Parasitoid dispersal and colonization lag in disturbed habitats: biological control of cereal leaf beetle metapopulations

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1 J. Appl. Entomol. ORIGINAL CONTRIBUTION Parasitoid dispersal and colonization lag in disturbed habitats: biological control of cereal leaf beetle metapopulations E. W. Evans, V. L. J. Bolshakova & N. R. Carlile Department of Biology, Utah State University, Logan, UT, USA Keywords annual crop, disturbance, ephemeral habitat, fragmentation, host-parasitoid, Tetrastichus julis Correspondence Edward W. Evans (corresponding author), Department of Biology, Utah State University, Logan, UT , USA. Received: August 15, 2014; accepted: November 5, doi: /jen Abstract Natural enemies of insect pests of annual crops have been hypothesized either to lag, or alternatively not to lag, behind their prey in dispersing to and colonizing new habitat. We examined parasitoid dispersal and parasitism of the cereal leaf beetle (Oulema melanopus [L.]; Coleoptera: Chrysomelidae) by the host-specific wasp Tetrastichus julis [Walker] (Hymenoptera: Eulophidae) in wheat fields of northern Utah to assess whether a colonization lag occurred. Equally high rates of parasitism of beetle larvae (including second instars early in the year) occurred in 2010 and 2011 in fields that were newly planted to wheat vs. in fields where wheat had been grown also the previous year. A caging experiment demonstrated that parasitism in these newly planted wheat fields did not arise from parasitoid adults that had matured within the fields; instead, upon emerging in other fields, parasitoid females dispersed a minimum of m to parasitize beetle larvae early in the spring in the newly planted fields. A transect study in 2012 revealed that T. julis females dispersed rapidly at least 600 m into a newly planted wheat field to parasitize most of the early maturing beetle larvae, which occurred at very low density. Thus, the parasitoid has very strong ability to match its host in dispersal over long distances across a highly disturbed agricultural landscape, and colonization lag appears of little importance in affecting biological control associated with this host parasitoid interaction. Introduction It is often useful to consider biological control as a metapopulation process of natural enemies tracking down their pest victims across space and time (Ives and Settle 1997; Rauch and Weisser 2007; Schellhorn et al. 2014). This perspective highlights the importance of the relative dispersal abilities of insect herbivores and their natural enemies (predators and parasitoids) among habitat patches (Kareiva 1990; Cronin and Reeve 2005). Success in classical and conservation biological control programmes in particular may vary widely depending on the ability of these natural enemies to find and contain the pest at multiple locations across often diverse landscapes. One aspect of dispersal in biological control of continuing interest has been the potential for significant lags in the colonization of new habitat patches by natural enemies following colonization by their prey. As explored by theory, prey outbreaks may ensue from such lags resulting in escape from predation over space (Hastings 1977; Taylor 1990). These lags hence may weaken the potential for pest suppression, especially in frequently disturbed (e.g., annual) crops (Price 1976; Risch 1987; Kogan et al. 1999; Van Driesche et al. 2008; Letourneau et al. 2012). As pointed out by Kaplan (2012) and Sivakoff et al. (2012), the general importance of such colonization lags is widely accepted. However, as stressed also by Sivakoff et al. (2012) and others (Jones et al. 1996; Harrison 2000; Cronin and Reeve 2005; Van Nouhuys 2005; Schellhorn et al. 2014), current understanding of natural enemy dispersal in relation to that of the 2014 Blackwell Verlag GmbH 1

2 Cereal leaf beetle parasitoid dispersal E. W. Evans, V. L. J. Bolshakova and N. R. Carlile prey in field settings is limited, and hence such acceptance is premature. The importance of colonization lag as applied to annual crops and other ephemeral habitats has also been questioned over the years on first principles. Given that the prey that exploit such habitats often are highly dispersive, associated natural enemies can be hypothesized as often under equally strong selective pressure also to be very dispersive (Ehler and Miller 1978; Hirose et al. 1996; Wiedenmann and Smith 1997; Sivakoff et al. 2012). Indeed, these natural enemies may be selected to be even more dispersive than their hosts or prey: not only must they constantly find new habitat patches just as their prey do, but they also must find that