Trophic interactions are often studied within habitat patches, but among-patch dispersal of individuals may influence local patch dynamics. Metacommunity concepts incorporate the effects of dispersal on local and community dynamics. There are few experimental tests of metacommunity theory using insects compared to those conducted in microbial microcosms. Using connected experimental mesocosms, we varied the density of the leafhopper Agallia constricta Van Duzee (Homoptera: Cicadellidae) and a generalist insect predator, the damsel bug (Nabis spp., Heteroptera: Nabidae), to determine the effects of conspecific and predator density and varying the time available to dispersal among mesocosms on predation rates, dispersal rates, and leafhopper survival. Conspecific and damsel bug density did not affect dispersal rates in leafhoppers, but this may be due to leafhoppers’ aversion to leaving the host plants or the connecting tubes between mesocosms hindering leafhopper movement. Leafhopper dispersal was higher in high-dispersal treatments. Survival rates of A. constricta were also lowest in treatments where dispersal was not limited. This is one of the first experimental studies to vary predator density and the time available to dispersal. Our results indicate that dispersal is the key to understanding short-term processes such as prey survival in predator-prey metacommunities. Further work is needed to determine how dispersal rates influence persistence of communities in multigenerational studies. Key words: dispersal, metacommunity, survival, Cicadellidae, Nabidae Trophic interactions of insects are often studied in local communi- colonize patches with abundant prey, however, an increased numer- ties (Beckerman et al. 1997, Schmitz et al. 1997, Schmitz 2003), but ical response by the predator and a subsequent population crash dispersal among communities may be important to local dynamics. after prey are overexploited may result (Holyoak and Lawler 1996b, Metacommunity concepts incorporate dispersal among local com- Kneitel and Miller 2003, Kondoh 2003). munities and how dispersal affects biodiversity and species inter- Intermediate dispersal rates are predicted to increase the persis- actions, such as predation, parasitism, herbivory, and competition tence time of both predators and their prey due to greater recoloni- (Leibold et al. 2004, Holyoak et al. 2005). There is a well-developed zation of vacant patches than at low dispersal rates if dispersal rates body of theory for metacommunities, but there are relatively few are low enough that predators cannot overexploit their prey (Brown experimental tests of dispersal on insect predator-prey interactions and Kodric-Brown 1977, Crowley 1981, Nachman 1987, Holyoak (but see Kareiva 1987; Demptser et al. 1995; Bowne and Bowers and Lawler 1996b). This has been shown in microbial communities 2004; Cronin and Haynes 2004; Cronin 2007, 2009; Bergerot et al. provided that dispersal-limited species are able to colonize new hab- 2010; Costa et al. 2013; Start and Gilbert 2016). itat patches (Holyoak and Lawler 1996a, b; Loreau and Mouquet Dispersal rates of individuals moving among habitat patches 1999; Mouquet and Loreau 2002; Kneitel and Miller 2003; Cadotte determine the extent to which predator and prey dynamics are cou- and Fukami 2005; Hauzy et al. 2007). pled in patchy landscapes. Dispersal of both predators and their Metacommunity persistence is difficult to study in larger organ- prey may stabilize predator-prey dynamics (Holt 2002, Briggs and isms due to longer generation times (but see Bonsall et al. 2002, Hoopes 2004), but higher levels of predator dispersal may uncou- 2005; Bull et al. 2006). However, persistence may be studied by ple these dynamics due to overexploitation of prey (Holyoak and quantifying the movements of predators and prey among habitat Lawler 1996b). At low predator dispersal rates, prey may escape in patches and their effects on prey survival. This provides insights into space from predators by colonizing empty habitat patches (Holyoak mechanisms of metacommunity dynamics operating within genera- and Lawler 1996b, Costa et al. 2013). If predators are able to tions. Individual-based explanations for short-term metacommunity © The Author(s) 2017. Published by Oxford University Press on behalf of Entomological Society of America. This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs licence (http://creativecommons. org/licenses/by-nc-nd/4.0/), which permits non-commercial reproduction and distribution of the work, in any medium, provided the original work is not altered