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Floral diversity, parasitoids and hyperparasitoids – A laboratory approach
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Basic and Applied Ecology 9 (2008) 588–597
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Floral diversity, parasitoids and hyperparasitoids – A laboratory approach Salah-Eddin Araj, Steve Wratten, Alison Lister, Hannah Buckley National Centre for Advanced Bio-Protection Technologies, PO Box 84, Lincoln University, Canterbury 7647, New Zealand Received 20 December 2006; accepted 7 August 2007
Abstract Adding floral resources to agro-ecosystems to improve biological control can enhance the survival, egg load, and parasitism rate of insect parasitoids. However, this may not always be the case because the herbivore may benefit from the added resource as much as, or more than the third-trophic level. In addition, the natural enemies of those in the third-trophic level may also derive improved fitness from the added resources. Both these processes will dampen trophic cascades, leading to less-effective biological control. In this study, the effect of adding different flowering plants on the longevity, egg load, aphid parasitism rates and hyperparasitism of Aphidius ervi Haliday (Hymenoptera: Braconidae) by its hyperparasitoid Dendrocerus aphidum Rondani (Hymenoptera: Megaspilidae) were investigated, using the pea aphid Acyrthosiphon pisum Harris (Homoptera: Aphididae) as the herbivore. Parasitoids exposed to buckwheat survived, on average, between four to five times as long as those in the control (water) and those in phacelia, alyssum and coriander treatments survived three to four times as long. Hyperparasitoids exposed to buckwheat survived five to six times as long as those in the control and three to five times longer with the other plants compared with the control. Almost all flower species significantly increased parasitoid and hyperparasitoid egg loads and the number of parasitised aphids and parasitised mummies compared with control. Understanding the factors influencing the dynamics of multitrophic interactions involving flowering plants, herbivores, parasitoids and hyperparasitoids is a fertile area for future research. One of the most challenging areas in contemporary ecology concerns the relative importance of different types of biodiversity mediating trophic interactions and thereby influencing the structure of communities and food webs. This paper begins to explore this using an experimental, laboratory-based approach. r 2007 Gesellschaft fu¨r O¨kologie. Published by Elsevier GmbH. All rights reserved.
Zusammenfassung Zusa¨tzliche Blu¨tenquellen in landwirtschaftlichen O¨kosystemen zur Verbesserung des biologischen Pflanzenschutzes ko¨nnen U¨berleben, Eiproduktion und Parasitierungsrate parasitoider Insekten fo¨rdern. Dies muss jedoch nicht immer zu verbessertem biologischen Pflanzenschutz fu¨hren, denn die Herbivoren ko¨nnen durch die zusa¨tzliche Nahrungsquelle ebenso oder sogar sta¨rker begu¨nstigt werden als die dritte Trophieebene. Auch die natu¨rlichen Feinde der Arten auf dem dritten Trophieniveau erfahren mo¨glicherweise durch die zusa¨tzliche Nahrungsquelle eine Steigerung ihrer U¨berlebensfa¨higkeit. Beide Vorga¨nge ko¨nnen die trophische Kaskade und folglich die biologische Scha¨dlingsbeka¨mpfung schwa¨chen.
Corresponding author. Tel.: +64 3 325 3838x8386; fax: +64 3 325 3864.
E-mail address: [email protected] (S.-E. Araj). 1439-1791/$ - see front matter r 2007 Gesellschaft fu¨r O¨kologie. Published by Elsevier GmbH. All rights reserved. doi:10.1016/j.baae.2007.08.001
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In der vorliegenden Studie wurden die Auswirkungen verschiedener Blu¨tenpflanzen auf Lebensdauer, Eiproduktion und Blattlaus-Parasitierungsraten von Aphidius ervi Haliday (Hymenoptera: Braconidae) sowie auf deren Hyperparasitierung durch Dendrocerus aphidum Rondani (Hymenoptera: Megaspilidae) untersucht, mit der Erbsenblattlaus Acyrthosiphon pisum Harris (Homoptera: Aphididae) als Herbivoren. Parasitoide, die Zugang zu Buchweizen hatten, lebten im Durchschnitt vier- bis fu¨nfmal so lange wie die Kontrollkulturen (Wasser), diejenigen mit Zugang zu Phacelia, Alyssum und Koriander drei- bis viermal so lange. Hyperparasitoide, die Zugang zu Buchweizen hatten, lebten fu¨nf-bis sechsmal so lange wie die Kontrollkulturen; mit den anderen Pflanzen lebten sie drei- bis fu¨nfmal so lange wie die Kontrolle. Fast alle Blu¨tenarten erho¨hten die Eiproduktion der Parasitoiden und Hyperparasitoiden sowie die Anzahl der parasitierten Blattla¨use und Blattlausmumien signifikant, verglichen mit der Kontrolle. Faktoren, die auf die multitrophische Interaktion zwischen Blu¨tenpflanzen, Herbivoren, Parasitoiden und Hyperparasitoiden einwirken, sind ein ergiebiges Gebiet zuku¨nftiger Forschung. Eines der interessantesten Felder moderner O¨kologie ist die relative Bedeutung verschiedener Arten von Biodiversita¨t, ihr Einfluss auf die trophische Interaktion und damit auf Strukturen von Artengemeinschaften und Nahrungsnetzen. Die vorliegende Studie untersucht diese Zusammenha¨nge anhand eines Laborexperiments. r 2007 Gesellschaft fu¨r O¨kologie. Published by Elsevier GmbH. All rights reserved. Keywords: Acyrthosiphon pisum; Aphidius ervi; Dendrocerus aphidum; Buckwheat; Phacelia; Alyssum; Coriander
Introduction The relationship between biodiversity and ecosystem function has emerged as an important issue in ecology during the last decade. Systematic experimental and observational studies of how changes in diversity interact at different trophic levels are required (De Deyn, Raaijmakers, Ruijven, Berendse, & van der Putten, 2004; Finke & Denno, 2002; Worm & Duffy, 2003). Most studies of the relationship between diversity and ecosystem function have been carried out involving only two trophic levels (Cardinale, Weis, Tilmon, Forbes, & Ives, 2006; Chapin et al., 2000; Hasegawa, 2004; Loreau, 2001; Loreau et al., 2001) and studies of ecosystem function using multitrophic communities have only rarely been reported (Duffy, 2002; Finke & Denno, 2002; Paine, 1966, 2002; Snyder & Wise, 2001). In particular, the role of hyperparasitoids (parasitic wasps that attack primary parasitoids) in the diversity–ecosystem function relationship has been investigated to a very small extent. Earlier work comprised a glasshouse experiment in which hyperparasitoids reduced parasitism to such an extent that plant biomass increased (Goergen & Neuenschwander, 1992). The preliminary field sampling of Stephens, France, Wratten, & Frampton (1998) showed only that higher numbers of a lacewing (Hemerobiidae) parasitoid, Anacharis sp. (Hymenoptera: Figitidae), were caught in yellow pan traps close to buckwheat flowers, Fagopyrum esculentum (Moench), compared with control plots, and did not explicitly test and identify the processes underlying this pattern. A better understanding of how parasitoids and hyperparasitoids exploit floral subsidies can help in
designing more efficient biological control strategies (Landis, Wratten, & Gurr, 2000), via ‘ecological engineering’ (Gurr, Wratten, & Altieri, 2004) at the landscape scale. To be efficient for biological control, these subsidies must at least increase the rate of predation or parasitism in the crop associated with the subsidy (Berndt, Wratten, & Hassan, 2002). Differences in body size of parasitoids and hyperparasitoids could lead to differential foraging performance on various floral architectures. Larger wasps have superior searching ability and can access nectar from flowers with both exposed and partially exposed nectaries (Patt, Hamilton, & Lashomb, 1999). Aphid parasitoids are a valuable model system for testing ideas about community interactions (Mu¨ller & Godfray, 1999) because aphids are ubiquitous in most terrestrial ecosystems and abundant in both natural and managed habitats (Brodeur & Rosenheim, 2000). Aphids are attacked by a wide array of pathogens, parasitoids and predators, the densities of which vary in space and time and which may significantly reduce aphid population growth (Dennis & Wratten, 1991; Mu¨ller & Godfray, 1999). The basis for the current work was to determine the relative value of different floral resources for a parasitoid and a hyperparasitoid and to determine if these resources can simultaneously benefit the fourth-trophic level, which may work to the detriment of aphid biocontrol. Indeed, this study has the potential to identify a plant species that enhances the ecological ‘fitness’ of the primary parasitoid more than that of the hyperparasitoid. The aim of this work was to measure the effects of a range of plant nectars on the longevity, egg load and parasitism rates of pea aphids by Aphidius ervi and hyperparasitism rates of A. ervi by Dendrocerus aphidum compared with water controls.
