cultivar affects apple resistance to the ... - Wiley Online Library

Agricultural and Forest Entomology (2015), 17, 337–346

DOI: 10.1111/afe.12112

Plant genotype and the preference and performance of herbivores: cultivar affects apple resistance to the florivorous weevil Anthonomus pomorum Karsten Mody† , Jana Collatz‡ and Silvia Dorn Applied Entomology, ETH Zurich, Institute of Agricultural Sciences, Schmelzbergstrasse 9/LFO, 8092, Zurich, Switzerland

Abstract

1 Plant resistance strongly depends on plant characteristics that affect herbivore preference or performance. Different plant genotypes may express specific characteristics that lead to differential resistance to herbivores. Few studies have investigated these aspects for weevils, a particularly speciose taxon of insect herbivores, on fruit tree cultivars, which are vegetatively propagated. 2 We studied the influence of apple cultivar on preference and performance of a fruit tree herbivore, the flower-feeding apple blossom weevil Anthonomus pomorum (Coleoptera: Curculionidae). We quantified field infestation of five different apple genotypes by the weevil at different collection dates as measure of preference, as well as the mass and emergence time of weevils developing on these cultivars as measures of performance. 3 Infestation of apple flower buds by A. pomorum differed significantly between cultivars. The collection date affected the number of infested flowers in a cultivar-specific way. 4 Weevil mass differed significantly between apple cultivars. The average mass of weevils from Ariwa, the cultivar producing the heaviest weevils, was 40% higher than the mass of weevils from Rewena, the cultivar producing the lightest weevils. 5 Weevil emergence time from infested flowers differed significantly between cultivars. Weevils emerged earliest from cultivars Ariwa and Retina, at an intermediate time from Discovery and Florina, and latest from Rewena. 6 The present study demonstrates that preference and performance of florivores feeding on fruit trees can strongly differ between apple cultivars representing specific tree genotypes. These differences may directly and indirectly affect herbivore and antagonist populations and can be considered for pest management. Keywords Antibiosis, antixenosis, apple Malus × domestica, coleopteran pests, flower bud infestation, herbivore–plant interactions, plant resistance, preference–performance hypothesis, sexual size dimorphism, tree phenology.

Introduction Herbivores respond to characteristics of their host plants (Schoonhoven et al., 2005; Carmona et al., 2011), which are influenced by the plant’s environment and by the plant’s Correspondence: Karsten Mody. Tel.: +49 (0)6151 16 75414; fax: +49 (0)6151 16 4926; e-mail: [email protected] † Present address: Ecological Networks, Institute of Biology, Technical University Darmstadt, Schnittspahnstrasse 3, 64287 Darmstadt, Germany. ‡ Present address: Agroscope, Institute for Sustainability Sciences (ISS), Reckenholzstrasse 191, 8046 Zurich, Switzerland.

© 2015 The Royal Entomological Society

genotype (Osier & Lindroth, 2006; Ballhorn et al., 2011). The importance of genotype effects for herbivore–plant interactions is pervasive in natural ecosystems (Johnson & Agrawal, 2005; Bangert et al., 2006), although it is even more obvious for crop plants in managed agricultural and forestry cropping systems (Stoeckli et al., 2008; Henery, 2011; Smith & Clement, 2012). Crop plants are usually represented by specific cultivars that express typical crop characteristics as a result of high genetic similarity. In the case of asexually propagated crop cultivars, such as most fruit trees, individual plants of the same cultivar are usually genetically identical (clones) (Miller & Gross, 2011) and thus express the greatest possible similarity in plant

338

K. Mody et al.

characteristics that influence herbivore–plant interactions, including plant resistance to herbivores (Smith & Clement, 2012). Host plant resistance refers to plant traits that reduce damage to the plant by reducing herbivore preference or enhancing escape from herbivores, or by leading to reduced herbivore performance (Karban & Baldwin, 1997; Strauss & Agrawal, 1999; Boege & Marquis, 2005; Mody et al., 2009). Herbivore preference relates to plant traits that determine the plant’s attractiveness or acceptability as a host (i.e. antixenosis resistance; Kogan & Ortman, 1978), whereas plant escape from a herbivore may be linked to plant traits that reduce encounters with this herbivore (e.g. via variable plant phenology that decreases coincidence of susceptible plant stages and herbivore occurrence). Herbivore performance relates to plant traits that affect the plant’s suitability as a host and thus the growth and fecundity of the herbivores (i.e. antibiosis resistance; Smith, 2005). Antixenosis resistance may show strong effects on host plant damage and crop loss, and it is particularly effective in situations where individual herbivores have the opportunity to choose between differently acceptable plants. Differences in host susceptibility may occur between plants that were grown under differing environmental conditions and cultural practices (Staley et al., 2010; Gutbrodt et al., 2012a; Costes et al., 2013), although they are generally most pronounced between cultivars (Clark et al., 2012; Smith & Clement, 2012). Among cultivars, differences in plant genotype may lead to differences in nutrient composition, secondary metabolites and morphological characteristics, as well as phenology (Minarro & Dapena, 2007; Wojdylo et al., 2008; Stoeckli et al., 2011). Antibiosis resistance can have immediate effects on host plant use by herbivores. Additionally, it may have an impact on herbivore population growth and thereby on longer-term ecosystem processes and pest management (Tiffin, 2000; Smith & Clement, 2012). Furthermore, it may affect organisms at the next trophic level that are relevant for the top-down control of herbivore populations (Sarfraz et al., 2009). In most instances, the preference of adult females determines host plant infestation by their offspring (Gripenberg et al., 2010). Female preference should be positively related to offspring performance unless female host selection is dominated by other factors, such as female avoidance of enemies or competitors (Hicks et al., 2008; Plath et al., 2012) or female incapability to reliably assess host quality (Murdoch et al., 2014). If positive preference–performance relationships occur, they may be expressed in fastest development and highest final body size of offspring on the preferred, most suitable host plant. Flowers or fruits are plant organs that have a decisive influence on reproductive output and crop yield; however, most knowledge on the expression of resistance is available for herbivores feeding on leaves (Kessler & Baldwin, 2002; van Dam, 2009). Much less is known about whether resistance is similarly expressed with respect to flower-feeders (McCall & Irwin, 2006; Oguro & Sakai, 2014) or fruit-feeders (Hern & Dorn, 2002; Whitehead & Poveda, 2011), although such resistance can often be expected in accordance with optimal defence considerations (Stamp, 2003). Among insect herbivores, weevils are particularly speciose and widespread (Hundsdoerfer et al., 2009) and many species play

