(Heteroptera: Miridae) predation in apple orchards

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Crop Protection 25 (2006) 705–711 www.elsevier.com/locate/cropro

Effectiveness of Hyaliodes vitripennis (Say) (Heteroptera: Miridae) predation in apple orchards Ge´rald Chouinarda,, Sylvie Bellerosea, Carole Brodeurb, Yvon Morinb a

Institut de recherche et de de´veloppement en agroenvironnement (IRDA), 3300 Sicotte Street, P.B. 480, St. Hyacinthe, Que., Canada J2S 7B8 b Agrilus Inc., 1350 St. Charles Street, St. Alexandre, Que., Canada J0S 1S0 Received 25 March 2005; received in revised form 28 September 2005; accepted 30 September 2005

Abstract The biology of Hyaliodes vitripennis Say (Heteroptera: Miridae) and its potential for biological control of mites and aphids were studied for 3 yr in apple orchard settings. Results showed a significant repressive effect of H. vitripennis on the European red mite, Panonychus ulmi Koch, the two-spotted spider mite, Tetranychus urticae Koch and a significant augmentative effect on the green aphids (Aphis pomi DeGeer and Aphis spiraecola Pagenstecher). The predator also precluded the action of naturally occurring predatory mites, either by resource competition or by direct predation, but the resultant effect was always detrimental to P. ulmi. r 2005 Elsevier Ltd. All rights reserved. Keywords: Aculus schlechtendali; Agistemus fleschneri; Phytoseiidae; Stigmaeidae; Predatory mites; Biological control; Apple pests; Predation

1. Introduction The European red mite, Panonychus ulmi Koch (Acari: Tetranychidae) is a key pest in apple orchards of northeastern North America, because broad spectrum insecticides used to control other pests reduce its predators (mainly from families Anthocoridae, Cecidomyidae, Coccinellidae, Chrysopidae, Hemerobiidae, Miridae, Phytoseiidae, Stigmaeidae and Syrphidae) and, therefore, reduce biological control of P. ulmi (Prokopy and Croft, 1994). In addition, phytophagous mites in general including species such as the two-spotted spider mite, Tetranychus urticae Koch (Acari: Tetranychidae) and the apple rust mite, Aculus schlechtendali Nalepa (Acari: Eriophyidae) pose important management problems, since they very quickly develop resistance to pesticides present in their environment (Croft, 1990). Aphids (the green apple aphid, Aphis pomi DeGeer and the spirea aphid, Aphis spiraecola Pagenstecher) can also become major foliage pests when populations of their natural predators (mainly from families Cecidomyidae, Coccinellidae, Chrysopidae, HeCorresponding author. Tel.: +1 450 778 6522; fax: +1 450 778 6539.

E-mail address: [email protected] (G. Chouinard). 0261-2194/$ - see front matter r 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.cropro.2005.09.014

merobiidae, Miridae and Syrphidae) are decimated by broad spectrum insecticides. Among those natural predators, Hyaliodes vitripennis Say (Heteroptera: Miridae), also known as the glassywinged soldier bug, is a native insect of North America, described in 1831 as Capsus vitripennis (Say, 1831). Relatively few details of its biology are known. Horsburgh (1969) described in detail its role in the repression of European red mite populations in Pennsylvania orchards. Others have described the natural fluctuations of Hyaliodes populations in commercial orchards of Nova Scotia, Canada (Chachoria, 1967; Lord, 1968, 1971; Sanford, 1964; Sanford and Lord, 1962). Although from these studies the insect appeared as well-distributed and relatively common in these apple orchards, to our knowledge the insect was not reported from commercial orchards for many years after, when the use of organo-synthetic insecticides became widespread. One study mentioned the presence of H. vitripennis in insecticide-free orchards located in Quebec, Canada (Braimah et al., 1982). Two species of Hyaliodes are found in Quebec: H. vitripennis and H. harti Knight (Braimah et al., 1982). Arnoldi (1986) found H. vitripennis to be the most common hemipteran predator in an insecticide-free orchard of