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Materials and methods
to ensure that flowers were continuously available for laboratory experiments.
Insect rearing Pea aphids were reared in the laboratory on potted plants of broad bean (Vicia faba L. cv. Cole’s Dwarf). A clonal culture was started with one female aphid being confined on one leaflet using a clip cage as described by Noble (1958). When the first 5–8 progeny had been produced, the female was discarded to ensure that the progeny and future colony were free of parasitoids. The resulting progeny were reared on broad bean plants in Perspex cages (64 45 40 cm) with a nylon mesh door. The colony was maintained continuously as parthenogenetic females at 2074 1C and RH 60–70% with a photoperiod of 16:8 h light:dark. Light intensity was 122 mmol/m2/s. Aphid mummies were collected from lucerne fields, then put singly into 600 ml gelatine capsules and kept in a transparent polystyrene box (20 10 5 cm) under the above conditions. When parasitoids or hyperparasitoids emerged, they were identified using the keys of Mertins (1985). An A. ervi colony was established using 10 males and 10 females, which were presented with second-instar pea aphids. The culture was subsequently maintained under the same rearing conditions that were used for the aphids (see above). A colony of D. aphidum was established from individuals (A. ervi or A. eadyi (Stary) (Hymenoptera: Braconidae)) emerging from parasitised pea aphids which had been collected as mummies from lucerne fields (see above). Ten males and ten females of D. aphidum were reared on newly formed mummies (containing aphid parasitoid pupae, which form approximately 9 days after oviposition by A. ervi (Walker & Cameron, 1981) and were maintained under the conditions described above. The identification of A. ervi and its parasitoids was confirmed by Dr. J. Berry of Landcare Research, Auckland, New Zealand, in April 2004, and key identification characters were recorded for future reference.
Flowering plants as nectar sources Phacelia (Phacelia tanacetifolia Bentham cv. Balo), buckwheat (cv. Katowase), alyssum (Lobularia maritima L. cv. Carpet of Snow) and coriander (Coriandrum sativum L. cv. Slowbolt) were assessed for their ability to enhance the ‘fitness’ and efficacy of A. ervi and D. aphidum. The four species have been shown in many studies to enhance the efficacy of parasitoids and predators against pests in other crop systems (Hickman & Wratten, 1996; Tooker & Hanks, 2000; White, Wratten, Berry, & Weigmann, 1995; Wratten & van Emden, 1995). Candidate plant species were grown in a greenhouse with 16:8 h light:dark and were sown at 2-week intervals
Experiment 1. The effect of flowers on A. ervi longevity The above flowering plant species were individually tested against a water control. For each treatment, a well-watered flowering, rooted shoot of the plant was used, to maximise quality and quantity of nectar available to the wasps. The flowering shoots were carefully inserted into a transparent polycarbonate jar (120 mm tall and 85 mm in diameter) through a bottom opening, which was then sealed with low-density polyurethane foam around the shoot. The top of the jar was removed and covered with fine nylon mesh. The jar was attached to a vertical wooden stake fixed to the plant pot. A foam-sealable (20 mm diameter) hole was cut into the wall of the jar to introduce parasitoids when required. Similar cages were used for water treatments via damp dental rolls provided on the mesh top of the cage. A completely randomised design was used with five treatments and seven replicates per treatment. One naı¨ ve female and one male of A. ervi were used per cage. Longevity of the parasitoids was recorded for all treatments. The test was conducted under the conditions described earlier and survival was recorded every 24 h.
Experiment 2. The effect of flowers on D. aphidum longevity The same flowering plant species and the same control and cage design as in Experiment 1 were used in this experiment. A completely randomised design with seven replicates was used as above. One female and one male D. aphidum (both naı¨ ve) were used per cage. Longevity of the hyperparasitoids was recorded for the treatments and control. Survival was recorded every 24 h.
Experiment 3. The effect of nectar feeding on the egg load of A. ervi Experimental cages with flowering plants, as described in Experiment 1, were set up in the laboratory. The treatments comprised the four flowering plant species and a water control (damp dental rolls). The five treatments were randomly allocated to each of 25 cages; i.e., five replicates/treatment. To assess parasitoid egg load after different lengths of time, the five cages in each treatment were each allocated to one of the five sampling times (6, 12, 24, 48 and 72 h), so that at each time, egg load was recorded for five mated, female parasitoids. To determine this, females were
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euthanised and dissected. Ovaries were removed by grasping the ovipositor with fine forceps and gently pulling until the ovipositor and ovaries became detached from the abdomen. Ovaries were placed on a microscope slide and stained with a 0.1% solution of methylene blue. Pressing gently on the cover slip caused the ovaries to burst, releasing the eggs, which were counted under a dissecting microscope at 63 magnification (Tylianakis, Didham, & Wratten, 2004).
Experiment 4. The effect of nectar feeding on the egg load of D. aphidum Experimental cages with flowering plants as described for Experiment 1 were set up in the laboratory. Fortyfive, mated, naı¨ ve female hyperparasitoids were assigned to each of the five treatments to examine the effects of floral resources on egg load. The treatments were the four flowering plant species and a control (damp dental rolls). Five randomly selected females for each treatment were euthanised and dissected at each of the nine time intervals (6, 24, 48, 72, 96, 120, 144, 168 and 192 h) to assess egg load.
Experiment 5. The effect of floral resources on parasitism of the pea aphid The four selected flowering plant species were compared with a water control consisting of damp dental rolls. For each treatment, a flowering shoot on a rooted plant of each plant species was utilized; the pot was regularly watered to maintain the quality and quantity of nectar available to the wasps. The shoots were inserted into a transparent polycarbonate jar (135 mm tall and 85 mm in diameter) through a circular opening (40 mm in diameter) from one of the sides, which was then sealed around the shoot with a piece of foam. The top of the jar was removed and covered with fine nylon mesh. The bottom was sealed with a Petri dish base (85 mm diameter). The jar was then attached to a vertical wooden stake fixed to the plant pot. A foamsealable (20 mm diameter) hole was cut into the wall of the jar to introduce parasitoids. Similar cages were used for the controls (water) with damp dental rolls provided on the mesh top of the cage. A randomised-block design was used with five treatments and seven replicates per treatment. This experiment was conducted under 2074 1C and RH 60–70% with a photoperiod of 16:8 h light: dark. Light intensity was 122 mmol/m2/s. Each experimental jar contained one naı¨ ve female and one male of A. ervi, a damp dental roll and a cut leaflet of a broad bean plant infested with 80–100 1–3-day-old pea aphids which were provided every day until the death of the female parasitoid. This provided an abundant population of
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new potential hosts so that maximum potential rates of parasitism could be achieved. The cut leaflets harbouring the aphids in each treatment were replaced daily until the death of the female parasitoid. The aphids exposed to parasitoids in this way were subsequently kept in a transparent container containing a rooted broad bean shoot. Aphids were examined daily for signs of mummification, and the number of parasitised aphids in each treatment was recorded. The experimental treatments were: control, with no additional resources provided, phacelia, buckwheat, alyssum and coriander.
