Figures
Abstract
Insect movement behavior is highly important in entomological population ecology, behavioral ecology and conservation, and in invasion ecology. In this study, we used an exotic lace bug (Corythucha ciliata) as a model organism to address the hypothesis that an insect species invading a new area has a high host location ability and rapid mobility by which it can be successfully carried to a new habitat. To test this hypothesis, three movement parameters (speed, duration and distance) of C. ciliata were assessed using laboratory and field observations. We found that 5th-instar nymphs of C. ciliata could move as far as 750 cm throughout their lifespan and that they moved an average of 0.038 m/min during the first 15 minutes after release, which was significantly farther than that of other instars. Of the tested nymphs, 21.85% could locate their host trees; of adults released 20 m from hosts, 11% reached the host trees on the first day, with an average flight distance of 22.14 m and a maximum flight distance of 27 m. The results of this study partly explain the mechanism of rapid diffusion. These results are also important for predicting population spread, improving eradication surveys, and managing future introductions of C. ciliata.
Citation: Wu H, Liu H (2016) Movement Behavior and Host Location Ability of Corythucha ciliata. PLoS ONE 11(3): e0152205. https://doi.org/10.1371/journal.pone.0152205
Editor: Baohong Zhang, East Carolina University, UNITED STATES
Received: December 11, 2015; Accepted: March 10, 2016; Published: March 28, 2016
Copyright: © 2016 Wu, Liu. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All relevant data are within the paper and its Supporting Information files.
Funding: This research was financially supported by grants from the National Natural Science Foundation of China [grant number 31440033] and the Projects of Shandong Science and Technology Plans [grant number 2013GGB22002]. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Introduction
Dispersal (i.e., the spatial redistribution of populations) is one of the most significant components of entomological population ecology, behavioral ecology and conservation [1–4]. Because dispersal is (in part) random movement of individuals, which underlies the redistribution in space of a population [5–8], there is a close relationship between movement (i.e., the spatial behavior of individuals) and dispersal. Movement of insects is of central importance for them to avoid natural enemies [9], search for food [10,11], secure mates [12], and find suitable habitats [12,13].
In insect population management, movement of individuals strongly influences the area over which management practices should be applied either to increase (conservation) or decrease (pest control) the abundance of a species of interest [14]. Information on movement parameters (speed, duration, and orientation) of insect pests is essential for their control. Meanwhile, understanding the movement behavior of natural enemies is also helpful for developing effective release techniques and for predicting the efficacy of releases [15–17].
Flying (by adults) and crawling (by larvae) are the two main methods of active movement of insects throughout their life history. Studies on the dispersal ability of adult insects abound in the literature [5,15–26]. In contrast, few studies have measured or modeled the parameters of insect movement in larval populations for most insects, partly due to the absence of effective attractants for larvae [27].
We focus on movement behavior in the sycamore lace bug, Corythucha ciliata (Say) (Hemiptera: Tingidae). This pest is native to North America but has successfully invaded many countries in Europe [28], Australia [29], and Asia [30–32]. In China, C. ciliata was initially discovered in 2006 in Wuhan, Hubei Province [33]. To date, infestations have been reported in Shanghai, Zhejiang, Anhui, Jiangsu, Guizhou, Sichuan, Chongqing, Hunan, Hubei, Henan, Shandong and Beijing [34]. C. ciliata is a specialist herbivore with a narrow host range within the genus Platanus. It has five generations per year in the above-mentioned distribution areas in China, with five immature instars per generation [35]. There are many other bioecological characteristics supporting the rapid spread of C. ciliata, such as high fecundity [36], high thermal tolerance [37,38], robust cold tolerance [39] and strong starvation resistance [40]. We hypothesize that this species may also have a high movement speed and a high capacity for host location, both of which play important roles in its rapid spread.
In the present study, we conducted laboratory and field observations to assess three movement parameters (speed, duration and distance) and the capacity of host location of C. ciliata under conditions of no food and no water. The study addressed the following specific questions: (1) How fast could C. ciliata nymphs move? (2) How far could nymphs at different ages move before they died? (3) What is the rate of colonization of new hosts by C. ciliata nymphs? (4) Could C. ciliata adults find their hosts within a certain distance? The findings of this study improve the understanding of the dispersal capacity of this new pest, which is important for predicting population spread, improving eradication surveys, and managing future introductions.
