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Influence of prey size and environmental factors on predation by Podisus maculiventris (Hemiptera: Pentatomidae) on viburnum leaf beetle (Coleoptera: Chrysomelidae) Gaylord A. Desurmont,1 Paul A. Weston Department of Entomology, Cornell University, Ithaca, New York 14853-2601, United States of America

Abstract—Experiments were conducted under laboratory conditions to determine the influence of the relative sizes of predator and prey, temperature, presence of refugia, size of the search area, and host-plant species on the predation performance of Podisus maculiventris (Say) nymphs against viburnum leaf beetle, Pyrrhalta viburni (Paykull), a new landscape pest in North America that feeds on the foliage of species of Viburnum L. (Caprifoliaceae). Predator handling time was positively correlated with body mass of the prey for all instars of P. maculiventris, but the rate of increase of handling time relative to prey mass decreased as predator age increased. Temperature was positively correlated with predation rates, but the presence of refugia did not have an impact on predation. The influence of host-plant species and size of the search area was tested on southern arrowwood (Viburnum dentatum L.) and American cranberrybush (Viburnum opulus L. var. americanum Aiton). There was a significant interaction between plant species and size of the search area, the species effect becoming significant as leaf surface area increased. In the case of southern arrowwood a negative correlation between size of the search area and predation rate was also detected. The identification of these factors adds valuable knowledge for using P. maculiventris as a biological-control agent against P. viburni. Résumé—Nous avons fait des expériences en conditions de laboratoire pour déterminer l’influence de la taille relative prédateur:proie, de la température, de la présence de refuges, de l’importance de la surface de recherche et de l’espèce de plante hôte sur la performance des larves prédatrices de Podisus maculiventris (Say) contre la galéruque de la viorne, Pyrrhalta viburni (Paykull), un nouveau ravageur des paysages en Amérique du Nord qui se nourrit du feuillage d’espèces de Viburnum L. (Caprifoliaceae). Il y a une corrélation positive entre le temps de manipulation et la masse de la proie chez tous les stades de P. maculiventris, mais le taux d’augmentation du temps de manipulation par unité de masse de la proie décroît à mesure que les prédateurs deviennent plus âgés. Il existe une corrélation positive entre la température et les taux de prédation, mais la présence de refuges n’affecte pas la prédation. Nous avons vérifié l’influence de l’espèce de plante hôte et de la taille de l’aire de recherche chez la viorne dentée (Viburnum dentatum L.) et la viorne trilobée (Viburnum opulus L. var. americanum Aiton). Il y a une interaction significative entre l’espèce de plante et la surface de l’aire de recherche, l’effet de l’espèce devenant significatif avec l’accroissement de la surface de la feuille. Nous avons aussi détecté une corrélation négative entre la surface de l’aire de recherche et le taux de prédation chez la viorne dentée. L’identification de ces facteurs apporte des renseignements importants pour l’utilisation de P. maculiventris comme agent de lutte biologique contre P. viburni. [Traduit par la Rédaction] Desurmont and Weston

Introduction The use of generalist predators for biological control has received a great deal of attention from

entomologists and intergrated pest management practitioners over recent decades. Although such organisms can effectively reduce populations of agricultural pests (e.g., Wei et al. 1995; Holland

Received 10 April 2007. Accepted 27 January 2008. 1

Corresponding author (e-mail: [email protected]).