subset of new habitat patches that are already occupied by the prey (Holt 2002; Van Nouhuys 2005). Specialist natural enemies in particular may be highly attuned to the dispersal capabilities of their prey. If the pest is well adapted to the disturbance regime of annual cropping systems, so too then may the specialist natural enemy be equally well adapted. Any lag between prey and natural enemy colonization of new habitat hence may often be minor at most and of relatively little importance to the success of biological control. There are thus two longstanding, alternative general lines of thought concerning the importance of colonization lag or lack thereof for biological control programmes associated with frequently disturbed crops. Case studies are needed to weigh the relative merits of these general hypotheses. Here we address these hypotheses by examining whether the cereal leaf beetle (CLB) (Oulema melanopus [L.]; Coleoptera: Chrysomelidae) outdisperses its host-specific parasitoid Tetrastichus julis [Walker] (Hymenoptera: Eulophidae) in colonizing fields of small grains in a diverse agricultural landscape. Because the crop is annual and because individual fields planted to small grains in one year may often be planted to another crop (e.g. safflower) in the following year, frequent dispersal among fields is required of both the pest and its parasitoid. The pest in fact leaves its natal field each summer to overwinter elsewhere, while the parasitoid overwinters in the soil in the field (Haynes and Gage 1981). A significant colonization lag therefore might be expected, particularly as the parasitoid physically is very small (2 mm length). But given that the wasp is a specialist natural enemy of the pest, selection may promote strong parasitoid dispersal matching that of its host. This programme of biological control against the CLB can be used as a test of the importance of colonization lags in annual cropping systems. We use local rates of parasitism in new habitat as measures of successful parasitoid colonization (thereby incorporating both the ability to reach the new habitat and the ability to search successfully for the host within the new habitat). We test for a significant colonization lag by comparing rates of beetle parasitism in fields of small grains that either were or were not planted to small grains the previous year as well and by determining rates of parasitism within newly created (planted) habitat at varying distance from the nearest source area for dispersing parasitoid adults. Materials and Methods Study system The CLB became a pest of wheat, barley, oats and other small grains in the 1960s in eastern North America following its accidental introduction from Europe (Haynes and Gage 1981). It subsequently became a pest in western North America also (Dosdall et al. 2011; Roberts and Walenta 2012) after first appearing in Utah in 1984 (Karren 1986). Several species of parasitoids were introduced in eastern North America in a successful programme in classical biological control against the CLB (Stehr 1970; Dysart et al. 1973). Among these species, only the larval parasitoid T. julis established upon subsequent introduction to western North America. This host-specific parasitoid was introduced in western North America first to Utah in the late 1980s and has since become widely established (Evans et al. 2006; Roberts and Walenta 2012). Cereal leaf beetle has a single generation each year. Eggs are laid singly or less often as pairs or triplets on the upper midribs of grain leaves. The larvae develop in early summer from eggs by feeding externally on the foliage and drop from the host plant to pupate in the soil. Adults emerge in midsummer and remain to feed on grain leaves for a few weeks. The adults then disperse often long distances to habitats far from grain fields where they overwinter as adults before returning to grain fields the next spring to feed again, and develop and lay their eggs (Haynes and Gage 1981; Honek 1991). Adults of the parasitoid T. julis emerge in the spring from the soil in the grain field in which they developed as larvae the previous year. These adults lay eggs within CLB larvae, with an average of 4 6 parasitoids sharing a single host individual (Dysart et al. 1973). The parasitoid larvae kill the host after it has prepared its pupal cell in the soil during the summer. Most parasitoid larvae complete their development in the soil the following early spring Blackwell Verlag GmbH