or transformed in any way, and that the work is properly cited. For commercial re-use, please contact firstname.lastname@example.org Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/1/2/4781595 by Ed 'DeepDyve' Gillespie user on 16 March 2018 2 Journal of Insect Science, 2017, Vol. 18, No. 1 dynamics include processes, such as predation (Bonsall et al. 2002, 1990; Schotzko and O’Keeffe 1989). Nabis americoferus (Carayon) 2005; Bull et al. 2006), herbivory (Matthiessen et al. 2007), and hab- (Hemiptera: Nabidae) and N. roseipennis Reuter both occur at our itat selection (Resetarits 2005, Binckley and Resetarits 2007). The study site, but it was not possible to differentiate between the species factors influencing dispersal among habitat patches are important in the field. Therefore, we randomly collected both of the species to understand as dispersal among habitat patches is thought to be from the field for use in our experiments. Previous work has indi- required for long-term metacommunity persistence (Holyoak et al. cated that any confounding effects of species are likely negligible 2005). (Östman and Ives 2003). Our aims in this study were to determine the effects of varying conspecific densities of the leafhopper Agallia constricta Van Duzee Experimental Mesocosms (Homoptera: Cicadellidae) and densities of a leafhopper predator, All experiments were conducted outdoors in arrays of caged pots of the damsel bug (Heteroptera: Nabidae, Nabis spp.), on A. contricta red clover (Trifolium pratense L.) during June to September 2008 dispersal rates and survival in connected sets of mesocosm cages at the Miami University Ecology Research Center. Cylindrical cages that regulated the time available for insect dispersal. First, we deter- were constructed using ‘no-see-um netting’ covering a wire frame mined if density-dependent dispersal occurred in A. constricta in the (28 cm × 40 cm [depth by height]) and a pot of red clover (30 cm × absence of predation, as documented in many other taxa, such as 10 cm [depth by height]) grown from the seed (Fig. 1). To remove birds, mammals, and insects (Denno and Peterson 1995, Fonseca any arthropods present on clover, pots were sprayed with organic and Hart 1996, Matthysen 2005). Specifically, we predicted greater pyrethrin insecticide before placing experimental insects in the meso- dispersal among local communities in high-density or high-dispersal cosms. After spraying, cages were placed in an open field with full treatments compared with low-density or low-dispersal treatments. sun. Pyrethrin insecticides degrade rapidly in sunlight with half-lives Second, we determined the effect of varying dispersal treatments and not exceeding 3 h (Antonious 2004). After 2 d, less than 0.05 μg of predator density on the dispersal rates of A. constricta. We predicted pesticide residue remains on 1 g of plant leaves (Antonious 2004). that leafhopper dispersal rates would be greatest in the high-dis- After 2 d, experimental leafhoppers were introduced to cages. persal and low-predator density treatments if differential dispersal Each cage contained a local community of clover, leafhoppers, and rates occurred between insect predators and prey. We further pre- predators, and three cages were linked by dispersal to create a meta- dicted that leafhopper survival would be greatest in the low-preda- community. The cages were connected using rectangular, vinyl rain tor density and intermediate levels of dispersal in accordance with gutter downspouts with the sides removed and lined with ‘no-see-um’ metacommunity theory. netting. Tubes were 10 cm × 50 cm (width by length), and dispersal was controlled by closing the ends of the tubes. Preliminary observations were conducted to ensure that leafhop- Materials and Methods pers and damsel bugs would move through the connecting tubes. Study Species Before the start of the experiment, leafhoppers were introduced into Insects were collected from clover and soybean fields at the Miami a connecting tube and observed over the course of an hour. The leaf- University Ecology Research Center, Oxford, OH, USA, during hoppers would either walk or hop along the length of the tube. After the summer of 2008. A. constricta is a generalist leafhopper that 1 h, a single damsel bug was added to the tube. Leafhoppers would consumes several families of plants, including legumes and grasses hop to the ceiling of the tube as the damsel bug approached and then (LaHue 1936, Black 1944, Nielson 1968). A. constricta is present at walk quickly away from the damsel bug toward the ends of the tube. our study