Tri-trophic interactions are resilient to large shifts in precipitation levels in a wheat agroecosystem

Tri-trophic interactions are resilient to large shifts in precipitation levels in a wheat agroecosystem

Agriculture, Ecosystems and Environment 301 (2020) 106981 Contents lists available at ScienceDirect Agriculture, Ecosystems and Environment journal ...

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Agriculture, Ecosystems and Environment 301 (2020) 106981

Contents lists available at ScienceDirect

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Tri-trophic interactions are resilient to large shifts in precipitation levels in a wheat agroecosystem


Tatyana A. Rand*, Debra K. Waters, Robert B. Srygley, David H. Branson United States Department of Agriculture-Agricultural Research Service, Pest Management Research Unit, Northern Plains Agricultural Research Laboratory, 1500 N Central Avenue, Sidney, MT 59270, United States



Keywords: Drought Irrigation Rainfall Herbivory Climate change Biological control Pest regulation Ecosystem services Natural enemies

Changing climatic conditions can fundamentally alter the interactions between species with important implications for agriculture. The impacts of shifts in precipitation on trophic interactions have been understudied relative to other climate drivers. We carried out field experiments to examine how precipitation, attack by parasitoid wasps (Bracon cephi (Gahan))(Hymenoptera: Braconidae) and their potential interaction affect the performance of a major pest of wheat, Cephus cinctus Norton (Hymenoptera: Cephidae), and its impact on wheat yield. We independently manipulated insects (no insects, +C. cinctus, or +C. cinctus and B. cephi) and precipitation (-50% to -70%, ambient, +70%) in a factorial design in each of two growing seasons. Crop-herbivoreparasitoid interactions were remarkably robust to our precipitation manipulations with no significant changes in C. cinctus infestation, survival or levels of parasitism observed in the first (wetter) year of the study. Despite slight declines in pest infestation and percent parasitism under precipitation addition relative to reduction in the second year, both insects had strong and significant impacts on crop yield. These effects were consistent across precipitation manipulations, as evidenced by the lack of a significant interaction between insect and precipitation treatments. The results suggest that natural enemy benefits to crop production in this system can be substantial, and are likely to be robust across a relatively wide range of precipitation levels. While rare, studies that examine climate influences within a tri-trophic context are critical to predicting how pest insects will ultimately impact crop production under changing climatic conditions.

1. Introduction Changing climatic conditions have wide ranging impacts on ecological communities, including fundamentally altering the interactions between species (Kareiva et al., 1993; Tylianakis et al., 2008; Jamieson et al., 2012; Walter, 2018). Such climatically driven shifts in species interactions can have important implications for agriculture, by altering the impact of herbivorous pests on crop plants, or the control of such pests by their natural enemies (Rosenzweig et al., 2001; Cock et al., 2013; Walthall et al., 2013). Understanding these interactions is critical to improving pest risk forecasting in the near-term, as well as guiding the development and implementation of effective pest management strategies under future climate scenarios, all important to building resilient agricultural systems (Rosenzweig et al., 2001; Gregory et al., 2009; Olfert et al., 2019). A majority of studies examining climate impacts on plant-herbivore or predator-prey interactions have focused on temperature and CO2, with precipitation comparatively less studied in this context (e.g., 7 of

98 studies reviewed by Tylianakis et al. (2008). Moreover, most precipitation studies have focused on drought conditions, with few simultaneously examining the influence of increases and decreases in precipitation on species interactions (Walter, 2018). The existing literature suggests that changes in precipitation can fundamentally alter the performance and abundance of insect herbivores, which can in turn influence their impacts on their host plants, including crops (Tylianakis et al., 2008; Walthall et al., 2013; Walter, 2018). However, the direction and magnitude of the influence of precipitation is inconsistent (Tylianakis et al., 2008; Walthall et al., 2013; Walter, 2018), and may depend in part on factors such as herbivore feeding guild and the direction, severity or timing of altered precipitation levels (Huberty and Denno, 2004; Branson, 2017). For example, while dry conditions have historically been associated with insect outbreaks (White, 1984; Rosenzweig et al., 2001), extreme drought can be detrimental to herbivorous crop pests (Criddle, 1922; Johnson et al., 2010). Furthermore, the impact of drought can vary depending on herbivore feeding guild (Huberty and Denno, 2004). Similarly, although wetter conditions are

Corresponding author. E-mail address: [email protected] (T.A. Rand). Received 8 July 2019; Received in revised form 22 April 2020; Accepted 25 April 2020 0167-8809/ Published by Elsevier B.V.