3 E. W. Evans, V. L. J. Bolshakova and N. R. Carlile Cereal leaf beetle parasitoid dispersal (Gage and Haynes 1975; Evans et al. 2006). Some larvae, however, emerge the same summer to parasitize late-developing host larvae. Thus rates of parasitism are high initially in the spring and decline thereafter until late in the season when the relatively few CLB larvae remaining are attacked by the partial second generation of the parasitoid (Gage and Haynes 1975; Evans et al. 2006, 2010, 2013). This study was carried out in Cache Valley in northern Utah, in fields surrounding the small town of Cove. Study sites were located within a largely continuous patchwork of fields, each varying generally between 6 and 24 (and up to 40) ha and lying either immediately adjacent to neighbouring fields or separated by roads (most of which were dirt or gravel). Individual fields in any given year were planted to either small grains or a variety of other crops including peas, lentils, radishes, corn, safflower and alfalfa. Parasitism in newly vs. previously planted grain fields Populations of CLB were sampled throughout the growing seasons in 2010 and 2011 to compare rates of parasitism in wheat fields that had been planted in the previous summer with small grains vs. in wheat fields that had been left fallow or planted with a crop other than small grains in the previous summer and hence were newly planted to wheat. Three previously planted and four newly planted wheat fields in 2010, and four previously planted and five newly planted wheat fields in 2011, were sampled generally twice weekly from early May through early July. Densities of CLB were determined for individual fields on each sampling occasion by counting the number of eggs and larvae per 0.09 m 2 at random locations (6 per field in 2010 and 6 9 per field in 2011, with adjacent locations m apart; Evans et al. 2006). Sampling locations were placed more than 50 m into each field from the nearest field edge. The number of degreedays ( C) accumulated since January 1 on each sampling date was determined (single-sine method with horizontal cut-off; Evans et al. 2014). Samples of up to 50 second instars and 60 fourth instars of CLB in 2010 and 25 of each in 2011, were collected as available during each census of each field and brought to the laboratory for dissection to score for parasitism. Samples of second and fourth instars, respectively, were collected on four and 10 dates in 2010 (between 4 18 June and 11 June 12 July) and on five and six dates in 2011 (between 8 22 June and 20 June 12 July). Samples were collected randomly within areas of newly planted fields that were m (2010) and m (2011) from the nearest edge of a field that had been planted in small grains during the previous summer and that could have served as the nearest potential source of colonist parasitoid females that parasitized CLB larvae in the spring. These nearest edges of source fields lay at varying direction (north, south, east or west) from individual sampling areas. Parasitism within caged plots A caging study was conducted in spring 2011 to determine whether adults of T. julis would emerge from the soil in fields that had been planted to wheat during the spring and summer in 2009 but not in 2010 (i.e. to determine whether diapausing individuals of T. julis remain in the soil for more than a year). Early in the growing season (on 17 May 2011, before parasitoid adults began emerging), two cages each were placed 2 m apart in each of three fields that had been planted with winter wheat the previous fall (2010) after having been planted to another crop (radishes or safflower) during the spring and summer of The cages were m with finely meshed screening that prevented adults of T. julis from entering or leaving the cages. A yellow, two-sided sticky trap card (15 by 30 cm) was attached to a wooden stake in the centre of each cage, with the bottom edge of the card 15 cm above the ground. On 18 May 2011, 30 CLB adults (captured by sweep net that day in a nearby wheat field) were released into each of the six cages. The cages were left undisturbed thereafter for 6 weeks until they were sampled for the presence (i.e. emergence within the cage) of T. julis adults, both by inspecting sticky traps and by collecting CLB larvae to dissect for parasitism. As available, up to 30 each of CLB third and fourth instars were collected from each cage on 28 June At the same time in each field, up to 30 each of CLB third and fourth instars were collected from uncaged wheat plants within 20 m of the cages. The CLB larvae were frozen and subsequently dissected in the laboratory to assess for parasitism by T. julis (numbers dissected from all three fields combined = 142 third and 72 fourth instars from caged wheat plants, and 78 third and 90 fourth instars from uncaged wheat plants). Parasitism along a transect Populations of CLB larvae were sampled in May 2012 along a transect extending 600 m into a large (40 ha) field of wheat. The field had lain fallow in spring and summer of the previous year (2011). It was planted with winter wheat in the fall of 2011 and was 2014 Blackwell Verlag GmbH 3