site from June to September, but it is most abundant in late The three levels of the dispersal treatment were based on the July and early August (Schroeder 2007). time the connecting tubes were open: a low level with tubes open Damsel bugs are generalist predators that prey on multiple insect 5% of the time per wk, or 8 h; an intermediate level with the tubes families including aphids, plant bugs, and leafhoppers (Lattin 1989, open 30% per wk, or 48 h; and a high dispersal level with the tubes Östman and Ives 2003). They are diurnal predators who actively open 100% of the time. The 5% dispersal treatment represented forage for their prey using chemoreception and vibrations (Donahoe the low end of metapopulation dispersal where each mesocosm was and Pitre 1977; Irwin and Shepard 1980; Braman and Yeargan predicted to behave as an isolated local patch, the 30% dispersal 1989, 1990; Schotzko and O’Keeffe 1989; Freund and Olmstead treatment represented the high end of where metacommunity dy- 2000). Damsel bugs are common predators in many agricultural namics are expected to occur among local patches, and the 100% systems (Irwin and Shepard 1980; Braman and Yeargan 1989, dispersal treatment represented a single, large, patchy community Fig. 1. Diagram of experimental unit from two views (A) above and (B) ground level. Each circle or cylinder represents a community connected by tubing to allow dispersal of insects among communities. A pot of red clover was placed in each cylinder. Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/1/2/4781595 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Journal of Insect Science, 2017, Vol. 18, No. 1 3 (cf. Holyoak and Lawler 1996a). We randomly assigned periods maximizers for reproduction, whereas males may spend less time when tubes were open to movement so that different replicates were foraging to find mates (Schoener 1971). open at different times during the experiment. Each mesocosm was sampled with a suction sampler 1 d after the damsel bugs were introduced and every 2 d thereafter. Surviving leafhoppers and damsel bugs were returned to the mesocosm from Preliminary Experiment which they were sampled. If a dead damsel bug was found during To quantify leafhopper movement among mesocosms, leafhoppers sampling, it was replaced to maintain a constant predator density in different mesocosms were dusted with a different color of fluores- throughout the course of the 7-d experiment. cent powder. A preliminary experiment was conducted to determine if damsel bugs prefer to prey on a particular color of powder. A total Statistical Analyses of 25 A. constricta were dusted with red, blue, or yellow fluores- cent powder and added to single-chamber mesocosms containing a Poisson regression was used to determine the effect of conspecific single pot of red clover. A control treatment with no powder was density and dispersal treatment on dispersal rates of A. constricta in also used. Five replicates were used for each treatment. Damsel bugs the absence of predation. Both main effects were tested along with were food-deprived for 2 d and were then added to the mesocosms their interaction. Dispersal was analyzed as the total number of leaf- 1 d after the leafhoppers. Mesocosms were vacuum-sampled with a hoppers that moved among mesocosms in each treatment over the modified portable vacuum (BioQuip Products, Rancho Dominguez, course of the experiment. Poisson regression was also used to de- California) 1 d after damsel bugs were added, and the number of termine the effect of damsel bug density and dispersal treatment on surviving leafhoppers was counted. One replicate in both the yellow leafhopper dispersal rates (glm function, R Development Core Team and blue powder treatments was not included in the analysis due 2009). Both main effects were tested along with their interaction. to the damsel bug dying during the experiment. Before the analysis, The roles of predation and dispersal in leafhopper survival were data were square-root transformed. Results were analyzed using a modeled using failure-time analysis (Fox 2001). It is possible that general linear model in SPSS (IBM Corp. 2017). There was no dif- some leafhoppers may have escaped capture by finding refuge in the ference in the number of leafhoppers consumed among the color clover despite our extensive sampling efforts. Failure-time analysis treatments and the control (F = 0.751; df = 3, 14; P = 0.540). Damsel allows for the possibility that some leafhoppers may not be recov- bugs were not dusted with different colored powder to avoid altering ered alive