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Plant diversity increases herbivore movement and vulnerability to predation
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Plant diversity increases herbivore movement and vulnerability to predation Cory S. Straub∗ , Nathan P. Simasek, Regan Dohm, Mark R. Gapinski, Ellen O. Aikens, Cody Nagy Department of Biology, Ursinus College, 601 E. Main Street, Collegeville, PA 19426-1000, USA Received 21 May 2013; accepted 9 December 2013
Abstract Understanding how changes in plant diversity affect agroecosystem functioning remains a key challenge. We examined how intercropping alfalfa, Medicago sativa, with orchardgrass, Dactylis glomerata, affects the potato leafhopper, Empoasca fabae, its host plant (alfalfa), and the efficiency of a leafhopper predator, Nabis americoferus. In a field experiment, intercropping reduced the reproductive efficiency of the leafhopper. Nabis was more effective at reducing leafhopper abundance, and protecting alfalfa from hopperburn, in the polyculture than in the monoculture of alfalfa. In a series of laboratory experiments, we investigated mechanisms by which intercropping could enhance the efficiency of Nabis. Intercropping resulted in changes in vegetation structure and the spatial distribution of leafhoppers, but there was little evidence that these factors influenced the efficiency of Nabis. Instead, orchardgrass, a nonhost for leafhoppers, increased leafhopper movement, and Nabis captured leafhoppers more efficiently when the herbivores were more mobile. These results indicate that intercropping with nonhost plants promotes leafhopper movement and vulnerability to predation, and reveal a novel mechanism by which plant diversity can reduce herbivory.
Zusammenfassung Zu verstehen, wie Änderungen der Pflanzendiversität die Funktion von Agrarökosystemen beeinflusst, bleibt eine wichtige Aufgabe. Wir untersuchten wie die Mischkultur von Alfalfa (Medicago sativa) und Wiesen-Knäuelgras (Dactylis glomerata) die Amerikanische Kartoffelzikade (Empoasca fabae), ihre Wirtspflanze und die Effizienz eines Zikadenräubers (Nabis americoferus) beeinflusst. In einem Freilandexperiment, reduzierte die Mischkultur die Fortpflanzungseffizienz der Kartoffelzikade. In der Mischkultur reduzierte Nabis die Zikadenabundanz und den Zikadenbrand auf Alfalfa mit größerer Effizienz als in der Reinkultur. In einer Reihe von Laborexperimenten untersuchten wir die Mechanismen, durch die die Mischkultur die Effizienz von Nabis steigern könnte. Mischkultur resultierte in Veränderungen der Vegetationsstruktur und der räumlichen Verteilung der Zikade, aber es gab kaum Hinweise, dass diese Faktoren die Effizienz von Nabis beeinflussten. Vielmehr verstärkte das Knäuelgras, das von den Zikaden nicht genutzt werden kann, die Bewegungen der Zikaden, und Nabis fing Zikaden mit höherer Effizienz, wenn diese mobiler waren. Diese Ergebnisse zeigen, dass Mischkultur mit Nicht-Wirten die Bewegungsaktivität der Zikaden erhöht und damit ihre Anfälligkeit für Prädation, und sie enthüllen einen neue Mechanismus, durch den die Pflanzendiversität den Herbivorendruck verringern kann. © 2013 Gesellschaft für Ökologie. Published by Elsevier GmbH. All rights reserved. Keywords: Biodiversity; Agriculture; Intercropping; Biological control; Resource concentration; Enemies hypothesis; Leafhopper
∗ Corresponding
author. Tel.: +1 610 409 3306; fax: +1 610 409 3633. E-mail address: [email protected] (C.S. Straub).
1439-1791/$ – see front matter © 2013 Gesellschaft für Ökologie. Published by Elsevier GmbH. All rights reserved. http://dx.doi.org/10.1016/j.baae.2013.12.004
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Introduction Understanding how changes in plant diversity affect agroecosystem functioning remains a key challenge for sustainable agriculture. Agricultural ecologists have long suspected that pest outbreaks, and the need for pesticides that threaten environmental and human health, may be reduced by increasing plant diversity within agricultural fields (Pimentel 1961). Numerous studies have investigated this possibility, and reviews of these studies have come to a similar conclusion – most of the time plant diversity reduces herbivore abundance and damage to crops (Andow 1991; Russell 1989; Letourneau et al. 2011; but see Bommarco & Banks 2003 for an important caveat). In the most recent of these reviews, the authors concluded that while crop diversification is generally effective in reducing herbivory, a mechanistic understanding for why these schemes work is often missing. This limits our ability to engineer, in a directed way, diversification schemes that will effectively control particular pest species (Letourneau et al. 2011). Explanations for how plant diversity reduces herbivore abundance and damage include the ‘resource concentration’ and ‘enemies’ hypotheses. The resource concentration hypothesis states that insect herbivores are more likely to find and remain on their host plants in monocultures, where their host plants are concentrated, than in polycultures, where their host plants are dispersed among nonhost plant species (Root 1973). Under the resource concentration hypothesis, plant diversity reduces herbivory by reducing the relative abundance of herbivores’ host plants. This, in turn, reduces herbivores’ encounter rate with, or residence time on, host plants (Fig. 1, upper pathway). The enemies hypothesis states that natural enemies are less abundant and/or effective in monocultures than in polycultures, because polycultures include plant species that provide enemies with alternative prey, shelter, or a favorable microclimate (Root 1973). Under the enemies hypothesis, plant diversity reduces herbivory by providing resources to enemies that control herbivore populations (Fig. 1, lower pathway). Diversification schemes that promote both the resource concentration and enemies hypotheses will be more effective than schemes that promote only one of them. However, these mechanisms are not always compatible. For example, increasing plant diversity may reduce herbivore abundance via a resource concentration effect, but may simultaneously reduce the foraging efficiency of natural enemies (Smith 1976; Sheehan 1986). The potato leafhopper, Empoasca fabae, provides an excellent opportunity to explore the mechanisms by which plant diversity reduces herbivory. Numerous studies have shown that increasing plant diversity can reduce the abundance of the potato leafhopper on focal crops (Oloumi-Sadeghi, Zavaleta, Lamp, Armbrust, & Kapusta 1987; Roltsch & Gage 1990; Lamp 1991; Andow 1992; Roda, Landis, & Miller 1997). Grass intercrops may be particularly effective, because potato leafhoppers cannot develop or reproduce on them (Lamp, Nielson, & Danielson 1994). The specific mechanism(s) by
which grass intercrops reduce leafhopper abundance are not fully understood, but it seems likely that a resource concentration effect contributes. Roda et al. (1997) showed that leafhoppers do not discriminate between their host plants and grasses until after contact, and that intercropping alfalfa with grasses causes them to emigrate from plant patches. Thus, grass intercrops could reduce leafhopper foraging efficiency and could potentially “push” leafhoppers out of intercropped fields if they repeatedly encounter grass intercrops. Pushing pests with nonhost intercrops is often more effective if they eventually encounter and remain on an attractive trap crop, as occurs in push-pull systems (Cook, Khan, & Pickett 2007). Pushing pests with nonhost plants could also be more effective if it increased their encounters with natural enemies, although this possibility has not been rigorously evaluated. In a previous study, we found that weedy grasses reduce leafhopper abundance and damage to alfalfa (Straub et al. 2013). The resource concentration effect likely contributed to this finding (Fig. 1), but there was also evidence for the enemies hypothesis. Specifically, the predator:prey ratio was higher in the weedy plots, and one predator, Nabis americoferus, was more effective in a microcosm experiment when grasses were present. Thus, this system appears to be one in which the resource concentration and enemies hypotheses are complementary, but the exact mechanism by which the enemies hypothesis operates remains unknown. In the earlier study, we hypothesized that the grasses reduced leafhoppers’ host plant encounter rate, and that leafhoppers compensated for this by increasing their host searching behavior. As a consequence, leafhoppers were more likely to encounter and be killed by predators. We call this the ‘movement-risk hypothesis’ (Fig. 1, dashed arrows). The purpose of the present study was to attempt to replicate the earlier finding that Nabis is more effective in polyculture, and to more rigorously examine the movement-risk hypothesis. In addition, the previous study (Straub et al. 2013) had two limitations: it was conducted in a laboratory setting, and fava bean was used as a surrogate for the focal crop, alfalfa. To address these issues, the present study was conducted in the field with alfalfa. Following the field experiment, we conducted a series of laboratory experiments to test assumptions of the movement-risk hypothesis and to evaluate an alternative hypothesis.
