Alternative prey disrupt biocontrol by a guild of generalist predators

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1 Biological Control 32 (2005) Alternative prey disrupt biocontrol by a guild of generalist predators A.M. Koss, W.E. Snyder Department of Entomology, Washington State University, Pullman, WA , United States Received 2 July 2004; accepted 3 October 2004 Available online 5 November 2004 Abstract We examined the potential of a guild of generalist predators to control Colorado potato beetles ( CPB, Leptinotarsa decemlineata) on potato. We were interested in determining whether beetle suppression would change with varying predator density, and with varying background densities of green peach aphids ( GPA, Myzus persicae), which are common alternative prey for the predators in the Weld. We conducted two Weld experiments where we manipulated predator densities and measured the impact of these manipulations on CPB and GPA densities. In the Wrst experiment, with low aphid densities, the predator guild signiwcantly reduced beetle and aphid densities. In the second Weld experiment, with higher aphid densities, predators did not reduce beetle densities and only slightly depressed aphid increase. In both Weld experiments, we were unable to maintain elevated predator densities in cages where we added more predators, possibly due to intraguild predation. In laboratory microcosms, we further examined beetle predation by two common predators, Nabis spp. and Geocoris spp., in the presence versus absence of aphids. The two predators responded diverently to a choice in prey. Geocoris spp. preyed upon aphids and eggs in rough proportion to the abundance of each, whereas Nabis spp. appeared to switch more readily to feeding on aphids. Overall, in both the Weld and the laboratory, we found evidence for a positive prey prey interaction, with the presence of aphids reducing predation of potato beetles Elsevier Inc. All rights reserved. Keywords: Predator assemblage; Intraguild predation; Myzus persicae; Leptinotarsa decemlineata; Solanum tuberosum 1. Introduction Biocontrol agents can be divided into two classes: generalists and specialists. The greatest attention has been paid to specialists as biocontrol agents, because they have a tight dynamical linkage to their prey and so can track and suppress pest outbreaks (Hassell and May, 1986; Murdoch, 1994; Murdoch et al., 1984; Turchin et al., 1999; Wang and Gutierrez, 1980). In contrast, generalist predators lack prey speciwcity and have longer generation times than many of their prey (Hassell and May, 1986; Murdoch et al., 1984; Riechert and Lockley, 1984), and may interfere with one another by killing other natural enemies, disrupting biological control (Polis et al., 1989; Rosenheim et al., 1995). * Corresponding author. Fax: address: wesnyder@wsu.edu (W.E. Snyder). On the other hand, generalist predators are polyphagous and can sustain themselves on a broad range of alternative prey when any single pest species is absent (Symondson et al., 2002). Alternative prey in agricultural systems may improve generalist predator survival when target pests are rare (Ehler and Miller, 1978; Eubanks and Denno, 2000a; Riechert and Lockley, 1984; Settle et al., 1996) or improve fecundity and speed development by supplying additional nutrition (Halaj and Wise, 2002; Toft and Wise, 1999). Thus, from the predator s standpoint, alternative prey should be benewcial. However, for the biocontrol practitioner alternative prey can have either benewcial or detrimental impacts on control of a target pest. Theoretical ecologists have proposed two scenarios. Negative prey prey interactions occur when the presence of one prey builds up densities of natural enemies that strengthen their attack on a second (target) prey. This is the case Holt (1977) calls apparent competition and is the goal of biocontrol practitioners, /$ - see front matter 2004 Elsevier Inc. All rights reserved. doi: /j.biocontrol

