treatments assessing either cannibalism or IGP in the absence of shared prey (aphids) were also prepared by adding either (i) ten C. carnea or (ii) ten C. carnea + one adult female H. axyridis, respectively, to mesocosms containing V. faba plants. The mesocosms were maintained at 18 °C (L:D 16:8) for 24 h after which time the number of C. carnea surviving was recorded. The experiment was done on eight occasions with six to 12 replicates per treatment (see supplementary information Table 2). The effects of shared prey species and H. axyridis on the logit-transformed proportion of C. carnea surviving at the end of the experiment were assessed using a LMM with a random model representing mesocosms within shelves within occasions, and a 2 × 4 factorial fixed model. In addition, the effect of aphid species, C. carnea and H. axyridis on the (untransformed) proportion of aphids surviving at the end of the experiment was analysed using a LMM with random model as above, and a 2 × 2 × 3 factorial fixed model.

The effect of shared prey density on IGP

Mesocosms containing a single pot of V. faba plants (four plants per pot) were prepared. A total of zero (control), 50, 200 or 500 three-day-old A. pisum nymphs were added to each of the mesocosms two days prior to the start of the experiment. Either ten 2nd-instar C. carnea or ten 2nd-instar C. carnea + one adult female H. axyridis were added to each mesocosm (eight treatments in total). The mesocosms were maintained at 18 °C (L:D 16:8) for 24 h after which time the number of C. carnea surviving was recorded. The experiment was done on six occasions with seven to nine replicates per treatment (see supplementary information Table 2). The effects of aphid density and presence of H. axyridis on the logit-transformed proportion of C. carnea surviving were assessed using a LMM with random model representing mesocosms within cage within shelves within occasions, and a 2 × 4 factorial fixed model.

Results

IGP of C. carnea by H. axyridis in Petri dish arenas

Overall more 2nd-instar C. carnea were consumed by 4th-instar H. axyridis than by either 2nd-instar or adult H. axyridis (Table 1), however, this could not be statistically tested as experiments were done on different occasions. The results of the survival analysis show that, over 180 min, the risk of 2nd-instar C. carnea being consumed by 2nd-instar H. axyridis was not different to that of aphid prey (\(\chi_{1}^{2}\) = 0.81, p = 0.368) whereas over the same observation period 2nd-instar C. carnea were less at risk of predation by 4th-instar H. axyridis than aphid prey (\(\chi_{1}^{2}\) = 13.10, p < 0.001). The risk of predation of 2nd-instar C. carnea by adult H. axyridis was not different to that of aphid prey (\(\chi_{1}^{2}\) = 3.56, p = 0.059). However, survival of prey was affected by the sex of the adult ladybird, with the threat from female H. axyridis being greater than the threat from males (\(\chi_{1}^{2}\) = 81.1, p < 0.001). Indeed, the overall proportion of 2nd-instar C. carnea consumed by female H. axyridis was more than double that of males (F1,44 = 49.29, p < 0.001) (Table 1). There was no interaction between the effect of prey or sex on survival (\(\chi_{1}^{2}\) = 0.478, p = 0.489). Cannibalism between 2nd-instar C. carnea larvae was observed in 36% of the replicates, with 11% of larvae being cannibalised.
Table 1

Mean percentage of intraguild prey (2nd and 3rd-instar C. carnea) and aphid prey eaten by H. axyridis larvae (2nd and 4th-instar) and adult H. axyridis (male and female) after 180 min

Intraguild prey

H. axyridis

life stage

Prey type

F

p

Intraguild

Aphid

2nd-instar

C. carnea

2nd-instar

26 (18–34)

22 (16–30)

F1,7 = 0.66

0.442

4th-instar

62 (45–77)

39 (24–57)

F1,9 = 4.31

0.068

Adult

41 (34–50)

47 (39–55)

F1,44 = 1.00

0.322

 Male

23 (16–33)

29 (21–40)

  

 Female

62 (51–72)

66 (55–75)

  

3rd-instar

C. carnea

2nd-instar

0

8 (4.0)

  

4th-instar

17 (11–24)

51 (40–62)

F1,9 = 35.56

<0.001

Adult

3 (1.5)

58 (4.1)

  

 Male

0

39 (5.7)

  

 Female

7 (3.0)

76 (5.0)

  

Means and 95% confidence intervals (in brackets) are back-transformed from the logit scale where comparative analyses were performed; otherwise overall % eaten are given with binomial SEs (in brackets). F statistics and p values are for the main effect of prey type from ANOVA

Predation of 3rd-instar C. carnea was considerably lower than that of 2nd-instar larvae by all life stages of H. axyridis assessed, with IGP not occurring in the treatments containing either 2nd-instar H. axyridis or adult male H. axyridis (Table 1). Over the 180 min observation period, the risk of predation of 3rd-instar C. carnea by 4th-instar H. axyridis was less than the risk of predation of aphid prey by 4th-instar H. axyridis (\(\chi_{1}^{2}\) = 34.1, p < 0.001). IGP by female adult H. axyridis occurred in a third of replicates with one to two C. carnea being consumed when IGP did occur. Cannibalism between 3rd-instar C. carnea only occurred in 19% of replicates with 4% of larvae being cannibalised.