Materials and Methods
Insects
Tested C. ciliata adults and nymphs were collected from London plane trees (Platanus acerifolia (Ait.) Willd.) at a nursery of Zhongjihuajing Garden Co., Ltd, in an experimental field of the Shandong Academy of Forestry and in the Licheng District of Ji'nan City (36.846°N, 117.32°E), which has had an infestation of C. ciliata for two years. All the P. acerifolia trees and insects were kept pesticide-free in the field.
Test of movement speed of C. ciliata nymphs
Based on the test methods of Bach [41], experiments on nymphal movement speed were carried out in flat soil ground devoid of vegetation from 1 August to 15 August, 2015. Each experiment was started at 8:00 a.m and involved drawing a circle on the ground to create an observation arena 0.8 m in diameter (The diameter of the circle was determined based on a prepared test of crawling distance of first-instar nymphs of C. ciliata on paper). Five nymphs, one of each instar, was placed in the center of the arena and observed until it crossed the circumference of the circle. When this occurred, their crawling time from center to the circumference of the circle was recorded. Any nymph that did not cross the circumference of the circle after 3 hours was discarded. Thirty individuals of each instar were tested for the treatment. Each experiment was conducted under sunny and warm weather conditions. The average maximum temperature was 28.03°C and minimum temperature 26.69°C. The average relative humidity was 81.79%. Wind was also mild during the experiments, averaging 2.28 m/s (Weather data were recorded by a weather station at Xinglong Town). A new observation arena was used for each experiment to avoid possible chemical cues from previous nymphs. Fig 1 showed a schematic view of the above experimental design.
The radius of the circle is 0.4m, Solid dot represents release point of nymphs.
Determination of crawling distance of C. ciliata nymphs
Experiments were carried out on square pieces of white paper (4 m×4 m) in the laboratory from 5 July to 15 July, 2015. Five nymphs, one of each instar, were placed in the center of the paper, and their respective movement tracks were drawn with marker throughout the experiment. Observation continued until the nymphs were dead. When each nymph died, the time was recorded, and the crawling distance was measured with a measuring tape. A nymph was considered dead if none of its appendages moved after all appendages were touched with a brush [33]. Thirty individuals of each instar were tested for the treatment. Each experiment was conducted on a new paper to avoid possible chemical cues from previous nymphs. The temperature was maintained in the laboratory at 26 ± 0.5°C and the relative humidity was 70 ± 5%. Fig 2 showed a schematic view of the above experimental design.
Side length of the square is 4m, Solid dot represents release point of nymphs.
Test of host location of C. ciliata nymphs
Experiments were carried out in a flat soil ground devoid of vegetation in Xinglong Town, Linyi County, Dezhou City (37.116°N, 116.745°E) from 16 August to 19 August, 2015. Before each experiment, four water-filled bottles were buried upright underground at 0.4 m north, south, east, and west from a central point. Then, four P. acerifolia branches with 3–5 leaves each were inserted into each bottle; each branch reached approximately 0.5 m above the ground, and there were no gaps in the surrounding soil. Thirty nymphs of each instar were placed in the center of the arena every morning at 8:00 a.m. The number of different ages of C. ciliata nymphs climbing up the branches was recorded over 24 hours, which was the longest lifespan for C. ciliata nymphs without food and water [35]. Populus canadensis branches of the same thickness and height were used as controls. Three replicates were evaluated for each treatment. During all the experiments the maximum temperature was 32.80°C and minimum temperature 23.20°C. The average relative humidity was 78.26%. The average wind speed was 2.11 m/s (Weather data were recorded by a weather station at Xinglong Town). Fig 3 showed a schematic view of the above experimental design.
Solid dot represents release point of nymphs; triangles represent position of the host. The distance from solid dot to the four triangles was all 40cm.