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southwestern Quebec, and noted that it appeared to be much more specific to apple trees than any other hemipteran predator present. This species is found in most northeastern American states (Horsburgh, 1969). H. vitripennis has two generations per year in Pennsylvania and spends the winter in the egg stage (Horsburgh, 1969). Gilliatt (1935) and Arnoldi et al. (1992) reported a single generation per year in Nova Scotia and Quebec, respectively. H. vitripennis feeds mostly on mites and aphids (Arnoldi, 1986) but also on leafhoppers and lepidopteran larvae (Horsburgh, 1969). Several authors have reported H. vitripennis predation on various species (Lord, 1949, 1968; Sanford and Lord, 1962). The only published quantitative study (Arnoldi et al., 1992) measured daily consumption rates on A. pomi , T. urticae and P. ulmi in no-choice tests performed under laboratory conditions. H. vitripennis was the most voracious of the eight mirid predators studied, and consumed more P. ulmi than any other prey presented. Populations of H. vitripennis were observed in 1992 in several commercial orchards of southwestern Quebec (Monteregians and Eastern Townships) (Brodeur et al., 1999; Chouinard et al., 1992a, b). These observations coincided with apparent cases of natural population decline of P. ulmi without acaricides, which led local consultants to suspect a regulatory role of H. vitripennis on P. ulmi in apple orchards. This is consistent with prey preference reported by Arnoldi et al. (1991, 1992). Here we provide expanded studies of the impact of H. vitripennis on apple tree pests such as phytophagous mites and aphids, under commercial apple orchard conditions. 2. Materials and methods 2.1. Collection of H. vitripennis Different source orchards were selected in southwestern Quebec to supply H. vitripennis individuals for trials taking place in 1996 (St. Alexandre: 451 140 2600 N, 731 70 800 W), 1997 and 2000 (St. Jean Baptiste: 451 310 1700 N, 731 90 3200 W). The destruction of the original source orchard compelled us to use a different orchard after the first year. Both source orchards were, however, located within a 50 km radius, had not been treated with insecticides at least 30 d prior to the collection date and had large populations of H. vitripennis (more than ten individuals per 3 min of observation), according to visual monitoring performed by scouts trained by the authors (Morin, unpublished data). The predators (second to fifth instar) were collected early in the morning of their introduction, and stored individually in 10 ml Solo cups with an apple leaf to prevent cannibalism and reduce stress. The cups were then placed in an ice chest (ca. 4 1C) to avoid excessive mortality during transportation to the release sites.

2.2. Releases into commercial orchards The experiment was carried out at three sites (ca. 0.2 ha each) planted with standard-sized apple trees, located in St. Jean Baptiste (451 280 4400 N, 731 50 3400 W) in 1996, in Bedford (451 70 0000 N, 721 590 0000 W) in 1997 and in Rougemont (451 270 1500 N, 731 20 000 W) in 2000. H. vitripennis was not present in those orchards according to visual monitoring data collected over the three previous years by scouts trained by the authors (Morin, unpublished data). Experimental trees (cv. McIntosh) were chosen within the central rows, observing a minimum distance of 7 m between each tree in order to minimize interaction between experimental units. Six (1996–1997) or four (2000) control trees and an equivalent number of treatment trees (where H. vitripennis were introduced) were then allotted at random within the experimental trees. Trees were of similar size (5 m), shape and condition. The collection and introduction of H. vitripennis nymphs took place on 23 July (1996), 17 July (1997) and 20 July (2000), 0–24 h following prey and predator density assessment. Predators were released at a rate of 100 (1996–1997) or 200 (2000) per tree on the pre-selected trees. The nymphs collected in the morning were delicately placed in early afternoon on the foliage of randomly selected branches of each of the trees. This was done by stapling the leaf from the cups to another in the tree or by letting the nymphs move by themselves onto a tree leaf. Naturally occurring insects and mites were used as prey source, and no additional introductions of prey were made. 2.3. Predator/prey assessment Populations of insects and mites present in the experimental trees were first assessed 0–1 d prior to introduction of predatory mirids. To assess nymphal and adult H. vitripennis population densities, each tree was observed for 3 min, according to Asquith and Colburn (1971), by placing oneself directly underneath the canopy at a distance of 50 cm from the tree limbs, and by moving in order to allow observation of all accessible surfaces within the allotted time. This method provides an accurate estimate of the number of Stethorus punctum LeConte (Coleoptera: Coccinellidae) individuals per tree (Asquith and Hull, 1979) and has also been successfully used for H. vitripennis (Brodeur et al., 1999; Firlej et al., 2003), since this predator also feeds primarily on spider mites, is also primarily found on the underside of leaves (Brodeur et al., 1999) and is readily visible for trained observers. Eggs and motile forms of Stigmaeidae, Phytoseiidae, Tetranychidae (P. ulmi, T. urticae) as well as motile forms of A. schlechtendali were counted by brushing 50 randomly selected leaves onto one oil-coated (30W viscosity) glass plate per tree using a leaf brushing machine (1996–1997) or by a presence–absence sampling method (Nyrop et al., 1989) performed on eight marked leaves from each of 20 randomly selected fruit clusters in each tree (2000). The