Materials and methods Field experiment An enclosure experiment was conducted in an alfalfa field intercropped with orchardgrass at Northern Star Farm in Trappe, PA, USA. The alfalfa (HarvestarTM 504VP) and orchardgrass (‘Potomac’) were seeded together at 20 and 4.5 kg/ha, respectively. The field was planted three years prior to the experiment, in late summer 2007, and the experiment took place from 30 June to 12 July 2010. Enclosures were
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Enemies hypothesis Fig. 1. Pathways by which plant diversity may reduce herbivore abundance and damage to host plants. Solid lines indicate established pathways. The dashed line indicates the hypothetical pathway tested in this study.
0.6 m × 0.6 m × 0.6 m (BugDorm model #3120, MegaView Science, Co., Ltd.) and were placed in the field approximately one week after the first harvest of the growing season. The enclosures were arranged in a roughly linear array, avoiding patches of bare ground, with ∼0.25 m separating each enclosure. The bottom edges were dug into the soil ∼5 cm and buried with sand to prevent arthropods from entering or leaving. Naturally occurring arthropods were removed from the enclosures using a leaf vacuum (Stihl SH 56C Shredder vac). Each enclosure was searched after vacuuming and remaining arthropods were removed by hand. Our central hypothesis was that intercropping alfalfa with grass would increase leafhoppers’ risk of predation. Therefore, plant diversity and predators were manipulated in a 2 (monoculture, polyculture) × 2 (Nabis present, Nabis absent) factorial design. Each of the four treatment combinations was replicated 12 times. In addition, eight enclosures (four monocultures, four polycultures) served as no-leafhopper controls. Enclosures were randomly assigned to treatment. The monoculture treatment was created by removing all orchardgrass (using the claw of a hammer) and by further pruning so that each of the enclosures contained ∼32 alfalfa stems. The polyculture treatment was created by pruning each enclosure to contain ∼16 alfalfa stems and by removing orchardgrass as necessary so that the total amount of plant material in polycultures (i.e., ∼16 alfalfa stems + orchardgrass) visually matched the total amount of plant material in the monocultures (i.e., ∼32 alfalfa stems). Adult leafhoppers were collected with sweep nets from a nearby alfalfa field and were introduced to the enclosures on the same day they were collected. All Nabis were collected within two days of the start of the experiment and were stored individually in plastic vials at 5 ◦ C until release into the enclosures. Treatments receiving leafhoppers were stocked with 30 adults. Treatments receiving Nabis were stocked with four individuals, which is within the range of densities found in the field (range, 0–6 individuals per 0.60 m3 , unpublished data).
The experiment lasted 13 days. For the first nine days, daily observations were made through a clear window in the enclosures. During 1-min scans, the number of adult leafhoppers observed within the enclosures was recorded. The time-averaged data from these nine observations were used as an index of leafhopper abundance. It is possible that leafhoppers were easier to observe in polyculture than in monoculture because the polyculture treatment increases leafhopper movement. If this is true, our estimates of leafhopper abundance could have been artificially inflated for the polyculture treatment. However, the hypothesis that Nabis is more effective in polyculture predicts that the difference in leafhopper abundance between the Nabis-present and Nabisabsent treatments should be greater in polyculture than in monoculture. Importantly, the observational bias described above, if present, would not have affected this comparison. At the end of the experiment, when destructive sampling could be conducted, the surviving adult leafhoppers were collected with aspirators. These data, which reflect only a single point in time, were used as an additional measure of adult leafhopper abundance. In addition, ten alfalfa stems were haphazardly selected and removed from each enclosure on day 13, and the number of leafhopper nymphs found on these stems was recorded. Nymphs were not added to the enclosures and so were most likely produced during the course of the experiment. Leafhopper injury to alfalfa was assessed by calculating the percentage of leaflets that showed “hopperburn”, or V-shaped yellow triangles, on the ten alfalfa stems. The fresh weight of the stems was also recorded.
Laboratory experiments investigating mechanisms The movement-risk hypothesis makes two assumptions: (1) potato leafhoppers move more in polyculture than in monoculture, and (2) greater movement makes leafhoppers
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grass monoculture (nonhost plants only) than in polyculture more vulnerable to predators. To evaluate the first assump(nonhost and host plants), but be more clumped in the latter tion, the movement of leafhoppers in monoculture (n = 10) treatment, the movement-risk hypothesis predicts that Nabis and polyculture (n = 10) was evaluated. The experimental microcosms were clear plastic tubes (15 cm diameter, 30 cm will kill more leafhoppers in a grass monoculture, while the height) encasing plants in a 17-cm diameter pot. The tubes ‘clumping-risk hypothesis’ makes the opposite prediction. To evaluate the relative importance of these two hypothehad a plastic mesh top with mesh holes (2 mm2 ) large enough for leafhoppers to easily pass through. The bottoms of 0.35-L ses, we conducted a 2 (grass monoculture, polyculture) × 2 plastic cups were cut off to create smaller tubes (8 cm diam(Nabis present, absent) factorial experiment. Each treatment eter, 7 cm height). These smaller tubes were placed on the combination was replicated ten times. Fava bean was used plastic mesh and served as supports for sticky traps. The as a surrogate for alfalfa because it is easier to cultivate in sticky traps were created by applying Tangle-trap® (Conthe greenhouse. The results observed in the field experiment described above were very similar to the results of a differtech Enterprises, Inc.) to the underside of clear plastic plates ent experiment in which fava was used as a surrogate for (15 cm diameter). The plates were placed on top of the smaller alfalfa (Straub et al. 2013), indicating that the substitution tubes, sticky-side down, and mesh fabric was placed over of fava for alfalfa does not change predator–prey dynamics the plate and connected to the larger tube with a rubber in this system. Orchardgrass and fava bean were grown in band. The mesh fabric allowed airflow into the microcosm but prevented leafhoppers from escaping. Thus, leafhopthe greenhouse and experimental plants were 6 and 2 weeks pers that passed through the plastic mesh became stuck in old, respectively. The orchardgrass monoculture included 12 the sticky trap. Alfalfa and orchardgrass were transplanted blades of grass and the polyculture included 6 blades of grass from the field and were ∼15 cm in height. Alfalfa monoculand one fava plant. Six adult leafhoppers from the laboratory tures included ∼12 stems of alfalfa and alfalfa polycultures colony were introduced to the microcosms, which were clear included ∼6 stems of alfalfa and a small bunch of orchardplastic tubes (15 cm diameter, 30 cm height) with a mesh top encasing plants in a 17-cm diameter pot. Before introducing