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et al. 1996; Aldrich and Cantelo 1999), their polyphagous habits and interactions with more complex food webs than exhibited by specialized natural enemies, such as the vast majority of hymenopteran parisitoids, often increase the difficulty of modeling or predicting their effect under field conditions. In a review on generalist predators, Symondson et al. (2002) consider a list of issues involved with the practical application of theoretical models of predator–prey interactions. The highly variable nature of the functional response, defined as the relationship between the density of prey and the number of prey items consumed by a predator in a certain area (Holling 1959) under field conditions in relation to a number of biotic and abiotic factors, is cited as a major cause of the inapplicability of most predator– prey models. These factors, which may include but are not limited to the presence of alternative prey, nature of the microenvironment, and interactions with other natural enemies, and their relative importance are highly predator species- and system-dependent. In the present study, we focus solely on the predation by one generalist predator, spined soldier bug (Podisus maculiventris (Say) (Hemiptera: Pentatomidae)), on an emerging landscape pest in North America, the viburnum leaf beetle (Pyrrhalta viburni (Paykull) (Coleoptera: Chrysomelidae)). Podisus maculiventris is a true generalist predator belonging to the pentatomid subfamily Asopinae; it has been reported to feed on over 75 species of insect prey in eight insect orders (McPherson 1982) and is present in various agroecosystems of North America (Evans 1982). Evaluation of the predation performance of P. maculiventris against various economically important pests (De Clercq and Degheele 1994; Hough-Goldstein 1998; Aldrich and Cantelo 1999) showed varying degree of efficacy in different systems with different prey. Eggs and nymphs of the predator are commercially available in North America and have been used for inundative releases against Mexican bean beetle (Epilachna varivestis Mulsant (Coleoptera: Coccinellidae)), Colorado potato beetle (Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae)), and various lepidopteran larvae (Glenister 1998). Podisus maculiventris is also one of the few natural enemies of P. viburni known in North America. Pyrrhalta viburni is an invasive univoltine chrysomelid specializing on species of Viburnum L. (Caprifoliaceae). Native to Eurasia, the insect was first detected in Canada in 1947 and in

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the United States of America, in Maine, in 1994, and is now becoming a major landscape pest in the northeastern United States of America and eastern Canada. Both larvae and adults feed on the leaves of native and exotic viburnums and can kill susceptible plants within a few years. Plants in managed landscapes and natural areas are at risk, and damage due to the beetle is both economic (loss of ornamental shrubs for landscape managers) and ecological (disappearance of dominant shrubs in forest understories and a threat to insect species associated with these plants). The few natural enemies of P. viburni known in North America are all generalist predators. Among them is P. maculiventris, and nymphs and adults of this species have been observed preying on larvae and adults of P. viburni under field conditions on numerous occasions (personal observation). In 2005, trials were performed under laboratory and field conditions to evaluate the potential of P. maculiventris as a biological-control agent against P. viburni. The results of these trials have confirmed that P. maculiventris is a promising predator against this particular pest: in the laboratory, P. maculiventris nymphs developed successfully with only P. viburni larvae and adults as prey, consuming, on average, 100.6 larvae or 16.9 adults during their development (Desurmont 2006). In the field, augmentative releases of P. maculiventris nymphs significantly reduced defoliation due to P. viburni larvae on naturally infested American cranberrybush (Viburnum opulus L. var. americanum Aiton) at a predator:prey ratio of 1 P. maculiventris nymph to 100 or fewer P. viburni larvae (Desurmont 2006). In addition to quantitative data on defoliation reduction, direct observations of P. maculiventris nymphs on infested shrubs during the field trials led to the identification of several factors likely to influence P. maculiventris predation on P. viburni: size of the prey, temperature, presence of refugia for the predator, size of the search area, and species of host plant. Young P. maculiventris nymphs (2nd instar) were more frequently observed preying on P. viburni larvae than were older nymphs (3rd, 4th, and 5th instars) in the field. It was not clear whether the young nymphs feed on a larger number of prey or simply take longer to consume a similar number of prey than later instar nymphs. Podisus maculiventris nymphs also developed at lower rates and exhibited reduced activity at lower temperatures in the field, which suggests that temperature may influence the rate of prey consumption. Related to this, nymphs were often observed inside natural refugia in the field (e.g., dried leaves, bark fissures), more © 2008 Entomological Society of Canada