4 Cereal leaf beetle parasitoid dispersal E. W. Evans, V. L. J. Bolshakova and N. R. Carlile colonized by CLB adults in spring The sampling transect extended west from the edge of an adjacent field planted to safflower in spring This adjacent field had been planted with wheat that was infested with parasitized CLB larvae during the spring and summer of 2011; the field served as the nearest potential source of colonist parasitoid females at all sampling stations along the transect. On 15 May 2012, when CLB were first hatching from eggs, all CLB larvae were collected as encountered during visual searches at each of eight distances (10, 50, 100, 200, 300, 400, 500 and 600 m) along the transect from the field edge (at each distance, larvae were collected along subtransects perpendicular to the main transect). Given the difficulty of finding CLB larvae at the very low densities that occurred in this field in 2012, sample sizes at individual distances varied from 6 34 larvae (all instars combined). CLB larval populations were sampled again on 21 May; because densities remained very low, all larvae were collected as encountered only at 10, 100, 300 and 600 m along the transect from the field edge (20 40 individuals were collected at each distance). Additional samples were collected at the two ends of the transect (i.e. at 10 and 600 m) on 29 May and 8 June. CLB densities were also quantified at each sampled distance along the transect on each sampling date by counting the number of eggs and larvae on the wheat foliage in 0.09 m 2 at six random locations. The CLB larvae collected on each sampling date were frozen and subsequently dissected in the laboratory to assess for parasitism by T. julis. Analyses All statistical analyses were conducted using SAS (SAS Institute 2002). The mean density of larvae at peak abundance (in late June) in newly vs. previously planted fields was compared in 2010 and 2011 using two-way ANOVA for ln-transformed number of larvae per 0.09 m 2 in each field. One-way ANOVA was used to compare early season rates of parasitism (logittransformed percentages of individuals parasitized) in newly vs. previously planted fields for second instars sampled between 200 and 300 degree-days (i.e. those individuals collected on 4 June 2010 or on 8, 13 and 17 June 2011) and for fourth instars between 300 and 400 degree-days (i.e. as collected on 11, 15, 18 and 21 June 2010 and 20, 23 and 27 June 2011). Results from 2010 and 2011 were combined, and results for second and fourth instars were analysed separately, to preserve homogeneity in variances between field types for each analysis. Following the early season, results for rates of parasitism (logit transformed) of CLB second and fourth instars in newly vs. previously planted fields were analysed individually for each sampling date by one-way ANOVA, with Bonferonni correction for P-values to reflect the multiple tests performed. This approach was used because variances (as well as means) for rates of parasitism differed widely among sampling dates as the season progressed and because not all fields could be sampled late in the season as CLB larval populations dwindled. Change in percentage parasitism of CLB individuals in a given field as they matured (i.e. from when the populations were sampled as second instars between 200 and 300 degree-days to when populations were sampled as fourth instars between 300 and 400 degree-days) was assessed with a two-tailed binomial test, with individual fields from both years combined serving as replicates. The potential influence of CLB larval density (as measured at peak abundance) within a field on the rate of parasitism of either second or fourth instars in that field was examined by Spearman rank correlation for fields sampled in 2010 and in 2011 and for both sets of fields combined. The simple presence or absence of parasitized individuals was compared by Fisher s exact test for samples of CLB larvae taken in late June 2011 from wheat foliage in caged plots vs. in adjacent uncaged areas. Rates of parasitism in 2012 were compared at differing distances along the 600-m transect through a newly planted wheat field for the CLB instar(s) present in largest numbers at each sampling date. The rate of parasitism was compared for first and second instars at seven distances sampled from the field s eastern edge on May 15, and for second instars at the four distances sampled on May 21, using logistic