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often found to favor insect herbivores (Shure et al., 1998; Rand, 2013; Leckey et al., 2014; Walter, 2018), negative effects have been observed for some groups (Barnett and Facey, 2016). Climatic impacts on higher trophic levels are rarely examined (Jamieson et al., 2012; Walter, 2018), but a handful of studies have found that herbivore-parasitoid interactions may also shift in response to changes in precipitation (Walter, 2018). Parasitism has been found to increase (Romo and Tylianakis, 2013), decrease (Aslam et al., 2013; Tariq et al., 2013), or remain unchanged (Godfrey et al., 1991; Staley et al., 2007) under drier conditions. Overall, the available literature suggests that both plantherbivore and herbivore-parasitoid interactions can be fundamentally altered by changing precipitation patterns. However, studies which integrate the impacts of altered interactions across multiple trophic levels on crop production are lacking. Here we examine how changes in precipitation affect the tri-trophic interactions between a dominant crop, wheat Triticum aestivum L. (Poaceae); wheat stem sawfly, Cephus cinctus Norton (Hymenoptera: Cephidae), a major wheat pest in the North American Great Plains; and the dominant natural enemy of this pest, the parasitoid wasp, Bracon cephi (Gahan) (Hymenoptera: Cephidae). Water is frequently the dominant factor limiting plant production in the northern Great Plains (Vermeire et al., 2009), including in dryland cropping systems (Hansen et al., 2012; Long et al., 2016). Wheat growing areas across the region experience large differences in precipitation. Precipitation varies both spatially, east to west, and temporally, with frequent fluctuations between drought and non-drought conditions across years (Hansen et al., 2012; Rand et al., 2014). Previous observational work suggests that annual fluctuations in precipitation may have strong influences on C. cinctus performance and impact on wheat (Criddle, 1922; Seamans, 1945; Holmes and Peterson, 1963). As documented for herbivores generally (Huberty and Denno, 2004; Jamieson et al., 2012; Walter, 2018), impacts within this system may be driven by a number of underlying mechanisms, such as direct effects of increased precipitation on insect performance, and indirect effects driven by changes in host plant condition or changes in the effectiveness of natural enemies. Reduced infestation of C. cinctus in wet years is thought to result from adult females laying fewer eggs and moving less because of suboptimal levels of sunshine during the spring (Criddle, 1915). Host plant mediated negative effects may result from larvae drowning when excessive moisture is created inside the wheat stem because of high summer precipitation (Seamans, 1945). Alternatively, mortality or poor condition of host plants during severe droughts can increase larval mortality (Criddle, 1922). More recent spatial studies have shown that crop infestation by C. cinctus declines with increasing annual precipitation from west to east, across Montana, North Dakota and South Dakota (Rand et al., 2014). In conjunction with changing temperatures, precipitation is also predicted to play a role in shifting the range of C. cinctus economic impacts under future climate scenarios (Olfert et al., 2019). Indirect negative effects of precipitation may additionally increase the susceptibility of C. cinctus to its dominant natural enemy, the parasitoid wasp, Bracon cephi. The wheat stem sawfly has a single generation a year, and thus is well synchronized with the wheat growing season. In contrast, B. cephi has two generations a year. Bracon cephi is thought to be negatively affected by hot or dry conditions that cause early maturation of wheat and associated larval hosts, which complete their summer stem-feeding stage before parasitoids can complete their second generation (Holmes et al., 1963; Morrill et al., 1994). However, evidence that parasitoids can attack C. cinctus larvae in their overwintering chambers, which remain after wheat harvest (Rand et al., 2011), suggests that this issue bears further scrutiny. Overall, the available literature suggests that climate, and in particular rainfall, is a major driver of C. cinctus population dynamics and thus potential impact on wheat yield. However, to date, manipulative work examining the effects of precipitation on C. cinctus dynamics is entirely lacking. As such, whether and how changes in precipitation

actually influence C. cinctus performance, attack by natural enemies, and their combined impact on wheat yield remains incompletely understood. As outlined above, this reflects a broader knowledge gap in our understanding of how plant-herbivore-natural enemy dynamics are predicted to shift in response to changes in precipitation more generally (Jamieson et al., 2012; Walter, 2018). In this study, we carried out manipulative field experiments repeated in two years to examine how precipitation, attack by parasitoid wasps, and their potential interactions affect C. cinctus performance and impact on crop yield. We set out to address the following questions: 1.) Do changes in precipitation affect C. cinctus performance in wheat (stem infestation levels, summer and/or overwinter larval survival)? 2.) Do changes in precipitation alter the performance (number of pupal cocoons) or potential impact (percent parasitism) of B. cephi on C. cinctus? 3.) Do changes in precipitation levels alter the impact of C. cinctus on crop yield, either via negative impacts on C. cinctus or by altering the efficacy of B. cephi? 2. Methods 2.1. Study system The study was carried out in the northern Great Plains of North America. The study region is comprised of rangeland, dominated by native cool and warm season grasses, and dryland cropping systems, dominated by wheat, pulse crops (peas and lentils) and oilseed crops (canola). Cephus cinctus is a grass-mining cephid wasp native to North America (Lesieur et al., 2016). It feeds on a large number of native and introduced wild grasses (Cockrell et al., 2017). This insect moved from native grass hosts onto wheat, as wheat became a dominant crop following settlement by Europeans. Damage to wheat occurs both due to yield reductions associated with stem mining, as well as lodging of the wheat just prior to harvest, caused by larval girdling (cutting) of the stem base to form a protected diapause chamber (called a stub) near the soil surface in which they overwinter. Although economic injury levels have not been developed for C. cinctus, management actions are recommended when infestation levels exceed 15% (Knodel et al., 2016). The native parasitoid, Bracon cephi, is the most important insect natural enemy of C. cinctus in wheat (Nelson and Farstad, 1953; Morrill et al., 1998; Meers, 2005). Parasitism can reach high levels and reduce economic damage by C. cinctus (Morrill et al., 1998; Buteler et al., 2008). However, parasitoid populations are highly variable across wheat fields and regions (Shanower and Waters, 2006; Rand et al., 2014). Female parasitoids paralyze, and then lay eggs on or near, larvae of C. cinctus within stems. Larvae develop as ectoparasitoids (Nelson and Farstad, 1953; Holmes et al., 1963). First-generation parasitoids develop rapidly and enter a short pupal stage, adults emerge, and a complete or partial second generation follows (Nelson and Farstad, 1953). Second-generation adult parasitoids may be present from mid-August through lateSeptember (Nelson and Farstad, 1953). Parasitoids overwinter as larvae inside cocoons in wheat stems and stubble. 2.2. Experimental design Manipulative field experiments were done in each of two summer growing seasons, 2015 and 2016. Wheat (the hard red spring wheat variety Reeder) was sown at the USDA -ARS -NPARL experimental farm near Sidney, MT, USA (47°46'15.01"N; 104°14'54.51"W) on 17 April, 2015, and 21 April, 2016. Reeder was chosen because it is the most commonly planted variety in the region and highly susceptible to C. cinctus attack. Cephus cinctus is generally absent from the study site, or occurs there in very low densities. Furthermore, the area seeded for the experiment was not previously planted to wheat, eliminating possible contamination from previous year’s stubble. In each year, six parallel 2