2 244 A.M. Koss, W.E. Snyder / Biological Control 32 (2005) to use alternative prey to increase attack rates on the target. However, positive prey prey interactions also can occur (Holt, 1977; van Baalen et al., 2001). Here, the presence of one prey draws predator attacks, freeing the second (target) prey from regulation by predators. This second scenario would result in the disruption of biological control (Settle and Wilson, 1990). The Colorado potato beetle ( CPB, Leptinotarsa decemlineata Say) is a particularly devastating pest of potatoes (Solanum tuberosum L.) throughout most of the world s potato growing regions. In our region insect pests are so damaging that many conventional growers rely on applications of broad-spectrum insecticides, and potatoes are among the more intensively treated crops in the northwestern United States (RuZe and Miller, 2003). However, newer selective pesticides have broadened growers control options, and at the same time organic potato production is growing rapidly (Koss et al., in press). Reduced intensity of the application of broadspectrum pesticides may allow a larger role for biological control (Hilbeck and Kennedy, 1996; Hough-Goldstein et al., 1993). CPB biological control evorts using predators have tended to focus on single species (Biever and Chauvin, 1992; Hough-Goldstein and McPherson, 1996), but some authors have advocated reliance on whole natural enemy guilds for control of potato pests (Tamaki and Weeks, 1972a,b; Walsh and Riley, 1868). We examined whether the presence of alternative prey, green peach aphids ( GPA, Myzus persicae Sulzer), might limit the impact of a guild of generalist predators on CPB. This is relevant to interactions in the Weld, because in local potato Welds CPB occur in most Welds throughout the season, whereas green peach aphid occurrence varies seasonally as aphids colonize Welds from south to north (Koss, 2003). Thus, Welds diver regionally and seasonally in the occurrence of the alternative prey, aphids, but generally not the occurrence of our target pest, potato beetles. As well as divering in pest densities, potato Welds diver several-fold in predator densities (Chang and Snyder, 2004). Thus, we also examined whether the strength of herbivore suppression changed with varied predator density. 2. Materials and methods 2.1. Study organisms The Colorado potato beetle and the green peach aphid are the two most injurious insect pests of potatoes in Washington (Biever and Chauvin, 1992; Mowry, 2001). In plant foliage, the predator guild in Washington potato Welds is numerically dominated by predatory hemipterans: two big-eyed bugs, Geocoris bullatus Stål and Geocoris pallens Say, and two damsel bugs, Nabis americoferus Carayon and N. alternatus Parshley (Koss, 2003; Tamaki and Weeks, 1972a,b). With live specimens the two Geocoris and two Nabis species cannot be reliably assigned to species (Tamaki and Weeks, 1972b); we used Weld-collected predators for our Weld and laboratory experiments, and so both our Geocoris and Nabis were a mixture of the two common species in each genus. Other common predators in the foliage include several other predatory bugs, and a diverse group of hunting and web-building spiders (Koss, 2003). Carabid and staphylinid beetles, and a diverse group of spiders, dominate the epigeal predator guild of local potato Welds (Koss et al., 2004). The most abundant ground-dwelling spiders are sheet web spiders in the family Linyphiidae (Koss et al., 2004) Field experiments We conducted two Weld experiments at the Washington State University Research Station in Othello, WA. Our experimental units were m cages covered on all sides, except the bottom, with a Lumite mesh screen (BioQuip, Gardena, California, USA). Each cage had a zipper on one side to allow entrance into the cage. The bottom of each cage was buried cm in the soil to obstruct arthropod movement. Cages enclosed eight potato plants in two rows of four. We conducted two Weld experiments, both of which included the following treatments: high predator densities (HIGH), average predator densities (AVG), and predators removed (O). We included Wve replicates of each caged treatment in each experiment, and also Wve 2 2- m reference plots were used to look for cage evects (total N D 20). After the Wrst experiment, cages were lifted and moved several rows over to a previously unused portion of the potato Weld. Predator densities, and guild composition, included in our cages were based on a concurrent, regional survey of generalist predator communities in Washington potato Welds (Table 1); details of the regional predator survey are published elsewhere (Koss et al., in press). In the Table 1 The number of predators of each taxon released into the three treatments O, AVG, and HIGH in the Weld cage experiments Predator taxa No./treatment O AVG HIGH Carabid beetles Geocoris spp Linyphiid spiders Nabis spp Orius spp Non-Linyphiid spiders Other predators Densities in AVG are based on the mean density of each taxon in a Weld survey of 15 production potato Welds in central Washington; densities in HIGH are based on the mean density for each taxon in the three survey Welds with the highest densities of that predator (Koss et al., in press).