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so at lower temperatures. We hypothesized that the presence of refugia might prompt predators to rest more at lower temperatures, reducing time spent searching and feeding, and thus decreasing predation rates. We also suspected that predation efficiency might be influenced by the species of host plant, owing to differences in plant architecture and leaf-surface characteristics. Taking into consideration current investigations of generalist predators, as well as observations emerging from our field trials, the current study had a double objective: to document the effect of prey size and several environmental factors on predation by a generalist hemipteran on a specific pest and to add valuable knowledge concerning the potential use of P. maculiventris as a biologicalcontrol agent against P. viburni. To fulfil these objectives, three laboratory experiments were designed. In the first experiment, handling time (time spent by a predator between impaling the prey and abandoning the carcass) for P. maculiventris at different stages of nymphal development against P. viburni larvae and adults that varied in body mass was recorded. In the second experiment the impacts of temperature and presence of refugia on predation by P. maculiventris nymphs on P. viburni adults were measured. Finally, the impacts of host-plant species and size of the search area on predation by P. maculiventris nymphs on P. viburni larvae were recorded on southern arrowwood (Viburnum dentatum L.) and American cranberrybush, the two commonest host plants of P. viburni in North America.

Materials and methods Insects All insects were reared in chambers held at 22 °C under a 12L:12D light regime. Podisus maculiventris nymphs were laboratory-reared in a colony started with adults collected in the field in pheromone traps (described in Aldrich et al. 1997) in mid-April 2005. Adults collected from these traps (over 130 P. maculiventris individuals collected over a period of 3 weeks) were maintained in the laboratory until death and eggs laid by females were collected and reared separately from the adults. During the experimental season the colony produced two successive generations of P. maculiventris. Both nymphs and adults of P. maculiventris were fed larvae of either greater wax moth, Galleria mellonella (L.) (Lepidoptera: Pyralidae), or yellow mealworm, Tenebrio molitor L. (Coleoptera: Tenebrionidae), depending

on availability, purchased at a local pet store or from Ja-Da Bait (Antigo, Wisconsin). First-instar P. maculiventris were not used in any experiments because they are not predaceous. Fresh plant material, generally shoots of southern arrowwood or American cranberrybush, was provided to the colonies once a week (P. maculiventris is a facultative plant feeder) and moisture was provided on cotton dental wicks. The predators were kept in rectangular plastic containers (30 cm × 22 cm × 10 cm) at low or moderate densities (not more than 100 predators per container) to avoid crowding and cannibalism. A large colony of P. viburni larvae was also reared for experimental purposes. The larvae were obtained from eggs collected in the field during the winter preceding the experiments. Egg-infested twigs of southern arrowwood were held in the refrigerator until needed, then transferred to a chamber held at 22 °C until hatching. Newly hatched larvae were transferred to southern arrowwood shoots (collected in the field) in rectangular plastic containers (30 cm × 22 cm × 10 cm) for rearing until the experiments were completed. Fresh shoots were provided at least twice a week. Bioassay arena Most bioassays were conducted in plastic containers (8.5 cm diameter × 8.5 cm height) with lids that had a portion of the plastic replaced with fine-mesh polyester netting (20 × 24/in.). Influence of prey size on handling time To evaluate the influence of prey size on handling time we measured the time taken by individuals of P. maculiventris (nymphal instars 2–5) to consume one prey item (P. viburni larval instars 1–3 or adults) in small plastic Petri dishes (4 cm diameter × 1.2 cm height). All the possible combinations of P. maculiventris nymphal instar and P. viburni life stage were tested. We used only nymphs that had molted 12–36 h before the experiment and had not fed since molting. The prey items were weighed immediately before the experiment. Handling time was recorded manually for the replicates involving P. viburni larvae and videorecorded (on successive 8 h tapes) for the replicates involving P. viburni adults. Fourteen replicates per combination of prey life stage and predator instar were initially planned, but because of a substantial number of failures (i.e., the predator did not attack the prey after 2 h in the Petri dish) and the difficulty in sychronizing our © 2008 Entomological Society of Canada


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Fig. 1. Correlation between prey (Pyrrhalta viburni) body mass and predator handling time for 2nd-instar (A), 3rd-instar (B), 4th-instar (C), and 5th-instar Podisus maculiventris (D). Curves were fitted using linear regression (Statistix® 8.0).