Assessing only the end point data at 180 min gave the same outcomes as the survival analyses, with one exception. The percentage of 2nd-instar C. carnea consumed by 4th-instar H. axyridis was not different to that of aphid prey (F1,9 = 4.31, p = 0.068) with 62% (95% CI 45–77%) C. carnea prey and 39% (95% CI 24–57%) aphid prey eaten (Table 1).

Effect of plant species on IGP

On plants the survival of C. carnea was reduced by the presence of 4th-instar H. axyridis (F1,36.5 = 8.57, p = 0.006), with mean proportions of 0.32 (95% CI 0.21–0.45) and 0.59 (95% CI 0.46–0.70) surviving in the presence or absence of the coccinellid, respectively. However, survival was not affected by plant species (F3,36.0 = 0.22, p = 0.885). There was no interaction between the presence/absence of 4th-instar H. axyridis larvae and plant species (F3,36.7 = 0.64, p = 0.594). The proportion of C. carnea surviving per treatment are shown in Fig. 1a. Similar results were found for adult H. axyridis: survival of C. carnea was reduced in the presence of the coccinellid (F1,50.1 = 20.42, p < 0.001), with mean proportions of 0.34 (95% CI 0.25–0.43) and 0.61 (95% CI 0.52–0.70) surviving in the presence and absence of the coccinellid. There was no effect of plant species on the survival of C. carnea (F3,49.0 = 0.50, p = 0.686). Proportions surviving in the individual treatments are shown in Fig. 1b. As with H. axyridis larvae, there was no interaction between the presence/absence of adult H. axyridis and plant species on survival of C. carnea (F3,49.9 = 1.16, p = 0.333).
Fig. 1

Mean proportion of 2nd instar C. carnea surviving in treatments with (Open image in new window) and without (□) a 4th-instar H. axyridis larvae and b adult female H. axyridis on V. faba, B. chinensis, H. vulgare and U. dioica plants. Error bars 95% confidence intervals back-transformed from the logit scale

The effect of shared prey species on IGP

The presence of adult female H. axyridis reduced survival of C. carnea (F1,59.6 = 16.63, p < 0.001) with a mean proportion of 0.32 (95% CI 0.23–0.42) and 0.49 (95% CI 0.39–0.59) C. carnea larvae surviving in the presence or absence of H. axyridis, respectively. However, the proportion of C. carnea surviving was not affected by aphid species (F3,58.9 = 1.33, p = 0.272) (see Fig. 2 for proportion surviving for individual treatments). There was no interaction between the presence or absence of H. axyridis and aphid species on C. carnea survival (F3,64.5 = 1.02, p = 0.391).
Fig. 2

Mean proportion of 2nd instar C. carnea surviving in the presence (Open image in new window) or absence (□) of H. axyridis with: no aphids (control), A. pisum, A. fabae or M. viciae. Error bars 95% confidence intervals back-transformed from the logit scale

There were effects of H. axyridis (F1,79.5 = 76.81, p < 0.001) and C. carnea (F1,84.4 = 33.75, p < 0.001) on aphid survival, with an overall mean proportion of 0.45 (95% CI 0.38–0.52) and 0.74 (95% CI 0.67–0.81) aphids surviving in the presence or absence of H. axyridis and 0.48 (95% CI 0.41–0.54) and 0.71 (95% CI 0.64–0.78) aphids surviving in the presence or absence of C. carnea. The proportion of aphids surviving at the end of the experiment differed between the three species (F2,79.6 = 18.55, p < 0.001), with an overall mean proportion of 0.53 (95% CI 0.45–0.61) A. pisum, 0.52 (95% CI 0.44–0.61) A. fabae and 0.72 (95% CI 0.65–0.81) M. viciae surviving (see Fig. 3 for the proportion of C. carnea surviving per treatment). However, while proportions of each aphid species surviving were affected by H. axyridis (F2,80.0 = 8.66, p < 0.001), with fewer M. viciae being consumed than the other species with the coccinellid present, this was not the case with C. carnea (F2,79.8 = 0.56, p = 0.573), with all three aphid species being consumed to a similar extent whether or not C. carnea was present (see Fig. 3 for the proportion of aphids surviving per treatment). There was an interaction between C. carnea and H. axyridis (F1,83.5 = 4.18, p = 0.044) but there was no three-way interaction between aphid species, C. carnea and H.axyridis (F2,82.9 = 0.33, p = 0.719).
Fig. 3

Mean proportion of aphids remaining in treatments with no aphid enemies (control) (□), 2nd instar C. carnea (Open image in new window), H. axyridis (Open image in new window) and 2nd instar C. carnea + adult H. axyridis (■) and the aphid species A. pisum, A. fabae and M. viciae. Error bars SE of the mean from untransformed data