regression to evaluate the hypothesis that the rate of parasitism would decline with increasing distance from the field edge. The eighth distance sampled on May 15 (300 m) was not included in the analysis because so few individuals (six for both instars combined) were collected at this distance on May 15. Rates of parasitism were compared at the two distances sampled (i.e. at the two ends of the transect) by Fisher s exact test for second and third instars on 29 May and for third and fourth instars on 8 June. Results Parasitism in newly vs. previously planted grain fields Egg laying by CLB females had commenced at first census in early May in both 2010 and The first CLB larvae were encountered during censusing when Blackwell Verlag GmbH

5 E. W. Evans, V. L. J. Bolshakova and N. R. Carlile Cereal leaf beetle parasitoid dispersal peak numbers of eggs occurred on the grain foliage in late May 2010 and early June 2011 [at C degree-days (dd)]. The abundance of CLB larvae varied greatly among fields in both years. At peak larval abundance in late June, the mean number of larvae (all instars combined) per 0.09 m 2 varied among the study fields from 0.5 to 10.5 in 2010 (x + SE = ) and from 1.0 to 25.9 in 2011 (x + SE = ). Overall, the mean density of larvae in the study fields did not differ significantly between 2010 and 2011 nor between previously vs. newly planted fields (two-way ANOVA for lntransformed number of larvae per m 2 at peak abundance: effect of year, F 1,12 = 0.30, P = 0.59; effect of field type, F 1,12 = 2.71, P = 0.13; interaction, F 1,12 = 0.32, P = 0.58). In both 2010 and 2011, second and fourth instars could be collected for assessing rates of parasitism beginning after 200 and 300 dd, respectively. Seasonal patterns of parasitism, as based on degreedays, were similar in the 2 years. Rates of parasitism of second instars were high among fields initially in the spring; overall nearly three-fourths of second instars that were collected before 300 dd were parasitized (fig. 1). Rates of parasitism among second instars declined sharply thereafter until second instars largely disappeared from field populations (at close to 350 dd). Rates of parasitism among fourth instars also were high in all fields (with an overall average of 90 95% of individuals parasitized) early in the season (before 400 dd). These rates declined as the spring and early summer progressed, before rebounding late in the season (in early July, after 600 dd) after the second generation of T. julis females had emerged (fig. 1). The high rates of parasitism of second instars early in the growing season (i.e. before 300 dd) did not differ significantly between newly vs. previously planted fields (fig. 2; ANOVA of percentage parasitism logit transformed for 2010 and 2011 combined, effect of field type: F 1,14 = 0.14, P = 0.71). There was also no significant difference between newly vs. previously planted fields in the very high rates of fourth instars as collected before 400 dd (fig. 2, ANOVA of percentage parasitism logit transformed for 2010 and 2011 combined, effect of field type: F 1,14 = 2.42, P = 0.14). As overall parasitism rates varied greatly over the course of the season thereafter (fig. 1), no significant difference occurred between newly and previously planted fields in the rates of parasitism of either second or fourth instars as sampled on a given date (P > 0.09 in all cases). Although rates of parasitism were already high among second instars early in the season, these rates increased significantly as the larvae matured. Thus, in every newly or previously planted field in both years, parasitism rates were higher among the earliest maturing larvae when assessed for parasitism as fourth instars than when assessed earlier in the spring as second instars (two-tailed binomial test: P < for 2010 [n = 7 fields] and P = for 2011 [n = 9 fields]; fig. 1). The modest variation among individual fields in these rates of parasitism of second and of fourth instars was unrelated to Fig. 1 The mean percentage (all fields combined) of second (small diamonds) and fourth instars (large circles) parasitized by T. julis as sampled at differing numbers of degree-days ( C) accumulated from January 1 in 2010 (filled symbols) and 2011 (open symbols). Fig. 2 The mean percentage (+SE) of early maturing CLB larvae parasitized by T. julis in newly vs. previously planted wheat fields as second instars before 300 degree-days (left) or as fourth instars before 400 degree-days (right). Results are presented for both 2010 (year 1) and 2011 (year 2). CLB, Cereal leaf beetle Blackwell Verlag GmbH 5