Experiment 6. The effect of the provision of floral resources on hyperparasitism of the pea aphid Experimental jars as used in Experiment 5 with the same flowering plants and control were set up in the laboratory. Each jar contained one naı¨ ve female and one male hyperparasitoid assigned to each of the five treatments; damp dental rolls were provided on the mesh top of the cage and a leaflet of a broad bean seedling infested with 60–70 newly formed mummies was added. This was replaced every 3 days. Each experiment ended with the death of the female hyperparasitoid. Thereafter, the number of hyperparasitoids was monitored and recorded, if no parasitoid or hyperparasitoid emerges, the mummy was dissected to determine if it is parasitized or hyperparasitsed. For the treatments and control, see Experiment 5.
Data analysis Survival analysis was used to compare the effect of the food resources on the longevity of A. ervi and D. aphidum by calculating the Kaplan–Meier estimate of the survival function. To determine the effect of nectar feeding on egg load of A. ervi and D. aphidum, untransformed data were analysed using analysis of variance (ANOVA). For A. ervi, the first 48 h were analysed separately from 72-h data because all the parasitoids had died in the control treatment by 72 h. Parasitism and hyperparasitism data were square-roottransformed to normalise variances and comparisons between treatments were made using one-way analysis of variance. All statistical analyses were conducted using GenStat 7.
Results A. ervi longevity Survival in the controls was 3–4 days for A. ervi females and 2–3 days for males. With buckwheat, survival was
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12–20 and 8–16 days for females and males, respectively. For phacelia, the equivalent data were 6–15 and 6–10 days, coriander 7–17 and 6–15 days and alyssum 7–16 and 5–14 days. Parasitoids exposed to buckwheat survived, on average, four to five times longer than those in the control and three to four times longer for the other flowering plants (Table 1 and Figs. 1A and B). Both female and male survival curves differed significantly between treatments. Females: (log-rank ¼ 49.59, Po0.001; Wilcoxon (Breslow) ¼ 45.53, Po0.001) (Fig. 1A). Males (logrank ¼ 48.91, Po0.001; Wilcoxon (Breslow) ¼ 45.31, Po0.001) (Fig. 1B). Longevity was significantly different between treatments (F4,30 ¼ 15.16, Po0.001) (Table 1). Individuals in the buckwheat treatment survived significantly longer than did those in control or other flowering plant treatments. Individuals in the phacelia, alyssum and coriander treatments survived significantly longer than did those in the control with no significant difference in longevity between the phacelia, coriander and alyssum treatments (Table 1). Females survived significantly longer than males (F1,30 ¼ 40.56, Po0.001) (Table 1, Figs. 1A and B). The interaction between sex and treatment was not significant (F4,30 ¼ 1.93, P ¼ 0.131).
D. aphidum longevity Survival times of D. aphidum females ranged from 6 to 12 days and males from 5 to 10 days in controls, 23–57 and 25–55 days, respectively, with buckwheat, 24–41 and 18–48 days with phacelia, 16–48 and 17–37 days with coriander and 18–36 and 18–27 days with alyssum. Hyperparasitoid individuals exposed to buckwheat survived, on average, five to six times
Table 1. Mean survival of A. ervi and D. aphidum (days) under different treatment and sexes Mean survival (days) of A. ervi
D. aphidum
Main effect of treatment Alyssum 9.1b Buckwheat 13.9a Control 2.9c Coriander 10.1b Phacelia 8.5b LSD (0.05) 2.93
23.5c 43.1a 7.3d 26.1bc 33.5b 7.76
Main effect of sex Female Male LSD (0.05)
28.5a 24.8b 2.85
10.0a 7.9b 0.68
Values followed by the same letter within a column are not significantly different (Po0.05).
Fig. 1. Kaplan–Meier estimates of survival functions of Aphidius ervi (A) females (B) males given access to water (control), buckwheat, phacelia, coriander or alyssum as floral nectar sources.
longer than those in the control and three to five times longer with the other flowering plants than the control (Table 1 and Figs. 2A and B). Female and male survival curves differed significantly between treatments. Females: (log-rank ¼ 59.17, Po0.001; Wilcoxon (Breslow) ¼ 52.32, Po0.001) (Fig. 2A). Males: (log-rank ¼ 63.28, Po0.001; Wilcoxon (Breslow) ¼ 55.33, Po0.001) (Fig. 2B). Longevity was significantly different between treatments (F4,30 ¼ 24.33, Po0.001) (Table 1). Individuals in
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Fig. 3. Mean number of mature eggs per female Aphidius ervi given access to water (control), buckwheat, phacelia, coriander or alyssum as floral nectar sources after 6, 12, 24, 48 and 72 h.
A. ervi egg load
Fig. 2. Kaplan–Meier estimates of survival functions of Dendrocerus aphidum (A) females (B) males given access to water (control), buckwheat, phacelia, coriander or alyssum as floral nectar sources.
Egg load for A. ervi females ranged from 26 to 105 across all treatments and time intervals (Fig. 3). Mean egg load varied significantly with treatment for the first 48 h (F4,20 ¼ 23.3, Po0.001) and with time (F3,60 ¼ 41.5, Po0.001) (Table 2). Buckwheat significantly increased egg load compared with all treatments except coriander and there was a significant difference between phacelia, coriander and alyssum compared with control. However, there was no significant difference between the latter three floral treatments (Table 2). The mean number of mature eggs per female A. ervi was significantly highest at 24 and 48 h. It was significantly lowest at 6 h (Table 2). The pattern of egg production over 48 h did not differ between the treatments (treatment time interaction effect); (F12,60 ¼ 1.2, P ¼ 0.32). At 72 h there was no significant difference between the flowers, whereas the control female parasitoids were dead (F3,16 ¼ 1.7, P ¼ 0.20).
D. aphidum egg load the buckwheat treatment survived significantly longer than did those in control, phacelia, coriander and alyssum and individuals in the phacelia, coriander and alyssum treatments survived significantly longer than did those in the control (Table 1). Individuals on the phacelia treatment survived longer than those on alyssum. Females survived significantly longer than males (F1,30 ¼ 7.08, Po0.001) (Table 1, Figs. 2A and B). There was no interaction between sex and treatment (F4,30 ¼ 0.23, P ¼ 0.92).
Egg load for D. aphidum females ranged from 6 to 35 across all treatments and time intervals (Fig. 4). Mean egg load varied significantly with treatment and time (F4,20 ¼ 5.53, P ¼ 0.004) and time (F8,160 ¼ 8.15, Po0.001) (Table 2). Buckwheat significantly increased egg load over all treatments except phacelia, and there was a significant difference between phacelia and coriander compared with the control treatment. There was no significant difference between phacelia, alyssum and coriander. Even though alyssum increased egg load
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Table 2. Mean number of mature eggs per female A. ervi and D. aphidum under different treatments and times Mean number of mature eggs per female
Main effect of treatment Alyssum Buckwheat Control Coriander Phacelia LSD (0.05) Main effect of time (h) 6 12 24 48 72 96 120 144 168 192 LSD (0.05)
A. ervi
D. aphidum
67.3b 79.3a 51.2c 72.8ab 70.8b 6.70
15.4bc 18.6a 13.5c 16.1b 17.6ab 2.45
48.4c 68.7b 77.2a 78.8a
12.2e
6.00
15.7cd 20.4a 19.0ab 17.9bc 16.2cd 15.2d 15.1d 14.3de 2.45
Values followed by the same letter within a column are not significantly different (Po0.05).