colonies of P. maculiventris and P. viburni, 98 replicates in total were used for the analysis (mean 6.1 replicates per combination). Each P. maculiventris individual was used only once to maintain independence among treatments and replicates. Comparisons of handling time for the different combinations of P. maculiventris instar and P. viburni life stage were performed using one-way ANOVA followed by all-pairwise comparisons using the LSD method with Statistix® 8.0 for Windows® (Analytical Software 2003). Handling time was regressed against prey mass for each predator instar and the comparisons of lines procedure was performed with untransformed data (linear models, linear regression, Statistix® 8.0). Figure 1 shows the untransformed data and associated equations and R2 values. Temperature and presence of refugia To investigate the influence of temperature, presence of refugia, and possible interactions between these two factors on the predation

performance of P. maculiventris, we measured predation by 4th-instar P. maculiventris nymphs caged with P. viburni adults. Individual predators and five P. viburni adults were placed in bioassay arenas described above (8.5 cm diameter × 8.5 cm height). One fresh southern arrowwood leaf was added to each arena as a food supply for the prey and a facultative food supply for the predator and was replaced if necessary. A moistened cotton ball was also added to each container. The predation performance of P. maculiventris nymphs was evaluated by counting the prey eaten every day for 8 days. Consumed prey items were replaced with new ones every day until the experiment was completed. In total, 20 replicates were used for this experiment. The replicates were divided equally in two chambers, one held at 17 °C, and the other at 22 °C. For half of the replicates in each chamber, a refugium consisting of a dried southern arrowwood leaf that had curled into a © 2008 Entomological Society of Canada

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rough cylinder was added to the Petri dish. The leaves were dried at 100 °C for 24 h before the experiment and thus could not be used as food by either P. viburni adults or P. maculiventris nymphs. To avoid a possible interaction between the fresh and dried leaves, the fresh leaves were placed at the bottom of each Petri dish and the refugia were attached to the inner side of the lid with a piece of labeling tape. Both predator and prey were freely moving and had no trouble climbing the sides of the containers. Presence or absence of the predator in the refugium was visually recorded for each replicate once a day (when consumed prey were replaced) until the experiment was completed. The differences in prey consumption between the different treatments were analyzed using two-factor ANOVA (SAS Institute Inc. 1997). The differences in frequency of resting (i.e., the number of times each predator was found inside the refugium during the experiment) between treatments were analyzed using an exact test of independence (StatXact® 4.0; Cytel Inc. 1996). To meet the assumption of independence among replicates, each individual predator was considered a replicate. Host-plant species and size of the search area To investigate the influence of host-plant species and size of the search area on the predation performance of P. maculiventris, a 2nd-instar P. maculiventris nymph, newly molted and starved for 12–24 h, was placed in a bioassay arena (8.5 cm diameter × 8.5 cm height) with six P. viburni 2nd-instar larvae. We added to the arena a shoot (with two to four leaves) of the host plant and a moistened cotton ball. For each replicate we used shoots with leaves of different sizes ranging from very young to fully expanded. The number of prey consumed was recorded for each replicate after 24 h. Prey consumption by P. maculiventris nymphs on both plant species was analyzed using a general linear model with host-plant species, leaf surface area of the shoot in each replicate, and their interaction as variables in the model (PROC GLM procedure; SAS Institute Inc. 1997). We used a total of 14 replicates with southern arrowwood and 10 replicates with American cranberrybush. The combined area of the leaves for each replicate was measured by scanning the leaves after the experiment with a flatbed scanner following the procedures of Weston and Desurmont (2002). Leaf surface area ranged from 2.5 to 55.5 cm2 for southern


arrowwood (26.5 ± 17.6 cm2; mean ± SD) and from 3.5 to 71.4 cm2 for American cranberrybush (34.9 ± 24.1 cm2). The correlation between leaf surface area and prey consumption was analyzed by regressing leaf surface area (cm2) on the number of prey consumed in 24 h for both plant species (Statistix® 8.0; Analytical Software 2003).

Results and discussion Influence of prey mass on handling time Handling time increased consistently with prey mass for all instars of P. maculiventris feeding on all larval stages of P. viburni (Table 1). Handling time increased further as prey reached the adult stage, except for 4th- and 5thinstar P. maculiventris, where handling time apparently leveled off between the 3rd instar and adult stage of the prey (comparisons between means could not be performed for 4th-instar P. maculiventris, owing to the small number of replicates against 1st- and 3rd-instar P. viburni). No data were collected for the combination of 5th-instar P. maculiventris and 1st-instar P. viburni because the predator always ignored the prey in those cases, apparently because of the small size of the prey relative to the size of the predator. Linear regressions between prey mass and handling time were significant and positive for the four instars tested, with P values ranging from 0.05) as determined by one-way ANOVA (all pairwise comparisons, LSD method, Statistix® 8.0).