grass so that there was a similar amount of plant material in mono- and polyculture. Thus, the polyculture treatment had the leafhoppers, they were anesthetized with CO2 . This process killed one leafhopper in several replicates. We corrected a similar alfalfa:grass ratio (∼1:1) as the field experiment. for this unintentional source of mortality by using the folAdult leafhoppers were collected from a laboratory colony reared on fava bean. Eight adult leafhoppers were aspirated lowing ratio as the response variable: number of leafhoppers alive at the end of the experiment/number of leafhoppers alive into plastic vials and introduced to each of the microcosms. at the beginning of the experiment. Some leafhoppers died or escaped during the introduction, so In addition to measuring leafhopper survival, observations the actual number of leafhoppers introduced varied between of leafhoppers were conducted with the goal of confirming five and eight. The percentage of leafhoppers captured by the that leafhoppers showed a clumped distribution in polyculsticky trap after 24 h (at 21 ± 4◦ C, 14:10 L:D) was recorded ture (i.e., preferred fava to grass) and moved more in the and provided an index of leafhopper movement. To evaluate the assumption that greater movement makes grass monoculture than in the polyculture. On six occasions leafhoppers more vulnerable to predation, leafhopper moveseparated by at least 3 h, the locations of leafhoppers in each replicate were recorded. The first and last observations ment was directly manipulated. Three adult leafhoppers were were separated by 55 h. During each observation, the numintroduced to Petri dishes (10 cm diameter, 1.5 cm height). There were two treatments: mobile leafhoppers (n = 15) and ber of leafhoppers observed at seven locations was recorded immobile leafhoppers (n = 15). The latter were immobilized for the movement analysis: vegetation (fava and/or grass), by freezing at −20 ◦ C for 10 min. The immobilized leafhopsoil, mesh ceiling, or one of four quadrats of the plastic pers were dead, but Nabis readily consumed dead leafhoppers tube. A movement index was created, which quantifies the upon encounter. A single, field-collected adult Nabis was extent to which leafhoppers changed their locations from starved for 24 h and introduced to each Petri dish. The total one observation period to the next. This was calculated as: number of leafhoppers captured in 1 h was recorded. 2 (A1 − A2)2 + (B1 − B2)2 + (C1 − C2)2 + (D1 − D2)2 + (E1 − E2)2 + (F 1 − F 2)2 + (G1 − G2)2 In addition to increasing leafhopper movement, intercropping alfalfa with orchardgrass could change the spatial distribution of leafhoppers. Specifically, leafhoppers in monoculture should be uniformly distributed, while leafhoppers in polyculture should be clumped because they aggregate on the fewer host plants (alfalfa stems) that are available. This clumped distribution could increase the efficiency of Nabis if, for example, it uses area-restricted searching behavior (e.g., Cronin 2009). Because leafhoppers should move more in a
where A–G represent the number of leafhoppers observed in the seven possible locations, and 1 and 2 represent the first and second observation period. The equation quantifies the extent to which leafhoppers changed their locations in between the first and second observation periods. There were six observation periods, providing five opportunities to calculate the movement index for each replicate. The mean of these five values was used in the statistical analysis. The experiment was terminated
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after 72 h and was conducted at 21 ± 4◦ C, 14:10 L:D.
Statistical analyses Data from the field experiment, and from the laboratory experiment comparing the movement-risk to clumping-risk hypothesis, were analyzed by ANOVA with plant diversity, predator, and the interaction term included in the model. A significant predator × plant diversity interaction is expected under the hypothesis that Nabis is more (or less) effective in polyculture. Significant ANOVAs were followed by Tukey post hoc tests. The Petri-dish experiment produced nonnormal data so the non-parametric Wilcoxon test was used. The abundance of leafhopper adults and nymphs at the end of the field experiment were log-transformed, and all proportional data were arcsine square-root transformed to improve normality. All analyses were conducted in JMP v. 8.0.2 (SAS Institute, Cary, North Carolina, USA).
Results Field experiment Nabis significantly reduced the leafhopper abundance index (F1,44 = 9.29, P = 0.004), and the effect of Nabis depended on plant diversity (Nabis × plant diversity interaction: F1,44 = 4.05, P = 0.050). There was no main effect of plant diversity on the leafhopper abundance index (F1,44 = 0.004, P = 0.952). Tukey post hoc tests indicated that Nabis had no effect on the leafhopper abundance index in monoculture, but significantly reduced the leafhopper abundance index in polyculture (Fig. 2A). These patterns were no longer evident at the end of the experiment when destructive sampling was conducted and the number of surviving adult leafhoppers was analyzed (P > 0.05 for plant diversity and Nabis main effects, and for the interaction term). Leafhoppers injured alfalfa, as evidenced by the hopperburn they caused (‘leafhoppers present and Nabis absent’ versus ‘leafhoppers and Nabis absent’, t30 = −3.48, P = 0.002). There was a marginally significant Nabis × plant diversity interaction (F1,44 = 3.67, P = 0.062). The main effect of Nabis on hopperburn was significant (F1,44 = 13.15, P < 0.001), but there was no main effect of plant diversity on hopperburn (F1,44 = 0.264, P = 0.61). Tukey post hoc tests indicated that Nabis significantly reduced hopperburn in polyculture but not in monoculture (Fig. 2B). There were significantly fewer leafhopper nymphs per alfalfa stem in polyculture than in monoculture (F1,44 = 4.74, P = 0.035). Nabis had no detectable effect on leafhopper nymph density in either plant treatment (P > 0.05 for Nabis and Nabis × plant diversity). Alfalfa stem weight did not differ among treatments (P > 0.05 for plant diversity, Nabis, and the interaction term).
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Laboratory experiments investigating mechanisms In the experiment examining leafhopper movement in the alfalfa monoculture and polyculture treatments, more leafhoppers were captured by sticky traps in polyculture (t18 = 2.39, P = 0.028; Fig. 3A). In the experiment examining the effect of leafhopper movement on predation risk, Nabis captured significantly more leafhoppers when they were mobile than when they were immobilized (Wilcoxon test, χ2 = 5.84, df = 1, P = 0.016; Fig. 3B). In the experiment designed to distinguish between the movement-risk and clumping-risk hypotheses, leafhoppers showed a clumped distribution in polyculture, as evidenced by the fact that leafhoppers were observed on the host and nonhost plant 94 and 6% of the time, respectively. As expected, leafhoppers moved more in the grass monoculture than in the polyculture (t19 = −4.29, P < 0.001; Fig. 4A). The effect of Nabis depended on plant diversity (Nabis × plant diversity, F1,36 = 5.82, P = 0.021; Nabis main effect, F1,36 = 21.35, P < 0.001; plant diversity main effect, F1,36 = 13.8, P < 0.001). Tukey-post hoc tests indicated that Nabis significantly reduced leafhopper survival in the grass monoculture, but not in polyculture (Fig. 4B).