Parasitism of the pea aphid The number of aphids parasitised ranged from 22 in the control treatments to 233 with buckwheat. There was a highly significant difference in the rates of parasitism between treatments (F4,30 ¼ 82.87, Po0.001) with the number of parasitised aphids per female A. ervi with buckwheat being significantly greater than for all other treatments. Although there was a significant difference between phacelia, alyssum and coriander compared with controls, there was no significant difference between these floral treatments (Table 3). Also, there was no significance difference between the treatments in the emergence of the parasitoids from the mummies.
Hyperparasitism of the pea aphid The number of parasitised aphid mummies ranged from 19 in the control treatments to 113 with buckwheat. There was a highly significant difference between the rates of parasitism between treatments (F4,30 ¼ 5.53, P ¼ 0.002) with the mean number of parasitised aphid mummies per female D. aphidum being much greater on the buckwheat, coriander and phacelia treatments compared to the control. There was no significant difference between buckwheat, coriander and phacelia, and no significant difference between coriander, phacelia and, alyssum (Table 3). Also, there was no significance difference between the treatments in the emergence of the hyperparasitoids from the mummies.
Discussion The goal of biological control programmes in agricultural systems is to initiate trophic cascades to enhance crop yield (Finke & Denno, 2002). However,
Table 3. Mean number of parasitised aphids per female A. ervi and parasitised aphid mummies per female D. aphidum
Fig. 4. Mean number of mature eggs per female Dendrocerus aphidum given access to water (control), buckwheat, phacelia, coriander or alyssum as floral nectar sources after 6, 24, 72, 96, 120, 144, 168 and 192 h. Tylianakis
relative to control, this was not significant (Table 2). The mean number of mature eggs per female D. aphidum was highest at 48 and 72 h and lowest at 6 h (Table 2). The pattern of egg load production over time did not differ between the treatments (treatment time interaction F32,160 ¼ 0.48, P ¼ 0.99).
Treatment
Mean number of parasitised aphids per female A. ervi
Mean number of parasitised mummies per female D. aphidum
Alyssum Buckwheat Control Coriander Phacelia LSD (0.05)
161.1 (12.7b) 203.0 (14.2a) 44.4 (6.5c) 75.3 (13.2b) 164.1 (12.8b) (0.97)
50.4 (7.1a) 74.0 (8.5a) 29.7 (5.4b) 66.4 (8.0a) 63.4 (7.8a) (1.50)
Values followed by the same letter within a column are not significantly different (Po0.05). Figures in parentheses are square-root-transformed values.
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when floral resources are added to agroecosystems to improve the ‘fitness’ of biological control agents, it is important that individuals in the third-trophic level benefit more than do those in the second or the fourth.
Parasitoid and hyperparasitoid longevity In the present work, the longevity of a parasitoid and its hyperparasitoid were both enhanced by flowering plants. Nectar quality and floral morphology are likely to contribute to the relative suitability of phacelia, alyssum and coriander for A. ervi and D. aphidum, as they do for other parasitoid species (Vattala, Wratten, Phillips, & Wa¨ckers, 2006). Buckwheat significantly increased longevity of A. ervi and D. aphidum compared with the other flowering plants. This was consistent with the results of other studies, which have shown buckwheat to have beneficial effects on other natural enemy species (Gurr & Wratten, 2000). D. aphidum lived 3 and 2.5 times longer than did A. ervi when they were provided with buckwheat and water, respectively. In terms of community dynamics, this suggests that D. aphidum with access to nectar could potentially affect top–down trophic cascades and may therefore indirectly increase aphid populations (Boenisch, Petersen, & Wyss, 1997) because of an increased rate of hyperparasitism with a consequent reduced effectiveness of primary parasitoids (Ho¨ller, Borgemeister, Haardt, & Powell, 1993). The longevity of females was significantly greater than males in both A. ervi and D. aphidum; possibly male ejaculates contain nutrients that are available to the females, thus providing a form of resource subsidy and also they can benefit from the presence of the eggs in their ovaries that can be resorbed. Egg resorption is presumed to increase life expectancy (Bell & Bohm, 1975; Collier, 1995; Heimpel, Rosenheim, & Kattari, 1997). Larger wasps are better at accessing deep nectaries (Idris & Grafius, 1993); this is true in the case of parasitoid species of the same trophic level and even for those within the same species. A. ervi that emerged from Acyrthosiphon kondoi Shinji survived for 4 days when it was fed on phacelia (M. Wade, unpubl. data.), but those that emerged from Acyrthosiphon pisum survived for 9 days when they were given phacelia. In contrast, D. aphidum (the fourth-trophic level) could reach deep nectaries and live 34 days longer with phacelia and 24 days longer with alyssum, even though this species is of similar size to A. ervi individuals emerging from A. kondoi.
Parasitoid and hyperparasitoid egg load and achieved fecundity The mean egg load of control A. ervi peaked at 70, with a corresponding mean of 44 mummies in similar
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adults that were permitted to reproduce. Corresponding data for A. ervi with buckwheat nectar were 93 and 203. A similar effect of sugar gel on egg load was shown for the aphidiid Aphidius rhopalosiphi De Stefani-Perez (Tylianakis et al., 2004). Corresponding data for D. aphidum were 18 and 30 for egg load and the number of parasitised mummies, in control, and 26 and 74 when buckwheat was provided. This confirms that this hyperparasitoid, even with nectar provided, has a lower potential and realised fecundity than does its host parasitoid. However, D. aphidum females in the control treatment could parasitise more mummies than their maximum egg load indicated compared with A. ervi. This may be due to relatively higher nutrient provision in D. aphidum eggs than in those of A. ervi; the eggs of D. aphidum are relatively large. Also, the larger eggs of the hyperparasitoid may lead to more ‘fit’ larvae, giving a higher survival rate to the pupal stage. Both A. ervi and D. aphidum were able to use the floral resources to mature eggs and increase their longevity, increasing their potential life-time fecundity. Survival time can also play an important role, as these two species are synovigenic, so females that live longer should mature more eggs. The number of parasitioid and hyperparasitoid progeny was in accordance with those expected from longevity and egg load experiments, but it is clear that D. aphidum produces fewer than half the total number of progeny than does A. ervi. There are several factors of potential importance to the effects of floral resources on biological control agents that were not addressed in this study such as additional species, habitat structure, resources such as aphid honeydew and the spatial dynamics of parasitoids and hyperparasitoids still need to be evaluated. In this study, effect of nectar on both wasp species was examined using a no-choice test; however, it is important also to test the effect of different floral nectars on a third- and fourth-trophic level using a choice-experiment approach. Also, the presence of flowering plant mixtures might modify the behaviour of the parasitoids and their hyperparasitoids and their effect on host population density. Recent laboratory results from the use of flowering plant mixtures indicate that the lifespan of parasitoid wasps with access to a combination of two flowering plants was higher than when provided with each flowering plant species alone (Wade, Kehrli, & Wratten, 2005). Prasad & Snyder (2006) gave an example of the targets of conservation biological control being generalists, in manipulative field experiments. Intraguild predation and predation of aphid alternative prey complicated and limited the effectiveness of conservation biological control. If aphid hyperparasitoids, which are mostly generalists, are benefiting from flowers more
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than are aphid parasitoids, biological control could be compromised. Further studies, including a field approach should make clear the relative importance of nectar as it affects population dynamics of parasitoids and their enemies. This research confirms that modifications that enhance habitat complexity have the potential to increase the abundance of hyperparasitoids in agroecosystems.
Acknowledgements We thank Mr. M. Stufkens of Crop and Food Research, Lincoln, New Zealand, for advice on the parasitoid culture. We also thank Dr. J. Berry of Landcare Research, Auckland, for her valued help in the identification of A. ervi and its hyperparasitoids. We thank Frauke Jonsson for translation of the Abstract into German.