an important role as pests and biocontrol agents in agricultural and forest systems (Cottrell & Wood, 2008; Stricker & Stiling, 2012; Wainhouse et al., 2014). Florivorous weevils in the genus Anthonomus, including the boll weevil Anthonomus grandis Boh. (Grigolli et al., 2013), the pepper weevil Anthonomus eugenii Cano (Speranza et al., 2014) and the strawberry blossom weevil Anthonomus rubi Herbst (Innocenzi et al., 2001), pose serious threats to their crop host plants. Strong damage by Anthonomus weevils may also occur in wild host plants (Torezan-Silingardi, 2011; Alves-Silva et al., 2015). Despite their economical and ecological importance, knowledge on plant resistance to weevils is lower than to other major groups of pest insects, such as aphids and lepidopterans (Smith, 2005). This lack of information is particularly true for studies on the resistance of perennial woody plants and the combined consideration of the different resistance types, namely plant acceptability (antixenosis) and suitability (antibiosis) for weevils on field-grown plants. To better understand the role of plant genotype on resistance to field populations of weevils in fruit trees, we studied both the preference and performance of the apple blossom weevil Anthonomus pomorum L. (Coleoptera: Curculionidae) on different cultivars of apple Malus × domestica Borkh. in a common field site. Apple is the main host of A. pomorum besides pear Pyrus communis L., and this univoltine herbivore, which attacks flower buds, is considered as the most damaging pest weevil of apple throughout Europe (Blommers, 1994). Post-diapausing adults of A. pomorum colonize apple orchards in early spring from adjacent forests (Hausmann et al., 2004; Dorn & Piñero, 2009). Oviposition occurs into closed flower buds, and feeding by weevil larvae kills the developing flower and causes characteristic brown ‘capped blossoms’. The vulnerable bud stage is restricted to a short window in time before flower opening (Toepfer et al., 2002), although it may occur at slightly different times for different apple cultivars depending on the cultivar’s flowering period. Based on their flowering time, we assume that different apple cultivars might be differently vulnerable to host searching female A. pomorum and that different cultivars might harbour weevil larvae that differ slightly in their developmental status. Reports of variable field infestation of different apple cultivars by A. pomorum led to the assumption that flower buds of different apple cultivars might differ in their susceptibility to A. pomorum (Kalinova et al., 2000; Mody et al., 2011). To our knowledge, the suitability of flower buds from different cultivars has not yet been studied directly. However, differences in both size and the sex ratio for parasitoids emerging from weevils from different cultivars strongly suggest that weevils developing in flower buds from different apple cultivars vary in characteristics (e.g. body size) that may affect parasitoid performance (Mody et al., 2012). Specifically, we assessed field infestation of five different apple cultivars by A. pomorum as a putative measure of florivore preference, and the mass and emergence time of A. pomorum developing on five different apple cultivars as measures of florivore performance. The assessment of weevils at different collection dates additionally aimed to answer methodological questions on the optimized sampling of herbivores characterized by a very restricted feeding period.

© 2015 The Royal Entomological Society, Agricultural and Forest Entomology, 17, 337–346

Cultivar-related resistance to insect florivores 339 Table 1 Background information on studied apple cultivars and on infesting Anthonomus pomorum weevils

Cultivar

BBCH stage/flowering timea

Sample size (number of trees)

Total flower number per sample

Total weevils recorded

Total weevils sexed and weighed

Julia Florina Discovery Retina Ariwa Rewena

51/early1,2 40/mid-late3 45/early1 47/mid-early2,4 40/mid-late4 NA/late3

10 20 20 20 20 20

5947 31 879 35 500 21 167 9352 Estimatedb

12 334 487 299 193 141

8 151 272 146 118 88

a

Indicators for cultivar phenology: BBCH (Meier, 2001) stage: bud development stage at the beginning of tree colonization by the weevil, as assessed at the trial site in the year prior to the reported study (U. Steiner, S. Dorn and K. Mody, unpublished data); flowering time: 1 Paprštein & Blazek (1996); 2 Mody et al. (2011); 3 Bodor & Toth (2008); 4 Kellerhals et al. (2003). NA, not available. b Total flower number (qualitatively assessed) comparable to that of Florina and Discovery.

Materials and methods

Sampling of infested flower buds

Study site

Development of weevils inside the flower buds was monitored regularly by examination of control samples of infested buds from end of April onwards. To assess pupation rate, at each examination, 25–30 capped blossoms (unopened flower buds with brownish, dead petals) from trees of different cultivars were opened and inspected visually but not included in the further analysis. Three time points (collections) were chosen for sampling of infested buds according to the approximate average proportion (based on control samples from all cultivars, excluding study tree individuals) of weevils that had reached the pupal stage at that time (collection 1: 50%, 3 May; collection 2: 75%, 7 May; collection 3: 95%, 14 May). On each sampling date, a third of the total of capped blossoms from each tree was picked, resulting in the complete removal of all infested flowers on sampling date 3. Capped blossoms picked at collections 1 and 2 were chosen to be equally distributed over the tree. Capped blossoms of each tree and sampling date were kept in Petri dishes (diameter 14 cm) laid out with a circular filter paper and with the lid secured by rubber bands. Filter papers were exchanged regularly to reduce humidity. Petri dishes were kept under outside conditions but protected from frost and direct sunshine.

The present study was conducted in an organic apple orchard in Steinmaur (47∘ 29’N, 8∘ 26’E, elevation 453 m, Northern Switzerland). Studied trees were dwarf trees (height 2.0–3.5 m; age 6–18 years) of the cultivars Julia, Florina, Discovery, Retina, Ariwa and Rewena, which were grafted on M9 rootstocks. Details on cultivars are provided in Table 1. The cultivar Rewena was used as a fifth study cultivar to replace the cultivar Julia, which, during the first sampling of infested buds (see below), showed a weevil infestation that was too low to allow further analyses. The studied trees grew in rows at a spacing of 4 × 2.5 m within a 0.7-ha block of dwarf trees that was surrounded by grassy strips. In the vicinity of the studied orchard block, there were solitary high stem trees, hedgerows and high stem orchards occupying an area of 9 ha. One row containing 10 of the studied Discovery trees was an edge row; all other rows lay within the plot. To confirm that a potentially higher infestation of edge rows by tree-colonizing A. pomorum (Brown et al., 1993; Toepfer et al., 2002) did not confound our findings in the present study, we compared the infestation of Discovery by A. pomorum between the edge row and the row within the plot, and no difference was detected (analysis of deviance; F 1,18 = 0.35, P = 0.560; for a description of the assessment of infestation, see below). The next spinney, as a possible alternative winter habitat for A. pomorum (Brown et al., 1993; Toepfer et al., 1999), was 150 m away. All trees were treated with Myco-San (aluminium sulphate) (Andermatt Biocontrol AG, Switzerland), a fungicide approved for organic production in Switzerland. No insecticides were applied during the study period.

Number of flowers The number of flowers on the studied trees was assessed by end of April (except for Rewena trees, for which the flower number was not assessed because flower development had progressed too far to allow accurate flower counting at the time when trees were included in the study as replacement for Julia trees). The number of flower clusters per tree was counted and multiplied with an average number of flowers per cluster, retrieved as the average flower number of 30 separate clusters from each cultivar.

