Density and Seasonal Dynamics of Bemisia tabaci (Gennadius) Mediterranean on Common Crops and Weeds around Cotton Fields in Northern China 1

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1 Journal of Integrative Agriculture Advance Online Publication 2013 Doi: /S (13) Density and Seasonal Dynamics of Bemisia tabaci (Gennadius) Mediterranean on Common Crops and Weeds around Cotton Fields in Northern China 1 ZHANG Xiao-ming 1, YANG Nian-wan 1, WAN Fang-hao 1 and Gabor L. LÖVEI 1,2 1 State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing , P.R.China 2 Department of Agroecology, Aarhus University, Flakkebjerg Research Centre, Denmark Abstract The density seasonal dynamics of Bemisia tabaci MED were evaluated over two-years in a cotton-growing area in Langfang, Hebei Province, northern China on cotton (Gossypium hirsutum L.) and six other, co-occurring common plants: common ragweed (Ambrosia artemisiifolia L.), piemarker (Abutilon theophrasti Medicus), sunflower (Helianthus annuus L.), sweet potato (Ipomoea batatas L.), soybean (Glycine max L.), and maize (Zea mays L.). The whitefly species identity was repeatedly tested and confirmed; seasonal dynamics on the various host plants was standardized by the quartile method. B. tabaci MED appeared on weeds (the common ragweed and piemarker) about 10 days earlier than on cotton, or the other cultivated plants. The peak population densities were observed over a span of two to three weeks on cotton, starting in early (2010) or mid- (2011) August. The common ragweed growing adjacent to cotton supported the highest B. tabaci densities (no. on 100 cm 2 leaf surface), fold higher than on cotton itself. Sunflower supported more B. tabaci than the other plants, and about fold higher than cotton did. Our results indicate that weeds (esp. the common ragweed) around cotton fields could increase the population density of B. tabaci MED on cotton, while sunflower could act as a trap crop for decreasing pest pressure on cotton. Key words: Bemisia tabaci, whitefly, cotton, sunflower, ragweed, population dynamics, seasonal dynamics, quartile method 1 ZHANG Xiao-ming, Tel: zxmalex@126.com; Correspondence Gabor L. LÖVEI, Tel: , Gabor.Lovei@agrsci.dk; WAN Fang-Hao, Tel: , wanfanghao@caas.cn 1

2 INTRODUCTION The tobacco whitefly, Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae), is a key agricultural pest in many regions of the world (Perring 2001; Jones 2003), with over 500 host plant species of 74 families (Stansly and Naranjo 2010). However, due to complexity and confusion with the taxonomy of the B. tabaci species complex (De Barro et al. 2011; Liu et al. 2012), most of the published records concerning host plants refer to an unknown number of cryptic species of the complex. B. tabaci infestation can decrease plant vigor and growth, and can cause chlorosis and uneven ripening (Perring 2001; Jones 2003). Direct feeding by adults and nymphs induces physiological disorders in host plants, thus resulting in shedding of immature fruits (Jones 2003). The honeydew produced by the nymphs, by promoting the growth of black sooty mold on leaves and reducing photosynthesis, often causes stunting (Jones 2003); in cotton (Gossypium hirsutum L.), lint contamination is an additional problem (Jones 2003). Whiteflies can also transmit more than 100 plant viruses, which cause destructive damage to many commercial plants and tremendous economic losses (Perring 2001; Jones 2003). Several of the cryptic species of the B. tabaci complex occur in China (De Barro et al. 2011; Hu et al. 2011; Liu et al. 2012). One of the relatively recent invaders, B. tabaci MED was first found in Kunming, Yunnan Province, in 2003 (Chu et al. 2005), and by 2010, it was present in more than 15 Chinese provinces (Teng et al. 2010; Hu et al. 2011). Before this invasion, the most important whitefly was the B. tabaci Middle East-Asia Minor 1 (MEAM1, formerly called B biotype ) (De Barro et al. 2011). However, because of the higher tolerance to extreme temperatures and greater resistance to insecticides (Horowitz et al. 2005; Rao et al. 2012; Sun et al. 2013), B. tabaci MED had rapidly became dominant across most regions of China (Teng et al. 2010; Sun et al. 2013). The wide and dynamic host range of B. tabaci MED can cause new, emerging problems, well illustrated by the recent discovery of serious infections of the cotton leaf curl Multan virus (CLCuMV) on Hibiscus rosa-sinensis L. and Abelmoschus esculentus (L.) Moench in Guangdong and Guangxi Provinces in Southern China (He et al. 2010). These two provinces are not cotton-growing areas, but the whitefly transmitting this virus is widely distributed and might bring the virus to other cotton-growing areas. If that happens, destructive losses are predicted (He et al. 2010). Cotton, the main crop during the summer growing season in Northern China, is one of the major hosts of B. tabaci MED. Due to increasing demand, the area devoted to this crop is increasing, and planted on about 500 million ha, with a total lint yield of>6.5 billion kg in 2011 (Wang et al. 2011). Cotton in China is typically planted in small fields (Li 2009). Independent management of these fields and still substantial pesticide use against sucking insect pests causes frequent between-field dispersal, often involving different host plants. Using insecticides is still the primary control approach of whitefly in China, and will probably remain so until biologically based management programs are available. Thus, the consideration of 2