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1.2 × 59.7 m strips of wheat (4-rows each) were planted with a 4-row plot seeder and 30.5 cm row spacing (Fig. S1). Each experimental wheat strip was separated by two, 1.2 m, fill strips. Fill strips were seeded to winter wheat (variety Jerry) in 2015 and left fallow and treated with a pre-emergence herbicide (Trifluralin 10 G, © Loveland Products, Inc.) at a rate of 5.6 kg/ha in 2016. Two 1.2 m fill strips were also seeded on the outer edges of the experimental area (Figure S1). The total experimental area was 24.4 × 59.7 m. Each experimental wheat strip was divided into nine, 6.1 m long sections, including a central 4.9 m experimental area, capped by a 0.6 m alley on each end (Figure S1). Within each experimental area, a 1.2 m section with dense wheat stand development was selected as an experimental plot (for a total of 54 plots). Each wheat plot was enclosed in a cage (Figure S2) consisting of a 1.2 m cube frame of PVC pipe (1.9 cm diameter SCH 40) covered with a skin made up of Lumite© screening (52 × 52 mesh size; 280 μ openings) on 12 June 2015 and 3 June 2016. Cages were fastened to the ground using metal rods, and the bottom buried into the soil (ca. 5 cm) to seal the cages. Cages were left in place for 8–10 weeks until just prior to wheat harvest. Each year, each plot was randomly assigned to one of nine treatments in a completely randomized 3 × 3 factorial design, with six replicates per treatment. We independently manipulated insects and precipitation with three levels each (Figure S1). Insect treatments included control plots with no insects, plots with C. cinctus added, and plots with both C. cinctus and B. cephi added. Precipitation treatments included a 50–70% precipitation reduction, controls with ambient precipitation levels, and ca. 70% precipitation addition (see section 2.3.2).

2.3.2. Precipitation treatments The three precipitation manipulations included precipitation reductions, achieved using passive rainout shelters, controls, exposed to ambient levels of precipitation, and precipitation additions, carried out using a drip irrigation system. Levels of exclusion and addition were chosen to encompass the gradient in precipitation in wheat growing regions from western Montana to eastern North Dakota, across which we had previously documented a strong association between average rainfall and C. cinctus infestation levels (Rand et al., 2014); our experimental site falls at the center of this gradient. Precipitation treatments were initiated in the first week of June in each year and ran until wheat grain ripened (Zadoks development stage 87–92) and plots were harvested 10–12 August 2015, and 15–17 August 2016. In order to examine the potential influence of precipitation on survival of C. cinctus in their overwintering chambers, irrigation treatments were continued through the middle of October in 2016, and resumed from the first week in May through the middle of July in 2017, when C. cinctus had finished emerging. Plots assigned to the precipitation exclusion treatments were covered with passive rainout shelters following Yahdjian and Sala (2002) and Gherardi and Sala (2013). Each rainout shelter consisted of a 2.29 m by 2.49 m (L x W) by 1.67–1.07 m (height, tallest to shortest dimensions) metal frame with v-shaped troughs, 12.7 cm wide, bent at 120° angle attached to the top (Figure S2). Troughs covered 50% and 70% of the surface in 2015 and 2016 respectively. Troughs were made from UV transparent acrylic with > 93% light transmission to minimize any impacts of reductions in UV light on plant growth and plant– insect interactions (Ballare et al., 2011). We increased the severity of the exclusion treatments in 2016, based on weak separation in soil moisture between ambient and exclusion treatments observed in 2015. Gutters were installed to catch the runoff, which drained into a 104 L halfbarrel. Barrels were emptied outside of the experimental area as needed to avoid overflowing. Wheat growth stage was quantified using the Zadoks scale (Zadoks et al., 1974) in each plot weekly from stem elongation through crop maturity. Plots assigned to precipitation addition treatments were irrigated weekly using a drip irrigation system consisting of T-Tape drip-tape (16 mm diameter, 15 mm wall thickness, 1.02 Lph flow rate per emitter; Rivulis Irrigation Inc., Sand Diego, CA, USA) with emitters spaced every 30.5 cm along each of the 4 rows of wheat. Plots were irrigated to increase precipitation 70% above ambient rainfall levels for the week, or above the 10-year average precipitation level for the interval, whichever was highest. This was done to ensure a strong gradient in moisture levels, even in a dry year when augmenting precipitation over ambient levels may have been insufficient. Historical and within season precipitation amounts were obtained from a weather station located at the experimental site ( Control plots were left exposed to ambient levels of precipitation. Percent soil moisture (volumetric water content) was monitored weekly with a soil moisture probe (HydroSense II, Campbell Scientific Inc., Logan UT, USA) with 12 cm rods, using the default calibration for a clay loam soil profile. Weekly monitoring spanned the duration of precipitation treatments, with a slightly delayed start in 2015 (30 June).

2.3. Experimental treatments 2.3.1. Insect treatments Insects, both C. cinctus and parasitoids, were collected from wheat fields near the study site using sweep nets, and added to experimental plots 3–5 times a week over the duration of their 3–4 week emergence period: 16 June to 8 July 2015, and 13 June to 8 July 2016. In 2015 we added 200 female and 200 male C. cinctus to each cage for both C. cinctus addition and B. cephi addition treatments, with the goal of achieving high (economic) levels of infestation by C. cinctus. In B. cephi addition treatments, we also added parasitoids at enemy-prey ratios reflecting a ca. 30% parasitism rate, within the range typically found in the field (Rand et al., 2014); 115 female and 45 males were added to each cage. Sex ratios for both insects were proportional to catches of males and females in the field. Based on very high observed infestation and parasitism levels in the experiment in 2015, we reduced the numbers of insects added to plots in 2016. In that year, 150 male and 150 female C. cinctus, and 65 female and 3 male B. cephi were added to each plot. Parasitoid numbers in 2016 were scaled to reflect more realistic densities on a per area basis, based on the number of insects that would be predicted to emerge per plot assuming an 80% infestation of C. cinctus and a 30% parasitism rate in the previous year. These numbers are again within the range of infestation and parasitism levels observed in the field (Shanower and Waters, 2006; Rand et al., 2014). No insects were added to control treatments. We provided parasitoids with a sugar source, consisting of a gel made of 20 g of sucrose and 20 g of honey mixed with 1 g of agar per 100 mL of water (Tylianakis et al., 2004), to ensure sufficient nutrition for these insects while confined in cages in which they were not able to forage on floral resources. Plastic strips containing three drops of the gel solution were carefully inserted through small zippered openings at the bottom of cages, which ensured insects would not escape. Strips were attached to stakes at mid-canopy height in each B. cephi addition cage and replaced weekly. Equivalent plastic strips, without sugar gel, were attached to stakes in the other two treatments to account for any disturbance associated with this process.