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Basic and Applied Ecology 9 (2008) 588–597
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Floral diversity, parasitoids and hyperparasitoids – A laboratory approach Salah-Eddin Araj, Steve Wratten, Alison Lister, Hannah Buckley National Centre for Advanced Bio-Protection Technologies, PO Box 84, Lincoln University, Canterbury 7647, New Zealand Received 20 December 2006; accepted 7 August 2007
Abstract Adding floral resources to agro-ecosystems to improve biological control can enhance the survival, egg load, and parasitism rate of insect parasitoids. However, this may not always be the case because the herbivore may benefit from the added resource as much as, or more than the third-trophic level. In addition, the natural enemies of those in the third-trophic level may also derive improved fitness from the added resources. Both these processes will dampen trophic cascades, leading to less-effective biological control. In this study, the effect of adding different flowering plants on the longevity, egg load, aphid parasitism rates and hyperparasitism of Aphidius ervi Haliday (Hymenoptera: Braconidae) by its hyperparasitoid Dendrocerus aphidum Rondani (Hymenoptera: Megaspilidae) were investigated, using the pea aphid Acyrthosiphon pisum Harris (Homoptera: Aphididae) as the herbivore. Parasitoids exposed to buckwheat survived, on average, between four to five times as long as those in the control (water) and those in phacelia, alyssum and coriander treatments survived three to four times as long. Hyperparasitoids exposed to buckwheat survived five to six times as long as those in the control and three to five times longer with the other plants compared with the control. Almost all flower species significantly increased parasitoid and hyperparasitoid egg loads and the number of parasitised aphids and parasitised mummies compared with control. Understanding the factors influencing the dynamics of multitrophic interactions involving flowering plants, herbivores, parasitoids and hyperparasitoids is a fertile area for future research. One of the most challenging areas in contemporary ecology concerns the relative importance of different types of biodiversity mediating trophic interactions and thereby influencing the structure of communities and food webs. This paper begins to explore this using an experimental, laboratory-based approach. r 2007 Gesellschaft fu¨r O¨kologie. Published by Elsevier GmbH. All rights reserved.
Zusammenfassung Zusa¨tzliche Blu¨tenquellen in landwirtschaftlichen O¨kosystemen zur Verbesserung des biologischen Pflanzenschutzes ko¨nnen U¨berleben, Eiproduktion und Parasitierungsrate parasitoider Insekten fo¨rdern. Dies muss jedoch nicht immer zu verbessertem biologischen Pflanzenschutz fu¨hren, denn die Herbivoren ko¨nnen durch die zusa¨tzliche Nahrungsquelle ebenso oder sogar sta¨rker begu¨nstigt werden als die dritte Trophieebene. Auch die natu¨rlichen Feinde der Arten auf dem dritten Trophieniveau erfahren mo¨glicherweise durch die zusa¨tzliche Nahrungsquelle eine Steigerung ihrer U¨berlebensfa¨higkeit. Beide Vorga¨nge ko¨nnen die trophische Kaskade und folglich die biologische Scha¨dlingsbeka¨mpfung schwa¨chen.
Corresponding author. Tel.: +64 3 325 3838x8386; fax: +64 3 325 3864.
E-mail address: [email protected] (S.-E. Araj). 1439-1791/$ - see front matter r 2007 Gesellschaft fu¨r O¨kologie. Published by Elsevier GmbH. All rights reserved. doi:10.1016/j.baae.2007.08.001
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In der vorliegenden Studie wurden die Auswirkungen verschiedener Blu¨tenpflanzen auf Lebensdauer, Eiproduktion und Blattlaus-Parasitierungsraten von Aphidius ervi Haliday (Hymenoptera: Braconidae) sowie auf deren Hyperparasitierung durch Dendrocerus aphidum Rondani (Hymenoptera: Megaspilidae) untersucht, mit der Erbsenblattlaus Acyrthosiphon pisum Harris (Homoptera: Aphididae) als Herbivoren. Parasitoide, die Zugang zu Buchweizen hatten, lebten im Durchschnitt vier- bis fu¨nfmal so lange wie die Kontrollkulturen (Wasser), diejenigen mit Zugang zu Phacelia, Alyssum und Koriander drei- bis viermal so lange. Hyperparasitoide, die Zugang zu Buchweizen hatten, lebten fu¨nf-bis sechsmal so lange wie die Kontrollkulturen; mit den anderen Pflanzen lebten sie drei- bis fu¨nfmal so lange wie die Kontrolle. Fast alle Blu¨tenarten erho¨hten die Eiproduktion der Parasitoiden und Hyperparasitoiden sowie die Anzahl der parasitierten Blattla¨use und Blattlausmumien signifikant, verglichen mit der Kontrolle. Faktoren, die auf die multitrophische Interaktion zwischen Blu¨tenpflanzen, Herbivoren, Parasitoiden und Hyperparasitoiden einwirken, sind ein ergiebiges Gebiet zuku¨nftiger Forschung. Eines der interessantesten Felder moderner O¨kologie ist die relative Bedeutung verschiedener Arten von Biodiversita¨t, ihr Einfluss auf die trophische Interaktion und damit auf Strukturen von Artengemeinschaften und Nahrungsnetzen. Die vorliegende Studie untersucht diese Zusammenha¨nge anhand eines Laborexperiments. r 2007 Gesellschaft fu¨r O¨kologie. Published by Elsevier GmbH. All rights reserved. Keywords: Acyrthosiphon pisum; Aphidius ervi; Dendrocerus aphidum; Buckwheat; Phacelia; Alyssum; Coriander
Introduction The relationship between biodiversity and ecosystem function has emerged as an important issue in ecology during the last decade. Systematic experimental and observational studies of how changes in diversity interact at different trophic levels are required (De Deyn, Raaijmakers, Ruijven, Berendse, & van der Putten, 2004; Finke & Denno, 2002; Worm & Duffy, 2003). Most studies of the relationship between diversity and ecosystem function have been carried out involving only two trophic levels (Cardinale, Weis, Tilmon, Forbes, & Ives, 2006; Chapin et al., 2000; Hasegawa, 2004; Loreau, 2001; Loreau et al., 2001) and studies of ecosystem function using multitrophic communities have only rarely been reported (Duffy, 2002; Finke & Denno, 2002; Paine, 1966, 2002; Snyder & Wise, 2001). In particular, the role of hyperparasitoids (parasitic wasps that attack primary parasitoids) in the diversity–ecosystem function relationship has been investigated to a very small extent. Earlier work comprised a glasshouse experiment in which hyperparasitoids reduced parasitism to such an extent that plant biomass increased (Goergen & Neuenschwander, 1992). The preliminary field sampling of Stephens, France, Wratten, & Frampton (1998) showed only that higher numbers of a lacewing (Hemerobiidae) parasitoid, Anacharis sp. (Hymenoptera: Figitidae), were caught in yellow pan traps close to buckwheat flowers, Fagopyrum esculentum (Moench), compared with control plots, and did not explicitly test and identify the processes underlying this pattern. A better understanding of how parasitoids and hyperparasitoids exploit floral subsidies can help in
designing more efficient biological control strategies (Landis, Wratten, & Gurr, 2000), via ‘ecological engineering’ (Gurr, Wratten, & Altieri, 2004) at the landscape scale. To be efficient for biological control, these subsidies must at least increase the rate of predation or parasitism in the crop associated with the subsidy (Berndt, Wratten, & Hassan, 2002). Differences in body size of parasitoids and hyperparasitoids could lead to differential foraging performance on various floral architectures. Larger wasps have superior searching ability and can access nectar from flowers with both exposed and partially exposed nectaries (Patt, Hamilton, & Lashomb, 1999). Aphid parasitoids are a valuable model system for testing ideas about community interactions (Mu¨ller & Godfray, 1999) because aphids are ubiquitous in most terrestrial ecosystems and abundant in both natural and managed habitats (Brodeur & Rosenheim, 2000). Aphids are attacked by a wide array of pathogens, parasitoids and predators, the densities of which vary in space and time and which may significantly reduce aphid population growth (Dennis & Wratten, 1991; Mu¨ller & Godfray, 1999). The basis for the current work was to determine the relative value of different floral resources for a parasitoid and a hyperparasitoid and to determine if these resources can simultaneously benefit the fourth-trophic level, which may work to the detriment of aphid biocontrol. Indeed, this study has the potential to identify a plant species that enhances the ecological ‘fitness’ of the primary parasitoid more than that of the hyperparasitoid. The aim of this work was to measure the effects of a range of plant nectars on the longevity, egg load and parasitism rates of pea aphids by Aphidius ervi and hyperparasitism rates of A. ervi by Dendrocerus aphidum compared with water controls.