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Table 1 Regression analysis of data collected following H. vitripennis releases in commercial orchards, St. Jean Baptiste, 1996 and Bedford, 1997 Total populations of

1996 P. ulmi T. urticae Phytoseiidae H. vitripennis (nymphs and adults) Stigmaeidae A. schlechtendali A. pomi+A. spiraecola 1997 P. ulmi T. urticae Phytoseiidae H. vitripennis (nymphs and adults) Stigmaeidae A. schlechtendali A. pomi+A. spiraecola

P. ulmi

T. urticae

Phytoseiidae

H. vitripennis

Stigmaeidae

A. schlechtendali

A. pomi+A. spiraecola

++

NS NS

NS NS

NS NS NS NS

NS NS NS NS NS

NS NS NS ++ NS NS

+++

NS NS

NS NS

+++ NS NS

NS NS NS NS NS

NS NS NS ++ NS

All sampling dates considered. Statistically significant relationships (positive or negative) are noted as follows: +/ ¼ pp0:05; + +/ ¼ pp0:01; + + +/ ¼ pp0:001; NS ¼ no significant correlation.

presence–absence sampling method was used in 2000 because European red mite was the sole mite species of significant abundance, and because it provided a quick and reliable estimate of the total number of eggs and motile forms under these circumstances. Aphid populations (A. spiraecola and A. pomi) were estimated on five shoots per tree, using an infestation rating obtained by averaging the scores obtained for each shoot according to aphid population levels (0 ¼ absent, 1 ¼ low, 2 ¼ moderate or 4 ¼ high) (Boule´ et al., 1999). Arthropod assessments were repeated 1 d after mirid introduction, then on 4–5 additional occasions depending on the year, during the 2–5 weeks following introduction of H. vitripennis. In order to detect an eventual dispersion of the introduced predators, visual assessments of H. vitripennis were also carried out in 1996 and 1997 on the four adjacent trees next to two apple trees randomly selected from those where H. vitripennis were introduced. No insecticides or acaricides were applied in July and August during those 3 yr, other than an annual application of phosalone targeted against the apple maggot, Rhagoletis pomonella Walsh (Diptera: Tephritidae) and a single application of tebufenozide in 2000 targeted against the codling moth, Cydia pomonella L. (Lepidoptera: Tortricidae). Both products are considered safe for H. vitripennis (Bostanian et al., 2000, 2001; Morin and Chouinard, 2001). 2.4. Data analysis Principal components analysis (SAS Institute Inc., 1985) was first used as a screening tool for data collected in 1996 and 1997 to allow the identification of a reduced number of mutually independent variables to submit to regression studies, each taking into account several of the variables measured during the experiment. Those independent