3 alternative or supplementary strategies to control whiteflies is of both economical and ecological importance. Understanding the performance and dynamics of B. tabaci on common plants in cotton-growing areas is necessary to develop such strategies. Whitefly can switch hosts for foraging and oviposition (Khan 2011; Simmons 1994). Under laboratory conditions, B. tabaci preferred cauliflower (Brassica oleracea var. botrytis L.) over cucumber (Cucumis sativus L.), cole (Brassica sp.) or lettuce (Lactuca sativa L.) (Yang et al. 2004). Cucumber is a favorable host plant for B. tabaci MEAM1, followed by tobacco (Nicotiana tabacum L.), and eggplant (Solanum melongena L.) (Zhang et al. 2010). B. tabaci shows non-preference for water spinach (Ipomoea aquatic Forsk), celery (Apium graveolens L. var. dulce (Miller) Pers.) and amaranth (Amaranthus sp.) (Zhou et al. 2008). All the above are laboratory studies - studies under field conditions are lacking. In order to clarify the relative suitability, and the seasonal dynamics of whiteflies on various co-occurring host plants in Northern China, we performed a two-years field survey on six common plants that often accompany cotton at a landscape scale. We used regular molecular testing to ensure that our data are obtained from B. tabaci MED. Using a standardized method to describe seasonal dynamics; we detected several weeks' differences in peak and main activity periods on the host plants studied. We found that common ragweed (Ambrosia artemisiifolia L.) was an important source of cotton-colonizing whitefly, and sunflower (Helianthus annuus L.) potentially could be used to lure away B. tabaci MED from cotton, thus decreasing pest pressure on this crop. RESULTS Seasonal population dynamics of B. tabaci MED Seasonal activity, 2010 In 2010, the length of the main immature activity period ranged from 15 days (on sunflower, sweet potato (Ipomoea batata L.), piemarker (Abutilon theophrasti Medicus) to 22 days (cotton, ragweed, soybean (Glycine max L.) and the activity peak was reached between 26 July (ragweed) and 23 August (sunflower, Table 1). For adults, the main activity period lasted 15 days on cotton, piemarker and ragweed, and 22 days on the others (Table 1). The earliest seasonal activity peak occurred on piemarker (26 July) and latest on sunflower (23 August) (Table 1) (Fig. 1). We observed no whiteflies on maize (Zea mays L.). 3