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Materials and methods
to ensure that flowers were continuously available for laboratory experiments.
Insect rearing Pea aphids were reared in the laboratory on potted plants of broad bean (Vicia faba L. cv. Cole’s Dwarf). A clonal culture was started with one female aphid being confined on one leaflet using a clip cage as described by Noble (1958). When the first 5–8 progeny had been produced, the female was discarded to ensure that the progeny and future colony were free of parasitoids. The resulting progeny were reared on broad bean plants in Perspex cages (64 45 40 cm) with a nylon mesh door. The colony was maintained continuously as parthenogenetic females at 2074 1C and RH 60–70% with a photoperiod of 16:8 h light:dark. Light intensity was 122 mmol/m2/s. Aphid mummies were collected from lucerne fields, then put singly into 600 ml gelatine capsules and kept in a transparent polystyrene box (20 10 5 cm) under the above conditions. When parasitoids or hyperparasitoids emerged, they were identified using the keys of Mertins (1985). An A. ervi colony was established using 10 males and 10 females, which were presented with second-instar pea aphids. The culture was subsequently maintained under the same rearing conditions that were used for the aphids (see above). A colony of D. aphidum was established from individuals (A. ervi or A. eadyi (Stary) (Hymenoptera: Braconidae)) emerging from parasitised pea aphids which had been collected as mummies from lucerne fields (see above). Ten males and ten females of D. aphidum were reared on newly formed mummies (containing aphid parasitoid pupae, which form approximately 9 days after oviposition by A. ervi (Walker & Cameron, 1981) and were maintained under the conditions described above. The identification of A. ervi and its parasitoids was confirmed by Dr. J. Berry of Landcare Research, Auckland, New Zealand, in April 2004, and key identification characters were recorded for future reference.
Flowering plants as nectar sources Phacelia (Phacelia tanacetifolia Bentham cv. Balo), buckwheat (cv. Katowase), alyssum (Lobularia maritima L. cv. Carpet of Snow) and coriander (Coriandrum sativum L. cv. Slowbolt) were assessed for their ability to enhance the ‘fitness’ and efficacy of A. ervi and D. aphidum. The four species have been shown in many studies to enhance the efficacy of parasitoids and predators against pests in other crop systems (Hickman & Wratten, 1996; Tooker & Hanks, 2000; White, Wratten, Berry, & Weigmann, 1995; Wratten & van Emden, 1995). Candidate plant species were grown in a greenhouse with 16:8 h light:dark and were sown at 2-week intervals
Experiment 1. The effect of flowers on A. ervi longevity The above flowering plant species were individually tested against a water control. For each treatment, a well-watered flowering, rooted shoot of the plant was used, to maximise quality and quantity of nectar available to the wasps. The flowering shoots were carefully inserted into a transparent polycarbonate jar (120 mm tall and 85 mm in diameter) through a bottom opening, which was then sealed with low-density polyurethane foam around the shoot. The top of the jar was removed and covered with fine nylon mesh. The jar was attached to a vertical wooden stake fixed to the plant pot. A foam-sealable (20 mm diameter) hole was cut into the wall of the jar to introduce parasitoids when required. Similar cages were used for water treatments via damp dental rolls provided on the mesh top of the cage. A completely randomised design was used with five treatments and seven replicates per treatment. One naı¨ ve female and one male of A. ervi were used per cage. Longevity of the parasitoids was recorded for all treatments. The test was conducted under the conditions described earlier and survival was recorded every 24 h.
Experiment 2. The effect of flowers on D. aphidum longevity The same flowering plant species and the same control and cage design as in Experiment 1 were used in this experiment. A completely randomised design with seven replicates was used as above. One female and one male D. aphidum (both naı¨ ve) were used per cage. Longevity of the hyperparasitoids was recorded for the treatments and control. Survival was recorded every 24 h.
Experiment 3. The effect of nectar feeding on the egg load of A. ervi Experimental cages with flowering plants, as described in Experiment 1, were set up in the laboratory. The treatments comprised the four flowering plant species and a water control (damp dental rolls). The five treatments were randomly allocated to each of 25 cages; i.e., five replicates/treatment. To assess parasitoid egg load after different lengths of time, the five cages in each treatment were each allocated to one of the five sampling times (6, 12, 24, 48 and 72 h), so that at each time, egg load was recorded for five mated, female parasitoids. To determine this, females were
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euthanised and dissected. Ovaries were removed by grasping the ovipositor with fine forceps and gently pulling until the ovipositor and ovaries became detached from the abdomen. Ovaries were placed on a microscope slide and stained with a 0.1% solution of methylene blue. Pressing gently on the cover slip caused the ovaries to burst, releasing the eggs, which were counted under a dissecting microscope at 63 magnification (Tylianakis, Didham, & Wratten, 2004).
Experiment 4. The effect of nectar feeding on the egg load of D. aphidum Experimental cages with flowering plants as described for Experiment 1 were set up in the laboratory. Fortyfive, mated, naı¨ ve female hyperparasitoids were assigned to each of the five treatments to examine the effects of floral resources on egg load. The treatments were the four flowering plant species and a control (damp dental rolls). Five randomly selected females for each treatment were euthanised and dissected at each of the nine time intervals (6, 24, 48, 72, 96, 120, 144, 168 and 192 h) to assess egg load.
Experiment 5. The effect of floral resources on parasitism of the pea aphid The four selected flowering plant species were compared with a water control consisting of damp dental rolls. For each treatment, a flowering shoot on a rooted plant of each plant species was utilized; the pot was regularly watered to maintain the quality and quantity of nectar available to the wasps. The shoots were inserted into a transparent polycarbonate jar (135 mm tall and 85 mm in diameter) through a circular opening (40 mm in diameter) from one of the sides, which was then sealed around the shoot with a piece of foam. The top of the jar was removed and covered with fine nylon mesh. The bottom was sealed with a Petri dish base (85 mm diameter). The jar was then attached to a vertical wooden stake fixed to the plant pot. A foamsealable (20 mm diameter) hole was cut into the wall of the jar to introduce parasitoids. Similar cages were used for the controls (water) with damp dental rolls provided on the mesh top of the cage. A randomised-block design was used with five treatments and seven replicates per treatment. This experiment was conducted under 2074 1C and RH 60–70% with a photoperiod of 16:8 h light: dark. Light intensity was 122 mmol/m2/s. Each experimental jar contained one naı¨ ve female and one male of A. ervi, a damp dental roll and a cut leaflet of a broad bean plant infested with 80–100 1–3-day-old pea aphids which were provided every day until the death of the female parasitoid. This provided an abundant population of
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new potential hosts so that maximum potential rates of parasitism could be achieved. The cut leaflets harbouring the aphids in each treatment were replaced daily until the death of the female parasitoid. The aphids exposed to parasitoids in this way were subsequently kept in a transparent container containing a rooted broad bean shoot. Aphids were examined daily for signs of mummification, and the number of parasitised aphids in each treatment was recorded. The experimental treatments were: control, with no additional resources provided, phacelia, buckwheat, alyssum and coriander.