The effect of shared prey density on IGP

Although adult female H. axyridis affected survival of C. carnea (F1,53.2 = 15.53, p < 0.001), with a mean proportion of 0.39 (95% CI 0.31–0.47) and 0.61 (95% CI 0.53–0.70) C. carnea surviving in the presence or absence of the coccinellid, respectively, there was no effect of aphid density on survival of C. carnea (F3,53.0 = 0.08, p = 0.968), nor was there an interaction between H. axyridis and aphid density (F3,53.8 = 0.80, p = 0.501). See Fig. 4 for the proportion of C. carnea surviving per treatment.
Fig. 4

Mean proportion of C. carnea remaining in the presence (Open image in new window) or absence (□) of H. axyridis and zero, 50, 200 or 500 A. pisum aphids. Error bars 95% confidence intervals back-transformed from the logit scale

Discussion

There is an increasing need to assess the factors that influence interactions between non-native and native species, particularly with respect to improving our understanding of the ecological impacts of non-native species, and to inform risk assessment strategies. Here we demonstrate the complex interplay between various biotic factors in determining the outcome of intraguild interactions between H. axyridis and C. carnea.

Previous research has demonstrated that adult female H. axyridis consumed 2nd-instar C. carnea larvae (Gardiner and Landis 2007). Our study supports these findings and reveals that 2nd-instar C. carnea larvae are also consumed by 2nd and 4th-instar H. axyridis larvae and adult male H. axyridis. In addition, IGP of C. carnea larvae is influenced by their developmental stage: 3rd-instar C. carnea are only minimally at risk of predation by 4th-instar and adult female H. axyridis and are not consumed by 2nd-instar H. axyridis larvae or adult male H. axyridis. This is in agreement with previous studies that have shown that the size of the intraguild prey is an important variable affecting IGP (see Polis et al. 1989; Lucas et al. 1997; Ingels and De Clercq 2011; in contrast see Michaud 2002; Felix and Soares 2004). Indeed, previous research has found that 2nd-instar H. axyridis and C. carnea were symmetrical intraguild predators, and that in paired experiments with these species the outcome is often in favour of the larger instar regardless of species (Nedvěd et al. 2013). Although we did not examine IGP of the pupae of either C. carnea or H. axyridis, this is considered a life-stage vulnerable to predation although coccinellid pupae have chemical and physical defences (Ware and Majerus 2008) and lacewing pupae are covered with a fine silk. The life stage of H. axyridis was also important in determining whether or not IGP occurred. As H. axyridis larvae increased in size, larger-sized C. carnea were consumed. This supports previous work which has shown that generalist predators may increase their prey range to include larger prey as they increase in size during development (e.g. Rosenheim et al. 1993). Whilst this is intuitive, it should be noted that the prey range of adult and larval coccinellids does differ (Harwood et al. 2009). For example, in a field study coccinellid adults did not consume parasitoid pupae whereas coccinellid larvae did (Meyhofer 2001). Our findings suggest that differences in size and in feeding mechanism between H. axyridis larvae and adults may facilitate the creation of feeding niches that could result in reduced competition between conspecifics. Chrysoperla carnea larvae are cannibalistic and this explains the low survival of C. carnea even in the absence of H. axyridis. This was seemingly independent of aphid density but could be as a consequence of the limited range of  aphid densities included within our experiments.

In the field there is a discrete window of time during which C. carnea individuals are at risk from IGP by H. axyridis. Eggs of C. carnea are consumed by H. axyridis (Phoofolo and Obrycki 1998) and, as 2nd-instar larvae of C. carnea are consumed, it can be assumed that 1st-instar C. carnea larvae are also consumed by H. axyridis. At 25 °C (as described in Honěk and Kocourek 1988 and Baverstock et al. 2011), development of C. carnea from oviposition to 3rd-instar requires 13.5 days. Therefore, the minimum amount of time that C. carnea would be at risk from IGP by H. axyridis is 13.5 days. The length of time that C. carnea is at risk from IGP is likely to increase in conditions that increase their development time (e.g. at lower temperatures and/or with a reduced quantity and quality of food). In contrast, H. axyridis may be at risk from predation by C. carnea at the egg stage (Phoofolo and Obrycki 1998; Santi and Maini 2006) and as small larvae (Wells 2011).

In this study predation by female H. axyridis was significantly greater than predation by male H. axyridis. Female and male H. axyridis are known to have different feeding characteristics. For example, females eat more prey than males (Hukusima and Kamei 1970; Roy et al. 2003; Soares et al. 2004; Tsaganou et al. 2004). However, it is not known whether diet preferences differ between the sexes. For example, female coccinellids may need to discriminate between appropriate and inappropriate prey more than males because high quality prey is important for ovary maturation (Honěk 1985). However, in this study, the preference for aphid or intraguild prey was always the same for female and male H. axyridis. In contrast, a previous study showed that starved female adult Coccinella septempunctata did not consume aphid cadavers infected with Pandora neoaphidis when this prey was offered without cues from aphid prey, whereas adult male coccinellids did (Roy et al. 2003).