Test of host location of C. ciliata adults
The experiments were performed in Xinglong Town, Linyi County, Dezhou City (37.116°N, 116.745°E); the collected P. acerifolia trees (height 1.0–1.5 m) were planted in a 30 m×50 m field parcel (11 tree rows×26 trees) in November 2014. There were no Platanus trees or C. ciliata insects nearby, only small numbers of jujube, poplar and elm trees. On 19 August 2015, 3–5 leaves bearing approximately 100 adults (regardless of sex) were placed at a release point that was 2 m away from the middle tree of the southern edge of the forest plot. All Platanus trees were visually surveyed at the second day after the initial release; the number of C. ciliata in each tree was enumerated, and the distance from the release point was measured with a measuring tape. The same process was conducted on 29 August 2015 and 8 September, with release distances of 10 m and 20 m, respectively. All of the adults that were found in Platanus trees were killed before additional insects were released. The interval of 10 days also ensured that there would be no living adults on Platanus trees because adult C. ciliata have a lifespan of 4–10 days in the field [42]. The release distances of 10 m and 20 m were based on the previous tests. Weather data were recorded by a weather station at Xinglong Town; weather during all experiments was sunny and warm, with an average temperature of 24.97±0.68°C. Wind was also mild during the experiments, averaging <4.80±0.12 m/s, and wind direction was predominantly from the southwest. Given the C. ciliata was not new invasive pest in Xinglong town and our test field was relatively closed and isolated, no host plants exist around. We signed a cooperation agreement with Xinglong Town People's government to kill all the C. ciliata in our test field after trial. A map of the study area is shown in Fig 4.
Circles represent sycamores, triangles represent poplars, squares represent elms, seven horns stars represent jujubes, and pentagram represent release points.
Statistical analyses
The results are presented as the mean values ± SE, and all the means of movement parameters were compared among the different ages of nymphs using one-way analysis of variance (ANOVA). The difference in the rate at which nymphs climbed up the branches (RNCB) for host trees and non-host trees was analyzed using the t-test for independent samples. Statistical analyses were performed with SPSS (version 15.0, 2006, SPSS, Inc., Chicago, IL). Prior to ANOVA, all data were checked for normality and equal variance. When treatment effects were significant (P <0.05), the means were compared using Tukey's test. Moving speed, distance, times and RNCB were log-transformed, and the distance per time was sine-transformed prior to statistical analysis.
Results
Moving speed, distance and times of C. ciliata nymphs
The different ages of C. ciliata nymphs tested showed large differences in moving speeds (moving speed: F3,83 = 39.15, P<0.001; crawling distance: F4,99 = 21.93, P<0.001; crawling times: F4,99 = 5.25, P<0.001), but there were no significant differences in crawling distance per unit time (F4,99 = 1.62, P>0.1). Both the moving speed and the crawling distance increased with the increase of the age of the C. ciliata nymphs. The 5th-instar nymphs moved significantly faster than other instars, and 2nd-instar nymphs moved significantly more slowly than 3rd-instar and 4th-instar nymphs, between which there was no significant difference. The moving speeds of nymphs from the 2nd, 3rd, 4th, and 5th instars were as shown in Table 1; 1st-instar nymphs was too small to be surveyed in this test. The crawling distance of the 1st-instar nymphs was significantly shorter than those of the other four instars throughout the life of each stage, averaging 41 cm. The mean crawling distance of 90.24 cm for 2nd-instar nymphs was also significantly shorter than those of the 3rd-instar, 4th-instar and 5th-instar nymphs, but there was no significant difference between these three instars (3rd instar: 165.21 cm; 4th instar: 174.72 cm; and 5th instar: 291.35 cm). One 5th-instar nymph moved 750 cm, which was the longest distance of all the tested nymphs. The tested 1st-instar nymphs crawled for approximately 8.75 minutes throughout their lifespan, which was significantly less than for the other four instars. The crawling times of 2nd to 5th instar nymphs were not significantly different at 16.89, 19.20, 18.78, and 22.70 minutes, respectively (Table 1).
Host location of C. ciliata nymphs
The t-test for independent samples showed that C. ciliata nymphs had significantly different location capabilities for host and non-host trees (t = 5.82, P<0.01). Approximately 21.85% of the tested nymphs climbed up the P. acerifolia branches with 3–5 leaves in four directions within 24 hours. By contrast, only 1.85% of the tested nymphs climbed the control (non-host: Populus canadensis) branches (Fig 5). Multiple comparisons revealed that there were no significant differences between the different instars in their ability to locate host trees. The rates at which the tested nymphs climbed up the branches of host trees during the 3rd, 4th, and 5th instars were 20.00%, 24.44% and 21.11%, respectively (Fig 6).
Host location of C. ciliata adults
At the second day after their release 2 m away from the forest edge, 20 adults were captured in the forest plot, accounting for 20% of the total released adults. Their average flight distance was 3.55 m, and the maximum distance was 6 m. When they were released 10 m away from the forest edge, 13% of the released adults could fly to the forest within one day. They flew an average of 12.96 m, with the longest distance being 19 m. Eleven adults were found in the forest at one day after the release at 20 m away from the forest edge; their average flight distance was 22.14 m, and one was captured 27 m away from the release point, which was the longest distance in that group. No adults were captured in the jujube, poplar and elm trees that were 2–8 m away from the release points (Table 2).