Weevil characteristics Petri dishes containing the capped blossoms were examined for the presence of freshly emerged A. pomorum weevils at 24-h intervals. All the weevils were removed from the Petri dishes on the day of emergence and immediately deep-frozen in Eppendorf tubes. Emergence was monitored from collection until no more insects had emerged for five consecutive days. The date of weevil emergence was determined as the number of days after the first weevil emerged from the collected capped blossoms. A proportion of the weevils inside the capped blossoms was parasitized by solitary hymenopteran parasitoids (data reported elsewhere), which emerged from the capped blossoms instead of weevils. Numbers of these parasitoids were added to the weevil numbers to assess total infestation. All remaining capped blossoms were dissected by the end of insect emergence, and weevils that were not fully developed and parasitoids were counted. Properly emerged weevils were dried at 40 ∘ C to mass constancy and weighed as a proxy of size (AB 204 high precision


340

K. Mody et al.

scale; Mettler Toledo, Switzerland). Sex was determined for the same weevils as described by Duan et al. (1999).

Statistical analysis Proportion data (sex ratio; tree infestation) were modelled using generalized linear models (GLM) with binomial errors, either by analysis of deviance (categorical explanatory variable: effects of tree cultivar) or by analysis of covariance [continuous and categorical explanatory variables: combined effects of tree cultivar, tree position (determined as the number of trees between studied tree and edge of row) and flower number]. Because data were overdispersed (residual deviance > 1.2 times greater than residual degrees of freedom), a quasibinomial error distribution was used (Crawley, 2007). Weevil mass and emergence were modelled by mixed linear models, with average weevil mass and emergence date (log-transformed to meet requirements of mixed models) per tree and collection as dependent variables, tree cultivar, collection date and weevil sex as fixed factors and individual tree identity as a random factor. The Benjamini–Hochberg correction for type I errors (false discovery rate control) was applied for multiple tests GLM and mixed models (Verhoeven et al., 2005). Statistical analyses were performed with r, version 2.13.0 (R Foundation for Statistical Computing, Austria) and SPSS, version 20.0 (IBM Corp., Armonk, New York).

Results Flower infestation Percent infestation by A. pomorum varied significantly between apple cultivars (analysis of deviance; F 4,89 = 7.14, P < 0.001) and was not affected by tree position in rows or flower number (cultivar: F 4,89 = 7.36, P < 0.001; tree position: F 1,89 = 2.98, P = 0.088; flower number: F 1,89 = 1.58, P = 0.212). Percentage infestation was lowest in Julia, followed by Florina, and highest in Ariwa, Discovery and Retina (Fig. 1). The total number of infested flowers (capped blossoms) differed significantly between apple cultivars and between collection dates (Table 2). It was significantly higher at the first

Percent infested flowers

2.5

a

b

c

c

c

Julia

Florina

Discovery

Retina

Ariwa

2.0

1.5

1.0

0.5

collection date than at subsequent collection dates (Fig. 2). Interaction effects between collection date and cultivar were also significant (Table 2). Consideration of flower number demonstrated that differences in the number of infested flowers between cultivars were mainly a result of differing numbers of flowers in the different apple cultivars (Tables 1 and 2).

Weevil size and sex ratio The size of A. pomorum differed between female and male weevils, with females being significantly heavier than male weevils (female: 1.27 mg ± 0.02, male: 1.15 mg ± 0.02) (Table 3). The difference in mass between females and males was most expressed in Rewena (females 17.5% heavier than males) and least expressed in Retina (females 6.4% heavier) (Fig. 3). The sex ratio of A. pomorum emerging from the studied apple cultivars was balanced (0.51 ± 0.02 mean female proportion). It was not affected by apple cultivar (analysis of deviance; F 4,90 = 1.47, P = 0.220). By contrast to sex ratio, the mass of male and female weevils strongly differed between weevils originating from different apple cultivars (Table 3). Weevils emerging from the apple cultivars Discovery, Retina and Ariwa were significantly heavier than weevils that stemmed from the cultivars Florina and Rewena (Fig. 3). Weevils from Rewena were significantly smaller than beetles from all other cultivars (Fig. 3). The average mass of weevils from Ariwa (i.e. the apple cultivar that produced the heaviest weevils) was 39.9% higher than the mass of weevils from Rewena. No influence of collection date on weevil mass was found (Table 3).

Weevil emergence The emergence of weevils from capped blossoms differed significantly between females and males, and between weevils from different apple cultivars (Table 3). Average emergence was earlier for females than for males in all studied apple cultivars except for Florina (Table 4). Weevils from Rewena showed the latest emergence; weevils from Florina and Discovery showed intermediate emergence; and weevils from Ariwa and Retina showed the earliest emergence (Tables 3 and 4). Weevils from Rewena emerged in average 5.1 days later than weevils from Ariwa. Besides cultivar, collection date strongly influenced weevil emergence, with beetles from the first collection date emerging significantly earlier than weevils sampled at the second and third collection dates. Weevils sampled at the third collection date emerged significantly later than all other weevils (Tables 3 and 4). Collection date did not change the effects of cultivar on weevil emergence (interaction between cultivar and collection not significant) (Table 3).

0

Figure 1 Infestation of apple flower buds by Anthonomus pomorum. Different lowercase letters (a, b, c) indicate significant differences (analysis of deviance with proportion data; post-hoc P < 0.05; false discovery rate control). For the number of trees and total number of flowers, see Table 1.

Discussion The findings of the present study on the resistance of apple Malus × domestica to the florivorous apple blossom weevil A. pomorum demonstrate that apple cultivars differ both in susceptibility to weevils in the field, as indicated by differences


Cultivar-related resistance to insect florivores 341 Table 2 Effectsa of apple cultivar and collection date on tree infestation (numbers of capped blossoms) without consideration of total flower number per tree and with consideration of flower number as covariate (cultivar Rewena not included) Source

Numerator d.f.

Without consideration of total flower number Cultivar 4 Collection 2 Cultivar × Collection 8 With consideration of total flower number Cultivar 3 Collection 2 Cultivar × Collection 6 Flowers 1

Denominator d.f.

F

P

Post-hoc

87.0 175.7 175.4

7.58 15.45 7.96

< 0.001 < 0.001 < 0.001

Da > Rtb , Fb ≥ Abc , Rwc C1a > C2b , C3b —

70.7 143.1 143.0 70.4

2.89 22.08 6.85 41.19

0.042 < 0.001 < 0.001 < 0.001

No differences after FDR C1a > C2b , C3b — —

Number infested flowers per tree

a Analyzed by mixed model analyses with ‘cultivar’ and ‘collection’ as fixed factors (random factor: tree ID); significant models (P values in bold) were followed by least significant difference post-hoc tests, to which false discovery rate (FDR) correction (Verhoeven et al., 2005) was applied. Contrasting superscript letters a,b,c refer to significant differences in the post-hoc tests for the respective factors ‘cultivar’ and ‘collection’. Significant differences are highlighted in bold. D, Discovery; Rt, Retina; A, Ariwa; F, Florina; Rw, Rewena; collection: C1–C3 = collections 1–3.