or dead during a sampling period (right-censored data), A. constricta’s behavioral response to predators. which occurred in 2% of the total of 2,400 leafhopper counts. The exact time of an animal’s death is often not known in empirical stud- ies. The interval in which death (failure) occurred is often all that Dispersal Experiments is known. Leafhopper survival under different treatment factors of To determine the effect of prey density and dispersal treatment on predation (0, 1, or 2 damsel bugs) and dispersal rate (5, 30, and dispersal and survival rates of A. constricta, three dispersal treat- 100%) were recorded after 1, 3, 5, and 7 d so that the time to mor- ments (5, 30, and 100%) were crossed with two different densities tality can be treated as a distribution of failure times. We expected of leafhoppers per mesocosm (25 or 50). Four replicate metacom- that leafhopper mortality would not occur at a constant rate as munities of each treatment were used for a total of 72 cages and 24 food-deprived damsel bugs were expected to have high feeding rates metacommunities. Only two mesocosms were stocked with leafhop- at the beginning of the experiment and then level off as they became pers to determine if leafhopper colonization rates of an empty meso- satiated or as prey encounter rates decreased. The predictor varia- cosm differed among density or dispersal treatments. Leafhoppers bles of predation and dispersal will influence these rates, a pattern were dusted with either red or yellow fluorescent powder to quan- that is suited to using nonparametric life-table analysis (Kalbfleisch tify movements among communities. Each community was sampled and Prentice 1980, PROC LIFETEST, SAS Institute 2003). Failure- with a suction-sampler 1 d after the damsel bugs were introduced time analysis has been used to measure predation rates over time in and every 2 d thereafter. Surviving leafhoppers were counted and intertidal communities (Petraitis 1998), and the survival probability returned to the community where they were sampled. The experi- of grasshoppers in response to spider presence (Danner and Joern ment was only conducted for 5 d because of the inclement weather 2003). caused by the remnants of Hurricane Ike moving through the Oxford area. A single 50-leafhopper, 5% dispersal replicate and a single 50-leafhopper, 30% dispersal replicate did not have tubes opened Results as a result of the experiment being terminated earlier than expected; In the absence of predation, <5% (2–16 leafhoppers) of the total however, tube-open times were randomly assigned across replicates, leafhoppers within each replicate moved among the mesocosms in so this should not have biased the results among treatments. all treatments, except in the 25 leafhoppers/100% dispersal treat- We also tested the effect of dispersal treatments on A. constricta ment, where 18 of the 200 (9%) total leafhoppers moved among survival probabilities and dispersal rates in the presence of preda- local patches. There was no effect of leafhopper density on leaf- tion. For this experiment, we used a fixed density of 50 leafhoppers hopper dispersal rate (Poisson regression, Wald’s Z = 0.44; P = 0.66). per local community, and we replicated the dispersal levels as in the There was no detectable density-dependent dispersal of leafhoppers previous experiment. One mesocosm was intentionally left empty at among patches in the absence of predation. There was a significant the beginning to serve as a refuge from predation. Leafhoppers were effect of dispersal treatment on the dispersal rate of leafhoppers dusted with either blue or red fluorescent powder to quantify move- with a greater number of leafhoppers dispersing in the 100% dis- ments among cages. One day later, either one or two damsel bugs persal treatment compared with the 30 and 5% dispersal treatments were added to each of the two mesocosm cages containing leafhop- (Z = 3.11; P = 0.0019). There was no interaction between density pers, for a total of either two or four per metacommunity. We used and dispersal treatment. There was also no difference among treat- only female damsel bugs in this experiment. Female damsel bugs are ments in survival time of A. constricta in the absence of predation more voracious than males (Lingren et al. 1968, Donahoe and Pitre (χ = 1.8637; df = 5; P = 0.8677, Table 1, Fig. 2). 