Discussion
The speed and distance of insect movement have been the focus in the vast majority of studies, whether of pests or natural enemies [20,21,43–47], and they are affected by both intrinsic (age, life cycle stage, gender, and physical condition) factors and extrinsic (conditions, resources, interactions with other organisms, and barriers to movement) factors [47]. Results from this study indicate that the moving speed increased with the age of C. ciliata nymphs, and similar results were obtained for the crawling distance as tested in the laboratory (Table 1). Fifth-instar nymphs moved an average of 0.038 m/min during the first 15 minutes after release, which was much faster than the average moving speed of the larvae of Altica subplicata LeC. (43 cm/day, which is equivalent to 0.0003 m/min) [41]. C. ciliata nymphs could move as far as 750 cm throughout their own lifespan, demonstrating that the nymphs also had strong diffusion potential in the forest. Although there were marked differences in crawling time between the different ages of C. ciliata nymphs tested (Table 1), the difference in crawling distance per unit time was not significant. This indicates that the older nymphs may have greater endurance than younger nymph, but the mechanism underlying this phenomenon requires further explanation.
Insects must try their best to search for, identify and locate new hosts as soon as possible to obtain essential nutrients for their growth and development once they are forced to leave their original hosts. Many studies have shown that plant volatiles are the main cues used by phytophagous insects in orientation to their host plants [48–54], and the visual cues such as plant shape and color also played an important role in the process [55–59]. The current study shows that 21.85% of the tested nymphs climbed the four P. acerifolia branches within 24 hours, whereas only 1.85% of the nymphs climbed the control branches (non-host: Populus canadensis) (Fig 5), which means that there may be not visual but chemical orientation toward host plants for C. ciliata nymphs. Some studies suggested that lavae ages also had influence on host location ability [59–61]. But this article showed different results that the tropism is not different between different instars of nymphs based on their rate of climbing the branches of host trees (3rd instar: 20.00%; 4th instar: 24.44%; 5th instar: 21.11%) for C. ciliata (Fig 6). The mechanism needs further study.
The flying wings of adults of C. ciliata are very delicate, and these insects therefore rarely fly very far [62]; however, Maceljski [63] writes that adults "are very mobile and are good fliers". Actual measurements of flying distance have been made in this paper and their maximum flying distance tested in one day was 27 m (Table 2). Due to limited space, adults of C. ciliata were not released at a further distance, and they may fly longer distances. However, the longest flying distance in one day (27 m) showed that the opinion from Maceljski [63] is correct. Not only that, C. ciliata adults could fly faster than many insect species that are larger or smaller than them, such as Lygus hesperus Knight (4.6 m/d), Anoplophora glabripennis Motchulsky (20 m/d) and Diaphorina citri Kuwayama (5.8 m/d) [21,44,64].
Mark-release-recapture methods are a very common method of estimating insect movement in many experiments [5,65–71]. The advantage of these methods is that they allow accurate characterization of dispersal behavior in the natural environment [72], but several key technical problems need to be solved. First, a long-term non-invasive marker should be selected for each insect species. The need to mark individual insects limits the size of the population that can be marked, reducing the likelihood of detecting rare long-distance dispersal events [73]. Second, the appropriate number of released insects to enable adequate recapture frequencies for statistical analyses [74] may result in density-dependent movement, leading to biased estimates of movement rate [5]. In addition, another critical problem may be the recapture method. For example, highly efficient attractants are often used in the re-identification of released adult populations. The observed dispersal distance would become shorter because the attractant shortens the dispersal distance by intercepting individuals who should have dispersed for longer distances [27]. Even if the problem above is solved, mark-release-recapture experiments have been limited by being conducted at relatively small scales [73], and predictions of movement only indicate how populations will respond in similar circumstances [75]. It must be clearly recognized that obtaining unbiased estimates of the distribution of animal dispersal distances in natural unbounded populations has long been known to be problematic [4]. Although following movement in the field is very difficult for small insects [76], some behaviors of both nymphs and adults of C. ciliata in this article were visually observed throughout the process of the release-recapture method, without disturbance from marking and luring that may affect movement behavior.