6 Cereal leaf beetle parasitoid dispersal E. W. Evans, V. L. J. Bolshakova and N. R. Carlile varying CLB larval density among fields (as sampled at peak abundance) both in each year individually and across the 2 years combined [Spearman rank correlation: P > 0.25 in all cases (i.e. for rates of parasitism of either second or fourth instars as sampled in individual fields in either 2010 and 2011 and in both years combined)]. The high rates of parasitism in both newly and previously planted fields early in the season occurred as CLB larval numbers were increasing. Thus, among CLB fourth instars, the absolute number of parasitized larvae in the fields rose rapidly early in the season in both years (fig. 3). A subsequent decline in this absolute number accompanied the general decrease in abundance of fourth instars in general (i.e. whether parasitized or not) in the latter half of the season, although the drop in absolute number of parasitized (vs. unparasitized) larvae was especially marked until late in the season when the second generation of parasitoid females emerged (fig. 3). Overall, in both years (and especially in 2011), relatively few CLB larvae escaped parasitism and such larvae mostly occurred at and after larval abundance peaked and before larvae became both rare and heavily parasitized late in the season (fig. 3). Parasitism within caged plots No adults of T. julis were caught by the sticky traps inside cages during the spring and early summer of 2011 in any of the three newly planted wheat fields where cages had been placed early in the spring. None of the fourth or third CLB instars recovered in late June from within the six cages in these fields were parasitized. In contrast, a mean (SE) of 71.1 (2.9) % of fourth instars and 30.1 (10.6)% of third instars were parasitized as collected from uncaged wheat plants in the three fields in the vicinity of the cages (Fisher s exact test of six cages with no parasitism vs. three collections outside cages with parasitism: twotailed P = 0.012). Parasitism along a transect Cereal leaf beetle densities were very low in 2012 in the wheat field through which the transect was placed. Only (x + SE) eggs and larvae per 0.09 m 2 were present at the first census, as taken on May 15 (304 dd) at close to the time of peak egg laying, with no relationship apparent between local egg or larval density and distance from the field edge (linear regression, P > 0.10 in both cases). The number of eggs on the foliage declined from mid-may to early June and was (x+se) on June 8 [ANOVA for egg densities (10 and 600 m combined) on May 15 vs. June 8: F 1,22 = 12.66, P = ]. The number of larvae per 0.09 m 2 did not increase significantly through the final census on June 8 (x + SE = ; one-way ANOVA for larval densities (10 and 600 m combined) on the four sampling dates: F 3,44 = 1.13, P = 0.35). On May 15, four-fifths of the larvae present were first instars and one-fifth were second instars (these relative abundances were independent of the distance from the field edge; logistic regression: v 2 = 0.33, d.f. = 1, P = 0.57). Overall, 29% of first instars, and 73.5% of second instars, were parasititized on May 15, with no relation between percentage parasitism and distance from the field edge for either instar (fig. 4; logistic regression: first instars, v 2 = 0.06, d.f. = 1, P = 0.81; second instars, v 2 = 0.03, d.f. = 1, P = 0.85). Thus high rates of parasitism were recorded at great distances into the field from the field edge. Consistent with these results, a female T. julis was observed ovipositing into a CLB second instar at 600 m on May 15 and three more T. julis adults were observed on nearby wheat foliage at this distance at this first census. When larvae were next sampled on May 21 (358 dd), two-thirds were second instars (first and third instars were of similar abundances among the remaining individuals). As on 15 May, there was no relation between percentage parasitism of second instars and Fig. 3 The mean number of CLB fourth instars per 0.09 m 2 occurring in censuses on individual dates in 2010 (left) and 2011 (right), and the number of these fourth instars that were parasitized (as estimated by multiplying the mean number of fourth instars present by the parasitism rate as determined for that given census date). CLB, Cereal leaf beetle Blackwell Verlag GmbH