The plant surface and structure determines the attachment, mobility and, therefore, the efficiency of herbivores and their natural enemy species (Kareiva and Sahakian 1990; Grevstad and Klepetka 1992; Eigenbrode et al. 1996; Legrand and Barbosa 2003; Aquilino et al. 2005; Straub and Snyder 2008; Reynolds and Cuddington 2012b). Mobility of adult H. axyridis is reduced on the underside of flat leaves (regardless of wax surface) and mobility of both H. axyridis and C. carnea is greater on plants with more branching and more ‘edgy plant shapes’ (fewer big flat surfaces) (Reynolds and Cuddington 2012b). In the current study IGP was investigated on dwarf broad bean, cabbage, barley and stinging nettle plants. These plants vary greatly in their architecture, leaf size and leaf surface properties. However, IGP of C. carnea by H. axyridis larvae and adults remained constant regardless of the plant species on which the interaction occurred. This would suggest that the escape behaviour of C. carnea and/or the foraging and IGP behaviours of H. axyridis were not affected by bean, cabbage, barley or stinging nettle plants. Gagnon and Brodeur (2014) also found that plant complexity did not affect IGP of Propylea quatuordecimpunctata (L.) by H. axyridis on soybean plants. However, this is in contrast to findings by Reynolds and Cuddington (2012a) in which aphid predation by H. axyridis was increased on pea plants with many branches compared to ‘near-isolines’ with more flat surfaces. The authors suggest that the flat undersides of leaves provide a refuge for A. pisum from predation by H. axyridis and C. carnea (Reynolds and Cuddington 2012b. It is possible that differences in leaf surface area will affect IGP of C. carnea by H. axyridis: reduced surface area would be predicted to increase encounter rate and hence IGP. It is possible that IGP of a less mobile intraguild prey, for example syrphid larvae, may be influenced to a greater extent by plant species than mobile intraguild prey such as C. carnea. This requires further investigation.

Increasing the scale of investigation from interactions on plants to interactions in habitats has revealed effects of changes in complexity. Previous studies have shown that an increase in habitat complexity can reduce IGP (and cannibalism) resulting in an increase in herbivore suppression (Finke and Denno 2006; Langellotto and Denno 2006). In the field a variety of refuges exist that C. carnea larvae can exploit. For example, C. carnea larvae can hide in flowers, in dried curled up leaves and in old syrphid pupal cases (personal observations). Indeed, large coccinellid larvae and adults cannot forage in curled wheat leaves (Kauffman and LaRoche 1994). Similar experiments to those of Agrawal and Karban (1997) and Roda et al. (2000), where refuges were added to plants, would determine whether such habitat complexity reduces IGP of C. carnea by H. axyridis. At the landscape scale heterogeneity had a beneficial effect on native and exotic coccinellid species in Chile (Grez et al. 2014). However, responses were not consistent between the two regions studied, and the mechanisms driving the responses are not fully understood, therefore more research is required into these complex interactions.

IGP of C. carnea by H. axyridis was not influenced by the shared prey species (A. pisum, A. fabae or M. viciae) despite the aphids varying in their suitability as prey for H. axyridis. Previous studies showed that H. axyridis was able to develop well on A. pisum whereas development took longer on A. fabae and was impeded completely on M. viciae (Soares et al. 2004; Tsaganou et al. 2004). Therefore, it would be intuitive to predict higher IGP in the presence of unsuitable aphids compared to optimal aphid prey. Indeed, previous work has demonstrated increased IGP in the presence of a less preferred shared prey (De Clercq et al. 2003) although in a further study H. axyridis was unable to detect inferior prey (Šenkeríková and Nedvěd 2013). Furthermore, Ungerová et al. (2010) have examined the suitability of different prey species for development of H. axyridis and revealed reduced development time of H. axyridis on A. fabae. Clearly the foraging behaviour of H. axyridis is complex and warrants further investigation but contradictory results between studies could be explained by differences in prey types selected and the context in terms of size and complexity of experimental arenas.

Numerous studies have shown that an increase in shared prey density decreased IGP (e.g. Lucas et al. 1998). Indeed, many studies with H. axyridis as the intraguild predator have shown that IGP is reduced with the addition of shared aphid prey (e.g. Kajita et al. 2000; Nóia et al. 2008; Ingels and De Clercq 2011; Gagnon and Brodeur 2014; Mirande et al. 2015). In our study aphid density did not affect IGP by H. axyridis. Our studies support the theories of Lucas et al. (1998) suggesting that adult H. axyridis face no risk from confrontations with C. carnea and there is no trade-off between predation risk and energetic gain. Therefore, confrontations are not avoided and IGP remains constant regardless of shared prey density. Indeed, on trees in urban areas in Belgium the level of IGP by adult H. axyridis increased with an increase in aphid density (Hautier et al. 2011). Results from our study suggest that A. pisum and C. carnea are either equally suitable (nutritionally) prey for adult H. axyridis or that H. axyridis does not, or cannot, differentiate between the two prey types. Previous studies in which the addition of aphids reduced IGP by H. axyridis may have used intraguild prey that were a less suitable for H. axyridis than aphids. Alternatively, the aphid densities used in the current study may not have been sufficiently high to affect IGP behaviour (De Clercq, personal communication).