In short, results from this study indicated that both the nymphs and adults of the sycamore lace bug, C. ciliata, have some active diffusion capacity, which may very helpful in the practice of prevention of C. ciliata. For instance, based on the maximum distance that the nymphs crawl all the host need spraying at a distance of 750cm where the leaves are infesting by nymphs. Similarly, the scope of prevention needs to expand to at least 27m if the harm was caused by adults.
Acknowledgments
We greatly thank Naomi T. and Lauren L. at American Journal Experts Company for improving the English language in this manuscript and three anonymous reviewers for providing constructive comments that greatly improved the quality of our paper. We thank Xinan WANG and Xianchen LI for helpful advice and comments. In addition, many thanks to Lijun XIN, Fengqi LIU, Xingxing HUO, Min LIU, Tianxing ZHOU and Zhen LIU for assistance in the laboratory and field.
Author Contributions
Conceived and designed the experiments: HW HL. Performed the experiments: HW HL. Analyzed the data: HW HL. Contributed reagents/materials/analysis tools: HW HL. Wrote the paper: HW HL.
References
- 1. Doak DF, Mills LS. A useful role for theory in conservation. Ecology. 1994;75: 615–626.
- 2.
Lidicker WZ Jr, Stenseth NC. To disperse or not to disperse: who does it and why? In: Stenseth NC, Lidicker WZ Jr, editors. Animal dispersal: small mammals as a model. London: Chapman and Hall; 1992. pp. 21–36.
- 3. Hedin J, Ranius T. Using radio telemetry to study dispersal of the beetle Osmoderma eremita, an inhabitant of tree hollows. Comput Electron Agric. 2002;35: 171–180.
- 4. Koenig WD, Van Vuren D, Hooge PN. Detectability, philopatry, and the distribution of dispersal distances in vertebrates. Trends Ecol Evol. 1996;11: 514–517. pmid:21237947
- 5.
Turchin P. Quantitative analysis of movement. Measuring and modeling population redistribution in animals and plants. Sunderland, MA: Sinauer Associates; 1998.
- 6. Nathan R, Getz WM, Revilla E, Holyoak M, Kadmon R, Saltz D, et al. A movement ecology paradigm for unifying organismal movement research. Proc Nalt Acad Sci. 2008;105: 19052–19059.
- 7. Schellhorn NA, Bianchi FJ, Hsu CL. Movement of entomophagous arthropods in agricultural landscapes: links to pest suppression. Annu Rev Entomol. 2014;59: 559–581. pmid:24397523
- 8. Allema AB, van der Werf W, Groot JC, Hemerik L, Gort G, Rossing WA, et al. Quantification of motility of carabid beetles in farmland. Bull Entomol Res. 2015;105: 234–244. pmid:25673121
- 9. Turchin P, Kareiva P. Aggregation in aphis varians: an effective strategy for reducing predation risk. Ecology. 1989;70: 1008–1016.
- 10. Kareiva P, Odell G. Swarms of predators exhibit “preytaxis” if individual predators use area-restricted search. American Naturalist. 1987;130: 233–270.
- 11. Morris W, Kareiva P. How insect herbivores find suitable host plants: the interplay between random and nonrandom movement. Insect-Plant Interactions. 1991;3: 175–208.
- 12. Lawrence WS. Effects of sex ratio on milkweed beetle emigration from host plant patches. Ecology. 1987;68: 539–546.
- 13. Johnson AR, Milne BT, Wiens JA. Diffusion in Fractcal landscapes: simulations and experimental studies of tenebrionid beetle movements. Ecology. 1992;73: 1968–1983.
- 14. Moerkens R, Leirs H, Peusens G, Gobin B. Dispersal of single- and double-brood populations of the European earwig, Forficula auricularia: a mark-recapture experiment. Entomol Exp Applicata. 2010;137: 19–27.
- 15. Smith SM. Biological control with Trichogramma: advances, successes, and potential of their use. Annu Rev Entomol. 1996;41: 375–406. pmid:15012334
- 16.
Orr DB, Garcia-Salazar C, Landis DA. Trichogramma nontarget impacts: a method for biological control risk assessment. In: Follett PA, Duan JJ, editors. Nontarget effects of biological control. Boston, MA: Kluwer Academic Publishers; 2000. pp. 111–125.
- 17. Wright MG, Hoffmann MP, Chenus SA, Gardner J. Dispersal behavior of Trichogramma ostriniae (Hymenoptera: Trichogrammatidae) in sweet corn fields: implications for augmentative releases against Ostrinia nubilalis (Lepidoptera: Crambidae). Biol Contr. 2001;22: 29–37.