3 A.M. Koss, W.E. Snyder / Biological Control 32 (2005) AVG cages, we released predators at the mean density for each taxon across the 15 potato Welds included in our survey (Table 1). HIGH predator density was the mean density of each taxon in the three Welds with the highest density of that predator (Table 1). In the Wrst experiment in early July, GPA had not yet colonized our study area, and so we had to artiwcially infest our plants with aphids. We added 20 GPA to each cage by placing aphid-infested leaxets into each cage. These leaxets were draped onto one haphazardly selected potato plant. Twenty-four hours were allowed for aphids to establish on the plants before predators were added to cages. In the second experiment, initiated in early August, a preliminary count of ambient aphids densities per cage was conducted before predators were released, and we found that each cage had an initial population of GPA (mean D 38.8, standard deviation D 8.72). Therefore, we did not need to release aphids in this second experiment and instead relied on these naturally occurring aphids. In both experiments, we removed all naturally occurring CPB from each cage. We did this because we were concerned that some cages, which by chance included several adult female CPB, would have very large CPB infestations, whereas others would have few or no beetles. In the Wrst experiment, two leaxets of 30 CPB eggs (total N/cage D 60 CPB eggs) each were attached to two randomly selected leaves on two diverent potato plants in each cage, immediately before predator release. Eggs were attached to potato foliage using a small drop of Elmer s glue (Borden, Columbus, OH, USA). The glue was entirely covered by the leaxet and should not alter predator behavior (Snyder and Ives, 2003). For the second experiment, clutches of 30 pre-laid CPB eggs were applied to each cage on day 0 and again on day 7 of the experiment. Our release method was slightly altered in this second release we placed leaf cuttings with eggs attached into 9-dram vials containing water and wrapped with ParaWlm (American National Can, Chicago, Illinois 60631, USA) at the top to avoid water evaporation and hold leaf cuttings Wrmly in each vial. Leaf cuttings in 9-dram vials were placed next to the base of a haphazardly selected potato plant so that predators could easily climb down to the leaf cuttings and potato beetle larvae would be able to emigrate to plants once they hatched from the eggs. Predators in the foliage were removed from all cages using a D-vac suction sampler before the start of the experiments (D-vac Company, Ventura, California, USA). Cages were suctioned twice to remove predators, with each suction period lasting approximately 4 min, a method that has been used successfully in the past (Snyder and Ives, 2003). We followed up these D-vac removals by carefully hand-searching each cage twice, with each search lasting ca. 5 min/cage, and again removing all predators that we observed by aspirating them into 9-dram vials. Collection bags, and predators in vials, were immediately stored in a cooler (4 7 C) and transported back to the laboratory to be hand sorted. Predators collected from the D-vac samples were housed individually in 9- dram vials. The next day, these predators were returned to the Weld and released into cages, in order to achieve the two predator addition treatments; the taxonomic makeup of the predators released, and total predator density, was the same in both Weld experiments (Table 1). At times additional predators were needed to complete treatments, and these were collected in local potato Welds in conjunction with our regional survey (Koss, 2003). To remove ground predators in the O treatment, we also included two live-catching pitfall traps in the removal cages [see Snyder and Wise (1999) for trap design]. Pitfall traps were checked weekly and trapped predators were returned to the laboratory for use in other experiments (Koss, 2003). We hand searched each of the eight plants in each cage, and within each reference plot, on days 0, 14, and 21 of both experiments, and recorded all CPB, GPA, and predators that we observed. Predators that we observed in O cages were collected and removed from cages after we recorded their presence. Each plot was searched for ca. 20 min. After the Wnal visual count on day 21, we D-vac suctioned each cage twice, for ca. 4 min per cage, to destructively sample Wnal predator densities Laboratory experiments Our laboratory experiments focused on two predator taxa, Geocoris spp. and Nabis spp., that are among the most abundant and voracious predators in local potato Welds (Koss et al., 2004). Predators were Weld collected at our research site