18.0±3.18a 16.3±1.55a 8.04±1.35 3.09±0.66ab 13.6±0.81 13.9±2.94 14.0±3.51 12.4±0.94 3 9 14 4 14.9±2.75a 9.57±1.4b 11.3±3.58 3.53±0.46a 9.67±2.25 10.8±4.94 10.3±11.3 11.0±4.72 3 11 2 8 2.06±1.84b 2.07±1.47c 1.65±2.06 1.67±0.47b 0.74±0.34 1.70±0.78 1.67±0.77 1.95±0.53 1.32±2.08b 0.57±2.69c 0.53 — 7 3 1 0 2nd 3rd 4th 5th

0.20±0.11 0.27±0.25 0.20 —

9 10 6 8

Body mass (mg) Handling time (h) Handling time (h)a n Predator instar

Body mass (mg)

n

Body mass (mg)

Handling time (h)

n

Body mass (mg)

3rd instar Prey life stage 2nd instar 1st instar

Table 1. Handling times of Podisus maculiventris nymphs (predator) across life stages of Pyrrhalta viburni (prey).

n

Adult

Handling time (h)


comparison of slopes procedure), no doubt because the size differential between predator and prey decreases with life stage of the predator. These results are consistent with those from a previous study conducted with P. maculiventris preying on Galleria mellonella larvae (Mukerji and LeRoux 1969), where handling time was found to increase with prey size, but decreased as predator age increased for a given prey size. In addition to these unsurprising findings, our results also show that the impact of prey body structure is negligible compared with that of prey mass on handling time in this particular system: the time spent handling soft-bodied prey (P. viburni larvae) and hard-bodied prey (P. viburni adults) varied similarly with prey mass for all P. maculiventris instars. These results illustrate the dynamic nature of handling time and, by extension, the functional response, and underline the difficulty of applying theoretical predation models to field situations. From a biological-control perspective, the results are helpful for understanding the predation performance of different instars of P. maculiventris against P. viburni but cannot be used to calculate predation rates in the field or predict which P. maculiventris nymphal stage would be the best biological-control agent. However, the fact that young P. maculiventris nymphs (2nd and 3rd instars) take a long time to handle large prey (>15 h to handle a single P. viburni adult) indicates that the potential for daily predation by the young predators on large prey is rather limited. During our 2005 field trials, 2nd-instar P. maculiventris nymphs were observed preying more frequently than other instars (Desurmont 2006): the results from this experiment indicate that this increased frequency of observed predation might not reflect an increased rate of predation by 2nd-instar nymphs but might simply be the consequence of the increased handling time required for 2ndinstar nymphs to consume their prey. However, no firm conclusion can be drawn concerning these two hypotheses without direct measurements of predation rates of P. maculiventris nymphs in the field. Temperature and presence of refugia Podisus maculiventris nymphs ate significantly more prey at 22 °C (7.2 ± 2.5; mean ± SE) than at 17 °C (3.9 ± 1.4) (Fig. 2). The effect of temperature was significant (F1,16 = 11.97, P = 0.0032), but neither the presence of refugia (F1,16 = 0.10, P = 0.7572) nor the © 2008 Entomological Society of Canada

198 Fig. 2. Influence of temperature and presence of refugia on the cumulative predation performance of 4th-instar Podisus maculiventris nymphs against Pyrrhalta viburni adults (mean + SE) over 8 days.