- 18. Rykken JJ, Jepson PC, Moldenke AR. Ground-dwelling arthropod distribution and movement across a fragmented riparian forest. Northwest Sci. 2011;85: 527–541.
- 19. Gordon PL, McKinlay RG. Dispersal of ground beetles in a potato crop; a mark-release study. Entomol Exp Applicata. 1986;40: 104–105.
- 20. Chapman AV, Kuhar TP, Schultz PB, Brewster CC. Dispersal of Trichogramma ostriniae (Hymenoptera: Trichogrammatidae) in potato fields. Environ Entomol. 2009;38: 677–685.
- 21. Bancroft JS. Dispersal and abundance of Lygus hesperus in field crops. Environ Entomol. 2005;34: 1517–1523.
- 22. Wright MG, Hoffmann MP, Chenus SA, Gardner J. Dispersal behavior of Trichogramma ostriniae (Hymenoptera: Trichogrammatidae) in sweet corn fields: implications for augmentative releases against Ostrinia nubilalis (Lepidoptera: Crambidae). Biological Control, 2001; 1: 29–37.
- 23. Tuda M, Shima K. Relative importance of weather and density dependence on the dispersal and on-plant activity of the predator Orius minutus. Population Ecology, 2002; 44: 251–257.
- 24. Langhof M, Meyhöfer R, Poehling HM, Gathmann A. Measuring the field dispersal of Aphidius colemani (Hymenoptera: Braconidae). Agriculture, ecosystems & environment, 2005; 107: 137–143.
- 25. Doukas D, Payne CC. Effects of UV-blocking films on the dispersal behavior of Encarsia formosa (Hymenoptera: Aphelinidae). Journal of economic entomology, 2007;1: 110–116.
- 26. Petit JN, Hoddle MS, Grandgirard J, Roderick GK, Davies N. Short-distance dispersal behavior and establishment of the parasitoid Gonatocerus ashmeadi (Hymenoptera: Mymaridae) in Tahiti: Implications for its use as a biological control agent against Homalodisca vitripennis (Hemiptera: Cicadellidae). Biological control, 2008; 45: 344–352.
- 27. Arakaki N, Hokama Y, Yamamura K. Estimation of the dispersal ability of Melanotus okinawensis (Coleoptera: Elateridae) larvae in soil. Appl Entomol Zool. 2010;45: 297–302.
- 28. Rabitsch W. Alien true bugs of Europe (Insecta: Hemiptera: Heteroptera). Zootaxa. 2008;1827: 1–44.
- 29. Dominiak B, Gillespie P, Worsley P, Löcker H. Survey for sycamore lace bug Corythucha ciliata (Say)(Hemiptera: Tingidae) in New South Wales during 2007. Gen Appl Entomol. 2008;37: 27–30.
- 30. Chung Y, Kwon T, Yeo W, Park C. Occurrence of the sycamore lace bug, Corythucha ciliata (Say)(Hemiptera: Tingidae) in Korea. Korean J Appl Entomol. 1996;35: 137–139.
- 31. Tokihiro G, Tanaka K, Kondo K. Occurrence of the sycamore lace bug, Corythucha ciliata (Say)(Heteroptera: Tingidae) in Japan. Res Bull Plant Protect Serv, Jpn. 2003;39: 85–87.
- 32. Ju R, Li Y, Wang F, Du Y. Spread of and damage by an exotic Lacebug,Corythuca ciliata(Say, 1832) (Hemiptera: Tingidae), in China. Entomol News. 2009;120: 409–414.
- 33. Li C-R, Xia W-S, Wang F-L. First records of Corythucha ciliata (Say) in China (Hemiptera,Tingidae). Acta Zootaxonomica Sinica. 2007;32: 944–946.
- 34. Wu H, Li D, Wang X, Wang L, Li X, Liu H. Debelopment situation and control measures for Corythucha ciliata in Shandong. Journal of Shandong Forestry Science and Technology. 2013;43: 108–110.
- 35. Ju R, Wang F, Li B. Effects of temperature on the development and population growth of the sycamore lace bug, Corythucha ciliata. J Insect Sci. 2011;11: 1–12.
- 36. D'Aguilar J, Pralavorio R, Rabasse J. Introduction into France of the plane tree lace bug: Corythucha ciliata (Say)(Heteroptera, Tingidae). Bull Soc Entomol Fr. 1977;82: 2–6.