2.3.3. Treatment of unanticipated aphid outbreaks in experimental cages An aphid outbreak occurred within experimental cages in 2015, and was treated 18–21 of July. Only B. cephi remained at the adult stage at this time, all C. cinctus adults had died and larvae are protected within stems. B. cephi adults were removed from cages using aspirators prior to treating. Cage skins were then removed, and the wheat and cage skins were thoroughly sprayed with Bonide® All Seasons Horticultural and Dormant Spray Oil at a concentration of 72.0 mL per 3.78 L of water. This self-emulsifying paraffinic oil smothers insects on contact and has no residual. As soon as the insecticide had dried, cage skins were replaced, and B. cephi were returned to their original cages within 24 h. Coccinellids (48 adult Hippodamia convergens) and Aphidius colemani 3

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aphid parasitoids (2 mL of Aphipar®, Koppert Biological Systems, Howell, MI, USA) were added to each cage to maintain low aphid densities throughout the remainder of the experiment. In 2016, aphids were again noticed in cages, and ca. 50 adult Hippodamia convergens were added weekly to cages to avoid outbreaks from 21 June –15 July. The aphid population began to crash soon after due to wheat senescence and predation. Aphid densities were quantified in each plot prior to treatment in each year by collecting two wheat stems from each of the four rows in each cage, which were returned to the laboratory, where all aphids were counted.

2.5. Statistical analysis Data were analyzed using generalized linear models in JMP version 14.1.0 (JMP®14 1989-2019). Years were analyzed separately due to slightly differing methodologies in each (different insect densities, different rainfall exclusion levels) that made direct comparisons untenable. The influence of precipitation on soil moisture levels was analyzed by taking a mean for each of the two soil moisture measurements per plot in each week, and then averaging this plot level mean over all weeks in which moisture was measured in a given growing season, 2015 or 2016. We additionally analyzed soil moisture levels measured in early Spring of 2017 (7–21 of April), to assess whether precipitation treatment influences persisted despite cessation of treatments overwinter. We ran generalized linear models (normal distribution, identity link) to examine effects of precipitation treatment (fixed factor with 3 levels) on soil moisture (volumetric water content) measured in each period. A similar model was used to examine precipitation influences on wheat growth stage, with the response variable in this case being the Zadoks stage on the last sample date prior to harvest. To test whether aphid densities varied systematically across treatments, we ran generalized linear models (normal distribution, identity link) with predictors including precipitation (3 levels) and insect (3 levels). We ran generalized linear models with a binomial distribution, logit link, to examine the influence of precipitation (3 levels), insect addition (2 levels: C. cinctus only, and C. cinctus plus B. cephi) and the potential interaction between precipitation and insect treatments, on the proportion of C. cinctus infested stems. The same model structure was used to examine treatment effects on the proportion of infested stems that were cut. We ran additional models to examine the effect of precipitation treatments (3 levels) on the proportion of C. cinctus larvae that were parasitized (binomial distribution, logit link) and the number of summer and winter cocoons per plot (Poisson distribution, log link). Yield and grain quality (protein) data were analyzed using generalized linear models (normal distribution, identity link) with predictors including precipitation (3 levels) and insect (3 levels) and their interaction term. Overdispersion tests were used to account for over-dispersed data in all models (SAS Institute Inc, 2019). Following significant, or marginally significant (P < 0.1), overall precipitation or insect treatment effects, we ran contrast tests to compare means among the levels within each treatment when all three treatment levels were included in models.

2.4. Sample collection and processing 2.4.1. Quantifying insect densities, survival and parasitism In order to quantify insect densities, survival, and parasitism levels, all wheat stems and stubs were collected from a randomly selected 25 cm sample of each of the four rows in each plot. Stems were collected just prior to harvest (see section on wheat performance below). For each stem we noted whether it was cut by C. cinctus or not, and then dissected it lengthwise. The number of C. cinctus larvae (dead or alive) was noted for each dissected stem. We calculated two estimates of C. cinctus performance, stem infestation and stem cutting. C. cinctus infestation levels were calculated by dividing the number of C. cinctus infested stems (i.e., those containing any evidence of larvae) by the total number of stems dissected per plot. Stem cutting by C. cinctus (an estimate of proportion of summer larvae surviving to diapause in the cut stem base) was calculated by dividing the total number of stems cut by C. cinctus in each plot, by the number of C. cinctus infested stems per plot. The number of B. cephi parasitoid cocoons (as evidenced by their presence and/or exit holes), which indicate successful parasitism events, was also quantified in each stem. We distinguished the number of summer (thin, delicate cocoon associated with an exit hole) and winter parasitoid cocoons (robust leathery cocoons without exit holes) (Nelson and Farstad, 1953; Wu et al., 2013). Parasitism levels, a measure of potential parasitoid impact on the host pest, were calculated as the total number of parasitoid cocoons divided by the total number of C. cinctus larvae across all sampled stems in each plot. In 2016, we additionally quantified a third C. cinctus performance parameter, larval overwintering survival. To do so, we collected all the wheat stubble in a second randomly selected 25 cm section of each wheat row in each plot that did not overlap the area removed in the previous sample. Samples were collected on 28 July 2017 after the C. cinctus emergence period had ended, and returned to the laboratory for processing. Stubs were separated out from the stubble, and dissected to quantify C. cinctus fate: successful emergence of the insect, or dead larvae or pupa or insect remains inside the stub. Overwintering survival (proportion surviving) was calculated by dividing the number of stubs with successful emergence of C. cinctus, by the total number of stubs collected per plot in 2017 samples.