1977, Propp 1982, Ma et al. 2005). The females are likely energy Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/1/2/4781595 by Ed 'DeepDyve' Gillespie user on 16 March 2018 4 Journal of Insect Science, 2017, Vol. 18, No. 1 Table 1. Survival probabilities (±SE) and mean (±SD) A. constricta Leafhoppers also had higher survival probabilities in the 1-damsel surviving per day in response to varied isolation and leafhopper bug/5% dispersal treatment than in the 2-damsel bug/30% dis- density persal treatment (χ = 9.41; df = 1; P = 0.0022, Table 2, Fig. 3) and the 2-damsel bug/100% dispersal treatment (χ = 4.75; df = 1; Dispersal Density Time Survival Mean A. constricta P = 0.0293, Table 2, Fig. 3). probability(±SE) (±SD) 5 25 24 0.891 ± 0.022 22.25 ± 1.3 Discussion 72 0.851 ± 0.025 21.25 ± 2.3 5 50 24 0.946 ± 0.012 47.00 ± 1.3 Leafhopper density did not affect dispersal rates among mesocosms, but 72 0.891 ± 0.016 44.38 ± 3.1 leafhoppers moved among mesocosms more in the 100% dispersal treat- 30 25 24 0.945 ± 0.016 23.63 ± 1.1 ment compared with the 5 and 30% treatments. Despite high conspecific 72 0.891 ± 0.025 21.50 ± 2.3 densities and the opportunity to disperse among mesocosms, leafhoppers 30 50 24 0.949 ± 0.011 47.50 ± 1.1 moved infrequently among habitat patches. Densities of A. constricta 72 0.870 ± 0.017 43.63 ± 3.0 −2 can be as high as 108 leafhoppers m in the field with a mean of 35 100 25 24 0.918 ± 0.019 22.75 ± 1.4 −2 72 0.840 ± 0.026 21.00 ± 1.2 leafhoppers m (Schroeder 2007). This is equivalent to a mean of 2.56 100 50 24 0.922 ± 0.013 46.00 ± 1.2 leafhoppers per mesocosm, which have an area of 0.073 m . Therefore, 72 0.870 ± 0.017 64.88 ± 1.7 densities in the mesocosms were 10–20 times greater than the observed field densities for the 25- and 50-leafhopper density treatments, respec- ‘Dispersal’ is the percentage of time per week that connecting tubes were tively, yet movement among patches was still infrequent. open to movement. ‘Density’ is the density of leafhoppers per mesocosm. A meta-analysis by Denno and Peterson (1995) determined that ‘Time’ is the hours since the experiment commenced. declining host-plant quality is the main factor influencing emigration in sap-feeding insects. All local habitat patches in our mesocosms were of similar quality, and there was no evidence of ‘hopper burn’, a yellowing of plant leaves resulting from leafhopper feeding. Hopper burn results in stunted growth, delayed maturation, and loss of yield (Kindler et al. 1973, Wilson et al. 1979). It is not known if A. constricta causes hopper burn, but Haynes and Crist (2009) suggested that potato leafhoppers (Homoptera: Cicadellidae, Empoasca fabae) may be more associated with reductions in plant biomass than A. constricta. Leafhoppers may also be averse to leaving host plants within mescosoms, or connecting tubes may not have been conducive to hopping modes of movement by leafhoppers. Insects show an aver- sion to leaving suitable habitat patches by exhibiting exploratory behavior along the patch edge or by not approaching the patch edge (Schtickzelle and Baguette 2003, Bowler and Benton 2005, Baguette and Van Dyck 2007, Fahrig 2007, Stasek et al. 2008, Cronin 2009, Costa et al. 2013). We did not observe A. constricta’s behavior as it approached the connecting tubes, but once leafhoppers entered a connecting tube, they may not have crossed the tube due to the 5% 30% 100% tubes’ length, small diameter, or perceived increased risk of mortality (Schtickzelle and Baguette 2003). Therefore, it is important to deter- Dispersal Treatment mine the scale at which leafhoppers perceive landscape features, such Fig. 2. The number of Agallia constricta that dispersed among mesocosms as the patch edge, and assess the risks of approaching and crossing in the three dispersal treatments in the absence of predation. The edges of the edge (Cronin 2003, Haynes and Cronin 2003, Schtickzelle and the boxes represent the 25th and 75th percentiles, the dark circle indicates Baguette 2003, Bowler and Benton 2005, Baguette and Van Dyck the mean, the dark line indicates the median, and the whiskers represent 2007, Fahrig 2007, Stasek et al. 2008). the highest and lowest number of leafhoppers eaten, excluding outliers. Box We predicted that A. constricta would have the highest dispersal widths are proportional to the square root of the number of leafhoppers that rates in the single damsel bug, 100% dispersal treatment. As predicted, dispersed in each treatment. leafhoppers did have the greatest dispersal rates in the 100% dispersal Damsel bug density had no effect on leafhopper movements treatment, though dispersal rates were generally low with <5% of each among mesocosms (Z = −0.566; P = 0.57). However, dispersal did local leafhopper population dispersed among mesocosms. Low dispersal have a significant