and used in feeding trials within 48 h. All predators were starved for 12 h (overnight) to standardize hunger level before being used in trials. CPB eggs were produced in the laboratory by adults collected in potato Welds near our study site in the summers of 2001 and 2002, with adults maintained at ambient day length at C, and fed on live potato plants. Eggs were harvested daily and placed in a refrigerator (5 C) to retard egg development. GPA came from a long-term laboratory colony, maintained in the same greenhouse as the CPB, which was originally initiated using GPA collected on potatoes near Prosser, WA, USA. Our microcosms were 8-cm wide 20-cm tall plastic cylinders, covered on the top with organdy mesh. Two round windows, approximately 3.5-cm in diameter, were cut into the sides of the tubes and covered with mesh to provide airxow and reduce condensation of water inside the tube. Each tube contained a single, ca 15-cm long potato stem cutting submerged in a 33.3-mL (9 dram) vial of water capped with a piece of ParaWlm to block arthropods from entering the water. Vials containing plant stems

4 246 A.M. Koss, W.E. Snyder / Biological Control 32 (2005) were buried in watered soil in 10-cm diameter pots. Burying the vials with stem cuttings in the soil helped retain moisture and kept the stem cuttings fresh for the duration of the experiment. The bottom of each plastic tube was twisted into the soil to form a seal with the edge of the pot. The experiment was run once with Geocoris spp. as the focal predator, and once with Nabis spp. as the focal predator. Four Geocoris were used in the former, while two Nabis were used in the latter, because the per capita feeding rate of Nabis spp. is ca. 2 that of Geocoris spp. (Koss et al., 2004). Treatments were: a control of 10 eggs only (CON); 10 eggs and predators (O); 10 eggs, 20 aphids, and predators (20); and 10 eggs, 200 aphids, and predators (200). Each treatment was replicated 10 times (total N D 40). Clutches of 10 L. decemlineata eggs, attached to small (61cm 2 ) pieces of potato foliage where they had been deposited by female CPB, were glued to each potato stem using a small drop of Elmer s glue. Aphids were applied to the foliage and then the microcosms were left undisturbed for 12 h (overnight). After this 12 h settling period CPB densities were counted by visually searching each tube for 1 min, after which Geocoris or Nabis spp. predators were added. We then again counted eggs in each microcosm at 24, 48, and 72 h after predator addition. After the last visual egg count at 72 h, we terminated the experiment and destructively sampled each microcosm and recorded the number of aphids, eggs, and predators remaining in each. The experiments were ended after 72 h because earlier work indicated that suycient predation occurred by this time to delineate treatment evects, but without complete depletion of either prey species (Koss et al., 2004). 3. Results 3.1. Field Experiment 1: early season aphid density Based on visual surveys made during the experiment, we were successful in decreasing predator densities in our O compared to the pooled AVG and HIGH treatments (F 1,13 D 25.17, P < 0.001; Fig. 1A); a signiwcant treatment time interaction is diycult to interpret (Wilks λ D 0.57, F 2,12 D 4.58, P D 0.033). Predator densities did not diver between AVG and HIGH in visual surveys (F 1,8 D 0.28, P D 0.61; Fig. 1A). OPEN predator densities diverged from AVG in the second week, leading to a signiwcant treatment time interaction (Wilks λ D 0.35, F 2,7 D 6.43, P D 0.026). Based on D-vac samples collected at the end of the experiment, predator densities signiwcantly divered among treatments (F 3,16 D 23.89, P <0.001; Fig. 1B); predator densities were lowest in O, equal in AVG and HIGH, and highest in OPEN. In Experiment 1, when aphid densities were naturally low, predators had a consistent evect through time [contrast of O versus pooled (AVG + HIGH); Wilks λ D 0.74, F 2,12 D 2.085, P D 0.17], signiwcantly reducing CPB densities (F 1,13 D 5.49, P D 0.036; Fig. 2A). CPB densities were statistically indistinguishable between AVG and HIGH predator densities (F 1,8 D 0.40, P D 0.55; Fig. 2A), and between AVG and OPEN (F 1,8 D 0.94, P D 0.36; Fig. 2A); both treatment evects were consistent through time (treatment time interactions, P >0.45) Statistics For the Weld and laboratory experiments visual samples were repeated in the same cages/microcosms through time, and thus those data were analyzed using multivariate repeated measures ANOVA in SYSTAT (SPSS, Chicago, Illinois, USA). We adopted the MANOVA approach for repeated measures analysis because it is relatively robust to modest violations in ANOVA