interaction between temperature and presence of refugia (F1,16 = 0.27, P = 0.6074) was significant. The influence of temperature on P. maculiventris has been documented in previous studies (e.g., De Clercq and Degheele 1992). The reduction in predation that we observed at the lower temperature during our experiment was likely the result of slower metabolism of the nymphs at 17 °C than at 22 °C. This is consistent with our observations from the 2005 field trials (Desurmont 2006) and a study investigating the effect of temperature on Podisus nigrispinus (Dallas) (Hemiptera: Pentatomidae) and P. maculiventris feeding on the beet armyworm, Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae) (Mohaghegh et al. 2001). The data do not support our hypothesis that the presence of refugia might have a negative impact on predation rates, especially at low temperatures. Resting inside refugia was found to be a consistent behaviour of the predator: P. maculiventris nymphs were found inside the refugia in 45% of our observations (n = 80), but the presence of refugia had no impact on predation, suggesting that the predator spent similar time budgets on resting, searching, and preying and had the same physiological needs whether refugia were present or not. The fact that predators were often found resting in the refugia provided is consistent with the results from our field trials (nymphs were found resting inside refugia in 57% of the observations) and from previous studies (e.g., Wiedenmann and O’Neil (1991) found that resting was a dominant


behaviour of P. maculiventris, which allocated more time to resting than to searching and feeding). Periods of rest are considered to be adaptations to save energy or to hide from potential predators, and hiding while resting makes sense for both purposes, the refugium possibly helping to save energy by providing protection from low temperatures or harsh environmental conditions and decreasing the probability of being attacked by a natural enemy. Several authors have reported that refugia are important for rearing P. maculiventris (Warren and Wallis 1971; De Clercq and Degheele 1993; Zanuncio et al. 1993) in order to avoid high mortality rates due to cannibalism for both nymphs and adults, thus reinforcing this hypothesis. Host-plant species and size of the search area There was no main effect of leaf surface area (F1,20 = 1.31, P = 0.2654) or host-plant species (F1,20 < 0.01, P = 0.949) on predation by P. maculiventris on P. viburni, although P. maculiventris nymphs consumed more prey when foraging on American cranberrybush (5.0 ± 0.5) than when foraging on southern arrowwood (2.9 ± 0.4). However, there was a significant effect of the interaction of plant species and leaf surface area on prey consumption (F1,20 = 11.36, P = 0.0196). Prey consumption was found to be inversely related to leaf surface area for southern arrowwood (y = –0.05x + 4.29, P = 0.048, r² = 0.28) but unrelated to leaf surface area for American cranberrybush (y = 0.02x + 4.22, P = 0.221, r² = 0.18) (Fig. 3). The difference in prey consumption observed on American cranberrybush and southern arrowwood at high surface leaf area is somewhat surprising. Both species are highly susceptible to P. viburni feeding, are closely related, and possess thin leaves with a smooth surface and few trichomes. However, differences in the shape and size of the leaves exist: American cranberrybush leaves are generally relatively large and maple leaf-shaped, whereas those of southern arrowwood are smaller and elliptical. Two hypotheses might explain the observed difference in prey consumption on the different hosts at high leaf surface area. First, searching efficiency may be decreased on southern arrowwood as leaf surface increases because of the ability of the prey to hide more easily from the predator. Indeed, southern arrowwood leaves are more heavily ribbed on the underside than © 2008 Entomological Society of Canada


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Fig. 3. Correlation between leaf surface area and predation performance of 2nd-instar Podisus maculiventris nymphs against 2nd-instar Pyrrhalta viburni larvae on southern arrowwood (Viburnum dentatum) (A) and American cranberrybush (Viburnum opulus var. americanum) (B). Curves were fitted using linear regression (Statistix® 8.0).

those of American cranberrybush and could provide refugia for larvae of P. viburni, especially the younger instars, which are smaller and tend to feed more extensively on the underside of leaves. Alternatively, the decreased predation efficiency of P. maculiventris on southern arrowwood may be due to differences in allelochemicals present in foliage of the two host plants: P. maculiventris predation and development can be negatively affected by plant allelochemicals indirectly ingested as a result of feeding on herbivores that eat noxious plants (Bozer et al. 1996; Weiser and Stamp 1998). Moreover, P. maculiventris is a facultative plant feeder and might be affected directly by

phytochemicals ingested with plant liquids. The negative correlation observed between P. maculiventris predation performance and leaf surface area of southern arrowwood might seem consistent with the hypothesis that leaves of this species provide refugia for the prey: the number of prey consumed decreases gradually with increasing leaf surface area of southern arrowwood, suggesting a decline in searching efficiency. However, plant allelochemicals might change with age, as has been demonstrated in several systems (e.g., Takabayashi et al. 1994; Thomas and Schafellner 1999), and the chemistry of fully expanded leaves might differ from that of young © 2008 Entomological Society of Canada