variables generally corresponded to the total number of individuals of each of the species surveyed and are listed in Table 1. Seven linear regression analyses (across all dates for release and control trees) were then made in 1996 and 1997 for total population counts of the seven variables listed in Table 1, each variable being successively used as the dependent variable of the additive model and the remaining ones as the independent variables. Since the selected variables followed a Poisson distribution, the analyses were performed following ‘‘square root+0.5’’ transformation. Comparisons between prey populations in release vs. control trees were then made for significant factors, using a t-test comparing means for each specific sampling date, except for indices, which were analyzed according to a Mann–Whitney test. Overall effects of the predator on each prey type were identified by means of an analysis of covariance, with prey counts at day 0 as a covariate. This procedure allowed us to take into account the variable levels of initial prey populations in the different treatments, as well as the possible interaction between treatment and time. Counts were analyzed using the MIXED procedure in SAS (Littell et al., 1996) after the log10(n+0.5) transformation to meet the assumption of normality. Since measurements were taken on unequally spaced intervals, the spatial power law structure for unequally spaced data was selected as the most appropriate covariance structure for our experiment (Littell et al., 1996). 3. Results and discussion For the duration of the trials in 1996 and 1997, H. vitripennis individuals were never seen on trees other than the release trees (Figs. 1A, F). Monitored populations



Fig. 1. Mean densities (7SE) of introduced H. vitripennis (A, F), and significant effects on naturally occurring preys: P. ulmi motile forms (B), aphid colonies (C), Phytoseiidae motile forms (D), total Phytoseiidae population (E), T. urticae motile forms (G), Stigmaeidae eggs (H), and total Stigmaeidae population (I). Mirid predators were released 23 July 1996 and 17 July 1997 (six release trees, 100 predators per tree). Significant overall and over time differences between treatments (analysis of covariance and t-test) are indicated by a star (pp0:05). No H. vitripennis were observed in control trees for all dates.

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gradually decreased over time in those trees, as more and more nymphs reached the adult stage and had the possibility to disperse. They were, however, observed several times during the year following their introduction in control, release and unsurveyed trees of the two orchards studied (Morin, unpublished data). Other studies (Firlej et al., 2003) also reported that introduction of immature stages of H. vitripennis can lead to its establishment in orchards where it had previously been absent. Our shortterm observations do not constitute a proof of establishment but they support this study. Population levels of the predator immediately following releases also approached those recorded during a survey of 13 apple orchards done in 1997 in eastern Quebec (average of six individuals per 3 min at peak populations; unpublished data). This makes our empirical choice of 100–200 individuals released per tree a realistic choice in terms of resulting predator populations. 3.1. Effect on tetranychid mites The regression analysis (Table 1) showed that, for all the apple trees in the 1996 study, a significant proportion of the variation in the total number of P. ulmi (p ¼ 0:0004) was explained by the total number of H. vitripennis. In 1997, a significant proportion of the variation in the total number of T. urticae motile forms and eggs was explained by the total number of H. vitripennis, and a significant effect of the predator on motile forms of that prey was also observed (Table 1). In both years, a significant proportion of the variation in the total number of P. ulmi was explained by the total number of T. urticae. H. vitripennis had a significant effect on motile forms of T. urticae in 1997 (F 1;9 ¼ 5:90, p ¼ 0:0381), when it was present in appreciable numbers (Fig. 1G). A significant effect was also found for P. ulmi populations in 1996 (on motile forms, July 26, Fig. 1B) and in 2000 (F 1;5;151 ¼ 12:30, p ¼ 0:0171) (Fig. 2). In all 3 yr, eggs and motile forms of P. ulmi developed less rapidly and overall levels were numerically lower in trees with H. vitripennis than in trees without the predator (Figs. 1B and 2). 3.2. Effect on predatory mites H. vitripennis had a significant negative effect on naturally occurring populations of phytoseids in 1996 (motile forms: F 1;11 ¼ 9:74, p ¼ 0:097; eggs and motile forms: F 1;11 ¼ 9:36, p ¼ 0:0109) (Figs. 1D, E) and stigmaeids (Agistemus fleschneri Summers) identified in the orchard in 1997 (eggs: F 1;9 ¼ 9:66, p ¼ 0:0126; eggs and motile forms: F 1;9 ¼ 9:23, p ¼ 0:0141) (Figs. 1H, I). Population variation of stigmaeids was more clearly explained by the total population of P. ulmi, aphids and H. vitripennis than by other variables (Table 1). Even though predation was not directly measured, our results suggest either that H. vitripennis feeds on the predatory mites or that it reduces the common resource (P. ulmi)