20 Collection 1 a 16

Collection 2 b Collection 3 b

12 8 4 0 Florina

Discovery

Retina

Ariwa

Rewena

Figure 2 Number of infested flowers (capped blossoms) per tree (mean ± SE) sampled at different collection dates. At collection 1, every third capped blossom was collected; at collection 2, every second capped blossom was collected and, at collection 3, every remaining capped blossom was collected. Different lowercase letters (a, b) indicate significant differences between collection dates (mixed model, least significant difference post-hoc P < 0.05; false discovery rate control). For the number of trees and total number of flowers, see Table 1.

in flower infestation, and in suitability to weevils developing in the flower buds, as shown by differences in weevil mass and emergence time. The present study thereby emphasizes that resistance by antixenosis, as well as resistance by antibiosis, may be affected by plant genotype in apple. The finding that the number of infested flowers changed with collection date in a cultivar-specific way indicates that differing responses of apple genotypes to flower infestation may occur, and that the infestation of flowers may depend on the flowering period and duration. In an applied context, the finding of date-dependent infestation levels advises the need for caution for monitoring schemes in that the relative infestation rate may be over- or underestimated by one-time assessment of herbivore load depending on plant genotype (i.e. the apple cultivar). The present study provides further evidence that different apple cultivars are differentially infested by A. pomorum (Kalinova et al., 2000; Mody et al., 2011) and also it indicates that the interactions between apple and A. pomorum are possibly affected by different resistance mechanisms, such as decreased acceptability or attractiveness (antixenosis resistance) and decreased suitability (antibiosis resistance). Regarding the increased escape of

distinct cultivars from infestation by A. pomorum as a result of a lack of synchronization, we found no convincing evidence that early or late flowering cultivars can predictably escape from this herbivore. Although very early flowering, as observed in cultivar Julia, may contribute to reduced infestation, there were significantly diverging infestation levels among the two early (Julia and Discovery) and the two relatively late flowering cultivars (Florina and Ariwa), with high as well as moderate or low infestation levels occurring in each of these phenological host categories. Differences in infestation are thus probably more strongly mediated by preference behaviour of host searching female A. pomorum. Thus, an understanding of the observed patterns, and, finally, an identification of apple traits that may be used for breeding less susceptible apple cultivars, should focus on plant traits that might guide females in search of their host. Because A. pomorum attacks flower buds at certain developmental stages (Toepfer et al., 2002), the traits of flower buds are particularly promising for explaining the observed differences in the susceptibility of different apple cultivars. As a particularly promising trait mediating the preference of host-searching females, volatile chemicals have been described; they differ among apple cultivars (Kalinova et al., 2000; Hern & Dorn, 2003) and may provide leading cues for females in search of a suitable oviposition site (Piskorski & Dorn, 2010; Collatz & Dorn, 2013). Becausee no information on the volatile profiles of the apple cultivars covered in the present study is available, we cannot relate the detected infestation patterns to any difference in volatile emission from the studied apple cultivars. Besides chemical plant characteristics, the physical properties of plant organs may also play an important role for plant resistance (McCall & Irwin, 2006; Carmona et al., 2011). The flower buds may, for example, differ in size, the physical strength of bud scales and in the hairiness of the bud (Bandeili & Müller, 2010; Panzavolta et al., 2012). Because we do not have information on physical properties such as strength or hairiness, the potential role of those characteristics for apple resistance to florivores is to be addressed by future studies. Independent of the underlying characteristics, the relative susceptibility of apple cultivars to infestation by A. pomorum might be relatively stable across different years that are characterized by differing environmental conditions. This assumption


342

K. Mody et al.

Table 3 Effectsa of apple cultivar, collection date and sex on mass and emergence of Anthonomus pomorum Source Mass Cultivar Collection Sex Cultivar × Collection Cultivar × Sex Coll × Sex Cultivar × Collection × Sex Emergence Cultivar Collection Sex Cultivar × Collection Cultivar × Sex Coll × Sex Cultivar × Collection × Sex

Numerator d.f.

Denominator d.f.

F

P

Post-hoc

4 2 1 8 4 2 8

79.5 268.6 261.2 267.2 261.1 260.0 259.0

24.10 0.52 30.60 1.85 0.52 0.12 0.55

< 0.001 0.595 < 0.001 0.068 0.724 0.886 0.818

Da , Rta , Aa > Fb > Rwc — F>M — — — —

4 2 1 8 4 2 8

63.4 276.5 259.2 272.9 259.8 259.6 258.9

24.91 36.25 6.67 1.64 1.46 0.15 3.08

< 0.001 < 0.001 0.010 0.114 0.214 0.858 0.002

Rwa > Fb , Db > Rtc , Ac C1a > C2b > C3c M>F — — — —

a

Analyzed by mixed model analyses with ‘cultivar’, ‘collection’ and ‘sex’ as fixed factors (random factor: tree ID); Significant models (P values in bold) were followed by least significant difference post-hoc tests, to which false discovery rate correction (Verhoeven et al., 2005) was applied. Emergence determined as the number of days after emergence of first weevil. Contrasting superscript letters a,b,c refer to significant differences in the post-hoc tests for the respective factors ‘cultivar’, ‘collection’ and ‘sex’. Significant differences are highlighted in bold. D, Discovery; Rt, Retina; A, Ariwa; F, Florina; Rw, Rewena; collection: C1–C3 = collections 1–3; M, male; F, female.

1.6

b

a

a

a

c

Weevil dry mass (mg)

1.4

Males Females

1.2 1.0 0.8 0.6 0.4 0.2 0 Florina Discovery

Retina

Ariwa

Rewena

Figure 3 Dry mass (mean ± SE) of male and female Anthonomus pomorum on different apple cultivars. Significant differences in weevil mass between cultivars are indicated by different lowercase letters (a, b, c) (mixed model, least significant difference post-hoc P < 0.05; false discovery rate control). For the number of A. pomorum, see Table 4.