3. Results Precipitation levels during the wheat growing season (May-August) at the study site were higher in 2015, 19.7 cm, compared with 2016, 14.7 cm, and both were below the long term average (2005−2014 = 22.1 cm). Average soil moisture levels (volumetric water content) in the ambient rainfall treatments were also correspondingly higher in 2015 (23.9%) compared with 2016 (12.7%). Precipitation manipulations significantly altered soil moisture levels through the wheat growing season in both 2015 (DF = 2,51; Chi-Square = 97.69; P < 0.0001) and 2016 (DF = 2,51; Chi-Square = 153.57; P < 0.0001). Mean soil moisture levels increased 39% and 148% across our precipitation manipulations in 2015 and 2016 respectively; all treatments differed significantly from one another in both years (Fig. 1). Significant differences in soil moisture across irrigation treatments observed in the 2016 growing season persisted through the following Spring (DF = 2,51; ChiSquare = 13.92; P < 0.0010). Wheat growth stage (Zadoks et al., 1974), measured on the last sampling date before harvest, did not significantly differ across treatments in 2015 (DF = 2,50, Chi-Square = 1.80, P = 0.4060; Mean

2.4.2. Wheat performance The aphid outbreak in 2015 resulted in minimal fill in the wheat kernels that year, so yield was not quantified. In 2016, wheat plots were harvested as the matured grain ripened (Zadoks development stage 87–92) 15–17 August. Wheat stems that had been cut and lodged were removed from plots, and the remaining standing wheat was hand harvested at a 20.3 cm height using scissors. Wheat heads removed from these samples were combined with heads removed from the uncut stems collected to quantify insect densities (see 2.4.1), and processed to quantify grain yield and quality for the entire plot. Wheat heads were manually threshed using a threshing board, and run through a CarterDay Dockage Tester to remove excess chaff. Seed was then weighed, and run through a FOSS Infratec™ 1241 grain analyzer (FOSS, Eden Prairie, MN, USA) to quantify protein content. 4

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Table 1 Results of generalized linear models examining effects of precipitation (PPT) and insect addition treatments (Insect) and their interactions on Cephus cinctus infestation (proportion of stems infested), cutting (proportion of infested stems cut by larvae), and grain yield (grams m-2) and protein (%). Models for C. cinctus responses included two insect treatments: C. cinctus addition and C. cinctus plus B. cephi additions, while plant models (yield and protein) also include a control treatment with no insects added. Year



2015 Infestation PPT Insect PPT*Insect 2015 Cutting PPT Insect PPT*Insect 2016 Infestation PPT Insect PPT*Insect 2016 Cutting PPT Insect PPT*Insect 2016 Yield PPT Insect PPT*Insect 2016 Protein PPT Insect PPT*Insect


Likelihood Ratio Chi-Square Prob > ChiSq

2,30 1,30 2,30 2,30 1,30 2,30 2,30 1,30 2,30 2,30 1,30 2,30 2,45 2,45 4,45 2,45 2,45 4,45

0.16 7.98 2.00 1.20 884.21 0.78 12.53 0.06 2.96 1.04 451.49 1.14 6.58 43.84 5.65 1.11 20.05 6.00

0.9244 0.0047 0.3683 0.5493 < .0001 0.6783 0.0019 0.8136 0.228 0.5934 < .0001 0.5657 0.0372 < .0001 0.2270 0.5746 < .0001 0.1991

Bold text indicates significant effects P < 0.05.

2016. In 2015, C. cinctus infestation levels were slightly but significantly higher in B. cephi addition treatments relative to C. cinctus only treatments (88 vs. 83% respectively; Fig. 2). Infestation levels did not differ with B. cephi addition in 2016 (Table 1). In both years, we found a dramatic reduction in C. cinctus cutting from an average of 74% (2015) and 86% (2016) in C. cinctus only treatments to less than 0.4% in the B. cephi addition treatments (Fig. 2). We found no significant effect of precipitation treatments on survival of overwintering larvae in C. cinctus only treatments in the 2016 experiment (DF = 2,15, Chi-Square = 2.78, P = 0.2488). A consistent pattern of decreased parasitism levels with increasing precipitation was observed in both years. Compared with reduction treatments, parasitism was 8.5 percentage points lower in the addition treatment in 2015 and 13.3 points lower in 2016 (Fig. 3). However, the effect of precipitation was only significant in 2016 (2015: DF = 2,15, ChiSquare = 3.14, P = 0.2085; 2016: DF = 2,15, ChiSquare = 8.28, P = 0.0159). In 2016, parasitism levels were significantly lower in precipitation addition relative to the reduction treatments (P = 0.005, Fig. 3). A similar tendency of reduced numbers of summer cocoons with increasing precipitation was observed in both years, and the effects of precipitation were marginally significant (2015: DF = 2,15, ChiSquare = 4.88, P = 0.0870; 2016: DF = 2,15, ChiSquare = 4.88, P = 0.0871). Significantly higher numbers of parasitoid summer cocoons occurred in precipitation reduction relative to the ambient treatment in 2015 (P = 0.0312) and in precipitation reduction relative to the addition treatment in 2016 (P = 0.0446; Fig. 3). The number of winter cocoons was not affected by precipitation manipulations in either year (2015: DF = 2,15, ChiSquare = 1.43, P = 0.4885; 2016: DF = 2,15, ChiSquare = 0.48, P = 0.7863; Fig. 3). Both precipitation and insect treatments significantly influenced grain yield in 2016, the year it was quantified, and the interaction was not significant (Table 1). Yield was significantly higher in precipitation addition treatments relative to reduction treatments (P = 0.01) while neither experimental treatment was significantly different from the ambient control (P ≥ 0.18 for both comparisons; Fig. 4). Cephus cinctus addition resulted in a 61.8% reduction in wheat yield relative to insectfree controls (P < 0.0001) while control and B. cephi addition

Fig. 1. Percent volumetric water content in the soil in each of three precipitation treatments over the course of the growing season in 2015 and 2016.