assumptions, compared to the univariate approach (von Ende, 2001). For the Weld cage experiments we examined three planned contrasts: (1) O vs. pooled predator addition treatments (pooled HIGH and AVG) to examine the evect of predators on pest densities, (2) HIGH vs. AVG to examine the evect of adding more predators to the system, and (3) AVG versus OPEN to look for diverences between caged and unmanipulated, uncaged plots (Snyder and Wise, 1999). Predator, GPA and CPB densities from Wnal destructive sampling in both Weld and laboratory experiments were analyzed using ANOVA followed by Tukey s HSD post hoc test. Data were log-transformed when necessary to meet ANOVA assumptions. Fig. 1. Generalist predator densities: (A) during the experiment and (B) at the end of the experiment for the early season experiment, and (C) during the experiment and (D) at the end of the experiment for the late season experiment. Treatments for both experiments: predators reduced (O); predators added at mean Weld density (AVG); predators added at high Weld density (HIGH); and uncaged open reference areas (Open). Letters in panels B and D represent means that are signiwcantly diverent (P < 0.05) using Tukey s post hoc test. In this and subsequent Wgures, error bars are 1 SE.

5 A.M. Koss, W.E. Snyder / Biological Control 32 (2005) OPEN and AVG, did not diver from one another (F 1,8 D 1.08, P D 0.75; F 1,8 D 1.04, P D 0.34, respectively; Fig. 2B). Both evects were consistent through time (treatment time interactions, P >0.20). Predators initially depressed aphid densities, but aphid densities converged in all treatments by the second week, leading to a signiwcant treatment time interaction (Wilks λ D 0.50, F 3,11 D 3.73, P D 0.045; Fig. 2D). The signiwcant predator evect was driven by a strong initial suppression in HIGH but little response in AVG (treatment time interaction: Wilks λ D 0.21, F 3,6 D 7.41, P D 0.019). Aphid densities did not diver in AVG versus OPEN (F 1,8 D 1.19, P D 0.31; Fig. 2D) Laboratory experiments Fig. 2. Densities of Colorado potato beetles in: (A) the early season and (B) the late season Weld experiments, and of green peach aphids in (C) the early season and (D) the late season Weld experiments. Treatments as in Fig. 1. Predators had a consistent evect on GPA through time [contrast of O versus pooled (AVG + HIGH); Wilks λ D 0.74, F 2,12 D 2.16, P D 0.16], signiwcantly reducing GPA densities (F 1,13 D 55.73, P <0.001; Fig. 2C). GPA population densities were lower under high than average predator densities (F 1,13 D 7.28, P D 0.027; Fig. 2C), an evect that was consistent through time (Wilks λ D 0.981, F 2,7 D 0.068, P D 0.935). Aphid densities were initially lower in open plots, but eventually converged to densities similar to those in the cages as aphids naturally colonized the Weld, leading to a signiwcant treatment time interaction (Wilks λ D 0.326, F 2,7 D 7.23, P D 0.02). For CPB egg predation by Geocoris spp., the four treatments diverged through time, leading to a statistically signiwcant treatment time interaction (Wilks λ D 0.32, F 6,66 D 8.49, P <0.001; Fig. 3A). Egg densities did not signiwcantly diver after 24 h (F 3,34 D 2.612, P D 0.067; Fig. 3A). However, by 72 h the treatments signiwcantly divered from one another (P < 0.05 for each comparison; 3.2. Field Experiment 2: later season aphid density Based on visual surveys, we were again successful in lowering predator densities in O compared to AVG and HIGH (F 1,13 D 8.05, P D 0.014; Fig. 1C); this evect was consistent through time (Wilks λ D 0.98, F 2,12 D 0.11, P D 0.90). Predator densities did not diver between AVG and HIGH (F 1,8 D 0.14, P D 0.72; Fig. 1C). Predators were signiwcantly more abundant in OPEN than AVG cages (F 1,8 D 9.04, P D 0.017; Fig. 1C). Both of these latter two evects did not vary through time (treatment time interactions; P > 0.15). In the Wnal D- vac sample, collected at the end of the experiment, predator densities signiwcantly varied by treatment (F 3,16 D 19.98, P < 0.001; Fig. 1D). Predator densities were lowest in O, higher in HIGH, and higher still in OPEN. Predator densities in AVG were intermediate between those in O and HIGH. Predators consistently (Wilks λ D 0.85, F 3,11 D 0.65, P D 0.60) failed to suppress CPB densities (F 1,13 D 0.11, P D 0.75; Fig. 2B). The two predator treatments, and Fig. 3. Densities of Colorado potato beetle eggs in laboratory microcosms containing: (A) four adult Geocoris or (B) two adult Nabis predators. Treatments for both experiments: microcosms containing 10 CPB eggs but no aphids or predators (con); predators and eggs but no aphids (O); predators, eggs and 20 aphids (20); and predators, eggs, and 200 aphids (200).