Recently the number of studies that have used molecular techniques to detect IGP in nature have increased (Thomas et al. 2013; Brown et al. 2015). However, C. carnea DNA has not been detected in the guts of 4th-instar H. axyridis larvae collected (mostly) from lime trees in five European countries (Brown et al. 2015). This suggests that the H. axyridis larvae evaluated had not preyed on C. carnea in the 24 h prior to sampling (Ingels et al. 2013). The authors suggested that this may have been due to a lack of temporal or spatial overlap in activity patterns and oviposition sites of H. axyridis and C. carnea on lime trees (Brown et al. 2015). More research is required to determine how frequently IGP occurs in other habitats.

In summary, the life stage and the sex of H. axyridis as well as the life stage of C. carnea are important variables affecting IGP and these attributes should be taken into consideration when assessing the potential threat of other invasive predators. Guidelines have been developed to determine the suitability of organisms for release as biological control agents (van Lenteren et al. 2003; van Lenteren and Loomans 2006) and these guidelines require information on the likelihood and magnitude of detrimental effects of any potential biological control agent on non-target species. The results from our study support the conclusions of van Lenteren et al. (2003): non-target effects are likely and consequently H. axyridis is not an acceptable biological control agent even though it is clearly an effective aphid predator. However, by evaluating multiple variables as in our study and so increasing the complexity of the study system we can suggest that the threat of H. axyridis to native arthropod communities may be less than originally perceived from small-scale studies. Including these variables and experimental scale in risk assessments of other species may, therefore, be of importance.

Notes

Acknowledgements

Thanks to Mike Majerus for his enthusiasm and support in the conception and start of this project—he was an inspiration. PMW was supported by the Biotechnology and Biological Sciences Research Council of the United Kingdom (BBSRC). JB was supported by the U.K. Department for Environment, Food and Rural Affairs (Defra). JKP was supported by Defra and BBSRC. Rothamsted Research is an Institute of the BBSRC. HER is in the Biological Records Centre (BRC) within the NERC Centre for Ecology & Hydrology. BRC is cofunded by NERC and the Joint Nature Conservation Committee.

Supplementary material

10526_2016_9775_MOESM1_ESM.docx (16 kb)
Supplementary material 1 (DOCX 15 kb)