4 Immatures: Densities of immatures on common ragweed exceeded (up to 50 times) the values observed on the other plants during the whole sampling season, with the highest densities recorded in late July, about two weeks earlier than on other plants (Fig. 2). After ragweed, sunflower supported the highest number of immatures (Fig. 2), and both were significantly (F 5, 24=51.13; P<0.0001) higher than densities on other plant species. Adults: Whitefly adults were first observed on 6 June, followed by a steady increase until the population reached the highest densities in mid-august on most plants, followed by a gradual decrease until early October. Densities on common ragweed were significantly (F 5, 24=50.82; P<0.0001) higher than on other host plants during the whole sampling season. The highest densities occurred in early August, two weeks earlier than that on cotton (Fig. 2). The highest density on ragweed was 81 adults 100cm -2 leaf surface, 4 times higher than on other plants (Fig. 2). Seasonal activity, 2011 In 2011, the main immature activity period ranged from 15 days (on sunflower and cotton) to 22 days (on most other host plants), and the activity peak was reached between 18 August (piemarker, ragweed) and 1 September (cotton, sunflower, Table 1). For adults, the main activity period lasted 15 days on piemarker and sunflower, and 32 days on sweet potato (Table 1). The earliest seasonal activity peak was on piemarker (9 August) and the latest on soybean (8 September) (Table 1, Fig. 1). The average immature density during the mean activity period was highest on common ragweed, followed by sunflower, cotton and sweet potato, with significant differences among plant species (F 5, 24=344.28; P<0.0001; Fig. 2). The overall trend of the seasonal dynamics curve in adults was similar to that in 2010: the whitefly adults were first observed on 7 July, followed by a steady increase until early September. The peak date in adults was about 7 days earlier than that of the immatures (Fig 1). On common ragweed, the population reached the peak in mid-august and it was about 15 days earlier than on other plants (Fig. 2). Population density of B. tabaci MED Population density, 2010 Immatures: In the early activity period, the density on common ragweed was 2.44 ind. cm -2 leaf while on other plants it was<0.1 ind. cm -2 (Fig. 3). During the main activity period, the densities on common ragweed reached 6.55 ind. cm -2 leaf while on other plants, 4

5 densities remained between ind. cm -2 and 0.58 ind. cm -2 (Fig. 3). The mean immature density on ragweed during the main activity period was significantly higher than on other host plants (F 5, 20=3.70, P=0.0155; Fig. 2), with no difference on sample dates (F 3, 72=0.07, P=0.9736; Fig. 2), and no significant interaction between plants and time (F 15, 72=0.15, P=0.9999; Fig. 2). In the late activity period, the densities sharply decreased on all plants, to 0.85 ind. cm -2 leaf on common ragweed, while around 0.08 ind. cm -2 on other plants (Fig. 3). Densities on common ragweed were significantly higher than on other plants (F 5, 24=32.94, and at early, middle and late activity periods, respectively; P< for all three periods; Fig. 3). Adults: During the early activity period, the density was<0.05 ind. cm -2 leaf on all host plants except on common ragweed, which was>0.15 ind. cm -2 (Fig. 3). In the main activity period, the population density on common ragweed was 0.44 ind. cm -2 leaf, while on other plants it was around 0.04 ind. cm -2 (Fig. 3). During the late activity period, the densities were<0.03 ind. cm -2 leaf on most plants (Fig. 3). The population density on common ragweed was significantly higher than that on other plants in all three activity periods (F 5, 24=34.92, and at early, middle and late activity seasons, respectively; P< for all three; Fig. 3). Population density, 2011 Immatures: In the early phase of the activity season, the density on common ragweed was 0.53 ind. cm -2 leaf while on other plants, densities were around 0.02 ind. cm -2. During the main activity period, the density on common ragweed reached 1.73 ind. cm -2 leaf while on other plants it ranged from 0.01 ind. cm -2 to 0.56 ind. cm -2. The seasonal mean density on ragweed was significantly higher than on other plants (F 5, 19=7.78, P=0.0004; Fig. 2). In the late activity period, the density on common ragweed was 0.92 ind. cm -2 leaf while on other plants densities were around 0.04 ind. cm -2. The density on common ragweed was significantly higher than that of the other plants, and density on sunflower had second higher densities on seven occasions creating significant differences (F 5, 24= and , in early and main activity periods, respectively; P<0.0001; Fig. 3). During the late activity period, population densities on common ragweed remained significantly higher than on other plants (F 5, 24=66.46; P<0.0001). Adults: In the early activity period, the mean density on common ragweed was 0.1 ind. cm -2 leaf, while the densities were<0.02 ind. cm -2 on all other plants. During the main activity period, the density on common ragweed reached 0.17 ind. cm -2 leaf while on other plants were around 0.02 ind. cm -2. In the late activity period, the densities decreased to<0.07 ind. cm -2 leaf on all plants. Throughout the season, densities on common ragweed were significantly higher than on the other plants (F 5, 24=72.25, and 11.66, at early, middle and late activity periods, respectively; all P<0.0001; Fig. 3). 5