effect on leafhopper movement with more leafhop- rates among mesocosms may have occurred because leafhoppers had pers dispersing in the 100% dispersal treatment compared with the 5 limited opportunities to jump or fly to escape from predation and thus and 30% treatments (Z = 2.22; P = 0.027). There was no interaction remained sedentary to escape predation. Damsel bugs search for prey between dispersal treatment and damsel bug density. Less than 5% both visually and chemically (Freund and Olmstead 2000), and they of the leafhoppers (1–12 leafhoppers) moved among local commu- may have been able to locate leafhoppers more efficiently after leafhop- nities in all treatments. We only observed three instances of damsel pers left the host plant. Leafhoppers will often walk or hop to escape bugs moving among communities. from predation (Larsen et al. 1992). Dispersal tubes between the sides A. constricta had a higher survival probability in the 1-damsel of mesocosms required leafhoppers to walk or hop horizontally between bug/5% dispersal treatment compared to the 1-damsel bug/100% mesocosms; if tubes had connected the tops of mesocosms, flying, or dispersal treatment (χ = 8.86; df = 1; P = 0.0029, Table 2, Fig. 3). vertical hopping movements might be facilitated between cages. As a Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/1/2/4781595 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Number ofAgal li a dispersed 0 1 2 3 4 5 Journal of Insect Science, 2017, Vol. 18, No. 1 5 Table 2. Survival probabilities (±SE) and mean (±SD) A. constricta surviving per day in response to varied isolation and damsel bug density Dispersal Density Time Survival probability (±SE) Mean A. constricta (±SD) 5a 1 24 0.427 ± 0.024 20.63 ± 6.2 72 0.261 ± 0.022 11.50 ± 5.8 120 0.149 ± 0.018 7.88 ± 2.5 168 0.0551 ± 0.012 4.13 ± 3.1 5a,b 2 24 0.400 ± 0.025 19.25 ± 6.7 72 0.153 ± 0.018 7.88 ± 4.1 120 0.100 ± 0.016 4.75 ± 3.0 168 0.0634 ± 0.013 2.88 ± 2.2 30a,b 1 24 0.359 ± 0.024 18.00 ± 5.1 72 0.228 ± 0.021 11.38 ± 4.6 120 0.151 ± 0.018 8.00 ± 6.0 168 0.0563 ± 0.012 3.38 ± 2.8 30b 2 24 0.370 ± 0.024 18.75 ± 5.0 72 0.119 ± 0.016 6.38 ± 2.3 120 0.046 ± 0.011 2.75 ± 1.3 168 0.0214 ± 0.0074 1.38 ± 1.1 100b 1 24 0.354 ± 0.024 17.88 ± 9.9 72 0.150 ± 0.018 7.38 ± 3.6 120 0.0528 ± 0.012 3.00 ± 3.0 168 0.0363 ± 0.010 2.25 ± 2.4 100b 2 24 0.373 ± 0.024 18.75 ± 6.3 72 0.193 ± 0.020 9.75 ± 4.7 120 0.0727 ± 0.013 3.88 ± 3.6 168 0.0337 ± 0.0091 1.63 ± 2.8 ‘Dispersal’ is the percentage of time per week that connecting tubes were open to movement. ‘Density’ is the density of damsel bugs per mesocosm. ‘Time’ is the hours since the experiment commenced. Different letters after dispersal treatments indicate a significant difference in survival probability (P < 0.05). predator or parasitoid density does (Hauzy et al. 2007, Bowler et al. 2013) or does not (French and Travis 2001) influence prey dispersal. Parasitoid dispersal rates may increase as the parasitoid:host ratio increases, resulting in a decreased competition with the conspecifics (French and Travis 2001). Adult damsel bug densities peak at 1 bug −2 m at our field site (Stasek et al. unpublished data). Therefore, dam- sel bugs in the two-predator treatments might have increased their dispersal rates to avoid encounters with the conspecifics. It was also predicted that the prey would have lower survival probabilities in habitat patches with two damsel bugs than those with only one damsel bug. The combined effect of the two damsel bugs preying on A. constricta resulted in slightly higher predation rates but did not double the predation rates found in the single damsel bug treatment (Table 2). As a result, leafhoppers may have been unable to escape predation in all treatments, resulting in a similar survival probability among dispersal treatments. Predator interference is an- other factor that would lower per predator feeding rates (Arditi and Akçakaya 1990), but other experiments in our study system showed no evidence of predator interference or cannibalism (Stasek 2009). A. constricta had a higher survival probability in the 1-damsel bug/5% dispersal treatment compared with the 1-damsel bug/100% Fig. 3. Survival probability of A. constricta. The y-axis is plotted on a dispersal treatment, the 2-damsel bug/ 100% dispersal treatment, logarithmic scale. ‘Low’, ‘med’, and ‘high’ represent 5, 30, and 100% dispersal and the 2-damsel bug/30% dispersal treatment. Leafhoppers in the treatments, respectively. ‘One’ and ‘two’ represent one and two damsel bugs 100% dispersal treatment were predicted to have lower survival added