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leaves. A similar pattern might be expected if older southern arrowwood leaves contain secondary compounds that have an impact on the predation performance of P. maculiventris directly (plant feeding) or indirectly (prey feeding). Distinguishing between these two hypotheses is not possible without further experimentation. The fact that we did not detect a significant species effect on predation performance when the leaf surface area was low may be linked with the higher rate of prey consumption observed on American cranberrybush than on southern arrowwood. Podisus maculiventris nymphs killed all the larvae provided as prey on American cranberrybush shoots in 40% of the replicates. Therefore, it is possible that we underestimated predation rates of P. maculiventris at low and high leaf surface areas and that the species effect on predation rate might actually be even larger than observed. Overall, the results of this research provide additional evidence for the importance of considering biological and environmental variables in both theoretical and applied studies of the use of generalist predators against pests. Although the influence of temperature and size of the search area has been studied for several predator–prey systems, the impact of other factors such as host-plant species and presence of refugia for the predators is often overlooked. The potential interactions between environmental factors, illustrated in our study by the significant interaction between size of the search area and host-plant species, underline the extreme difficulty of predicting predation rates in a dynamic environment. In addition, the results of our handling-time trial provide additional evidence of the dynamic nature of the functional response, i.e., it changes with life stage and size of predator and prey. These findings have significant implications for improving augmentative releases of P. maculiventris to control P. viburni. First, variations in handling time with prey mass and predator age suggest that early release of predatory nymphs is preferable in order to increase the chances of successful pest control. The release of P. maculiventris nymphs when P. viburni larvae are still at an early stage of development (preferably 1st instar) should result in greater predation efficiency and less plant damage than if the nymphs are released when P. viburni larvae are already advanced in their development, since the nymphs are able to handle only a limited number of large prey per day.


Resting inside refugia, a consistent behaviour of P. maculiventris, is also interesting from a practical perspective. It is plausible that predators might remain longer on plants providing plenty of refugia rather than on plants lacking refugia. High leaving rates of predators on annual crops such as tomatoes and potatoes have been observed (Aldrich and Cantello 1999). Old viburnum shrubs offer predators plenty of refugia of various types (dried leaves, bark crevices, etc.), but this is not necessarily the case with very young plants. The fact that the presence of refugia does not have a negative impact on predation makes it reasonable to hypothesize that for the same predator:prey ratio, predator releases might be more effective on old shrubs than on young shrubs because the predators are retained longer in the release area. Although speculative, this hypothesis would be worth considering in future experiments. Our results also show that host-plant species plays a role in the efficacy of P. maculiventris predation against P. viburni: P. maculiventris nymphs consumed more prey on old American cranberrybush leaves than on old southern arrowwoodleaves. However, the predation performance of P. maculiventris against other Viburnum species susceptible to P. viburni is unknown. Therefore, extending studies of the influence of the host plant on the predation efficiency of P. maculiventris to other susceptible Viburnum species that vary in both physical and chemical characteristics would be valuable for pest-management purposes. In our particular system we have shown that the relative sizes of predator and prey, temperature, host-plant species, and size of the search area influence predation by P. maculiventris nymphs on P. viburni larvae and adults. Although this list is far from exhaustive, the identification of these variables is a first step in evaluating the potential of P. maculiventris as a reliable biological-control agent against P. viburni in North America.

Acknowledgments We thank Maria Derval Diaz and Juan Pablo De Lima Costa Salazar for their help with experiments. Françoise Vermeylen (statistical consulting, Cornell University) helped with the statistical analyses. Thanks are also extended to Ann Hajek (Cornell University), who reviewed the manuscript and provided many helpful comments. Funds for this project came from © 2008 Entomological Society of Canada


Cooperative State Research Education and Extension Service (CSREES) under Agreement No. NYC-139403 and from the New York State Integrated Pest Management Program.

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