Experiment 6. The effect of the provision of floral resources on hyperparasitism of the pea aphid Experimental jars as used in Experiment 5 with the same flowering plants and control were set up in the laboratory. Each jar contained one naı¨ ve female and one male hyperparasitoid assigned to each of the five treatments; damp dental rolls were provided on the mesh top of the cage and a leaflet of a broad bean seedling infested with 60–70 newly formed mummies was added. This was replaced every 3 days. Each experiment ended with the death of the female hyperparasitoid. Thereafter, the number of hyperparasitoids was monitored and recorded, if no parasitoid or hyperparasitoid emerges, the mummy was dissected to determine if it is parasitized or hyperparasitsed. For the treatments and control, see Experiment 5.
Data analysis Survival analysis was used to compare the effect of the food resources on the longevity of A. ervi and D. aphidum by calculating the Kaplan–Meier estimate of the survival function. To determine the effect of nectar feeding on egg load of A. ervi and D. aphidum, untransformed data were analysed using analysis of variance (ANOVA). For A. ervi, the first 48 h were analysed separately from 72-h data because all the parasitoids had died in the control treatment by 72 h. Parasitism and hyperparasitism data were square-roottransformed to normalise variances and comparisons between treatments were made using one-way analysis of variance. All statistical analyses were conducted using GenStat 7.
Results A. ervi longevity Survival in the controls was 3–4 days for A. ervi females and 2–3 days for males. With buckwheat, survival was
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12–20 and 8–16 days for females and males, respectively. For phacelia, the equivalent data were 6–15 and 6–10 days, coriander 7–17 and 6–15 days and alyssum 7–16 and 5–14 days. Parasitoids exposed to buckwheat survived, on average, four to five times longer than those in the control and three to four times longer for the other flowering plants (Table 1 and Figs. 1A and B). Both female and male survival curves differed significantly between treatments. Females: (log-rank ¼ 49.59, Po0.001; Wilcoxon (Breslow) ¼ 45.53, Po0.001) (Fig. 1A). Males (logrank ¼ 48.91, Po0.001; Wilcoxon (Breslow) ¼ 45.31, Po0.001) (Fig. 1B). Longevity was significantly different between treatments (F4,30 ¼ 15.16, Po0.001) (Table 1). Individuals in the buckwheat treatment survived significantly longer than did those in control or other flowering plant treatments. Individuals in the phacelia, alyssum and coriander treatments survived significantly longer than did those in the control with no significant difference in longevity between the phacelia, coriander and alyssum treatments (Table 1). Females survived significantly longer than males (F1,30 ¼ 40.56, Po0.001) (Table 1, Figs. 1A and B). The interaction between sex and treatment was not significant (F4,30 ¼ 1.93, P ¼ 0.131).
D. aphidum longevity Survival times of D. aphidum females ranged from 6 to 12 days and males from 5 to 10 days in controls, 23–57 and 25–55 days, respectively, with buckwheat, 24–41 and 18–48 days with phacelia, 16–48 and 17–37 days with coriander and 18–36 and 18–27 days with alyssum. Hyperparasitoid individuals exposed to buckwheat survived, on average, five to six times
Table 1. Mean survival of A. ervi and D. aphidum (days) under different treatment and sexes Mean survival (days) of A. ervi
D. aphidum
Main effect of treatment Alyssum 9.1b Buckwheat 13.9a Control 2.9c Coriander 10.1b Phacelia 8.5b LSD (0.05) 2.93
23.5c 43.1a 7.3d 26.1bc 33.5b 7.76
Main effect of sex Female Male LSD (0.05)
28.5a 24.8b 2.85
10.0a 7.9b 0.68
Values followed by the same letter within a column are not significantly different (Po0.05).
Fig. 1. Kaplan–Meier estimates of survival functions of Aphidius ervi (A) females (B) males given access to water (control), buckwheat, phacelia, coriander or alyssum as floral nectar sources.
longer than those in the control and three to five times longer with the other flowering plants than the control (Table 1 and Figs. 2A and B). Female and male survival curves differed significantly between treatments. Females: (log-rank ¼ 59.17, Po0.001; Wilcoxon (Breslow) ¼ 52.32, Po0.001) (Fig. 2A). Males: (log-rank ¼ 63.28, Po0.001; Wilcoxon (Breslow) ¼ 55.33, Po0.001) (Fig. 2B). Longevity was significantly different between treatments (F4,30 ¼ 24.33, Po0.001) (Table 1). Individuals in
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Fig. 3. Mean number of mature eggs per female Aphidius ervi given access to water (control), buckwheat, phacelia, coriander or alyssum as floral nectar sources after 6, 12, 24, 48 and 72 h.
A. ervi egg load
Fig. 2. Kaplan–Meier estimates of survival functions of Dendrocerus aphidum (A) females (B) males given access to water (control), buckwheat, phacelia, coriander or alyssum as floral nectar sources.
Egg load for A. ervi females ranged from 26 to 105 across all treatments and time intervals (Fig. 3). Mean egg load varied significantly with treatment for the first 48 h (F4,20 ¼ 23.3, Po0.001) and with time (F3,60 ¼ 41.5, Po0.001) (Table 2). Buckwheat significantly increased egg load compared with all treatments except coriander and there was a significant difference between phacelia, coriander and alyssum compared with control. However, there was no significant difference between the latter three floral treatments (Table 2). The mean number of mature eggs per female A. ervi was significantly highest at 24 and 48 h. It was significantly lowest at 6 h (Table 2). The pattern of egg production over 48 h did not differ between the treatments (treatment time interaction effect); (F12,60 ¼ 1.2, P ¼ 0.32). At 72 h there was no significant difference between the flowers, whereas the control female parasitoids were dead (F3,16 ¼ 1.7, P ¼ 0.20).
D. aphidum egg load the buckwheat treatment survived significantly longer than did those in control, phacelia, coriander and alyssum and individuals in the phacelia, coriander and alyssum treatments survived significantly longer than did those in the control (Table 1). Individuals on the phacelia treatment survived longer than those on alyssum. Females survived significantly longer than males (F1,30 ¼ 7.08, Po0.001) (Table 1, Figs. 2A and B). There was no interaction between sex and treatment (F4,30 ¼ 0.23, P ¼ 0.92).
Egg load for D. aphidum females ranged from 6 to 35 across all treatments and time intervals (Fig. 4). Mean egg load varied significantly with treatment and time (F4,20 ¼ 5.53, P ¼ 0.004) and time (F8,160 ¼ 8.15, Po0.001) (Table 2). Buckwheat significantly increased egg load over all treatments except phacelia, and there was a significant difference between phacelia and coriander compared with the control treatment. There was no significant difference between phacelia, alyssum and coriander. Even though alyssum increased egg load
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Table 2. Mean number of mature eggs per female A. ervi and D. aphidum under different treatments and times Mean number of mature eggs per female
Main effect of treatment Alyssum Buckwheat Control Coriander Phacelia LSD (0.05) Main effect of time (h) 6 12 24 48 72 96 120 144 168 192 LSD (0.05)
A. ervi
D. aphidum
67.3b 79.3a 51.2c 72.8ab 70.8b 6.70
15.4bc 18.6a 13.5c 16.1b 17.6ab 2.45
48.4c 68.7b 77.2a 78.8a
12.2e
6.00
15.7cd 20.4a 19.0ab 17.9bc 16.2cd 15.2d 15.1d 14.3de 2.45
Values followed by the same letter within a column are not significantly different (Po0.05).