6 248 A.M. Koss, W.E. Snyder / Biological Control 32 (2005) Tukey s post hoc test), with the exception that the CON and 200 treatments were not statistically distinguishable (P D 0.91; Tukey s post hoc test). Determined by destructive sampling after the 72-h visual sample, signiwcantly more aphids remained in the 200 aphid than the 20 aphid treatment (F 1,18 D , P <0.001; Fig. 4A). Final egg densities were lowest where no aphids were provided (treatment O), intermediate where 20 aphids were provided (treatment 20), and highest in the 200 and CON treatments (Overall F 3,36 D 33.89, P <0.001; Fig. 4C). Final Geocoris spp. densities were highest in 20, lowest in O, and intermediate in 200 (F 2,27 D 3.08, P D 0.062; Fig. 4E). For Nabis spp. predation on CPB eggs the magnitude of treatment diverences increased through time, leading to a signiwcant treatment time interaction (Wilks λ D 0.66, F 6,70 D 2.68, P D 0.021; Fig. 3B). At the Wrst sample at 24 h Nabis spp. ate signiwcantly more eggs when no aphids were present than when 20 or 200 aphids were provided (F 3,36 D 18.41, P < 0.001; Fig. 3B). Egg densities gradually declined in the two treatments including aphids until these treatments were signiwcantly Fig. 4. Final densities of: (A) aphids when paired with Geocoris spp., (B) aphids when paired with Nabis spp., (C) beetle eggs when paired with Geocoris spp., (D) beetle eggs when paired with Nabis spp., (E) Geocoris spp. predators and (F) Nabis spp. predators. Data, and thus treatments, are from the same experiment presented in Fig. 3. Letters represent means that are signiwcantly diverent (P < 0.05) using Tukey s post hoc test. lower than CON densities at 72 h (P < 0.01), although egg densities remained lowest in the treatment without aphids (P < 0.05). Through destructive sampling after 72 h we found that aphid densities remained signiwcantly higher in the 200 than 20 aphid treatment (F 1,18 D , P < 0.001; Fig. 4B). Egg densities were lowest in O, intermediate in 20 and 200, and highest in CON (F 3,36 D 19.43, P < 0.001; Fig. 4D). Nabis spp. densities were lowest in O, intermediate in 20, and highest in 200 (F 2,27 D 6.80, P D 0.004; Fig. 4F). 4. Discussion Some authors include nutritional suitability as a criterion for deciding what constitutes alternative prey. For example, Hodek and Honek (1996) and Soares et al. (2004) use the term alternative prey only in cases where predators cannot develop on that prey as a monotypic diet, although the predator gains some nutritional benewt from that prey species. In contrast, we adopted the dewnition used by Holt (1977), arbitrarily designating Colorado potato beetles ( CPB ) our target prey, and green peach aphids ( GPA ) the alternative prey, for the experiments we report here. That is, by alternative prey we mean nothing more than that, from the standpoint of CPB biocontrol, aphids served as an additional potential prey item. Similarly, from the standpoint of GPA control roles are reversed and CPB are the alternative prey, a scenario that we report on elsewhere (Koss et al., 2004). Some optimal foraging models assume a link between an animal s foraging choices and its resulting nutritional gain (Stephens and Krebs, 1986), but this relationship may be tenuous in our potato system. For example, coccinellid beetles (Coleoptera: Coccinellidae) of several species feed heavily on CPB eggs even though inclusion of these prey signiwcantly reduces predator survivorship (Hazzard and Ferro, 1991; Munyaneza and Obrycki, 1998; Snyder and Clevenger, 2004). In potato Welds in our region potato beetles are present in most Welds throughout the season, but densities of aphids vary seasonally (Koss, 2003). We examined how varying background densities of aphids might alter the impact of a guild of generalist predators on CPB. If predators had a strong aynity for feeding on CPB, then the presence of aphids would have had little impact on CPB biocontrol. However, if predators had a strong aynity for attacking aphids, CPB control should have quickly degenerated once aphids entered the system. The results of our Weld experiments suggest that the truth lies nearer to the latter scenario. In our early season experiment, when initial aphid densities were naturally low, predators signiwcantly reduced densities of both CPB and GPA. In our second experiment later in the season, when aphid densities were naturally higher, we saw no evidence of predators impacting CPB. However, even at the