Zadoks ± SE = 90.85 ± 0.35 on 8 August) but did differ in 2016 (DF = 2,48, Chi-Square = 12.56, P = 0.0019). In 2016, Zadoks stage, measured on 12 August, was delayed in irrigated (Mean Zadoks ± SE = 85.53 ± 0.57) and ambient (86.19 ± 0.69) relative to exclusion (88.89 ± 0.80; P = 0.0008, P = 0.0067) but did not differ between ambient and irrigated treatments (P = 0.5000). Aphid infestation did not differ across either precipitation or insect treatments in 2015 (Insect treatments: DF = 2,48, Chi-Square = 1.66, P = 0.4370; Precipitation treatments: DF = 2,48, Chi-Square = 1.20, P = 0.5498) or 2016 (Insect treatments: DF = 2,49, Chi-Square = 0.66, P = 0.7199; Precipitation treatments: DF = 2,49, Chi-Square = 0.10, P = 0.9574), and thus was not a factor confounding our treatment effects. Cephus cinctus responses (percent infestation, percent cutting and overwintering survival) to precipitation and insect treatments varied with year and the response variable examined, but significant interactions between treatments were never observed in any model (Table 1). In 2015, there were no significant effects of precipitation treatments on either the proportion of stems infested by C. cinctus or the proportion of infested stems that were cut by larvae (Table 1, Fig. 2). In 2016, we found a significant effect of precipitation treatments on C. cinctus infestation, which declined slightly with increasing precipitation (Table 1, Fig. 2). Mean infestation levels were significantly higher in the precipitation reduction treatment relative to addition (62 vs 53%, P = 0.0004) but did not differ between the two experimental treatments and ambient controls (P > 0.05). Although the treatments were not significantly different (Table 1; Fig. 2), a similar tendency was observed for percent cutting, with cutting reduced from 93% in the precipitation reduction treatment to 78% in the precipitation addition treatment in 5

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Fig. 2. Performance of wheat stem sawfly (Cephus cinctus) in wheat plants. The percentage of stems infested by C. cinctus (top panels) and the percentage of infested stems that were cut (bottom panels) are shown for the two insect addition treatments (C. cinctus alone and C. cinctus + B. cephi) applied in each precipitation treatment in 2015 and 2016.

treatments did not significantly differ from each other (P = 0.29). Grain protein levels did not significantly differ across precipitation treatments (Table 1). However, levels were significantly higher in C. cinctus addition plots (mean ± SE = 17.44 ± 0.49) compared with controls without insects (mean ± SE = 15.07 ± 0.44; P ≤ 0.0001) or those to which both C. cinctus and B. cephi were added (mean ± SE = 15.11 ± 0.35; P ≤ 0.0001); the latter two treatments did not significantly differ from one another (P = 0.9397).

4.1. Effects of precipitation manipulations on pest herbivores Cephus cinctus performance varied only slightly across precipitation manipulations; percent infestation and summer larval survival to stem cutting decreased slightly from dry to wet conditions in only the second year of the study, when manipulations resulted in more extreme differences in soil moisture. Previous reviews have found that insect herbivore responses to drought depend on how different feeding guilds respond to various drought induced changes in their host plants, such as reduced water content, increased nitrogen availability and changes in secondary chemistry (Huberty and Denno, 2004). Within the chewing guild, gall formers and free living chewers generally respond negatively, while wood borers and leaf miners tend to respond positively, to drought (Huberty and Denno, 2004; Walter, 2018). As a grass stem miner, C. cinctus might be expected to respond most similarly to other miners that benefit from increased nitrogen associated with drought stressed plants (Huberty and Denno, 2004). This is consistent with the observed trend towards increased C. cinctus performance under drier conditions. However, the pattern could alternatively reflect herbivore responses to changes in plant moisture levels thought to be important in this system (Criddle, 1922; Seamans, 1945; Holmes and Peterson, 1963). We found no previous experimental work to suggest that wetter conditions can negatively affect internally feeding chewing insects, as was the trend in our study. In fact, studies that examine impacts of increased precipitation levels have generally documented increases in

4. Discussion Experimental field studies examining how independently manipulating herbivores, parasitoids and precipitation affects crop productivity are lacking. Yet this tri-trophic approach is critical to predicting pest impacts on crop production under changing climatic conditions. Surprisingly, we found that crop-herbivore-parasitoid interactions were remarkably robust in the face of large changes in precipitation and associated soil moisture levels, that varied 148% across our treatments in the second, drier, year of the study. Despite slight declines in pest and parasitoid success under wetter conditions in that year, both insects had strong and significant impacts on crop yield. Furthermore, these impacts were consistent across precipitation manipulations, as evidenced by the lack of a significant interaction term in our model. The positive implication, from a pest management perspective, is that natural enemy benefits to crop production are likely to be robust to large changes in precipitation levels in this system. 6

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Fig. 3. Bracon cephi performance and impact on C. cinctus in each of three precipitation treatments in 2015 and 2016. Performance parameters included the mean number of summer and winter parasitoid cocoons observed within wheat stems in each treatment. The percentage of C. cinctus larvae that were parasitized is a measure of potential impact of the parasitoid.

herbivore abundance or pressure associated with wetter conditions. This may result from beneficial changes in host plant quality or reductions in predation (Shure et al., 1998; Leckey et al., 2014; Karban et al., 2017). The patterns we observed are consistent with anecdotal references in the historical literature on C. cinctus specifically, which describe eggs and early instar larvae drowning in excessive moisture produced in wheat stems in wet years (Seamans, 1945). The pattern is also consistent with early work suggesting that high moisture levels in solid-stemmed wheat cultivars confers resistance to C. cinctus by increasing egg mortality (Holmes and Peterson, 1964). Thus, more work examining how genetically or environmentally mediated changes in stem moisture affect C. cinctus larval survival may yield important insights into how climate and crop resistance impact C. cinctus population dynamics.