Parasitism of the pea aphid The number of aphids parasitised ranged from 22 in the control treatments to 233 with buckwheat. There was a highly significant difference in the rates of parasitism between treatments (F4,30 ¼ 82.87, Po0.001) with the number of parasitised aphids per female A. ervi with buckwheat being significantly greater than for all other treatments. Although there was a significant difference between phacelia, alyssum and coriander compared with controls, there was no significant difference between these floral treatments (Table 3). Also, there was no significance difference between the treatments in the emergence of the parasitoids from the mummies.
Hyperparasitism of the pea aphid The number of parasitised aphid mummies ranged from 19 in the control treatments to 113 with buckwheat. There was a highly significant difference between the rates of parasitism between treatments (F4,30 ¼ 5.53, P ¼ 0.002) with the mean number of parasitised aphid mummies per female D. aphidum being much greater on the buckwheat, coriander and phacelia treatments compared to the control. There was no significant difference between buckwheat, coriander and phacelia, and no significant difference between coriander, phacelia and, alyssum (Table 3). Also, there was no significance difference between the treatments in the emergence of the hyperparasitoids from the mummies.
Discussion The goal of biological control programmes in agricultural systems is to initiate trophic cascades to enhance crop yield (Finke & Denno, 2002). However,
Table 3. Mean number of parasitised aphids per female A. ervi and parasitised aphid mummies per female D. aphidum
Fig. 4. Mean number of mature eggs per female Dendrocerus aphidum given access to water (control), buckwheat, phacelia, coriander or alyssum as floral nectar sources after 6, 24, 72, 96, 120, 144, 168 and 192 h. Tylianakis
relative to control, this was not significant (Table 2). The mean number of mature eggs per female D. aphidum was highest at 48 and 72 h and lowest at 6 h (Table 2). The pattern of egg load production over time did not differ between the treatments (treatment time interaction F32,160 ¼ 0.48, P ¼ 0.99).
Treatment
Mean number of parasitised aphids per female A. ervi
Mean number of parasitised mummies per female D. aphidum
Alyssum Buckwheat Control Coriander Phacelia LSD (0.05)
161.1 (12.7b) 203.0 (14.2a) 44.4 (6.5c) 75.3 (13.2b) 164.1 (12.8b) (0.97)
50.4 (7.1a) 74.0 (8.5a) 29.7 (5.4b) 66.4 (8.0a) 63.4 (7.8a) (1.50)
Values followed by the same letter within a column are not significantly different (Po0.05). Figures in parentheses are square-root-transformed values.
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when floral resources are added to agroecosystems to improve the ‘fitness’ of biological control agents, it is important that individuals in the third-trophic level benefit more than do those in the second or the fourth.
Parasitoid and hyperparasitoid longevity In the present work, the longevity of a parasitoid and its hyperparasitoid were both enhanced by flowering plants. Nectar quality and floral morphology are likely to contribute to the relative suitability of phacelia, alyssum and coriander for A. ervi and D. aphidum, as they do for other parasitoid species (Vattala, Wratten, Phillips, & Wa¨ckers, 2006). Buckwheat significantly increased longevity of A. ervi and D. aphidum compared with the other flowering plants. This was consistent with the results of other studies, which have shown buckwheat to have beneficial effects on other natural enemy species (Gurr & Wratten, 2000). D. aphidum lived 3 and 2.5 times longer than did A. ervi when they were provided with buckwheat and water, respectively. In terms of community dynamics, this suggests that D. aphidum with access to nectar could potentially affect top–down trophic cascades and may therefore indirectly increase aphid populations (Boenisch, Petersen, & Wyss, 1997) because of an increased rate of hyperparasitism with a consequent reduced effectiveness of primary parasitoids (Ho¨ller, Borgemeister, Haardt, & Powell, 1993). The longevity of females was significantly greater than males in both A. ervi and D. aphidum; possibly male ejaculates contain nutrients that are available to the females, thus providing a form of resource subsidy and also they can benefit from the presence of the eggs in their ovaries that can be resorbed. Egg resorption is presumed to increase life expectancy (Bell & Bohm, 1975; Collier, 1995; Heimpel, Rosenheim, & Kattari, 1997). Larger wasps are better at accessing deep nectaries (Idris & Grafius, 1993); this is true in the case of parasitoid species of the same trophic level and even for those within the same species. A. ervi that emerged from Acyrthosiphon kondoi Shinji survived for 4 days when it was fed on phacelia (M. Wade, unpubl. data.), but those that emerged from Acyrthosiphon pisum survived for 9 days when they were given phacelia. In contrast, D. aphidum (the fourth-trophic level) could reach deep nectaries and live 34 days longer with phacelia and 24 days longer with alyssum, even though this species is of similar size to A. ervi individuals emerging from A. kondoi.
Parasitoid and hyperparasitoid egg load and achieved fecundity The mean egg load of control A. ervi peaked at 70, with a corresponding mean of 44 mummies in similar
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adults that were permitted to reproduce. Corresponding data for A. ervi with buckwheat nectar were 93 and 203. A similar effect of sugar gel on egg load was shown for the aphidiid Aphidius rhopalosiphi De Stefani-Perez (Tylianakis et al., 2004). Corresponding data for D. aphidum were 18 and 30 for egg load and the number of parasitised mummies, in control, and 26 and 74 when buckwheat was provided. This confirms that this hyperparasitoid, even with nectar provided, has a lower potential and realised fecundity than does its host parasitoid. However, D. aphidum females in the control treatment could parasitise more mummies than their maximum egg load indicated compared with A. ervi. This may be due to relatively higher nutrient provision in D. aphidum eggs than in those of A. ervi; the eggs of D. aphidum are relatively large. Also, the larger eggs of the hyperparasitoid may lead to more ‘fit’ larvae, giving a higher survival rate to the pupal stage. Both A. ervi and D. aphidum were able to use the floral resources to mature eggs and increase their longevity, increasing their potential life-time fecundity. Survival time can also play an important role, as these two species are synovigenic, so females that live longer should mature more eggs. The number of parasitioid and hyperparasitoid progeny was in accordance with those expected from longevity and egg load experiments, but it is clear that D. aphidum produces fewer than half the total number of progeny than does A. ervi. There are several factors of potential importance to the effects of floral resources on biological control agents that were not addressed in this study such as additional species, habitat structure, resources such as aphid honeydew and the spatial dynamics of parasitoids and hyperparasitoids still need to be evaluated. In this study, effect of nectar on both wasp species was examined using a no-choice test; however, it is important also to test the effect of different floral nectars on a third- and fourth-trophic level using a choice-experiment approach. Also, the presence of flowering plant mixtures might modify the behaviour of the parasitoids and their hyperparasitoids and their effect on host population density. Recent laboratory results from the use of flowering plant mixtures indicate that the lifespan of parasitoid wasps with access to a combination of two flowering plants was higher than when provided with each flowering plant species alone (Wade, Kehrli, & Wratten, 2005). Prasad & Snyder (2006) gave an example of the targets of conservation biological control being generalists, in manipulative field experiments. Intraguild predation and predation of aphid alternative prey complicated and limited the effectiveness of conservation biological control. If aphid hyperparasitoids, which are mostly generalists, are benefiting from flowers more
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than are aphid parasitoids, biological control could be compromised. Further studies, including a field approach should make clear the relative importance of nectar as it affects population dynamics of parasitoids and their enemies. This research confirms that modifications that enhance habitat complexity have the potential to increase the abundance of hyperparasitoids in agroecosystems.
Acknowledgements We thank Mr. M. Stufkens of Crop and Food Research, Lincoln, New Zealand, for advice on the parasitoid culture. We also thank Dr. J. Berry of Landcare Research, Auckland, for her valued help in the identification of A. ervi and its hyperparasitoids. We thank Frauke Jonsson for translation of the Abstract into German.
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