References

  1. Agrawal AA, Karban R (1997) Domatia mediate plant-arthropod mutualism. Nature 387:562–563CrossRefGoogle Scholar
  2. Aquilino KM, Cardinale BJ, Ives AR (2005) Reciprocal effects of host plant and natural enemy diversity on herbivore suppression: an empirical study of a model tritrophic system. Oikos 108:275–282CrossRefGoogle Scholar
  3. Baverstock J, Porcel M, Clark SJ, Copeland JE, Pell JK (2011) Potential value of the fibre nettle Urtica dioica as a resource for the nettle aphid Microlophium carnosum and its insect and fungal natural enemies. BioControl 56:215–223CrossRefGoogle Scholar
  4. Brown PMJ, Adriaens T, Bathon H, Cuppen J, Goldarazena A, Hagg T, Kenis M, Klausnitzer BEM, Kovar I, Loomans AJ, Majerus MEN, Nedvěd O, Pedersen J, Rabitsch W, Roy HE, Ternois V, Zakharov I, Roy DB (2008) Harmonia axyridis in Europe: spread and distribution of a non-native coccinellid. BioControl 53:5–22CrossRefGoogle Scholar
  5. Brown PMJ, Frost R, Doberski J, Sparks TIM, Harrington R, Roy HE (2011) Decline in native ladybirds in response to the arrival of Harmonia axyridis: early evidence from England. Ecol Entomol 36:231–240CrossRefGoogle Scholar
  6. Brown PMJ, Ingels B, Wheatley A, Rhule EL, De Clercq P, van Leeuwen T, Thomas A (2015) Intraguild predation by Harmonia axyridis (Coleoptera: Coccinellidae) on native insects in Europe: molecular detection from field samples. Entomol Sci 18:130–133CrossRefGoogle Scholar
  7. Colunga-Garcia M, Gage SH (1998) Arrival, establishment, and habitat use of the multicolored Asian lady beetle (Coleoptera: Coccinellidae) in a Michigan landscape. Environ Entomol 27:1574–1580CrossRefGoogle Scholar
  8. DAISIE European Invasive Alien Species Gateway (http://www.europe-aliens.org)
  9. De Clercq P, Peeters I, Vergauwe G, Thas O (2003) Interaction between Podisus maculiventris and Harmonia axyridis two predators used in augmentative biological control in greenhouse crops. BioControl 58:39–55CrossRefGoogle Scholar
  10. Eigenbrode SD, Castagnola T, Roux MB, Steljes L (1996) Mobility of three generalist predators is greater on cabbage with glossy leaf wax than on cabbage with a wax bloom. Entomol Exp Appl 81:335–343CrossRefGoogle Scholar
  11. European Commission (2002) Thematic report on alien invasive species. Second report of the European Community to the Conference of the Parties of the Convention on Biological Diversity. Office for Official Publications of the European Communities, LuxembourgGoogle Scholar
  12. Felix S, Soares AO (2004) Intraguild predation between the aphidophagous ladybird beetles Harmonia axyridis and Coccinella undecimpunctata (Coleoptera: Coccinellidae): the role of body weight. Eur J Entomol 101:237–242CrossRefGoogle Scholar
  13. Finke DL, Denno RF (2006) Spatial refuge from intraguild predation: implications for prey suppression and trophic cascades. Oecologia 149:265–275CrossRefPubMedGoogle Scholar
  14. Gagnon AE, Brodeur J (2014) Impact of plant architecture and extraguild prey density on intraguild predation in an agroecosystem. Entomol Exp Appl 152:165–173CrossRefGoogle Scholar
  15. Gardiner MM, Landis DA (2007) Impact of intraguild predation by adult Harmonia axyridis (Coleoptera: Coccinellidae) on Aphis glycines (Hemiptera: Aphididae) biological control in cage studies. Biol Control 40:386–395CrossRefGoogle Scholar
  16. Grevstad FS, Klepetka BW (1992) The influence of plant architecture on the foraging efficiencies of a suite of ladybird beetles feeding on aphids. Oecologia 92:399–404CrossRefPubMedGoogle Scholar
  17. Grez AA, Zaviezo T, Hernández J, Rodríguez-San A, Paz Acuña P (2014) The heterogeneity and composition of agricultural landscapes influence native and exotic coccinellids in alfalfa fields. Agricul Forest Entomol 16:382–390CrossRefGoogle Scholar
  18. Harwood J, Yoo H, Greenstone M, Rowley D, O’Neil R (2009) Differential impact of adults and nymphs of a generalist predator on an exotic invasive pest demonstrated by molecular gut-content analysis. Biol Invasions 11:895–903CrossRefGoogle Scholar
  19. Hautier L, Martin GS, Callier P, de Biseau JC, Gregoire JC (2011) Alkaloids provide evidence of intra-guild predation on native coccinellids by Harmonia axyridis in the field. Biol Invasions 13:1805–1814CrossRefGoogle Scholar
  20. Honěk A (1985) Habitat preferences of aphidophagous coccinellids [Coleoptera]. Entomophaga 30:253–264CrossRefGoogle Scholar
  21. Honěk A, Kocourek F (1988) Thermal requirements for development of aphidophagous Coccinellidae (Coleoptera), Chrysopidae, Hemerobiidae (Neuroptera), and Syrphidae (Diptera): some general trends. Oecologia 76:455–460CrossRefPubMedGoogle Scholar
  22. Hukusima S, Kamei M (1970) Effects of various species of aphids as food on development, fecundity and longevity of Harmonia axyridis Pallas (Coleoptera: Coccinellidae). Res Bull Faculty Agric Gifu Univ 29:53–66Google Scholar