6 DISCUSSION Seasonal phenology was formally defined and characterized by the quartile method (Fazekas et al. 1997), which is helpful when one compares the between-year, between-host or between-habitat dynamics (Fazekas et al. 1997). This is an advance over a traditional description of seasonal dynamics that only points out incidental peaks in captures or activity. The quartile method considers the numbers over a whole season, and is thus less sensitive to occasional positive or negative influences on a species activity or trappability, helping to separate a population dynamics trend from the occasion-specific noise. It does not replace the more detailed analysis of population trends (e.g. the life cycle analysis, Southwood & Henderson 2000), but is a useful first step in describing dynamics. The differences in both the dates when population peak was reached and density fluctuations were significant among the studied host plants. Common ragweed supported the highest whitefly density (of both immatures and adults) in both years, while sunflower had the second highest density of immature whiteflies. This indicated that the whiteflies have well-defined host plant requirements. Both of the preferred plants (common ragweed, and sunflower) have denser leaf hairs than the other investigated plants. Leaf hair densities may positively affect B. tabaci oviposition and subsequent nymphal densities (Chu et al. 2001). Resistance against B. tabaci in cotton is significantly correlated with leaf hairiness, with seasonal variability due to differences in leaf color, shape, and hair types (Alexander et al. 2004), indicating that several morphological plant traits cumulatively contribute to whitefly population levels (Sial et al. 2003). Low abundance, higher level of both parasitism and oviposition rates of Bemisia argentifolii are also connected to leaf hair density on certain soybean isolines in Florida, USA (McAuslane 1996), which lead the author to suggest soybean as a trap crop to reduce whitefly infestations on peanut(arachis hypogea L.) (McAuslane 1996). In our case, soybean was less suitable as host plant than the other crops tested. No whitefly was observed on maize, probably because of low leaf hair density and an upright leaf structure. Therefore, maize may function as a physical barrier or repellent plant rather than a sink or source for B. tabaci. Whiteflies showed various reactions to piemarker. Adult density on piemarker was higher than on cotton when intercropped in single line, strip or plot within the cotton field (Lin et al. 2006). Piemarker planted within wild cabbage (Brassica oleracea L.) plots can reduce adult numbers by % (Tan et al. 2011). Piemarker can also attract more whiteflies than cowpea [Vigna unguiculata (L.) Walp.], or eggplant, at least under glasshouse conditions (Cai et al. 2011). However, spraying 6