Despite some interesting trends, however, precipitation induced reductions in herbivore performance were very minor in this study. These reductions only manifested in the drier of the two study years when manipulations resulted in a stronger gradient in soil moisture (Figs. 1 and 2). Thus, overall, the results suggest the C. cinctus is resistant to relatively large changes in precipitation amounts ( ± 70%). This contrasts with previous descriptive work showing that precipitation levels are highly correlated with C. cinctus infestation levels across a large-scale geographic gradient (Rand et al., 2014), as well as modelling work implicating precipitation as a driver of shifts in the economic range of C. cinctus under future climate scenarios (Olfert et al., 2019). The lack of correspondence is unlikely due to a mismatch between the degree of precipitation change across treatments in this study relative to past work, since precipitation manipulations bracketed the 7

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densities were also higher in these treatments. Positive density-dependent parasitism, in which the rate of parasitism increases with increasing host density, is fairly commonly observed in parasitoids generally (Walde and Murdoch, 1988) and has been previously found in this system specifically (Rand et al., 2012). The patterns are also consistent with work showing that changes in host density can be an important factor underlying changing patterns of parasitism across moisture gradients (Rand, 2013). In contrast to the number of summer cocoons, the number of winter cocoons did not differ across precipitation treatments. This likely reflects a saturation effect, in which low densities of host larvae remained following parasitism by the initial generation of parasitoids, such that all remaining hosts were parasitized regardless of the number of adult parasitoids emerging from summer cocoons. At lower levels of parasitism, or higher relative host densities, one might expect a higher number of summer cocoons to translate into a concomitant increase in the number of winter cocoons, and thus, to higher populations of parasitoids in the following year. Overall, we found that B. cephi was little affected by changes in precipitation. Hence, we found no evidence, in this system, that higher trophic levels are differentially sensitive to changes in climate resulting in altered interaction intensity as predicted by theory (Voigt et al., 2003).

Fig. 4. Grain yield of the wheat crop in the different combinations of insect addition and precipitation treatments in 2016.

variation in levels observed across the geographic gradient (Rand et al., 2014). Furthermore, the +70% treatment is within the range of increased spring precipitation predicted under future climate change scenarios for the region (Whitlock et al., 2017). Instead, the mismatch suggests that factors correlated with precipitation levels, for example reduced solar radiation associated with more cloudy days, may be more important than moisture levels per se in driving C. cinctus dynamics. Alternatively, it is possible that direct effects of rainfall on C. cinctus adults, not captured with our experimental design, may play a more important role than host-plant mediated impacts on larval performance in determining these patterns.

4.3. Effects of precipitation, insects and their potential interactions on crop yield Grain yield increased significantly across precipitation treatments, as would be predicted in a water limited dryland cropping system. As expected, C. cinctus also strongly and significantly reduced yield, as found in previous work (Seamans et al., 1945; Holmes, 1977). Wheat yield was 61.8% lower in C. cinctus addition treatments relative to controls without insects. Interestingly, however, grain quality (percent protein), was significantly higher in the C. cinctus addition treatments. This contrasts with previous work showing neutral to negative impacts of C. cinctus on protein depending on the wheat variety (Holmes, 1977). Plant stress is known to increase protein levels, but such observations are usually associated with abiotic stresses such as drought (White, 1984) rather than herbivory stress, and the former had no effect on protein in this study. Adding parasitoids to the system initiated a trophic cascade which resulted in significantly and dramatically increased wheat yield, compared with treatments with the pest, C. cinctus, alone. In fact, yield in parasitoid addition treatments attained the levels observed in control plots to which no insects were added. Levels of parasitism, which averaged 58% in 2016, were within the range naturally observed in field surveys (Shanower and Waters, 2006; Rand et al., 2014), suggesting that positive cascading impacts of parasitoids on yield likely occur in the field.

4.2. Effects of precipitation manipulations on parasitoid number and parasitism levels Previous work suggests that increased precipitation may increase the susceptibility of C. cinctus to Bracon cephi by extending the wheat growing season, thereby providing more time for parasitoids to attack hosts and complete their second generation (Holmes et al., 1963; Morrill et al., 1994). This is consistent with the general idea that increasing herbivore development time can increase enemy impacts by increasing the time they are susceptible to attack (Price et al., 1980), and may be an important mechanism underlying climate impacts on parasitism (Coley, 1998). In our study, we found no evidence that parasitoid impacts on C. cinctus survival increased across precipitation treatments. In fact, parasitism levels were consistently lower in precipitation addition treatments relative to reduction treatments in both years, and significantly so in 2016. Wheat phenology was delayed slightly in precipitation treatments relative to exclusions in 2016, but all treatments reached maturity and were harvestable within two days of each other. Cephus cinctus development is tightly synchronized with host plant development. Decreasing plant moisture as wheat matures serves as a primary cue for larvae to drop to the base of the stem and cut it to form their diapause chambers (Holmes, 1979). Thus, given relatively little variation in wheat maturation timing associated with differences in precipitation, a major shift in the amount of time herbivores are susceptible to attack within the wheat stems is unlikely in this system. Reductions in parasitism associated with drought stress can be driven by changes in host insect quality or development stage (Aslam et al., 2013; Tariq et al., 2013), while increases may be associated with increases in the number of eggs laid by females (Romo and Tylianakis, 2013). In our study, both parasitism levels and the number of B. cephi summer cocoons were higher in precipitation reduction relative to addition treatments. These patterns likely reflect a positive response of the parasitoids to shifts in densities of their host, given that C. cinctus