  23. Ingels B, De Clercq P (2011) Effect of size, extraguild prey and habitat complexity on intraguild interactions: a case study with the invasive ladybird Harmonia axyridis and the hoverfly Episyrphus balteatus. BioControl 56:871–882CrossRefGoogle Scholar
  24. Ingels B, Aebi A, Hautier L, van Leeuwen T, De Clercq P (2013) Molecular analysis of the gut contents of Harmonia axyridis (Coleoptera: Coccinellidae) as a method for detecting intra-guild predation by this species on aphidophagous predators other than coccinellids. Eur J Entomol 110:567–576CrossRefGoogle Scholar
  25. Kajita Y, Takano F, Yasuda H, Agarwala BK (2000) Effects of indigenous ladybird species (Coleoptera: Coccinellidae) on the survival of an exotic species in relation to prey abundance. Appl Entomol Zool 35:473–479CrossRefGoogle Scholar
  26. Kareiva P, Sahakian R (1990) Tritrophic effects of a simple architectural mutation in pea plants. Nature 345:433–434CrossRefGoogle Scholar
  27. Kauffman WC, LaRoche SL (1994) Searching activities by Coccinellids on rolled wheat leaves infested by the Russian wheat aphid. Biol Control 4:290–297CrossRefGoogle Scholar
  28. Koch RL, Venette RC, Hutchison WD (2006) Predicted impact of an exotic generalist predator on monarch butterfly (Lepidoptera: Nymphalidae) populations: a quantitative risk assessment. Biol Invasions 8:1179–1193CrossRefGoogle Scholar
  29. Langellotto GA, Denno RF (2006) Refuge from cannibalism in complex-structured habitats: implications for the accumulation of invertebrate predators. Ecol Entomol 31:575–581CrossRefGoogle Scholar
  30. Legrand A, Barbosa P (2003) Plant morphological complexity impacts foraging efficiency of adult Coccinella septempunctata L. (Coleoptera: Coccinellidae). Environ Entomol 32:1219–1226CrossRefGoogle Scholar
  31. Lucas E (2005) Intraguild predation among aphidophagous predators. Eur J Entomol 102:351–363CrossRefGoogle Scholar
  32. Lucas E, Coderre D, Brodeur J (1997) Instar-specific defence of Coleomegilla maculata lengi (Col.: Coccinellidae): Influence on attack success of the intraguild predator Chrysoperla rufilabris (Neur.: Chrysopidae). Entomophaga 42:3–12CrossRefGoogle Scholar
  33. Lucas E, Coderre D, Brodeur J (1998) Intraguild predation among aphid predators: characterization and influence of extraguild prey density. Ecology 79:1084–1092CrossRefGoogle Scholar
  34. Majerus M, Strawson V, Roy HE (2006) The potential impacts of the arrival of the harlequin ladybird, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), in Britain. Ecol Entomol 31:207–215CrossRefGoogle Scholar
  35. Meyhofer R (2001) Intraguild predation by aphidophagous predators on parasitised aphids: the use of multiple video cameras. Entomol Exp Appl 100:77–87CrossRefGoogle Scholar
  36. Michaud JP (2002) Invasion of the Florida citrus ecosystem by Harmonia axyridis (Coleoptera: Coccinellidae) and asymmetric competition with a native species, Cycloneda sanguinea. Environ Entomol 31:827–835CrossRefGoogle Scholar
  37. Mirande L, Desneux N, Haramboure M, Schneider MI (2015) Intraguild predation between an exotic and a native coccinellid in Argentina: the role of prey density. J Pest Sci 88:155–162CrossRefGoogle Scholar
  38. Nedvěd O, Fois X, Ungerova D, Kalushkov P (2013) Alien vs. Predator—the native lacewing Chrysoperla carnea is the superior intraguild predator in trials against the invasive ladybird Harmonia axyridis. Bull Insectol 1:73–78Google Scholar
  39. Nóia M, Borges I, Soares AO (2008) Intraguild predation between the aphidophagous ladybird beetles Harmonia axyridis and Coccinella undecimpunctata (Coleoptera: Coccinellidae): The role of intra and extraguild prey densities. Biol Control 46:140–146CrossRefGoogle Scholar
  40. Pell JK, Baverstock J, Roy HE, Ware RL, Majerus MEN (2008) Intraguild predation involving Harmonia axyridis: a review of current knowledge and future perspectives. BioControl 53:147–168CrossRefGoogle Scholar
  41. Phoofolo MW, Obrycki JJ (1998) Potential for intraguild predation and competition amongst predatory Coccinellidae and Chrysopidae. Entomol Exp Appl 89:47–55CrossRefGoogle Scholar
  42. Polis G, Myers C, Holt R (1989) The ecology and evolution of intra-guild predation: potential competitors that eat each other. Annu Rev Ecol Syst 20:297–330CrossRefGoogle Scholar
  43. Reynolds PG, Cuddington K (2012a) Effects of plant gross morphology on predator consumption behaviour. Entomol Soc Am 41:508–515Google Scholar
  44. Reynolds PG, Cuddington K (2012b) Effects of plant gross morphology on predator searching behaviour. Entomol Soc Am 41:516–522Google Scholar
  45. Roda A, Nyrop J, Dicke M, English-Loeb G (2000) Trichomes and spider-mite webbing protect predatory mite eggs from intraguild predation. Oecologia 125:428–435CrossRefGoogle Scholar
  46. Rosenheim JA, Wilhoit LR, Armer CA (1993) Influence of intraguild predation among generalist insect predators on the suppression of a herbivore population. Oecologia 96:439–449CrossRefPubMedGoogle Scholar