is supported by the observation that the cultivar Julia was least infested in the present study, as well as in an independent study conducted in a different year and in a different orchard (Julia less infested than cultivars Retina and Nela; Mody et al., 2011). By contrast to variation in susceptibility to attack by A. pomorum, we are not aware of any studies that had addressed the suitability of flowers of different apple cultivars for A. pomorum development. The finding in the present study that weevils developing in different apple cultivars show marked differences in mass, as well as in emergence time, now provides clear evidence that the flowers from different apple cultivars differ in suitability for the weevils. This finding is in line with previous indirect evidence gained from parasitoid wasps, which differed in body size when emerging from A. pomorum weevils that had

fed on different apple cultivars (Mody et al., 2012). To better understand the observed patterns of host plant suitability for the herbivore, information on flower characteristics relevant to florivores is needed. Flowers may not only differ conspecifically in size and nutrient composition, but also in defensive chemical and physical properties (Herrera, 2009; Tsuchimatsu et al., 2014). For apple flowers, this information is limited, although there is some evidence of differences among cultivars in flower size (Schneider et al., 2004; Mody et al., 2011), nectar composition (Toth et al., 2003; Farkas et al., 2012) and stigma characteristics (Farkas et al., 2012). Larger flower buds might provide more resources to florivores and thereby enhance growth of the herbivore. For the studied system, however, such resource quantity does not appear to be the decisive determinant of weevil performance because buds from suitable cultivars might be large (Retina; Mody et al., 2011) or small (Ariwa; U. Steiner, S. Dorn and K. Mody, unpublished data). Hence, it is likely to be resource quality that substantially contributes to host suitability for the developing herbivore. Although we do not have information on defensive or nutritional traits of flower buds of the different apple cultivars, other studies show that variability in defensive and nutritional values exists within plant species (Gols et al., 2008; Gutbrodt et al., 2012b; Moore et al., 2014) and that flowers are differentially attacked not only across conspecific plants, but also within plants (Kovach et al., 1999; Herrera, 2009). Preference–performance relationships are regularly expected, although they are not necessarily detected in nature. A determining factor appears to be diet breadth because polyphagous species are less likely to be choosy compared with oligophagous species (Gripenberg et al., 2010). This difference arises from imperfect adaptations, imperfect decisions and a prolonged decision time in species with a broader host range (Bernays, 2001). By revealing that a cultivar showing relatively low infestation (Florina) was also less suitable than other more preferred


Cultivar-related resistance to insect florivores 343 Table 4 Day of emergence (mean ± SE; number of days after emergence of first weevil) of male (M) and female (F) Anthonomus pomorum collected at three different dates from different apple cultivars Cultivar

Sex (n)

Collection 1

Collection 2

Collection 3

Total average

Florina

M (72) F (79) M (127) F (145) M (64) F (82) M (58) F (60) M (51) F (37)

4.25 (0.31) 5.20 (0.38) 4.06 (0.17) 4.16 (0.16) 3.91 (0.46) 2.89 (0.17) 4.14 (0.30) 3.64 (0.32) 7.36 (0.68) 6.17 (0.53)

5.96 (0.30) 6.67 (0.55) 5.42 (0.32) 5.65 (0.31) 4.48 (0.34) 5.24 (0.42) 4.71 (0.21) 3.56 (0.35) 8.65 (0.69) 6.44 (0.87)

6.46 (0.52) 6.24 (0.45) 7.31 (0.83) 5.61 (0.37) 7.56 (0.98) 5.69 (0.50) 5.33 (0.50) 6.00 (0.46) 9.58 (0.38) 9.38 (0.29)

5.67 (0.25) 5.97 (0.27) 4.65 (0.18) 4.61 (0.15) 5.14 (0.39) 4.61 (0.26) 4.62 (0.18) 4.17 (0.25) 8.31 (0.40) 7.62 (0.39)

Discovery Retina Ariwa Rewena

cultivars (Ariwa, Retina, Discovery), the present study suggests that preference–performance relationships may play a role in apple infestation by the oligophagous species A. pomorum. Emergence time was used as another indicator of weevil performance. Because the time of oviposition was not precisely known, the developmental time was not directly determinable. However, because oviposition depends on bud development (Toepfer et al., 2002), the onset of flowering appears to be a meaningful proxy for establishing a sequence of oviposition for the studied apple cultivars. Accordingly, earliest oviposition would be expected to occur on Julia (marginally infested) and Discovery, followed by (and in the sequence) Retina, Florina, Ariwa and Rewena. Assuming a similar developmental time, emergence of adult weevils would be expected in the same sequence, starting with Julia and Discovery and ending with Ariwa and Rewena. Because this was not the case, with the earliest emergence being from late flowering Ariwa and mid-early Retina, we conclude that the developmental rate of A. pomorum differs between apple cultivars, indictaing that Ariwa and Retina are the cultivars favouring fast development. In combination with the observed highest growth performance (highest body mass) on the same cultivars, the clear difference in suitability of the different cultivars is emphasized. The finding that the cultivar Florina was relatively more resistant than most other cultivars covered in the present study is in accordance with reports of high resistance of this cultivar to other pest insects such as aphids (Rat-Morris, 1994; Qubbaj et al., 2005; Dapena et al., 2009), and particularly also to fungal and bacterial diseases such as apple scab Venturia inaequalis Wint. and fire blight Erwinia amylovora Winslow (Le Roux et al., 2010; Slatnar et al., 2012). It thereby emphasizes the need and possible opportunities for a better understanding of the basis of plant resistance to multiple biotic stresses (Stoeckli et al., 2008; Smith & Clement, 2012; Seifi et al., 2013). For many insects, shifts in sexual size dimorphism (SSD) and in sex ratio can be observed as a consequence of variation in resource quality. The effects of resource quality on SSD are particularly found for species with larger females (female-biased SSD) because female size is generally more sensitive to environmental variation than male size (Teder & Tammaru, 2005). In the present study, we found a pronounced female-biased SSD but no positive response of female-biased SSD to increasing resource quality as represented by flowers from different apple cultivars.

By contrast, we found female-biased SSD to be strongest for weevils emerging from Rewena, the poorest host cultivar. This finding indicates that male growth may be even more strongly constrained by poor host quality than female growth in the florivorous A. pomorum. The finding of a balanced sex ratio demonstrates that, for A. pomorum, variable resource quality is not leading to sex-biased developmental mortality, which otherwise might reflect differing tolerance of sexes to a given environment (Carriere, 2003; Kapranas et al., 2011). A biased sex ratio as a result of sex ratio adjustment by females (West & Sheldon, 2002; Uller et al., 2007), which is often found in insects with haplodiploid sex determination, was not expected to occur in the weevil A. pomorum with a chromosomal sex determination system (Kageyama et al., 2012). Repeated sampling of infested flowers revealed that the number of infested flowers was not stable across the sampling period and that the changes in the number of infested flowers were not consistent in the different apple cultivars. Although the numbers of infested flowers remained relatively constant in Florina and Ariwa, they strongly decreased from the first to the third sampling in Retina and Discovery. By contrast, in Rewena, the highest numbers of infested flowers were found in the last sampling. This strong influence of sampling date on the number and constancy of infested flowers indicates that the flowering period may affect the occurrence of infested flowers at a given time and it also suggests that different cultivars may differently respond to flower infestation, with abortion of infested flowers in a cultivar-specific way (particularly in Discovery, where a large number of fallen capped blossoms was observed; J. Collatz, personal observation) (Stephenson, 1981). In conclusion, the present study contributes to our understanding of how plant genotype affects plant resistance to florivores, a group of herbivores that has been rarely studied in the context of plant resistance (McCall & Irwin, 2006; Hanley et al., 2009). By demonstrating that the performance and possibly also the preference of the florivorous weevil A. pomorum differ among apple cultivars, the present study may help to identify plant traits that should be studied more intensively to better understand tree resistance to florivores. Such information on tree characteristics that contribute to tree resistance to florivores may be used for breeding resistant fruit tree cultivars (Stoeckli et al., 2009; Kumar et al., 2012) and for interfering with herbivore population development (Greenberg et al., 2005). Because the detected


344

K. Mody et al.

differences in performance of florivores developing on different cultivars may also affect natural enemies of the florivores such as parasitoids (Hardy & Ode, 2007; Mody et al., 2012), our findings support other studies that highlight the need to consider combined bottom-up and top-down approaches for increasing sustainability in orchards (Zehnder et al., 2007; Simon et al., 2010).