per mesocosm. probabilities than the 5 and 30% dispersal treatments. We expected the damsel bug to move freely among communities in the 100% result, leafhoppers may have also chosen to remain sedentary to escape treatment and consume their leafhopper prey. However, we observed predation rather than moving among habitat patches (Östman and Ives only three instances of damsel bugs moving among habitat patches 2003), which is observed in planthoppers exposed to predation by spi- in all of our trials. Because we did not mark damsel bugs individually ders (Finke and Denno 2002, 2006). to avoid altering A. constricta’s behavior, it is possible that damsel Contrary to our predictions, damsel bug density had no effect bugs may have moved among habitat patches at greater rates than on the dispersal rates of leafhoppers. Previous studies show that we observed. Leafhoppers may have also emigrated from habitat Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/1/2/4781595 by Ed 'DeepDyve' Gillespie user on 16 March 2018 6 Journal of Insect Science, 2017, Vol. 18, No. 1 Arditi, R., and H. R. Akçakaya. 1990. Underestimation of mutual interference patches at greater rates than we observed, thus increasing their en- of predators. Oecologia. 83: 358–361. counter rates with damsel bugs. Damsel bugs are voracious pred- Baguette, M., and H. Van Dyck. 2007. Landscape connectivity and animal ators and may have consumed immigrating leafhoppers before we behavior: functional grain as a key determinant for dispersal. Landsc. observed the interpatch movements. Ecol. 22: 1117–1129. There was no difference between the 5 and 30% dispersal treat- Beckerman, A. P., M. Uriarte, and O. J. Schmitz. 1997. Experimental evidence ments on leafhopper survival in the single damsel bug treatment, for a behavior-mediated trophic cascade in a terrestrial food chain. Proc. contrary to our predictions. We predicted that the 30% dispersal Natl. Acad. Sci. U.S.A. 94: 10735–10738. treatment would have the greatest survival time because a greater Bergerot, B., R. Julliard, and M. Baguette. 2010. Metacommunity dynamics: proportion of leafhoppers would disperse to other local communities decline of functional relationship along a habitat fragmentation gradient. to escape predation than in the 5% dispersal treatment, and damsel PLoS One. 5:1–6. bugs would not be able to follow leafhoppers once the tubes were Bernstein, C. 1984. Prey and predator emigration responses in the acarine sys- tem Tetranychus urticae-Phytoseiulus persimilis. Oecologia. 61: 134–142. closed (Brown and Kodric-Brown 1977, Crowley 1981, Nachman Binckley, C. A., and W. J. Resetarits, Jr. 2007. Effects of forest canopy on habi- 1987, Holyoak and Lawler 1996b). This was likely due to the fact tat selection in treefrogs and aquatic insects: implications for communities that there was no difference in dispersal rates of leafhoppers between and metacommunities. Oecologia. 153: 951–958. the 5 and 30% dispersal treatments. Black, L. M. 1944. Some viruses transmitted by Agallian leafhoppers. Proc. Most experimental metacommunity studies use prototozoans Am. Philos. Soc. 88: 132–144. to assess persistence due to their short generation times (Holyoak Bonsall, M. B., D. R. French, and M. P. Hassell. 2002. Metapopulation structures and Lawler 1996a,b; Forbes and Chase 2002; Kneitel and Miller affect persistence of predator-prey interactions. J. Anim. Ecol. 71: 1075–1084. 2003; Cadotte and Fukami 2005; Cadotte 2006; Hauzy et al. 2007). Bonsall, M. B., J. C. Bull, N. J. Pickup, and M. P. Hassell. 2005. Indirect effects However, it is important to understand the short-term behaviors and spatial scaling affect the persistence of multispecies metapopulations. that influence dispersal among local patches, such as predation risk Proc. Biol. Sci. 272: 1465–1471. Bowler, D. E., and T. G. Benton. 2005. Causes and consequences of animal dis- (Resetarits 2005), habitat quality (Binckley and Resetarits 2007), persal strategies: relating individual behaviour to spatial dynamics. Biol. patch arrangement (Bull et al. 2006), number of habitat patches Rev. Camb. Philos. Soc. 80: 205–225. (Bonsall et al. 2002, 2005), and connectivity (Matthiessen et al. Bowler, D. E., S. Yano, and H. Amano. 2013. The non-consumptive effects of a 2007, Start and Gilbert 2016). This study is one of the first experi- predator on spider mites depend on predator density. J. Zoology. 289: 52–59. ments to manipulate dispersal rates of predators and prey on prey Bowne, D. R., and M. A. Bowers. 