Discussion Intercropping alfalfa with orchardgrass increased predation of adult leafhoppers and protected alfalfa from herbivory, as predicted by the enemies hypothesis. However, the increased efficiency of Nabis appears to result from greater leafhopper movement in polyculture, not from alternative resources provided by plant diversity. Thus, the results of this study reveal a novel mechanism by which the enemies hypothesis may operate (Fig. 1, dashed arrows). Moreover, these results suggest that, when plant diversity increases herbivore movement, the resource concentration and enemies hypotheses may often be complementary. The hypothesis that Nabis is more effective in polyculture than in monoculture was tested with three different response variables: the (time-averaged) abundance index, plant injury in the form of hopperburn, and the abundance of adult leafhoppers surviving at the end of the experiment. Results from the abundance index and the hopperburn data indicated that Nabis was more effective at killing adult leafhoppers, and protecting alfalfa from herbivory, in polyculture than in monoculture. However, analysis of adult leafhopper abundance at the end of the experiment revealed no significant treatment effects. This inconsistency probably occurred because, after 13 days, mortality from senescence obscured the effects of Nabis. Indeed, the maximum number of adult leafhoppers recovered from a (predator-free) enclosure at the end of the experiment was six, indicating 80%
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Fig. 4. Leafhopper movement and survival in grass monoculture and polyculture containing grass and a legume. (A) Leafhopper movement index. (B) Percent survival of leafhoppers in grass mono- and polyculture. Different letters indicate significant differences as determined by Tukey post hoc tests (P < 0.05). Data are means ± S.E.M. Please cite this article in press as: Straub, C. S., et al. Plant diversity increases herbivore movement and vulnerability to predation. Basic and Applied Ecology (2013), http://dx.doi.org/10.1016/j.baae.2013.12.004
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mortality in this enclosure. Thus, the abundance index and the hopperburn data, which show the cumulative effects of leafhopper feeding, may better reflect the trophic interactions that occurred during the experiment. Moreover, these data are consistent with the results of an earlier laboratory study of this system (Straub et al. 2013). The number of leafhopper nymphs per stem of alfalfa was lower in polyculture than in monoculture. The fresh weight of alfalfa stems in mono- and polyculture was similar, suggesting that differences in alfalfa quality did not contribute to the result. A more likely mechanism is that the grasses directly interfered with adult leafhoppers’ ability to locate alfalfa and thus reduced their opportunity to oviposit, as expected under the resource concentration hypothesis (Fig. 1, upper pathway). Nabis has the ability to feed on leafhopper adults, nymphs, and eggs (Martinez & Pienkowski 1982), and we expected that nymph abundance would mirror adult abundance, with Nabis reducing nymphs more in polyculture than in monoculture. However, there were no main or interactive effects of Nabis on nymphs. While this result was somewhat surprising, it should be noted that the mean abundance of nymphs did follow the same pattern as the adult abundance index and hopperburn, but there was more variation in nymph numbers within treatments. The source of this variation may have been the sex ratio of adult leafhoppers, which was not standardized across enclosures. Random differences in sex ratio could have affected the number of nymphs that were produced by the adult generation and obscured the effects of Nabis on nymph abundance. Future studies should attempt to standardize the sex ratio. The movement-risk hypothesis (Fig. 1, dashed arrows) assumes that intercropping with grass increases leafhopper movement. In the laboratory, more leafhoppers were captured by sticky traps when the alfalfa was intercropped with orchardgrass, validating this assumption. The finding that intercropping promotes leafhopper movement is consistent with the results of a similar study (Roda et al. 1997), and with the general view that intercropping can promote pest movement out of agricultural fields (Vandermeer 1989; Banks & Ekbom 1999; Cook et al. 2007). Of course, the movementrisk hypothesis assumes that plant diversity will increase herbivores’ movement within the field, and not just out of the field. While this has not yet been demonstrated for the potato leafhopper, it is a reasonable assumption with empirical support from other systems (e.g., Risch 1981). A second assumption of the movement-risk hypothesis is that greater movement increases leafhoppers’ vulnerability to predation. This assumption was supported by the Petri-dish experiment, in which Nabis captured mobile leafhoppers at a significantly higher rate than leafhoppers immobilized by freezing. It should be noted that immobilizing leafhoppers by freezing also killed them, which introduces a confounding factor that could have influenced the results. However, our observations indicate that the variation in capture rate was caused by differences in leafhopper movement, with moving leafhoppers being detected more easily. Nabis appeared to
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detect the live, mobile prey almost immediately after the trial began and responded by orienting toward the prey and adopting either a sit-and-wait or a sit-and-pursue strategy. Most often, they captured leafhoppers that walked or flew within striking range of their raptorial forelegs. In contrast, when the leafhoppers were immobile, Nabis roamed around the dish without orienting toward its prey. When their antennae passed over an immobile leafhopper, they struck with their raptorial forelegs. Thus, Nabis readily accepted the dead, immobile leafhoppers, but they were slower to detect them. Nabis are known to use both vision and olfaction to locate prey (Freund & Olmstead 2000). Our behavioral observations suggest that leafhopper movement provided visual cues that were immediately detected by Nabis and that, in the absence of such visual cues, Nabis relied on olfactory cues that were only detectable if they were very close to their prey. The finding that Nabis is more effective against mobile prey is consistent with studies of other visually oriented predatory arthropods. Prey movement has been experimentally manipulated by freezing (Eubanks & Denno 2000), by using video projections in which prey movement is varied (Persons & Uetz 1997), and by utilizing host plants that vary in quality (Kaneda 1986; Johnson & Gould 1992). In each of these cases, greater movement by prey resulted in higher predation risk, as predicted by the movement-risk hypothesis. In the experiment comparing the movement-risk and clumping-risk hypotheses, the grass monoculture increased leafhopper movement and vulnerability to Nabis. This finding favors the movement-risk hypothesis, although it is possible that clumping promotes leafhopper predation to a lesser degree. A third hypothesis for how grasses enhance the predation of leafhoppers is that Nabis is more effective on structurally simple grasses than on structurally complex legumes. However, this ‘vegetation structure-risk hypothesis’ is unlikely to explain why Nabis was more effective in polyculture than in a legume monoculture. In the polyculture treatments and in the absence of Nabis, leafhoppers were observed on the grass 0.02% and 6% of the time in the field and laboratory experiment, respectively. When Nabis was present, there was still a strong preference for alfalfa with leafhoppers observed on grass 5% and 9% of the time in the field and laboratory experiment, respectively. Thus, leafhoppers spent little time on the grass when legumes were present and so it is unlikely that they were captured there. It is widely accepted that prey face a tradeoff between foraging activity and predator avoidance, such that greater foraging activity increases energy intake but comes at the cost of a higher encounter rate with predators (McNamara & Houston 1987; Anholt & Werner 1995; Lima 1998). It is also widely recognized that intercropping with nonhost plants causes pests to move more in search of their hosts (Vandermeer 1989). Taken together, these observations suggest that intercropping can promote pest movement and vulnerability to predation. The results of this study confirm this movement-risk hypothesis, and reveal a novel mechanism by which plant diversity can reduce herbivory.
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Importantly, this mechanism may be exploited to improve pest management. ‘Push–pull’ systems, where nonhost intercrops are combined with trap crops, can have synergistic effects on pest suppression (Cook et al. 2007). ‘Push-ambush’ systems, where nonhost intercrops are combined with management practices that increase predator abundance, such as floral provisioning (Landis, Wratten, & Gurr 2000) or manipulation of herbivore-induced plant volatiles (HIPVs, Mumm & Dicke 2010), may do the same. It is possible that the movement-risk hypothesis depends on enemy foraging mode, with enemies that primarily ambush or stalk their prey benefiting from increased prey movement more than enemies that actively roam (Huey & Pianka 1981). Studies investigating which types of enemy benefit from increased prey movement, and which types of management practices can best attract these enemies, may yield advances in ecologically based pest management.
Acknowledgments The authors thank the Ursinus College Department of Biology and the UC Summer Fellows program for financial assistance. The authors also offer thanks to Matthew Wismer of Northern Star farm for allowing them to work in his alfalfa field, to George Didden Greenhouses, Inc. for the pots used in the experiments, and to William E. Snyder and three anonymous reviewers for comments that greatly improved the manuscript.
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Sheehan, W. (1986). Response by specialist and generalist natural enemies to agroecosystem diversification: A selective review. Environmental Entomology, 15, 456–461. Smith, J. G. (1976). Influence of crop background on natural enemies of aphids on Brussels sprouts. Annals of Applied Biology, 83, 15–29. Straub, C. S., Simasek, N., Gapinski, N. P., Dohm, M. R., Aikens, R., & Muscella, E. O. S. (2013). Influence of nonhost plant diversity and natural enemies on the potato leafhopper, Empoasca fabae, and pea aphid, Acyrthosiphon pisum, in alfalfa. Journal of Pest Science, 86, 235–244. Vandermeer, J. (1989). The ecology of intercropping. Cambridge: Cambridge University Press.