Acknowledgements We thank Ursula Steiner for assessments of flower characteristics; Valery Knoll for help with data collection, weighing weevils and weevil sex determination; Hans Brunner for his support and for the permission to work in his orchard; and Helena Maura Torezan-Silingardi and two anonymous reviewers for their constructive comments on the manuscript.

References Alves-Silva, E., Bächtold, A., Barônio, G.J., Torezan-Silingardi, H.M. & Del-Claro, K. (2015) Ant–herbivore interactions in an extrafloral nectaried plant: are ants good plant guards against curculionid beetles? Journal of Natural History, 49, 841–851. Ballhorn, D.J., Kautz, S., Jensen, M., Schmitt, I., Heil, M. & Hegeman, A.D. (2011) Genetic and environmental interactions determine plant defences against herbivores. Journal of Ecology, 99, 313–326. Bandeili, B. & Müller, C. (2010) Folivory versus florivory-adaptiveness of flower feeding. Naturwissenschaften, 97, 79–88. Bangert, R.K., Allan, G.J., Turek, R.J. et al. (2006) From genes to geography: a genetic similarity rule for arthropod community structure at multiple geographic scales. Molecular Ecology, 15, 4215–4228. Bernays, E.A. (2001) Neural limitations in phytophagous insects: implications for diet breadth and evolution of host affiliation. Annual Review of Entomology, 46, 703–727. Blommers, L.H.M. (1994) Integrated pest management in European apple orchards. Annual Review of Entomology, 39, 213–241. Bodor, P. & Toth, M. (2008) Floral phenology and fruit set investigation of scab resistant apple varieties in Hungary 2007–2008. Bulletin of University of Agricultural Sciences & Veterinary – Horticulture, 65, 242–247. Boege, K. & Marquis, R.J. (2005) Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends in Ecology and Evolution, 20, 441–448. Brown, M.W., Szentkiralyi, F. & Kozar, F. (1993) Spatial and temporal variation of apple blossom weevil populations (Col., Curculionidae) with recommendations for sampling. Journal of Applied Entomology, 115, 8–13. Carmona, D., Lajeunesse, M.J. & Johnson, M.T.J. (2011) Plant traits that predict resistance to herbivores. Functional Ecology, 25, 358–367. Carriere, Y. (2003) Haplodiploidy, sex, and the evolution of pesticide resistance. Journal of Economic Entomology, 96, 1626–1640. Clark, K.E., Hartley, S.E., Brennan, R.M., MacKenzie, K. & Johnson, S.N. (2012) Oviposition and feeding behaviour by the vine weevil Otiorhynchus sulcatus on red raspberry: effects of cultivars and plant nutritional status. Agricultural and Forest Entomology, 14, 157–163. Collatz, J. & Dorn, S. (2013) A host-plant-derived volatile blend to attract the apple blossom weevil Anthonomus pomorum – the essential volatiles include a repellent constituent. Pest Management Science, 69, 1092–1098. Costes, E., Lauri, P.E., Simon, S. & Andrieu, B. (2013) Plant architecture, its diversity and manipulation in agronomic conditions, in relation with pest and pathogen attacks. European Journal of Plant Pathology, 135, 455–470.

Cottrell, T.E. & Wood, B.W. (2008) Movement of adult pecan weevils Curculio caryae within pecan orchards. Agricultural and Forest Entomology, 10, 363–373. Crawley, M.J. (2007) The R Book. John Wiley & Sons, Chichester, U.K. van Dam, N.M. (2009) Belowground herbivory and plant defenses. Annual Review of Ecology, Evolution, and Systematics, 40, 373–391. Dapena, E., Minarro, M. & Blazquez, M.D. (2009) Evaluation of the resistance to the rosy apple aphid using a genetic marker. Acta Horticulturae, 814, 787–790. Dorn, S. & Piñero, J. (2009) How do key tree-fruit pests detect and colonize their hosts: mechanisms and application for IPM. Biorational Tree-Fruit Pest Management (ed. by M. Aluja, T. C. Leskey and C. Vincent), pp. 85–109. CABI Publishers, U.K. Duan, J.J., Weber, D.C., Hirs, B.A. & Dorn, S. (1999) A new character for sex differentiation of adults of Anthonomus pomorum L. (Col., Curculionidae). Journal of Applied Entomology Zeitschrift für Angewandte Entomologie, 123, 319–320. Farkas, A., Mihalik, E., Dorgai, L. & Buban, T. (2012) Floral traits affecting fire blight infection and management. Trees-Structure and Function, 26, 47–66. Gols, R., Wagenaar, R., Bukovinszky, T., van Dam, N.M., Dicke, M., Bullock, J.M. & Harvey, J.A. (2008) Genetic variation in defense chemistry in wild cabbages affects herbivores and their endoparasitoids. Ecology, 89, 1616–1626. Greenberg, S.M., Spurgeon, D.W., Sappington, T.W. & Setamou, M. (2005) Size-dependent feeding and reproduction by boll weevil (Coleoptera: Curculionidae). Journal of Economic Entomology, 98, 749–756. Grigolli, J.F.J., de Souza, L.A., Fraga, D.F., Funichello, M. & Busoli, A.C. (2013) Within plant distribution of Anthonomus grandis (Coleoptera: Curculionidae) feeding and oviposition damages in cotton cultivars. Ciencia E Agrotecnologia, 37, 78–84. Gripenberg, S., Mayhew, P.J., Parnell, M. & Roslin, T. (2010) A meta-analysis of preference–performance relationships in phytophagous insects. Ecology Letters, 13, 383–393. Gutbrodt, B., Dorn, S. & Mody, K. (2012a) Drought stress affects constitutive but not induced herbivore resistance in apple plants. Arthropod–Plant Interactions, 6, 171–179. Gutbrodt, B., Dorn, S., Unsicker, S.B. & Mody, K. (2012b) Species-specific responses of herbivores to within-plant and environmentally mediated between-plant variability in plant chemistry. Chemoecology, 22, 101–111. Hanley, M.E., Lamont, B.B. & Armbruster, W.S. (2009) Pollination and plant defence traits co-vary in Western Australian Hakeas. New Phytologist, 182, 251–260. Hardy, I.C.W. & Ode, P.J. (2007) Why biocontrol practitioners should be more interested in parasitoid sex ratios. Biocontrol News and Information, 28, 49–51. Hausmann, C., Samietz, J. & Dorn, S. (2004) Monitoring the dynamics of orchard colonisation by Anthonomus pomorum in spring. Entomologia Experimentalis et Applicata, 110, 207–216. Henery, M.L. (2011) The constraints of selecting for insect resistance in plantation trees. Agricultural and Forest Entomology, 13, 111–120. Hern, A. & Dorn, S. (2002) Induction of volatile emissions from ripening apple fruits infested with Cydia pomonella and the attraction of adult females. Entomologia Experimentalis et Applicata, 102, 145–151. Hern, A. & Dorn, S. (2003) Monitoring seasonal variation in apple fruit volatile emissions in situ using solid-phase microextraction. Phytochemical Analysis, 14, 232–240. Herrera, C.M. (2009) Multiplicity in Unity: Plant Subindividual Variation and Interactions with Herbivores. University of Chicago Press, Chicago, Illinois. Hicks, B.J., Leather, S.R. & Watt, A.D. (2008) Changing dynamics of the pine beauty moth (Panolis flammea) in Britain: the loss of enemy free space? Agricultural and Forest Entomology, 10, 263–271.