2004. Interpatch movements in spatially survival in insects. Our results demonstrated that neither conspecific structured populations: a literature review. Landsc. Ecol. 19: 1–20. nor predator density had an effect on dispersal rates, while dispersal Braman, S. K., and K. V. Yeargan. 1989. Intraplant distribution of three Nabis treatment did affect dispersal rates of leafhoppers with 100% treat- species (Hemiptera: Nabidae), and impact of N. roseipennis on green clo- ment having a greater number of leafhoppers moving among habitat verworm populations in soybean. Environ. Entomol. 18: 240–244. patches. This suggests that dispersal is key to understanding short- Braman, S. K., and K. V. Yeargan. 1990. Phenology and abundance of Nabis americoferus, N. roseipennis, and N. rufusculus (Hemiptera: Nabidae) and term persistence in predator-prey metacommunities. Dispersal rates their parasitoids in alfalfa and soybean. J. Econ. Entomol. 83: 823–830. expressed per generation could be 2–3 times larger in longer term, Briggs, C. J., and M. F. Hoopes. 2004. Stabilizing effects in spatial parasitoid-host multigenerational experiments. Further work is needed to determine and predator-prey models: a review. Theor. Popul. Biol. 65: 299–315. the factors which facilitate or hinder dispersal of predators and their Brown, J. H., and A. Kodric-Brown. 1977. Turnover rates in insular biogeog- prey in metacommunities and how predator numerical response and raphy: effect of immigration on extinction. Ecology. 58: 445–449. dispersal rates vary in response to prey patches. Bull, J. C., N. J. Pickup, M. P. Hassell, and M. B. Bonsall. 2006. Habitat shape, Future experiments should focus on varying both predator and metapopulation processes and the dynamics of multispecies predator-prey prey densities as well as dispersal rates to determine the factors influ- interactions. j. Anim. Ecol. 75: 899–907. encing predation rates of predators within generations. Variation in Cadotte, M. W. 2006. Metacommunity influences on community richness at intraspecific and interspecific dispersal rates has only been conducted multiple spatial scales: a microcosm experiment. Ecology. 87: 1008–1016. Cadotte, M. W., and T. Fukami. 2005. Dispersal, spatial scale, and species in a few studies (Bernstein 1984, French and Travis 2001, Hauzy et al. diversity in a hierarchically structured experimental landscape. Ecol. Lett. 2007). A. constricta densities in the field vary dramatically over the 8: 548–557. course of spring and summer with a peak density occurring in late July Costa, A., A. Min, C. K. Boone, A. P. Kendrick, R. J. Murphy, W. C. Sharpee, K. and early August at our study site (Schroeder 2007). The numerical F. Raffa, and J. D. Reeve. 2013. Dispersal and edge behavior of bark beetles and functional responses of damsel bugs may also vary as A. constricta and predators inhabiting red pine plantations. Agric. For. Entomol. 15: 1–11. abundance changes, and damsel bugs may disperse more or less in Cronin, J. T. 2003. Matrix heterogeneity and planthopper-parasitoid interac- response to the changing A. constricta densities. tions in space. Ecology. 84: 1506–1516. Cronin, J. T. 2007. From population sources to sieves: the matrix alters host-parasitoid source-sink structure. Ecology. 88: 2966–2976. Acknowledgments Cronin, J. T. 2009. Habitat edges, within-patch dispersion of hosts, and para- sitoid oviposition behavior. Ecology. 90: 196–207. We thank Ann Rypstra, Bruce Steinly, Hank Stevens, and Mike Vanni for Cronin, J. T., and K. J. Haynes. 2004. An invasive plant promotes unstable their insightful comments and suggestions on the manuscript. We also thank host-parasitoid patch dynamics. Ecology. 85: 2772–2782. Rodney Kolb, Ashley Boerger, Matt Bramble, and the staff of the Miami Crowley, P. H. 1981. Dispersal and the stability of predator-prey interactions. University Ecology Research Center for helping us construct the mesocosms Am. Nat. 118: 673–701. and all of the valuable help they gave to us in the field. This research was Danner, B. J., and A. Joern. 2003. Resource-mediated impact of spider pre- funded by the Miami University Zoology Summer Field Workshop. dation risk on performance in the grasshopper Ageneotettix deorum (Orthoptera: Acrididae). Oecologia. 137: 352–359. References Cited Dempster, J. P., D. A. Atkinson, and M. C. French. 1995. The spatial popula- Antonious, G. F. 2004. Residues and half-lives of pyrethrins on field-grown tion dynamics of insects exploiting a patchy food resource: II. Movements pepper and tomato. J. Environ. Sci. Health. B. 39: 491–503. between patches. Oecologia. 104: 354–362. 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