7 E. W. Evans, V. L. J. Bolshakova and N. R. Carlile Cereal leaf beetle parasitoid dispersal Fig. 4 The percentages of CLB first and second instars on May 15, and of second instars on May 21, that were parasitized, as found at differing distances from the field s edge along a transect in a newly planted wheat field in The distance from the field s edge represents the minimal distance a female would have flown to find the host. [Note that only six larvae (all unparasitized) were found at 300 m on May 15 and that samples were taken only at four distances on May 21]. CLB, Cereal leaf beetle. distance from field edge (fig. 4; logistic regression: v 2 = 0.05, d.f. = 1, P = 0.83). There were also no significant differences (Fisher exact tests) in rates of larval parasitism between the two ends of the transect (10 and 600 m) as sampled on May 29 (414 dd, with overall rates of parasitism of 54% and 74% for second and third instars, respectively) and on June 8 (516 dd, with overall rates of parasitism of 20% and 58% for third and fourth instars, respectively). Discussion The results presented here collectively reveal strong dispersal ability of T. julis adults upon emergence from overwintering in the soil in fields planted in the previous year to small grains. As shown by the caging study, the high rates of parasitism of CLB larvae in newly planted fields of wheat early in the spring do not arise from local emergence of overwintering parasitoids within these fields (i.e. from individuals of T. julis with an extended diapause lasting beyond a single year). Rather, it appears that such parasitism arises from immigration of T. julis adults emerging from overwintering sites elsewhere (in other fields) at least one to several hundred m away. Such longdistance dispersal perhaps is to be expected in parasitoids attacking insect pests of annual crops. Adults of T. julis begin emerging from the soil in the spring as CLB eggs begin hatching (Gage and Haynes 1975), and the earliest maturing CLB larvae in newly planted wheat fields in this study were parasitized soon after hatching by T. julis females arriving from elsewhere. Thus, it can be deduced that long-distance dispersal of T. julis adults over hundreds of metres occurs very early in the spring (i.e. very soon after the adults wasps emerge), from overwintering sites to other sites within newly planted fields. Such strong dispersal is consistent with the rapid establishment and spread of the wasp in southern Ontario in the early 1970s (Harcourt et al. 1977). It might seem surprising that such a small parasitoid as T. julis can rapidly disperse so far upon emerging from the soil in the spring. Indeed, other small parasitoids may disperse typically only a few metres or tens of metres (e.g. Pickett and Pitcairn 1999; Cronin 2003; Darrouzet-Nardi et al. 2006). But other species disperse long distances. Minute fairy flies (Anagrus spp., Mymaridae; length 1.5 mm), for example, disperse up to several kilometres to find their hosts, as in the case of A. delicatus dispersing more than 1 km across open water (Antolin and Strong 1987). Egg parasitoids (scelionids) of tussock moths similarly were found to disperse up to 500 m to reach isolated hosts (Brodmann et al. 1997). Wind conditions affect parasitoid flight behaviour (Messing et al. 1997); long-distance dispersal of small parasitoids may be aided by wind (Kristensen et al. 2013), but may also occur upwind (Corbett and Rosenheim 1996). Such strong dispersal capabilities can lead to rapid, far-ranging expansions of parasitoid populations across large landscapes (Gould et al. 1992; Pickett and Pitcairn 1999). Small, partially bivoltine species of braconids of the genus Peristenus, for example, have expanded outward from initial release areas by an estimated km/year following their introductions in North America (Day et al. 2000; Pickett et al. 2013). Such long-distance dispersal potential is impressive and likely of much importance for biological control. Yet even more importance may lie with the dispersal capability of the parasitoid relative to that of its host, and correspondingly with its ability to discover and parasitize new, distantly located populations of the host (Kareiva 1990; Cronin and Reeve 2005; Rauch and Weisser 2007). The parasitoid s dispersal ability can be limited in comparison with the dispersal ability of its host, resulting in low rates of parasitism at new, distantly located populations of the host (e.g., Kruess and Tscharntke 1994, 2000; Maron and Harrison 1997; Maron et al. 2001). In such cases, the strength of the species interaction may be compromised by the lag between colonization of new habitat by a pest host and by its parasitoid. This could weaken biological control especially 2014 Blackwell Verlag GmbH 7