7 A.M. Koss, W.E. Snyder / Biological Control 32 (2005) higher aphid densities present later in the season, predators initially slowed aphid population growth. Still, aphid densities eventually converged in all treatments, perhaps due to predator satiation (Southwood and Comins, 1976; Symondson et al., 2002; van Emden, 1988). In the later experiment, aphid densities were not particularly high mean aphid densities at the initiation of the experiment were <5/plant suggesting that most predators are fairly quick to abandon feeding on CPB eggs as aphid density increases. It is important to note that, while caging was necessary to maintain predator treatments, cages likely prevented predator immigration with rising aphid density. Thus, both Weld experiments probably underestimated the true impact of predators in the Weld, assuming predators are strongly attracted to rising aphid densities (Snyder and Ives, 2003). The laboratory experiments allowed us to more carefully examine how biocontrol of CPB eggs by two prominent predator taxa, Geocoris spp. and Nabis spp. bugs, changes as aphids are added to the system. These two predators are among the most abundant predators in Washington potato Welds (Tamaki and Weeks, 1972a,b), and are the most voracious common predators of GPA and CPB under no-choice conditions in the laboratory (Koss et al., 2004). The two predators responded diverently to the availability of aphids as alternative prey. Geocoris spp. appeared to feed on each prey roughly relative to its abundance as aphid densities increased, consumption of CPB eggs by Geocoris spp. decreased in equal measure. In contrast, Nabis spp. appeared to switch more rapidly to feeding on aphids than did Geocoris spp. When Nabis spp. had no choice but to feed on CPB eggs, they attacked these prey at a high rate, but Nabis spp. fed less frequently on the target prey whenever aphids were present, regardless of aphid density. Overall, our results are similar to those reported by Hazzard and Ferro (1991), who found that the predatory coccinellid Coleomegilla maculata reduced the number of CPB eggs it attacked in the presence of green peach aphids. It is unclear why the predators might diver in their attack rates on potato beetle eggs as aphid density changed. These diverences could be due either to diverences in nutritional requirements or diverences in hunting strategies. For example, Eubanks and Denno (2000b) found that Geocoris punctipes is attracted to the movement of aphid prey, and will consume aphids even though Helicoverpa zea (corn earworm) eggs may be nutritionally superior. More work is needed both on prey selection by Geocoris spp. and Nabis spp., and on the development of both predators feeding on CPB versus GPA. Alternative prey can either improve or disrupt biological control (Snyder et al., 2004). Harmon et al. (2000) found that coccinellid beetles had the highest densities, and exerted the strongest control of aphids, in alfalfa plots containing dandelions. The beetles were drawn to these patches to feed on dandelion pollen, but once there also ate aphids (Harmon et al., 2000). This is an example of a negative prey prey interaction, with the presence of alternative prey (pollen) bolstering predator densities and thus ultimately improving biocontrol of the target pest (pea aphids). On the other hand, including multiple prey in a system can disrupt biological control, because predators may feed on nontarget prey, rather than the pest (Holt, 1977; van Baalen et al., 2001). For example, Halaj and Wise (2002) increased densities of predatory wolf spiders and ground beetles by augmenting densities of non-pest prey, collembola and other detritivores, through the addition of compost. However, despite a threefold increase in predator densities, control of herbivorous