4.4. Conclusions Our results re-inforce previous studies suggesting that parasitoids can have important positive cascading influences on crop yield (Buteler et al., 2008; Beres et al., 2011; Cárcamo et al., 2016). We significantly expand on previous work by demonstrating that such cascading influences are consistent across a wide range of precipitation levels, as evidenced by the lack of a significant interaction term in our yield model. This study provides an unusual empirical example in which tritrophic interactions were found to be remarkably robust in the face of relatively large shifts in a major climatic variable. Though rare, studies such as this that examine climate effects on plant production within a tri-trophic context will be critical to predicting and mitigating pest impacts in the face of shifting climatic conditions (Rosenzweig et al., 2001; Gregory et al., 2009; Olfert et al., 2019). 8

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Declaration of Competing Interest

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The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgements We thank the numerous technicians and field assistants who aided us with field and lab work: Dora Alvarez, Laura Senior, Morgan Manger, Lance Turner, Kayleigh Hauri, Ellen Titus, Rhonda Lawhead, Alison Berka, Tess Ler, Connor Schilling and Marie-Kate Williams. Thanks to John Gaskin for comments on an earlier draft of the manuscript. Funding: This research was funded in part by a grant from the Montana Wheat and Barley Committee (Grant number 16894) Appendix A. Supplementary data Supplementary material related to this article can be found, in the online version, at doi: References Aslam, T.J., Johnson, S.N., Karley, A.J., 2013. Plant‐mediated effects of drought on aphid population structure and parasitoid attack. J. Appl. Ent. 137, 136–145. Ballare, C.L., Caldwell, M.M., Flint, S.D., Robinson, S.A., Bornman, J.F., 2011. Effects of solar ultraviolet radiation on terrestrial ecosystems. Patterns, mechanisms, and interactions with climate change. Photochem. Photobiol. Sci. 10, 226–241. Barnett, K.L., Facey, S.L., 2016. Grasslands, invertebrates, and precipitation: a review of the effects of climate change. Front. Plant Sci. 7, 1196. Beres, B.L., Cárcamo, H.A., Weaver, D.K., Dosdall, L.M., Evenden, M.L., Hill, B.D., McKensie, R.H., Yang, R., Spaner, D.M., 2011. Integrating the building blocks of agronomy and biocontrol into an IPM strategy for wheat stem sawfly. Prairie Soils Crops J. 4, 54–64. Branson, D.H., 2017. Effects of altered seasonality of precipitation on grass production and grasshopper performance in a northern mixed prairie. Environ. Entomol. 46, 589–594. Buteler, M., Weaver, D.K., Miller, P.R., 2008. Wheat stem sawfly-infested plants benefit from parasitism of the herbivorous larvae. Agric. Forest Entomol. 10, 347–354. Cárcamo, H.A., Beres, B.L., Larson, T.R., Klima, C.L., Wu, X.-H., 2016. Effect of wheat cultivars and blends on the oviposition and larval mortality of Cephus cinctus (Hymenoptera: cephidae) and parasitism by Bracon cephi (Hymenoptera: braconidae). Environ. Entomol. 45, 397–403. Cock, M.J., Biesmeijer, J.C., Cannon, R.J., Gerard, P.J., Gillespie, D., Jimenez, J.J., Lavelle, P.M., Raina, S.K., 2013. The implications of climate change for positive contributions of invertebrates to world agriculture. CABI Reviews 8, 1–28. Cockrell, D.M., Griffin-Nolan, R.J., Rand, T.A., Altilmisani, N., Ode, P.J., Peairs, F., 2017. Host plants of the wheat stem sawfly (Hymenoptera: Cephidae). Environ. Entomol. 46, 847–854. Coley, P.D., 1998. Possible effects of climate change on plant/herbivore interactions in moist tropical forests. Climat. Chang. 39, 455–472. Criddle, N., 1915. Hessianfly and the western wheat stem sawfly in Manitoba, Saskatchewan and Alberta. Can. Dep. Agric. Entomol. Branch Bull. 11, 1–23. Criddle, N., 1922. The Western Wheat Stem Sawfly and its Control. Dominion of Canada Department of Agriculture Pamphlet No.6. pp. 1–8. Gherardi, L.A., Sala, O.E., 2013. Automated rainfall manipulation system: a reliable and inexpensive tool for ecologists. Ecosphere 4 art18. Godfrey, L., Godfrey, K., Hunt, T., Spomer, S., 1991. Natural enemies of European corn borer Ostrinia nubilalis (Hübner)(Lepidoptera: Pyralidae) larvae in irrigated and drought-stressed corn. J. Kansas. Entomol. Soc. 64, 279–286. Gregory, P.J., Johnson, S.N., Newton, A.C., Ingram, J.S., 2009. Integrating pests and pathogens into the climate change/food security debate. J. Exp. Bot. 60, 2827–2838. Hansen, N.C., Allen, B.L., Baumhardt, R.L., Lyon, D.J., 2012. Research achievements and adoption of no-till, dryland cropping in the semi-arid US Great Plains. Field Crops Res. 132, 196–203. Holmes, N., 1977. The effect of the wheat stem sawfly, Cephus cinctus (Hymenoptera: Cephidae), on the yield and quality of wheat. Can. Entomol. 109, 1591–1598. Holmes, N., 1979. The wheat stem sawfly. Proceedings of the Twenty-Sixth Annual Meeting of the Entomological Society of Alberta 2–13. Holmes, N., Peterson, L., 1963. Effects of variety and date of seeding spring wheats and location in the field on sex ratio of the wheat stem sawfly, Cephus cinctus Nort (Hymenoptera: Cephidae). Can. J. Zool. 41, 1217–1222. Holmes, N., Peterson, L., 1964. Resistance to the wheat stem sawfly, Cephus cinctus Nort. Can. Entomol. 96 120-120. Holmes, N.D., Nelson, W.A., Peterson, L.K., Farstad, C.W., 1963. Causes of variations in effectiveness of Bracon cephi (Gahan) (Hymenoptera: Braconidae) as a parasite of the wheat stem sawfly. Can. Entomol. 95, 113–126. Huberty, A.F., Denno, R.F., 2004. Plant water stress and its consequences for herbivorous


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