- 37. Ju R, Chen G, Wang F, Li B. Effects of heat shock, heat exposure pattern, and heat hardening on survival of the sycamore lace bug, Corythucha ciliata. Entomol Exp Applicata. 2011;141: 168–177.
- 38. Ju RT, Gao L, Zhou XH, Li B. Tolerance to high temperature extremes in an invasive lace bug, Corythucha ciliata (Hemiptera: Tingidae), in subtropical China. PLOS ONE. 2013;8: e54372. pmid:23365664
- 39.
Halbert SE, Meeker JR. The Sycamore lace Bug, Corythucha ciliata (Say):(Hemiptera: Tingidae). Gainesville, FL: Fla. Dept. Agric. & Consumer Services, Division of Plant Industry; 1998.
- 40. Wu H, Li X, Liu H. Starvation resistance of invasive lace Bug Corythucha ciliata (Hemiptera: Tingidae) in China. Entomol Fenn. 2016;27: In Press.
- 41. Bach CE. Movement behavior of Altica subplicata (Coleoptera: Chrysomelidae): larval orientation and movement. J Kans Entomol Soc. 1993;66: 86–89.
- 42. Kim C, Jeong J. Ecological studies on the sycamore lace bug, Corythucha ciliata (Hemiptera: Tingidae). I. Developmental characteristics, adult behavior and sex ratio. Journal of Research Forests of Kangwon National University. 1999;19: 1–5.
- 43. Gui H-Y, Ge F. Diffusion of Bemisia tabaci in early spring in Beijing and Hebei regions. Chinese Journal of Applied Entomology. 2011;48: 38–42.
- 44. Kobori Y, Nakata T, Ohto Y, Takasu F. Dispersal of adult Asian citrus psyllid, Diaphorina citri Kuwayama (Homoptera: Psyllidae), the vector of citrus greening disease, in artificial release experiments. Appl Entomol Zool. 2011;46: 27–30.
- 45. Schneider JC. Dispersal of a highly vagile insect in a heterogeneous environment. Ecology. 1999;80: 2740–2749.
- 46. Taylor DB, Moon RD, Campbell JB, Berkebile DR, Scholl PJ, Broce AB, et al. Dispersal of stable flies (Diptera: Muscidae) from larval development sites in a Nebraska landscape. Environ Entomol. 2010;39: 1101–1110. pmid:22127160
- 47. Rudd NT, McEvoy PB. Local dispersal by the cinnabar moth Tyria jacobaeae. Ecol Appl. 1996;6: 285–297.
- 48. Fein BL, Reissig WH, Roelofs WL. Identification of apple volatiles attractive to the apple maggot Rhagoletis pomouella. J Chem Ecol,1982; 8:1473–1487. pmid:24414891
- 49. Ascoli A, Albert PJ. Orientation behavior of second-instar larvae of eastern spruce budworm Choristoneura fumiferana (Clem) (Lepidoptera:Tortricidae) in a Y-type olfactometer. J Chem Ecol. 1985; 11:837–845. pmid:24310270
- 50. Huang XP, Mack TP, Berger RS. Olfactory responses of lesser cornstalk borer(Lepidoptera: Pyralidae) larvae to peanut plant parts. Entomol Soc Am, 1990; 19:1289–1295.
- 51. Tokro PG, Saxena KN. Effect of olfactory and visual stimuli on the orientation of the 4th instar larvae of the stem borer Chilo partellus Swinhoe (Lepidoptera:Pyralidae). Acta Biol Hung, 1991; 42:397–406. pmid:1841489 [PubMed—indexed for MEDLINE]
- 52. Ruther S, Thiemann K. Response of the pollen beetle Meligethes aeneus to volatiles emitted by intact plants and conspecifics. Ent Exp & Appl, 1997; 84:183–188.
- 53. Mondy N, Pracros P, Fermaud M, Corio Costet MF. Olfactory and gustatory behavior by larvae of Lobesia botrana in response to Botrytis cinerea. Entomol Experi Appl, 1998; 88:1–7.
- 54. Kalinová B., Stránský K., Harmatha J., Čtvrtečka R., Žd'árek J. Can chemical cues from blossom buds influence cultivar preference in the apple blossom weevil (Anthonomus pomorum)?. Entomologia Experimentalis et Applicata, 2000; 1: 47–52.