Cultivar-related resistance to insect florivores 345 Hundsdoerfer, A.K., Rheinheimer, J. & Wink, M. (2009) Towards the phylogeny of the Curculionoidea (Coleoptera): reconstructions from mitochondrial and nuclear ribosomal DNA sequences. Zoologischer Anzeiger, 248, 9–31. Innocenzi, P.J., Hall, D.R. & Cross, J.V. (2001) Components of male aggregation pheromone of strawberry blossom weevil, Anthonomus rubi Herbst (Coleoptera: Curculionidae). Journal of Chemical Ecology, 27, 1203–1218. Johnson, M.T.J. & Agrawal, A.A. (2005) Plant genotype and environment interact to shape a diverse arthropod community on evening primrose (Oenothera biennis). Ecology, 86, 874–885. Kageyama, D., Narita, S. & Watanabe, M. (2012) Insect sex determination manipulated by their endosymbionts: incidences, mechanisms and implications. Insects, 3, 161–199. Kalinova, B., Stransky, K., Harmatha, J., Ctvrtecka, R. & Zd’arek, J. (2000) Can chemical cues from blossom buds influence cultivar preference in the apple blossom weevil (Anthonomus pomorum)? Entomologia Experimentalis et Applicata, 95, 47–52. Kapranas, A., Hardy, I.C.W., Morse, J.G. & Luck, R.F. (2011) Parasitoid developmental mortality in the field: patterns, causes and consequences for sex ratio and virginity. Journal of Animal Ecology, 80, 192–203. Karban, R. & Baldwin, I.T. (1997) Induced Responses to Herbivory. University of Chicago Press, Chicago, Illinois. Kellerhals, M., Angstl, J. & Weibel, F. (2003) Porträt schorfresistenter Apfelsorten. Schweizerische Zeitschrift für Obst- und Weinbau, 19, 6–14. Kessler, A. & Baldwin, I.T. (2002) Plant responses to insect herbivory: the emerging molecular analysis. Annual Review of Plant Biology, 53, 299–328. Kogan, M. & Ortman, E.F. (1978) Antixenosis – a new term proposed to define Painter’s ‘nonpreference’ modality of resistance. Bulletin of the Entomological Society of America, 24, 175–176. Kovach, J., Rieckenberg, R., English-Loeb, G. & Pritts, M. (1999) Oviposition patterns of the strawberry bud weevil (Coleoptera: Curculionidae) at two spatial scales and implications for management. Journal of Economic Entomology, 92, 1358–1363. Kumar, S., Bink, M., Volz, R.K., Bus, V.G.M. & Chagne, D. (2012) Towards genomic selection in apple (Malus x domestica Borkh.) breeding programmes: prospects, challenges and strategies. Tree Genetics & Genomes, 8, 1–14. Le Roux, P.M.F., Khan, M.A., Broggini, G.A.L., Duffy, B., Gessler, C. & Patocchi, A. (2010) Mapping of quantitative trait loci for fire blight resistance in the apple cultivars ‘Florina’ and ‘Nova Easygro’. Genome, 53, 710–722. McCall, A.C. & Irwin, R.E. (2006) Florivory: the intersection of pollination and herbivory. Ecology Letters, 9, 1351–1365. Meier, U. (2001) Growth Stages of Mono- and Dicotyledonous Plants. BBCH Monograph. Federal Biological Research Centre for Agriculture and Forestry, Germany. Miller, A.J. & Gross, B.L. (2011) From forest to field: perennial fruit crop domestication. American Journal of Botany, 98, 1389–1414. Minarro, M. & Dapena, E. (2007) Resistance of apple cultivars to Dysaphis plantaginea (Hemiptera: Aphididae): role of tree phenology in infestation avoidance. Environmental Entomology, 36, 1206–1211. Mody, K., Eichenberger, D. & Dorn, S. (2009) Stress magnitude matters: different intensities of intermittent water stress produce non-monotonic resistance responses of host plants to insect herbivores. Ecological Entomology, 34, 133–143. Mody, K., Spoerndli, C. & Dorn, S. (2011) Within-orchard variability of the ecosystem service ‘parasitism’: effects of cultivars, ants and tree location. Basic and Applied Ecology, 12, 456–465. Mody, K., Spoerndli, C. & Dorn, S. (2012) How parasitoid sex ratio, size and emergence time are associated with fruit tree cultivar,