7 piemarker leaf crude extract can significantly decrease whitefly numbers on potato (Solanum tuberosum L.) leaves (Zhao et al. 2010). Apparently, not only the host plant species itself, but its proportion in the landscape and its planting pattern can affect whitefly population densities. Trap crops can also attract natural enemies to the fields and enhance naturally occurring biological control (Landis 2000) but the role of natural enemies in determining the final density was not considered in this study. Whiteflies first appeared on weeds, especially on common ragweed which grew near cotton fields, greenhouses and ditches; at this stage, very few occurred on other plants. Whiteflies cannot overwinter in the field in northern China, and the founders of summer field populations usually come from greenhouse-grown vegetables (Zhou et al. 2006). There were several greenhouses in the study area, and whiteflies could disperse en masse from these to the outside plants after the plastic film was removed in late April. Common ragweed started to grow about 15 days earlier than cotton, and thus became an important source for whiteflies colonizing other crops. The start of the population build-up depends on the planting date, as well as the release of the whitefly colonizers from the greenhouses, and this can explain the differences detected between 2010 and In 2011, planting happened later, so the whitefly field season differed accordingly. The differences registered in our study depended on host plant quality and host plant availability in time, but not on host resource quantity. We found no reports in the literature on the use of sweet potato as a trap crop in whitefly control. The main damage of the whitefly caused to sweet potato is via virus transmission. Whiteflies transmit the sweet potato Sunken Vein Virus (SPSVV) (Ames et al. 1997), and can transmit the sweet potato chlorotic stunt virus (SPCSV) and the sweet potato feathery mottle virus (SPFMV) (Reed et al. 2009). There was a high degree of whitefly damage on sweet potato observed in our study, but due to the above risk, its use as a trap crop cannot to be recommended. CONCLUSION Our results demonstrated that common ragweed and sunflower can attract whiteflies, especially during their main activity period. The common ragweed was the most attractive host plant, but is listed as a quarantine agricultural pest because of its agricultural importance, notorious allergenicity, and its impacts on biodiversity in China (Wan et al. 1995). It is also an important source of whiteflies colonizing cotton in northern China, and can boost whitefly population density on fully-grown cotton. Thus this host plant, even if attractive to whiteflies, would not be suitable as a trap or a barrier crop, 7

8 and should be eliminated as much as possible in cotton growing areas. MATERIALS AND METHODS Field arrangement The study was done in Langfang, Hebei Province ( N, E, northern China). The farm is in a typical agricultural region with mixture of various crop plants. Cotton and maize were the main crops in this area; other crops were planted as a mosaic among cotton and maize fields in a non-regular arrangement. Numerous weeds (mainly common ragweed and piemarker) were growing adjacent to ditches and roads. The total region surveyed was>30 ha. There were a total of 42 field plots, covering>30 ha on the farm, including 11 plots of cotton (Gossypium hirsutum L.), 10 plots of maize (Zea mays L.), 7 plots of soybean (Glycine max L.), 5 plots each of sweet potato (Ipomoea batatas L.) and sunflower (Helianthus annuus L.), 3 plots of sorghum (Sorghum vulgare L.) and 1 plot of foxtail millet [Setaria italica (L.) Beauv.]. We surveyed existing experimental plots of six common plants, sunflower, soybean, sweet potato, maize, piemarker, and common ragweed. We also included cotton as the control crop. For each candidate host plant, five non-adjacent field plots of>200 m 2 each were randomly chosen. None of the sites were treated with pesticides. On each plot, 5 plants were randomly chosen on each survey occasion. Plant survey On the survey site as well as around it, there were numerous glasshouses with plastic cover that were opened once the temperature became warm. This provided ample and multiple sources of whitefly colonists. Most of the crops were planted in early May, and we immediately started checking the target plants every three or four days for whitefly presence; detailed sampling was initiated when whiteflies started colonizing cotton and the other plants. In northern China, this usually happens in early July (Lin et al. 2002). Weekly sampling was carried out from this time until the end of the growing season (26 June - 9 October, a total of 15 occasions in 2010, 7 July - 22 September, a total of 12 samples in 2011). Whitefly densities were estimated by counting individuals on two leaves of similar age each at the upper, middle and lower positions of the plant (Naranjo and Flint 1995). Adults were counted in situ; afterwards, the leaves were cut, individually placed in plastic bags, and brought to the laboratory to count immatures (nymphs and pupae) under a dissecting microscope (20 magnification). The area of each leaf was measured by a leaf area measuring instrument (Yaxin-1242), from which standardized density data (no. of individuals per 100 cm 2 leaf surface) were obtained. 8