- 55. WyATT TD, Vastiau K, Birch MC. Orientation of flying male Anobium punctatum (Coleoptera: Anobiidae) to sex pheromone: separating effects of visual stimuli and physical barriers to wind. Physiological Entomology, 1997; 2: 191–196.
- 56. Prokopy RJ, Owens ED. Visual detection of plants by hebivorous insects. Annu Rev Entomol, 1983; 28:337–364.
- 57. Cornelius ML, Duan JJ, Messing RH. Visual stimuli and the response of female oriental fruit flies (Diptera: Tephritidae) to fruit-mimicking traps. J Econ Entomol,1999; 1:121–129.
- 58. De Groot P, Nott R. Evaluation of traps of six different designs to capture pine sawyer beetles (Coleoptera: Cerambycidae). Agricultural and Forest Entomology, 2001; 2: 107–111.
- 59. McIntosh RL, Katinic PJ, Allison JD, Borden JH, Downey DL. Comparative efficacy of five types of trap for woodborers in the Cerambycidae, Buprestidae and Siricidae. Agricultural and Forest Entomology, 2001; 2: 113–120.
- 60. Fan J, Zhang L, Wang G, Ma S, Shao H. Host plant selection and nutrient utilization of beet armyworm larvae. Chinese Agricultural Science Bulletin, 2011; 30:233–236.
- 61. Wei J, Luo Y, Shi J, Wang D, Shen S. Larval instar impact on host selection suitability of asian gypsy moth (Lymantria dispar asiatica, AGM). Plant Quarantine, 2012;4:6–10.
- 62.
Wade O. The sycamore lace-bug:(Corythucha ciliata, Say). Stillwater, OK: Oklahoma Agricultural and Mechanical College, Agricultural Experiment Station; 1917.
- 63. Maceljski M. Current status of Corythuca ciliata in Europe. EPPO Bull. 1986;16: 621–624.
- 64. Bancroft JS, Smith MT. Dispersal and influences on movement for Anoplophora glabripennis calculated from individual mark-recapture. Entomol Exp Applicata. 2005;116: 83–92.
- 65.
Okubo A, Levin SA. Diffusion and ecological problems: modern perspectives. New York, NY: Springer Science & Business Media; 2013.
- 66. Kareiva PM. Local movement in herbivorous insects: applying a passive diffusion model to mark-recapture field experiments. Oecologia. 1983;57: 322–327.
- 67. Hanski I, Kuussaari M, Nieminen M. Metapopulation structure and migration in the butterfly Melitaea cinxia. Ecology. 1994;75: 747–762.
- 68. Kuussaari M, Nieminen M, Hanski I. An experimental study of migration in the Glanville fritillary butterfly Melitaea cinxia. J Anim Ecol. 1996;65: 791–801.
- 69. Ginzel MD, Hanks LM. Evaluation of synthetic hydrocarbons for mark—recapture studies on the red milkweed beetle. J Chem Ecol. 2002;28: 1037–1043.
- 70. Wang R, Wang Y, Chen J, Lei G, Xu R. Contrasting movement patterns in two species of chequerspot butterflies, Euphydryas aurinia and Melitaea phoebe, in the same patch network. Ecol Entomol. 2004;29: 367–374.
- 71. Wang X, Chen H, Ma C, Li Z. Chinese White pine beetle, Dendroctonus armandi (Coleoptera: Scolytinae), population density and dispersal estimated by mark-release-recapture in Qinling Mountains, Shaanxi, China. Appl Entomol Zool. 2010;45: 557–567.
- 72. Wang R, Ovaskainen O, Cao Y, Chen H, Zhou Y, Xu C, et al. Dispersal in the Glanville fritillary butterfly in fragmented versus continuous landscapes: comparison between three methods. Ecol Entomol. 2011;36: 251–260.
- 73. Sivakoff FS, Rosenheim JA, Hagler JR. Relative dispersal ability of a key agricultural pest and its predators in an annual agroecosystem. Biol Contr. 2012;63: 296–303.
- 74. Cronin JT, Hyland K, Abrahamson WG. The pattern, rate, and range of within-patch movement of a stem-galling fly. Ecol Entomol. 2001;26: 16–24.
- 75. Schwarz CJ, Arnason AN. A general methodology for the analysis of capture-recapture experiments in open populations. Biometrics. 1996;52: 860–873.
- 76. Mascanzoni D, Wallin H. The harmonic radar: a new method of tracing insects in the field. Ecol Entomol. 1986;11: 387–390.