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Plant diversity increases herbivore movement and vulnerability to predation Cory S. Straub∗ , Nathan P. Simasek, Regan Dohm, Mark R. Gapinski, Ellen O. Aikens, Cody Nagy Department of Biology, Ursinus College, 601 E. Main Street, Collegeville, PA 19426-1000, USA Received 21 May 2013; accepted 9 December 2013
Abstract Understanding how changes in plant diversity affect agroecosystem functioning remains a key challenge. We examined how intercropping alfalfa, Medicago sativa, with orchardgrass, Dactylis glomerata, affects the potato leafhopper, Empoasca fabae, its host plant (alfalfa), and the efficiency of a leafhopper predator, Nabis americoferus. In a field experiment, intercropping reduced the reproductive efficiency of the leafhopper. Nabis was more effective at reducing leafhopper abundance, and protecting alfalfa from hopperburn, in the polyculture than in the monoculture of alfalfa. In a series of laboratory experiments, we investigated mechanisms by which intercropping could enhance the efficiency of Nabis. Intercropping resulted in changes in vegetation structure and the spatial distribution of leafhoppers, but there was little evidence that these factors influenced the efficiency of Nabis. Instead, orchardgrass, a nonhost for leafhoppers, increased leafhopper movement, and Nabis captured leafhoppers more efficiently when the herbivores were more mobile. These results indicate that intercropping with nonhost plants promotes leafhopper movement and vulnerability to predation, and reveal a novel mechanism by which plant diversity can reduce herbivory.
Zusammenfassung Zu verstehen, wie Änderungen der Pflanzendiversität die Funktion von Agrarökosystemen beeinflusst, bleibt eine wichtige Aufgabe. Wir untersuchten wie die Mischkultur von Alfalfa (Medicago sativa) und Wiesen-Knäuelgras (Dactylis glomerata) die Amerikanische Kartoffelzikade (Empoasca fabae), ihre Wirtspflanze und die Effizienz eines Zikadenräubers (Nabis americoferus) beeinflusst. In einem Freilandexperiment, reduzierte die Mischkultur die Fortpflanzungseffizienz der Kartoffelzikade. In der Mischkultur reduzierte Nabis die Zikadenabundanz und den Zikadenbrand auf Alfalfa mit größerer Effizienz als in der Reinkultur. In einer Reihe von Laborexperimenten untersuchten wir die Mechanismen, durch die die Mischkultur die Effizienz von Nabis steigern könnte. Mischkultur resultierte in Veränderungen der Vegetationsstruktur und der räumlichen Verteilung der Zikade, aber es gab kaum Hinweise, dass diese Faktoren die Effizienz von Nabis beeinflussten. Vielmehr verstärkte das Knäuelgras, das von den Zikaden nicht genutzt werden kann, die Bewegungen der Zikaden, und Nabis fing Zikaden mit höherer Effizienz, wenn diese mobiler waren. Diese Ergebnisse zeigen, dass Mischkultur mit Nicht-Wirten die Bewegungsaktivität der Zikaden erhöht und damit ihre Anfälligkeit für Prädation, und sie enthüllen einen neue Mechanismus, durch den die Pflanzendiversität den Herbivorendruck verringern kann. © 2013 Gesellschaft für Ökologie. Published by Elsevier GmbH. All rights reserved. Keywords: Biodiversity; Agriculture; Intercropping; Biological control; Resource concentration; Enemies hypothesis; Leafhopper
∗ Corresponding
author. Tel.: +1 610 409 3306; fax: +1 610 409 3633. E-mail address: [email protected] (C.S. Straub).
1439-1791/$ – see front matter © 2013 Gesellschaft für Ökologie. Published by Elsevier GmbH. All rights reserved. http://dx.doi.org/10.1016/j.baae.2013.12.004
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Introduction Understanding how changes in plant diversity affect agroecosystem functioning remains a key challenge for sustainable agriculture. Agricultural ecologists have long suspected that pest outbreaks, and the need for pesticides that threaten environmental and human health, may be reduced by increasing plant diversity within agricultural fields (Pimentel 1961). Numerous studies have investigated this possibility, and reviews of these studies have come to a similar conclusion – most of the time plant diversity reduces herbivore abundance and damage to crops (Andow 1991; Russell 1989; Letourneau et al. 2011; but see Bommarco & Banks 2003 for an important caveat). In the most recent of these reviews, the authors concluded that while crop diversification is generally effective in reducing herbivory, a mechanistic understanding for why these schemes work is often missing. This limits our ability to engineer, in a directed way, diversification schemes that will effectively control particular pest species (Letourneau et al. 2011). Explanations for how plant diversity reduces herbivore abundance and damage include the ‘resource concentration’ and ‘enemies’ hypotheses. The resource concentration hypothesis states that insect herbivores are more likely to find and remain on their host plants in monocultures, where their host plants are concentrated, than in polycultures, where their host plants are dispersed among nonhost plant species (Root 1973). Under the resource concentration hypothesis, plant diversity reduces herbivory by reducing the relative abundance of herbivores’ host plants. This, in turn, reduces herbivores’ encounter rate with, or residence time on, host plants (Fig. 1, upper pathway). The enemies hypothesis states that natural enemies are less abundant and/or effective in monocultures than in polycultures, because polycultures include plant species that provide enemies with alternative prey, shelter, or a favorable microclimate (Root 1973). Under the enemies hypothesis, plant diversity reduces herbivory by providing resources to enemies that control herbivore populations (Fig. 1, lower pathway). Diversification schemes that promote both the resource concentration and enemies hypotheses will be more effective than schemes that promote only one of them. However, these mechanisms are not always compatible. For example, increasing plant diversity may reduce herbivore abundance via a resource concentration effect, but may simultaneously reduce the foraging efficiency of natural enemies (Smith 1976; Sheehan 1986). The potato leafhopper, Empoasca fabae, provides an excellent opportunity to explore the mechanisms by which plant diversity reduces herbivory. Numerous studies have shown that increasing plant diversity can reduce the abundance of the potato leafhopper on focal crops (Oloumi-Sadeghi, Zavaleta, Lamp, Armbrust, & Kapusta 1987; Roltsch & Gage 1990; Lamp 1991; Andow 1992; Roda, Landis, & Miller 1997). Grass intercrops may be particularly effective, because potato leafhoppers cannot develop or reproduce on them (Lamp, Nielson, & Danielson 1994). The specific mechanism(s) by
which grass intercrops reduce leafhopper abundance are not fully understood, but it seems likely that a resource concentration effect contributes. Roda et al. (1997) showed that leafhoppers do not discriminate between their host plants and grasses until after contact, and that intercropping alfalfa with grasses causes them to emigrate from plant patches. Thus, grass intercrops could reduce leafhopper foraging efficiency and could potentially “push” leafhoppers out of intercropped fields if they repeatedly encounter grass intercrops. Pushing pests with nonhost intercrops is often more effective if they eventually encounter and remain on an attractive trap crop, as occurs in push-pull systems (Cook, Khan, & Pickett 2007). Pushing pests with nonhost plants could also be more effective if it increased their encounters with natural enemies, although this possibility has not been rigorously evaluated. In a previous study, we found that weedy grasses reduce leafhopper abundance and damage to alfalfa (Straub et al. 2013). The resource concentration effect likely contributed to this finding (Fig. 1), but there was also evidence for the enemies hypothesis. Specifically, the predator:prey ratio was higher in the weedy plots, and one predator, Nabis americoferus, was more effective in a microcosm experiment when grasses were present. Thus, this system appears to be one in which the resource concentration and enemies hypotheses are complementary, but the exact mechanism by which the enemies hypothesis operates remains unknown. In the earlier study, we hypothesized that the grasses reduced leafhoppers’ host plant encounter rate, and that leafhoppers compensated for this by increasing their host searching behavior. As a consequence, leafhoppers were more likely to encounter and be killed by predators. We call this the ‘movement-risk hypothesis’ (Fig. 1, dashed arrows). The purpose of the present study was to attempt to replicate the earlier finding that Nabis is more effective in polyculture, and to more rigorously examine the movement-risk hypothesis. In addition, the previous study (Straub et al. 2013) had two limitations: it was conducted in a laboratory setting, and fava bean was used as a surrogate for the focal crop, alfalfa. To address these issues, the present study was conducted in the field with alfalfa. Following the field experiment, we conducted a series of laboratory experiments to test assumptions of the movement-risk hypothesis and to evaluate an alternative hypothesis.