within-orchard tree position and ants. Biological Control, 60, 305–311. Moore, B.D., Andrew, R.L., Külheim, C. & Foley, W.J. (2014) Explaining intraspecific diversity in plant secondary metabolites in an ecological context. New Phytologist, 201, 733–750. Murdoch, G., Clift, A.D. & Mansfield, S. (2014) Adoption of exotic plants by an endemic Australian weevil, Orthorhinus cylindrirostris (Coleoptera: Curculionidae). Environmental Entomology, 43, 1168–1173. Oguro, M. & Sakai, S. (2014) Difference in defense strategy in flower heads and leaves of Asteraceae: multiple-species approach. Oecologia, 174, 227–239. Osier, T.L. & Lindroth, R.L. (2006) Genotype and environment determine allocation to and costs of resistance in quaking aspen. Oecologia, 148, 293–303. Panzavolta, T., Bracalini, M., Croci, F. et al. (2012) Asian chestnut gall wasp in Tuscany: gall characteristics, egg distribution and chestnut cultivar susceptibility. Agricultural and Forest Entomology, 14, 139–145. Paprštein, F. & Blazek, J. (1996) Pollination relations of new apple cultivars. Acta Horticulturae, 423, 135–144. Piskorski, R. & Dorn, S. (2010) Early-season headspace volatiles from apple and their effect on the apple blossom weevil Anthonomus pomorum. Chemistry & Biodiversity, 7, 2254–2260. Plath, M., Dorn, S., Riedel, J., Barrios, H. & Mody, K. (2012) Associational resistance and associational susceptibility: specialist herbivores show contrasting responses to tree stand diversification. Oecologia, 169, 477–487. Qubbaj, T., Reineke, A. & Zebitz, C.P.W. (2005) Molecular interactions between rosy apple aphids, Dysaphis plantaginea, and resistant and susceptible cultivars of its primary host Malus domestica. Entomologia Experimentalis et Applicata, 115, 145–152. Rat-Morris, E. (1994) Analyse des relations entre Dysaphis plantaginea Passerini (Insecta, Auchenorryncha) et sa plante hôte Malus x domestica Borkh.: étude de la résistance du cultivar Florina. Thesis, Université de Tours. Sarfraz, M., Dosdall, L.M. & Keddie, B.A. (2009) Host plant nutritional quality affects the performance of the parasitoid Diadegma insulare. Biological Control, 51, 34–41. Schneider, D., Eisikowitch, D., Goldway, M. & Stern, R.A. (2004) A comparative study of the superior fertility of ‘Smoothee Golden Delicious’ apple. Journal of Horticultural Science & Biotechnology, 79, 596–601. Schoonhoven, L.M., van Loon, J.J.A. & Dicke, M. (2005) Insect–Plant Biology. Oxford University Press, U.K. Seifi, A., Visser, R.G.F. & Bai, Y.L. (2013) How to effectively deploy plant resistances to pests and pathogens in crop breeding. Euphytica, 190, 321–334. Simon, S., Bouvier, J.C., Debras, J.F. & Sauphanor, B. (2010) Biodiversity and pest management in orchard systems. A review. Agronomy for Sustainable Development, 30, 139–152. Slatnar, A., Mikulic-Petkovsek, M., Halbwirth, H., Stampar, F., Stich, K. & Veberic, R. (2012) Polyphenol metabolism of developing apple skin of a scab resistant and a susceptible apple cultivar. Trees-Structure and Function, 26, 109–119. Smith, C.M. (2005) Plant Resistance to Arthropods: Molecular and Conventional Approaches. Springer, The Netherlands. Smith, C.M. & Clement, S.L. (2012) Molecular bases of plant resistance to arthropods. Annual Review of Entomology, 57, 309–328. Speranza, S., Colonnelli, E., Garonna, A.P. & Laudonia, S. (2014) First record of Anthonomus eugenii (Coleoptera: Curculionidae) in Italy. Florida Entomologist, 97, 844–845. Staley, J.T., Stewart-Jones, A., Pope, T.W. et al. (2010) Varying responses of insect herbivores to altered plant chemistry under organic and conventional treatments. Proceedings of the Royal Society Series B, Biological Sciences, 277, 779–786.


346

K. Mody et al.

Stamp, N. (2003) Out of the quagmire of plant defense hypotheses. Quarterly Review of Biology, 78, 23–55. Stephenson, A.G. (1981) Flower and fruit abortion: proximate causes and ultimate functions. Annual Review of Ecology and Systematics, 12, 253–279. Stoeckli, S., Mody, K., Gessler, C., Patocchi, A., Jermini, M. & Dorn, S. (2008) QTL analysis for aphid resistance and growth traits in apple. Tree Genetics & Genomes, 4, 833–847. Stoeckli, S., Mody, K., Patocchi, A., Kellerhals, M. & Dorn, S. (2009) Rust mite resistance in apple assessed by quantitative trait loci analysis. Tree Genetics & Genomes, 5, 257–267. Stoeckli, S., Mody, K., Dorn, S. & Kellerhals, M. (2011) Association between herbivore resistance and fruit quality in apple. Hortscience, 46, 12–15. Strauss, S.Y. & Agrawal, A.A. (1999) The ecology and evolution of plant tolerance to herbivory. Trends in Ecology and Evolution, 14, 179–185. Stricker, K.B. & Stiling, P. (2012) Herbivory by an introduced Asian weevil negatively affects population growth of an invasive Brazilian shrub in Florida. Ecology, 93, 1902–1911. Teder, T. & Tammaru, T. (2005) Sexual size dimorphism within species increases with body size in insects. Oikos, 108, 321–334. Tiffin, P. (2000) Are tolerance, avoidance, and antibiosis evolutionarily and ecologically equivalent responses of plants to herbivores? American Naturalist, 155, 128–138. Toepfer, S., Gu, H. & Dorn, S. (1999) Spring colonisation of orchards by Anthonomus pomorum from adjacent forest borders. Entomologia Experimentalis et Applicata, 93, 131–139. Toepfer, S., Gu, H.N. & Dorn, S. (2002) Phenological analysis of spring colonisation of apple trees by Anthonomus pomorum. Entomologia Experimentalis et Applicata, 103, 151–159. Torezan-Silingardi, H.M. (2011) Predatory behavior of Pachodynerus brevithorax (Hymenoptera: Vespidae, Eumeninae) on endophytic

herbivore beetles in the Brazilian tropical savanna. Sociobiology, 57, 181–189. Toth, E.N., Szabo, L.G., Botz, L. & Orosz-Kovacs, Z. (2003) Effect of rootstocks on floral nectar composition in apple cultivars. Plant Systematics and Evolution, 238, 43–55. Tsuchimatsu, T., Yoshitake, H. & Ito, M. (2014) Herbivore pressure by weevils associated with flower color polymorphism in Geranium thunbergii (Geraniaceae). Journal of Plant Research, 127, 265–273. Uller, T., Pen, I., Wapstra, E., Beukeboom, L.W. & Komdeur, J. (2007) The evolution of sex ratios and sex-determining systems. Trends in Ecology & Evolution, 22, 292–297. Verhoeven, K.J.F., Simonsen, K.L. & McIntyre, L.M. (2005) Implementing false discovery rate control: increasing your power. Oikos, 108, 643–647. Wainhouse, D., Inward, D.J.G. & Morgan, G. (2014) Modelling geographical variation in voltinism of Hylobius abietis under climate change and implications for management. Agricultural and Forest Entomology, 16, 136–146. West, S.A. & Sheldon, B.C. (2002) Constraints in the evolution of sex ratio adjustment. Science, 295, 1685–1688. Whitehead, S.R. & Poveda, K. (2011) Herbivore-induced changes in fruit–frugivore interactions. Journal of Ecology, 99, 964–969. Wojdylo, A., Oszmianski, J. & Laskowski, P. (2008) Polyphenolic compounds and antioxidant activity of new and old apple varieties. Journal of Agricultural and Food Chemistry, 56, 6520–6530. Zehnder, G., Gurr, G.M., Kuhne, S., Wade, M.R., Wratten, S.D. & Wyss, E. (2007) Arthropod pest management in organic crops. Annual Review of Entomology, 52, 57–80. Accepted 4 March 2015 First published online 17 April 2015