pests was not improved, apparently because many predators preferred to feed on one another and on the detritivores rather than on herbivorous pests (Halaj and Wise, 2002). Unfortunately, the experiments reported here revealed interactions more like those reported by Halaj and Wise (2002), with the addition of aphids to the system dexecting predator attacks on the potato beetle target, indirectly protecting CPB and weakening their control. That is, our data are consistent with a positive prey prey interaction (van Baalen et al., 2001), where the presence of a preferred prey (aphids) reduced evective control of the target (potato beetles). While we consistently found that aphid prey reduced the evectiveness of CPB control, our experiments covered very short (72 h for the laboratory experiments) to intermediate (3 weeks for the Weld experiments) time periods. At times, benewcial prey can disrupt biocontrol in the short term, but improve it in the long term. For example, Eubanks and Denno (2000a) found that including high-quality plant food, an important noninsect food for the Geocoris predators they worked with, lowered predator-feeding rates on pests in small arenas. However, over longer time periods in the Weld, high quality plant food increased predation rates on pests by allowing the predators to reach higher densities (Eubanks and Denno, 2000a). Further work is needed in our system to address how short- versus long-term impacts of alternative prey might diver. However, our experiments provide some evidence that longer-term impacts of aphid availability might diver from those in the short-term. In the open reference plots, predator densities consistently increased throughout the season, possibly due to predators being attracted to increasing aphid densities. Additional Weld experiments are needed, where the seasonal abundance of aphids is experimentally manipulated in un-caged plots, to determine the longerterm impact of aphid prey on CPB control. Still, annual crops such as potatoes are ephemeral. There is only a narrow window of time for crop production, about 90 days for potatoes in our region, so that short-term impacts of alternative prey are likely important.

8 250 A.M. Koss, W.E. Snyder / Biological Control 32 (2005) Much recent work has focused on the role of intraguild predation in limiting the biocontrol evectiveness of generalist predators (Polis et al., 1989; Rosenheim et al., 1995). In both of our Weld experiments, we had diyculty increasing predator densities in our HIGH predator treatment. Despite more than doubling the number of predators added to HIGH cages, elevated predator densities were never sustained for the duration of the experiment. Because predators could not escape from the cages, this convergence in predator densities might have been due to intraguild predation. For example, the two predator taxa we focused on, Nabis spp. and Geocoris spp., have been shown to feed heavily on one another, with all larger stages feeding on all smaller stages (Raymon, 2000). In potatoes, generalist predators have had mixed success in biocontrol programs. Predatory pentatomids have been extensively studied as augmentative control agents (e.g., Biever and Chauvin, 1992; Hough-Goldstein and McPherson, 1996). While evective if released at a suyciently high rate, these releases can be prohibitively expensive on a large scale (Tipping et al., 1999). Conservation of naturally occurring predators may be a more cost-evective strategy. For example, Ferro and co-workers have demonstrated that the coccinellid beetle Coleomegilla maculata can contribute to biocontrol of potato pests if the beetles can be drawn into Welds from surrounding crops (Hazzard and Ferro, 1991). Similarly, applying straw mulch to potato crops can attract predatory ground beetles, improving biological control (Stoner et al., 1996; Zehnder and Hough- Goldstein, 1990). Our work reported here provides support for the view of Walsh and Riley (1868) and Tamaki and Weeks (1972a,b) that guilds of natural enemies can substantially reduce densities of potato pests. 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