Materials and methods Field experiment An enclosure experiment was conducted in an alfalfa field intercropped with orchardgrass at Northern Star Farm in Trappe, PA, USA. The alfalfa (HarvestarTM 504VP) and orchardgrass (‘Potomac’) were seeded together at 20 and 4.5 kg/ha, respectively. The field was planted three years prior to the experiment, in late summer 2007, and the experiment took place from 30 June to 12 July 2010. Enclosures were
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Resource concentration hypothesis
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Concentration of herbivores’ host plants
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+ Herbivore movement
Plant diversity
+
Herbivores’ host plant encounter rate (and fitness)
Abundance of enemy resources, microclimate
+ +
Enemy impact
Herbivore abundance, plant damage
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Enemies hypothesis Fig. 1. Pathways by which plant diversity may reduce herbivore abundance and damage to host plants. Solid lines indicate established pathways. The dashed line indicates the hypothetical pathway tested in this study.
0.6 m × 0.6 m × 0.6 m (BugDorm model #3120, MegaView Science, Co., Ltd.) and were placed in the field approximately one week after the first harvest of the growing season. The enclosures were arranged in a roughly linear array, avoiding patches of bare ground, with ∼0.25 m separating each enclosure. The bottom edges were dug into the soil ∼5 cm and buried with sand to prevent arthropods from entering or leaving. Naturally occurring arthropods were removed from the enclosures using a leaf vacuum (Stihl SH 56C Shredder vac). Each enclosure was searched after vacuuming and remaining arthropods were removed by hand. Our central hypothesis was that intercropping alfalfa with grass would increase leafhoppers’ risk of predation. Therefore, plant diversity and predators were manipulated in a 2 (monoculture, polyculture) × 2 (Nabis present, Nabis absent) factorial design. Each of the four treatment combinations was replicated 12 times. In addition, eight enclosures (four monocultures, four polycultures) served as no-leafhopper controls. Enclosures were randomly assigned to treatment. The monoculture treatment was created by removing all orchardgrass (using the claw of a hammer) and by further pruning so that each of the enclosures contained ∼32 alfalfa stems. The polyculture treatment was created by pruning each enclosure to contain ∼16 alfalfa stems and by removing orchardgrass as necessary so that the total amount of plant material in polycultures (i.e., ∼16 alfalfa stems + orchardgrass) visually matched the total amount of plant material in the monocultures (i.e., ∼32 alfalfa stems). Adult leafhoppers were collected with sweep nets from a nearby alfalfa field and were introduced to the enclosures on the same day they were collected. All Nabis were collected within two days of the start of the experiment and were stored individually in plastic vials at 5 ◦ C until release into the enclosures. Treatments receiving leafhoppers were stocked with 30 adults. Treatments receiving Nabis were stocked with four individuals, which is within the range of densities found in the field (range, 0–6 individuals per 0.60 m3 , unpublished data).
The experiment lasted 13 days. For the first nine days, daily observations were made through a clear window in the enclosures. During 1-min scans, the number of adult leafhoppers observed within the enclosures was recorded. The time-averaged data from these nine observations were used as an index of leafhopper abundance. It is possible that leafhoppers were easier to observe in polyculture than in monoculture because the polyculture treatment increases leafhopper movement. If this is true, our estimates of leafhopper abundance could have been artificially inflated for the polyculture treatment. However, the hypothesis that Nabis is more effective in polyculture predicts that the difference in leafhopper abundance between the Nabis-present and Nabisabsent treatments should be greater in polyculture than in monoculture. Importantly, the observational bias described above, if present, would not have affected this comparison. At the end of the experiment, when destructive sampling could be conducted, the surviving adult leafhoppers were collected with aspirators. These data, which reflect only a single point in time, were used as an additional measure of adult leafhopper abundance. In addition, ten alfalfa stems were haphazardly selected and removed from each enclosure on day 13, and the number of leafhopper nymphs found on these stems was recorded. Nymphs were not added to the enclosures and so were most likely produced during the course of the experiment. Leafhopper injury to alfalfa was assessed by calculating the percentage of leaflets that showed “hopperburn”, or V-shaped yellow triangles, on the ten alfalfa stems. The fresh weight of the stems was also recorded.
Laboratory experiments investigating mechanisms The movement-risk hypothesis makes two assumptions: (1) potato leafhoppers move more in polyculture than in monoculture, and (2) greater movement makes leafhoppers
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grass monoculture (nonhost plants only) than in polyculture more vulnerable to predators. To evaluate the first assump(nonhost and host plants), but be more clumped in the latter tion, the movement of leafhoppers in monoculture (n = 10) treatment, the movement-risk hypothesis predicts that Nabis and polyculture (n = 10) was evaluated. The experimental microcosms were clear plastic tubes (15 cm diameter, 30 cm will kill more leafhoppers in a grass monoculture, while the height) encasing plants in a 17-cm diameter pot. The tubes ‘clumping-risk hypothesis’ makes the opposite prediction. To evaluate the relative importance of these two hypothehad a plastic mesh top with mesh holes (2 mm2 ) large enough for leafhoppers to easily pass through. The bottoms of 0.35-L ses, we conducted a 2 (grass monoculture, polyculture) × 2 plastic cups were cut off to create smaller tubes (8 cm diam(Nabis present, absent) factorial experiment. Each treatment eter, 7 cm height). These smaller tubes were placed on the combination was replicated ten times. Fava bean was used plastic mesh and served as supports for sticky traps. The as a surrogate for alfalfa because it is easier to cultivate in sticky traps were created by applying Tangle-trap® (Conthe greenhouse. The results observed in the field experiment described above were very similar to the results of a differtech Enterprises, Inc.) to the underside of clear plastic plates ent experiment in which fava was used as a surrogate for (15 cm diameter). The plates were placed on top of the smaller alfalfa (Straub et al. 2013), indicating that the substitution tubes, sticky-side down, and mesh fabric was placed over of fava for alfalfa does not change predator–prey dynamics the plate and connected to the larger tube with a rubber in this system. Orchardgrass and fava bean were grown in band. The mesh fabric allowed airflow into the microcosm but prevented leafhoppers from escaping. Thus, leafhopthe greenhouse and experimental plants were 6 and 2 weeks pers that passed through the plastic mesh became stuck in old, respectively. The orchardgrass monoculture included 12 the sticky trap. Alfalfa and orchardgrass were transplanted blades of grass and the polyculture included 6 blades of grass from the field and were ∼15 cm in height. Alfalfa monoculand one fava plant. Six adult leafhoppers from the laboratory tures included ∼12 stems of alfalfa and alfalfa polycultures colony were introduced to