  47. Roy DB (2008) Harmonia axyridis in Europe: spread and distribution of a non-native coccinellid. BioControl 53:5–21CrossRefGoogle Scholar
  48. Roy HE, Alderson PG, Pell JK (2003) Effect of spatial heterogeneity on the role of Coccinella septempunctata as an intra-guild predator of the aphid pathogen Pandora neoaphidis. J Invertebr Pathol 82:85–95CrossRefPubMedGoogle Scholar
  49. Roy HE, Adriaens T, Isaac NJB, Kenis M, Onkelinx T, San Martin G, Brown PMJ, Hautier L, Poland RL, Roy DB, Comont R, Eschen R, Frost R, Zindel R, Van Vlaenderen J, Nedvěd O, Ravn HP, Grégoire J-C, de Biseau J-C, Maes D (2012) Invasive alien predator causes rapid declines of native European ladybirds. Divers Distrib. doi:10.1111/j.1472-4642.2012.00883.x Google Scholar
  50. Roy HE, Brown PMJ, Adriaens T, Berkvens N, Borges I, Clusella-Trullas S, Comont RF, De Clercq P, Eschen R, Estoup A, Evans EW, Facon B, Gardiner MM, Gil A, Grez AA, Guillemaud T, Haelewaters D, Herz A, Honek A, Howe AG, Hui C, Hutchison WD, Kenis M, Koch RL, Kulfan J, Lawson Handley L, Lombaert E, Loomans A, Losey J, Lukashuk AO, Maes D, Magro A, Murray KM, San Martin G, Martinkova Z, Minnaar IA, Nedvěd O, Orlova-Bienkowskaja MJ, Osawa N, Rabitsch W, Ravn HP, Rondoni G, Rorke SL, Ryndevich SK, Saethre M-G, Sloggett JJ, Soares AO, Stals R, Tinsley MC, Vandereycken A, van Wielink P, Viglasova S, Zach P, Zakharov IA, Zaviezo T, Zhao Z (2016) The harlequin ladybird, Harmonia axyridis: global perspectives on invasion history and ecology. Biol Invasions 18:997–1044CrossRefGoogle Scholar
  51. Santi F, Maini S (2006) Predation upon Adalia bipunctata and Harmonia axyridis eggs by Chrysoperla carnea larvae and Orius laevigatus adults. Bull Insectol 59:53–58Google Scholar
  52. Šenkeříková P, Nedvěd O (2013) Preference among three aphid species by predatory ladybird beetle Harmonia axyridis in laboratory. IOBC-WPRS Bull 94:123–130Google Scholar
  53. Soares AO, Coderre D, Schanderl H (2004) Dietary self-selection behaviour by the adults of the aphidophagous ladybeetle Harmonia axyridis (Coleoptera: Coccinellidae). J Anim Ecol 73:478–486CrossRefGoogle Scholar
  54. Straub CS, Snyder WE (2008) Increasing enemy biodiversity strengthens herbivore suppression on two plant species. Ecology 89:1605–1615CrossRefPubMedGoogle Scholar
  55. Thomas AP, Trotman J, Wheatley A, Aebi A, Zindel R, Brown PMJ (2013) Predation of native coccinellids by the invasive alien Harmonia axyridis (Coleoptera: Coccinellidae): detection in Britain by PCR-based gut analysis. Ins Conserv Divers 6:20–27CrossRefGoogle Scholar
  56. Tsaganou FC, Hodgson CJ, Athanassiou CG, Kavallieratos NG, Tomanovic A (2004) Effect of Aphis gossypii Glover, Brevicoryne brassicae (L.), and Megoura viciae Buckton (Hemiptera: Aphidoidea) on the development of the predator Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae). Biol Control 31:138–144CrossRefGoogle Scholar
  57. Ungerová D, Kalushkov P, Nedvěd O (2010) Suitability of diverse prey species for development of Harmonia axyridis and the effect of container size. IOBC-WPRS Bull 58:165–174Google Scholar
  58. van Lenteren JC, Loomans AJ (2006) Environmental risk assessment: methods for comprehensive evaluation and quick scan. In: Bigler F, Babendreier D, Kuhlmann U (eds) Environmental impact of invertebrates for biological control of arthropods. CABI Publishing, pp 254–272Google Scholar
  59. van Lenteren JC, Babendreier D, Bigler F, Burgio G, Hokkanen HM, Kuske S, Loomans AJ, Menzler-Hokkanen I, van Rijn PC, Thomas MB, Tommasini MG (2003) Environmental risk assessment of exotic natural enemies used in inundative biological control. BioControl 48:3–8CrossRefGoogle Scholar
  60. VSNi (2010) GenStat for Windows 13th Edition. VSNi, Hemel Hempstead, UK. https://www.vsni.co.uk/
  61. Wagner DL, van Driesche RG (2010) Threats posed to rare or endangered insects by invasions of non-native species. Ann Rev Entomol 55:547–568CrossRefGoogle Scholar
  62. Ware RL, Majerus MEN (2008) Intraguild predation of immature stages of British and Japanese coccinellids by the invasive ladybird Harmonia axyridis. BioControl 53:169–188CrossRefGoogle Scholar
  63. Wells PM (2011) Intraguild predation by Harmonia axyridis: effects on native enemies and aphid suppression. PhD thesis, University of Cambridge, UKGoogle Scholar
  64. Williams F, Eschen R, Harris A, Djeddour D, Pratt C, Shaw R, Varia S, Lamontagne-Godwin J, Thomas S, Murphy S (2010) The economic cost of invasive non-native species on Great Britain. CABI Proj No VM10066Google Scholar

Copyright information

© International Organization for Biological Control (IOBC) 2016

Authors and Affiliations

  • P. M. Wells
    • 1
  • J. Baverstock
    • 1
  • S. J. Clark
    • 1
  • F. M. Jiggins
    • 2
  • H. E. Roy
    • 3
  • J. K. Pell
    • 1
    • 4
  1. 1.Rothamsted ResearchHarpendenUK
  2. 2.University of CambridgeCambridgeUK
  3. 3.Centre for Ecology and HydrologyWallingfordUK
  4. 4.J.K. Pell ConsultingLutonUK

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