Fig. 2. Mean densities (7SE) of introduced H. vitripennis, and significant effects on naturally occurring P. ulmi in a southwestern Quebec apple orchard, 2000. Mirid predators were released 20 July (four release trees, 200 predators per tree). Significant overall and over time differences between treatments (analysis of covariance and Mann–Whitney test) are indicated by stars ( pp0:05; pp0:01; pp0:001). For analysis of covariance on P. ulmi: F 1;5 ¼ 12:30, p ¼ 0:0171; on H. vitripennis: F 1;5 ¼ 26:46, p ¼ 0:0036).

sufficiently to affect predatory mite populations. Intraguild predation (IGP) (Lucas et al., 1998) by H. vitripennis has been reported by Provost et al. (2005), who evaluated it within a guild of mite predators [H. vitripennis, Amblyseius fallacis (Acari: Phytoseiidae) and Harmonia axyridis Pallas (Coleoptera: Coccinellidae)] feeding on T. urticae on apple tree seedlings. They concluded that the intensity of IGP between H. vitripennis and A. fallacis was low, and that the interaction did not affect the predation efficacy (an additive effect was reported on the shared prey). According to our results, IGP can only be pointed as one of several factors that possibly played a role in natural settings.

3.3. Effect on other arthropods A significant proportion of the variation in the infestation index of aphids was explained by total number of H. vitripennis in 1996 but not in 1997 (Table 1). H. vitripennis was associated with increased aphid populations (F 1;11 ¼ 12:28, p ¼ 0:0049) in 1996 (Fig. 1C). Possible explanations for this include IGP (on unsurveyed species) and the relative preference of the predator for tetranychids



over aphids, as demonstrated by other studies (Arnoldi et al., 1992; Brodeur et al., 1999). Under the conditions of our study, H. vitripennis had no visible effect on naturally occurring A. schlechtendali populations (Table 1). Although apple rust mite was reported by Horsburgh (1969) as a suitable prey for H. vitripennis in Pennsylvania, our results suggest that A. schlechtendali is not a major prey of H. vitripennis when P. ulmi or T. urticae are present. 4. Conclusion These field results are consistent with previous laboratory studies (Arnoldi et al., 1991, 1992) and allow for a more accurate description of H. vitripennis predation on apple trees. Although it is a polyphagous insect, H. vitripennis is able to exert a significant repressive effect on spider mite populations. H. vitripennis resurgence in commercial orchards, due to changing pesticide use practices, may open opportunities to enhance biological control of P. ulmi and T. urticae. This predator is relatively tolerant to some insecticides used in orchards (Bostanian et al., 2000, 2001), but recent studies (Provost et al., 2003a, b) suggest that the use of insecticides at sub-lethal rates may result in increased attack rates of H. vitripennis adults on other mite predators such as A. fallacis. Although the predator can be maintained in the laboratory for a period of time (Horsburgh and Asquith, 1969), egg deposition and emergence are still problematic (Firlej, 2002) and mass rearing as well as inundative or augmentative releases are not possible yet. Quebec’s IPM guidelines already recognized the importance of this predator for growers and rated it as being ‘‘moderately’’ abundant, having a ‘‘high’’ rate of predation, and being ‘‘highly’’ interesting for biological control of mites in apple orchards (Morin and Chouinard, 2001). The presence of this mirid in Quebec’s orchards appears as rather unique, and an integrated pest management program based on the use of selective control agents is currently being studied for the conservation of this predator and its establishment following inoculative releases. Acknowledgements The authors wish to thank E´ric Bazin, Marie-He´le`ne Bourgault, Christelle Danjou, Sandra Gagnon, Martine Gigue`re, Nathalie Laplante, Christiane Lefebvre, David Somerville and Sandrine Vallin for their help with experiment field work, Tessa Webb for translation, Daniel Cloutier and Miche`le Grenier for help with statistical analysis, as well as Noubar Bostanian, Jacques Brodeur, Daniel Cormier, Annabelle Firlej, Francine Pelletier and Charles Vincent for their constructive criticisms. This research was financially supported by grants by the CORPAQ (#4312) and the FCAR (#1999-IR-161500).

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