8 Cereal leaf beetle parasitoid dispersal E. W. Evans, V. L. J. Bolshakova and N. R. Carlile in frequently disturbed (e.g. annual) crops (Kogan et al. 1999; Van Driesche et al. 2008). As pointed out by (Kaplan 2012) and Sivakoff et al. (2012), such colonization lags that undermine biological control are widely accepted as the norm. A colonization lag is not apparent, however, in the present study. The dispersal capability of T. julis is sufficiently strong for this parasitoid to find and parasitize the great majority of cereal leaf beetle larvae developing early in the growing season throughout the patchwork of annually planted fields of small grains mixed among fields of other crops that constitutes the farming landscape studied here. The host beetle hence derives little to no escape in space, as larvae that mature far from vs. within source areas of overwintering wasps are equally at high risk of parasitism. This was particularly apparent in 2012, when newly emerged, overwintered T. julis females succeeded in rapidly dispersing at least 600 m into a newly planted wheat field to find and parasitize most of the early maturing larvae of a population of CLB that occurred at very low density. Escape from parasitism by the host in this landscape mosaic of agricultural fields lies in time rather than space: there is reduced risk of parasitism (especially in years with warm springs; Evans et al. 2013) among beetle larvae that mature later in the growing season as the shift from first to second generation parasitoid adults occurs (following which parasitism rates again rise to high levels; see also Evans et al. 2006). Similar results have been reported by others in non-agricultural settings. The fairy flies that disperse a kilometre or more across open water, for example, parasitize their leafhopper hosts on small offshore islets at even higher rates than on the mainland, reflecting that they recruit to these isolated locations in greater numbers than do their hosts (Antolin and Strong 1987). Additional species of parasitoids have been documented to disperse as well or better than their hosts across hundreds of metres between habitat patches in fragmented landscapes, such that parasitism rates vary little among sites (Van Nouhuys and Hanski 2002; Esch et al. 2005; Van Nouhuys 2005; Elzinga et al. 2007). It thus appears that despite common belief to the contrary, strong dispersal by natural enemies often may preclude any significant colonization lag in their exploitation of their prey in newly created habitat. In particular, specialist parasitoids whose hosts inhabit ephemeral habitats may be under strong selection to disperse as well or better than their hosts. The present study of T. julis and the cereal leaf beetle reveals strong ability of the parasitoid to keep up with its host in dispersing rapidly over long distances across a highly disturbed landscape subject to major, annual reconfiguration. This ability reinforces the general point that the practice of biological control in annual crops should not be viewed as inevitably compromised by colonization lag as created by frequent habitat disturbance (Van den Bosch et al. 1976; Ehler and Miller 1978; Gilstrap 1997; Wiedenmann and Smith 1997). Acknowledgements We thank J. Anderson, M. Innes, N. Pitigala, C. Rogers, J. Smith, V. Weerasekera and D. Wright for field and laboratory assistance, C. Allen for permitting us to sample his fields and two anonymous reviewers for very helpful comments on the manuscript. Support was provided by the Utah Agricultural Experiment Station, the Utah Department of Agriculture and Food and the USDA APHIS. References Antolin MF, Strong DR, Long-distance dispersal by a parasitoid (Anagrus delicatus, Mymaridae) and its host. Oecologia 7, Brodmann PA, Wilcox CV, Harrison S, Mobile parasitoids may restrict the spatial spread of an insect outbreak. J Anim Ecol 66, Corbett A, Rosenheim JA, Quantifying movement of a minute parasitoid, Anagrus epos (Hymenoptera: Mymaridae), using fluorescent dust marking and recapture. Biol Control 6, Cronin JT, Patch structure, oviposition behavior, and the distribution of parasitism risk. Ecol Monogr 73, Cronin JT, Reeve JD, Host-parasitoid spatial ecology: a plea for a landscape-level synthesis. P R Soc B 271, Darrouzet-Nardi A, Hoopes MF, Walker JD, Briggs CJ, Dispersal and foraging behaviour of Platygaster californica: hosts can t run, but they can hide. Ecol Entomol 31, Day WH, Tilmon KJ, Romig RF, Eaton AT, Murray KD, Recent range expansions of Peristenus digoneutis (Hymenoptera: Braconidae), a parasite of the tarnished plant bug (Hemiptera: Miridae), and high temperatures limiting its geographic distribution in North America. J New York Entomol Soc 108, Dosdall LM, Carcamo H, Olfert O, Meers S, Hartley S, Gavloski J, Insect invasions of agroecosystems in the western Canadian prairies: case histories, patterns, and implications for ecosystem function. Biol Invasions 13, Blackwell Verlag GmbH

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