9 B. tabaci identification To check the identity of the whiteflies present in the study area, we took regular samples of three-five whitefly adults from each plant on each census occasion. These were tested using the method in Boykin et al. (2007) based on the mtcoi sequences. All the B. tabaci collected from the six different plant species belonged to B. tabaci MED (no adults occurred on maize). Describing seasonal activity The seasonal activity curve was standardized following the method by Fazekas et al. (1997). This method divides the seasonal activity into three periods: early, main and late, and formally identifies the start and end of each of these, as well as the date of the seasonal activity peak. First, the numbers observed are summed to construct a cumulative curve, which is then graphed against time (time on the horizontal, cumulative densities on the vertical axis (Fig. 1) (Fazekas et al. 1997). The three cardinal points are the dates when 25%, 50% and 75% of the total densities are reached. These also divide the curve into four segments. The start of the main activity period is from the date when the cumulative densities reach 25% of the total (the start of the second quartile on the vertical axis), and the end is the date when 75% (the end of the third quartile on the vertical axis) is reached. The date when the cumulative curve reaches 50% is the date of the activity peak (notice that this is not linked to a density peak observed at a given time it is a product of the cumulative curve, so it can also fall on a date when no census was made). The formally defined early activity period extended from the start of the census to the beginning of the main activity period, and the likewise formalized late activity period lasted from the end of the main activity period until the end of the observations, when activity stopped (Fazekas et al. 1997). Data analysis Census data were initially subjected to a one-way ANOVA (repeated measures).differences in whitefly densities were compared among host plants on the same dates, as well as among weeks of each host plants, constrained by season (identified as above) by Tukey s HSD (P=0.05). The data were log 10 (x+1) transformed to meet the normalization assumption. A significance level of P=0.05 was used for all tests. Data analyses were performed using SAS version 8 (SAS Institute 1999). Acknowledgements This research was funded by grants from the National Natural Science Foundation of China ( ), the National Basic Research and Development Program of China (2009CB119200) and 9

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13 Table 1 Main activity periods and peak activity dates of immature and adult Bemisia tabaci MED on different host plants at Langfang, Hebei Province, China. Plants were arranged according to the date of the peak immature activity. Year, plant species 2010 Common ragweed Immatures Main activity period (duration in days) Peak activity date Adults Main activity period (duration in days) Peak activity date 26 Jul.-16 Aug. (22) 26 Jul. 26 Jul.-9 Aug. (15) 2 Aug. Soybean 2-23 Aug. (22) 2 Aug. 26 Jul.-16 Aug.(22) 2 Aug. Cotton 9-30 Aug. (22) 9 Aug Aug. (15) 16 Aug. Sweet Aug. (15) 16 Aug. 16 Aug.-6 Sept. (22) 16 Aug. potato Piemarker 2-16 Aug. (15) 16 Aug. 26 Jul.-9 Aug. (15) 26 Jul. Sunflower 9-23 Aug. (15) 23 Aug Aug. (22) 23 Aug Piemarker 2-18 Aug. (17) 18 Aug. 26 Jul.-9 Aug. (15) 9 Aug. Common ragweed 18 Aug.-8 Sept. (22) 18 Aug. 28 Jul.-18 Aug. (22) 11 Aug. Sweet potato 11 Aug.-1 Sept. (22) 25 Aug. 11 Aug.-11 Sept. (32) 1 Sept. Soybean 18 Aug.-8 Sept. (22) 25 Aug. 25 Aug.-15 Sept. (22) 8 Sept. Sunflower 18 Aug.-1 Sept. (15) 1 Sept. 18 Aug.-1 Sept. (15) 25 Aug. Cotton 25 Aug.-8 Sept. (15) 1 Sept. 11 Aug.-1 Sept. (22) 1 Sept. 13

14 Fig. 1 Cumulative seasonal activity curves of Bemisia tabaci MED in crops (A) and weeds (B) in 2010 and weeds (B) in 2010 and

15 Fig. 2 Seasonal dynamics of Bemisia tabaci MED (mean±se) on different host plants in Langfang, northern China, in 2010 and Note the logarithmic scale on the vertical axis. 15

16 Fig. 3 Comparison of the mean densities (±SE) by activity periods (early, main, and late, established by the quartile method) for Bemisia tabaci MED on different host plants in Langfang, Hebei Province, China, in 2010 and Bars with different letters above indicate significant differences (Tukey HSD test; P<0.05) in whitefly densities among different host plants. 16