the microcosms, which were clear included ∼6 stems of alfalfa and a small bunch of orchardplastic tubes (15 cm diameter, 30 cm height) with a mesh top encasing plants in a 17-cm diameter pot. Before introducing grass so that there was a similar amount of plant material in mono- and polyculture. Thus, the polyculture treatment had the leafhoppers, they were anesthetized with CO2 . This process killed one leafhopper in several replicates. We corrected a similar alfalfa:grass ratio (∼1:1) as the field experiment. for this unintentional source of mortality by using the folAdult leafhoppers were collected from a laboratory colony reared on fava bean. Eight adult leafhoppers were aspirated lowing ratio as the response variable: number of leafhoppers alive at the end of the experiment/number of leafhoppers alive into plastic vials and introduced to each of the microcosms. at the beginning of the experiment. Some leafhoppers died or escaped during the introduction, so In addition to measuring leafhopper survival, observations the actual number of leafhoppers introduced varied between of leafhoppers were conducted with the goal of confirming five and eight. The percentage of leafhoppers captured by the that leafhoppers showed a clumped distribution in polyculsticky trap after 24 h (at 21 ± 4◦ C, 14:10 L:D) was recorded ture (i.e., preferred fava to grass) and moved more in the and provided an index of leafhopper movement. To evaluate the assumption that greater movement makes grass monoculture than in the polyculture. On six occasions leafhoppers more vulnerable to predation, leafhopper moveseparated by at least 3 h, the locations of leafhoppers in each replicate were recorded. The first and last observations ment was directly manipulated. Three adult leafhoppers were were separated by 55 h. During each observation, the numintroduced to Petri dishes (10 cm diameter, 1.5 cm height). There were two treatments: mobile leafhoppers (n = 15) and ber of leafhoppers observed at seven locations was recorded immobile leafhoppers (n = 15). The latter were immobilized for the movement analysis: vegetation (fava and/or grass), by freezing at −20 ◦ C for 10 min. The immobilized leafhopsoil, mesh ceiling, or one of four quadrats of the plastic pers were dead, but Nabis readily consumed dead leafhoppers tube. A movement index was created, which quantifies the upon encounter. A single, field-collected adult Nabis was extent to which leafhoppers changed their locations from starved for 24 h and introduced to each Petri dish. The total one observation period to the next. This was calculated as: number of leafhoppers captured in 1 h was recorded. 2 (A1 − A2)2 + (B1 − B2)2 + (C1 − C2)2 + (D1 − D2)2 + (E1 − E2)2 + (F 1 − F 2)2 + (G1 − G2)2 In addition to increasing leafhopper movement, intercropping alfalfa with orchardgrass could change the spatial distribution of leafhoppers. Specifically, leafhoppers in monoculture should be uniformly distributed, while leafhoppers in polyculture should be clumped because they aggregate on the fewer host plants (alfalfa stems) that are available. This clumped distribution could increase the efficiency of Nabis if, for example, it uses area-restricted searching behavior (e.g., Cronin 2009). Because leafhoppers should move more in a
where A–G represent the number of leafhoppers observed in the seven possible locations, and 1 and 2 represent the first and second observation period. The equation quantifies the extent to which leafhoppers changed their locations in between the first and second observation periods. There were six observation periods, providing five opportunities to calculate the movement index for each replicate. The mean of these five values was used in the statistical analysis. The experiment was terminated
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after 72 h and was conducted at 21 ± 4◦ C, 14:10 L:D.
Statistical analyses Data from the field experiment, and from the laboratory experiment comparing the movement-risk to clumping-risk hypothesis, were analyzed by ANOVA with plant diversity, predator, and the interaction term included in the model. A significant predator × plant diversity interaction is expected under the hypothesis that Nabis is more (or less) effective in polyculture. Significant ANOVAs were followed by Tukey post hoc tests. The Petri-dish experiment produced nonnormal data so the non-parametric Wilcoxon test was used. The abundance of leafhopper adults and nymphs at the end of the field experiment were log-transformed, and all proportional data were arcsine square-root transformed to improve normality. All analyses were conducted in JMP v. 8.0.2 (SAS Institute, Cary, North Carolina, USA).
Results Field experiment Nabis significantly reduced the leafhopper abundance index (F1,44 = 9.29, P = 0.004), and the effect of Nabis depended on plant diversity (Nabis × plant diversity interaction: F1,44 = 4.05, P = 0.050). There was no main effect of plant diversity on the leafhopper abundance index (F1,44 = 0.004, P = 0.952). Tukey post hoc tests indicated that Nabis had no effect on the leafhopper abundance index in monoculture, but significantly reduced the leafhopper abundance index in polyculture (Fig. 2A). These patterns were no longer evident at the end of the experiment when destructive sampling was conducted and the number of surviving adult leafhoppers was analyzed (P > 0.05 for plant diversity and Nabis main effects, and for the interaction term). Leafhoppers injured alfalfa, as evidenced by the hopperburn they caused (‘leafhoppers present and Nabis absent’ versus ‘leafhoppers and Nabis absent’, t30 = −3.48, P = 0.002). There was a marginally significant Nabis × plant diversity interaction (F1,44 = 3.67, P = 0.062). The main effect of Nabis on hopperburn was significant (F1,44 = 13.15, P < 0.001), but there was no main effect of plant diversity on hopperburn (F1,44 = 0.264, P = 0.61). Tukey post hoc tests indicated that Nabis significantly reduced hopperburn in polyculture but not in monoculture (Fig. 2B). There were significantly fewer leafhopper nymphs per alfalfa stem in polyculture than in monoculture (F1,44 = 4.74, P = 0.035). Nabis had no detectable effect on leafhopper nymph density in either plant treatment (P > 0.05 for Nabis and Nabis × plant diversity). Alfalfa stem weight did not differ among treatments (P > 0.05 for plant diversity, Nabis, and the interaction term).
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Laboratory experiments investigating mechanisms In the experiment examining leafhopper movement in the alfalfa monoculture and polyculture treatments, more leafhoppers were captured by sticky traps in polyculture (t18 = 2.39, P = 0.028; Fig. 3A). In the experiment examining the effect of leafhopper movement on predation risk, Nabis captured significantly more leafhoppers when they were mobile than when they were immobilized (Wilcoxon test, χ2 = 5.84, df = 1, P = 0.016; Fig. 3B). In the experiment designed to distinguish between the movement-risk and clumping-risk hypotheses, leafhoppers showed a clumped distribution in polyculture, as evidenced by the fact that leafhoppers were observed on the host and nonhost plant 94 and 6% of the time, respectively. As expected, leafhoppers moved more in the grass monoculture than in the polyculture (t19 = −4.29, P < 0.001; Fig. 4A). The effect of Nabis depended on plant diversity (Nabis × plant diversity, F1,36 = 5.82, P = 0.021; Nabis main effect, F1,36 = 21.35, P < 0.001; plant diversity main effect, F1,36 = 13.8, P < 0.001). Tukey-post hoc tests indicated that Nabis significantly reduced leafhopper survival in the grass monoculture, but not in polyculture (Fig. 4B).
Discussion Intercropping alfalfa with orchardgrass increased predation of adult leafhoppers and protected alfalfa from herbivory, as predicted by the enemies hypothesis. However, the increased efficiency of Nabis appears to result from greater leafhopper movement in polyculture, not from alternative resources provided by plant diversity. Thus, the results of this study reveal a novel mechanism by which the enemies hypothesis may operate (Fig. 1, dashed arrows). Moreover, these results suggest that, when plant diversity increases herbivore movement, the resource concentration and enemies hypotheses may often be complementary. The hypothesis that Nabis is more effective in polyculture than in monoculture was tested with three different response variables: the (time-averaged) abundance index, plant injury in the form of hopperburn, and the abundance of adult leafhoppers surviving at the end of the experiment. Results from the abundance index and the hopperburn data indicated that Nabis was more effective at killing adult leafhoppers, and protecting alfalfa from herbivory, in polyculture than in monoculture. However, analysis of adult leafhopper abundance at the end of the experiment revealed no significant treatment effects. This inconsistency probably occurred because, after 13 days, mortality from senescence obscured the effects of Nabis. Indeed, the maximum number of adult leafhoppers recovered from a (predator-free) enclosure at the end of the experiment was six, indicating 80%
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Fig. 2. Effect of plant diversity and Nabis on leafhoppers and alfalfa. (A) Time-averaged index of adult leafhopper abundance. (B) Percentage of alfalfa leaflets with “hopperburn”. Different letters indicate significant differences as determined by Tukey post hoc tests (P < 0.05). Data are means ± S.E.M. 60
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Fig. 4. Leafhopper movement and survival in grass monoculture and polyculture containing grass and a legume. (A) Leafhopper movement index. (B) Percent survival of leafhoppers in grass mono- and polyculture. Different letters indicate significant differences as determined by Tukey post hoc tests (P < 0.05). Data are means ± S.E.M. Please cite this article in press as: Straub, C. S., et al. Plant diversity increases herbivore movement and vulnerability to predation. Basic and Applied Ecology (2013), http://dx.doi.org/10.1016/j.baae.2013.12.004
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mortality in this enclosure. Thus, the abundance index and the hopperburn data, which show the cumulative effects of leafhopper feeding, may better reflect the trophic interactions that occurred during the experiment. Moreover, these data are consistent with the results of an earlier laboratory study of this system (Straub et al. 2013). The number of leafhopper nymphs per stem of alfalfa was lower in polyculture than in monoculture. The fresh weight of alfalfa stems in mono- and polyculture was similar, suggesting that differences in alfalfa quality did not contribute to the result. A more likely mechanism is that the grasses directly interfered with adult leafhoppers’ ability to locate alfalfa and thus reduced their opportunity to oviposit, as expected under the resource concentration hypothesis (Fig. 1, upper pathway). Nabis has the ability to feed on leafhopper adults, nymphs, and eggs (Martinez & Pienkowski 1982), and we expected that nymph abundance would mirror adult abundance, with Nabis reducing nymphs more in polyculture than in monoculture. However, there were no main or interactive effects of Nabis on nymphs. While this result was somewhat surprising, it should be noted that the mean abundance of nymphs did follow the same pattern as the adult abundance index and hopperburn, but there was more variation in nymph numbers within treatments. The source of this variation may have been the sex ratio of adult leafhoppers, which was not standardized across enclosures. Random differences in sex ratio could have affected the number of nymphs that were produced by the adult generation and obscured the effects of Nabis on nymph abundance. Future studies should attempt to standardize the sex ratio. The movement-risk hypothesis (Fig. 1, dashed arrows) assumes that intercropping with grass increases leafhopper movement. In the laboratory, more leafhoppers were captured by sticky traps when the alfalfa was intercropped with orchardgrass, validating this assumption. The finding that intercropping promotes leafhopper movement is consistent with the results of a similar study (Roda et al. 1997), and with the general view that intercropping can promote pest movement out of agricultural fields (Vandermeer 1989; Banks & Ekbom 1999; Cook et al. 2007). Of course, the movementrisk hypothesis assumes that plant diversity will increase herbivores’ movement within the field, and not just out of the field. While this has not yet been demonstrated for the potato leafhopper, it is a reasonable assumption with empirical support from other systems (e.g., Risch 1981). A second assumption of the movement-risk hypothesis is that greater movement increases leafhoppers’ vulnerability to predation. This assumption was supported by the Petri-dish experiment, in which Nabis captured mobile leafhoppers at a significantly higher rate than leafhoppers immobilized by freezing. It should be noted that immobilizing leafhoppers by freezing also killed them, which introduces a confounding factor that could have influenced the results. However, our observations indicate that the variation in capture rate was caused by differences in leafhopper movement, with moving leafhoppers being detected more easily. Nabis appeared to
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detect the live, mobile prey almost immediately after the trial began and responded by orienting toward the prey and adopting either a sit-and-wait or a sit-and-pursue strategy. Most often, they captured leafhoppers that walked or flew within striking range of their raptorial forelegs. In contrast, when the leafhoppers were immobile, Nabis roamed around the dish without orienting toward its prey. When their antennae passed over an immobile leafhopper, they struck with their raptorial forelegs. Thus, Nabis readily accepted the dead, immobile leafhoppers, but they were slower to detect them. Nabis are known to use both vision and olfaction to locate prey (Freund & Olmstead 2000). Our behavioral observations suggest that leafhopper movement provided visual cues that were immediately detected by Nabis and that, in the absence of such visual cues, Nabis relied on olfactory cues that were only detectable if they were very close to their prey. The finding that Nabis is more effective against mobile prey is consistent with studies of other visually oriented predatory arthropods. Prey movement has been experimentally manipulated by freezing (Eubanks & Denno 2000), by using video projections in which prey movement is varied (Persons & Uetz 1997), and by utilizing host plants that vary in quality (Kaneda 1986; Johnson & Gould 1992). In each of these cases, greater movement by prey resulted in higher predation risk, as predicted by the movement-risk hypothesis. In the experiment comparing the movement-risk and clumping-risk hypotheses, the grass monoculture increased leafhopper movement and vulnerability to Nabis. This finding favors the movement-risk hypothesis, although it is possible that clumping promotes leafhopper predation to a lesser degree. A third hypothesis for how grasses enhance the predation of leafhoppers is that Nabis is more effective on structurally simple grasses than on structurally complex legumes. However, this ‘vegetation structure-risk hypothesis’ is unlikely to explain why Nabis was more effective in polyculture than in a legume monoculture. In the polyculture treatments and in the absence of Nabis, leafhoppers were observed on the grass 0.02% and 6% of the time in the field and laboratory experiment, respectively. When Nabis was present, there was still a strong preference for alfalfa with leafhoppers observed on grass 5% and 9% of the time in the field and laboratory experiment, respectively. Thus, leafhoppers spent little time on the grass when legumes were present and so it is unlikely that they were captured there. It is widely accepted that prey face a tradeoff between foraging activity and predator avoidance, such that greater foraging activity increases energy intake but comes at the cost of a higher encounter rate with predators (McNamara & Houston 1987; Anholt & Werner 1995; Lima 1998). It is also widely recognized that intercropping with nonhost plants causes pests to move more in search of their hosts (Vandermeer 1989). Taken together, these observations suggest that intercropping can promote pest movement and vulnerability to predation. The results of this study confirm this movement-risk hypothesis, and reveal a novel mechanism by which plant diversity can reduce herbivory.
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Importantly, this mechanism may be exploited to improve pest management. ‘Push–pull’ systems, where nonhost intercrops are combined with trap crops, can have synergistic effects on pest suppression (Cook et al. 2007). ‘Push-ambush’ systems, where nonhost intercrops are combined with management practices that increase predator abundance, such as floral provisioning (Landis, Wratten, & Gurr 2000) or manipulation of herbivore-induced plant volatiles (HIPVs, Mumm & Dicke 2010), may do the same. It is possible that the movement-risk hypothesis depends on enemy foraging mode, with enemies that primarily ambush or stalk their prey benefiting from increased prey movement more than enemies that actively roam (Huey & Pianka 1981). Studies investigating which types of enemy benefit from increased prey movement, and which types of management practices can best attract these enemies, may yield advances in ecologically based pest management.
Acknowledgments The authors thank the Ursinus College Department of Biology and the UC Summer Fellows program for financial assistance. The authors also offer thanks to Matthew Wismer of Northern Star farm for allowing them to work in his alfalfa field, to George Didden Greenhouses, Inc. for the pots used in the experiments, and to William E. Snyder and three anonymous reviewers for comments that greatly improved the manuscript.
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