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Changes in population density of Aleurocanthus
camelliae (Hemiptera: Aleyrodidae) and parasitism
rate of Encarsia smithi (Hymenoptera: Aphelinidae) during the early invasion stages
Ryuji Uesugi*, Kaori Yara, Yasushi Sato Tea Pest Management Research Team, Department of Tea, National Agriculture and Food Research Organization (NARO), Institute of Vegetable and Tea Science (NIVTS), Kanaya-Shishidoi, Shimada, Shizuoka 428-8501, Japan
* Corresponding author: Phone and Fax: 029-838-8939; E-mail:
[email protected]
Abstract
Invasive pest insects are often controlled by non-native natural enemies introduced from the original home range of the target pests. The non-native parasitoid wasp Encarsia smithi (Silvestri), which naturally migrated to tea plantations in Japan, is a potential agent for the biological control of the invasive camellia spiny whitefly Aleurocanthus camelliae Kanmiya & Kasai. To evaluate the effectiveness of E. smithi as a pest control agent, we surveyed 27 tea plantation sites in Shizuoka Prefecture, Japan to identify any changes in the population densities of A. camelliae 1–3 years after the initial detection in 2010 and also to estimate the parasitism rates of E. smithi. The results suggested that parasitism by E. smithi considerably affected the field mortality rates of A. camelliae. Wasps rapidly spread to the region where whiteflies expanded their distribution and controlled population outbreaks in many sites. However, at some sites where the population density of A. camelliae increased rapidly, the parasitism rates of E. smithi tended to remain at low levels or declined. Overall, our results suggested that parasitism by E. smithi could be used as an effective measure for the control of A. camelliae populations in tea plantations. Keywords Aleurocanthus camelliae, Classical biological control, Encarsia smithi, Invasive pest species, Population dynamics 1
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Introduction
The camellia spiny whitefly Aleurocanthus camelliae Kanmiya & Kasai is one of the most important pest insects of the tea plant Camellia sinensis (L.) Kuntze in China (Xie 1995; Xuefen et al. 1997; Han and Cui 2003), Taiwan (Hsiao and Shiau 2004), and Japan (Yamashita and Hayashida 2006). A. camelliae damages tea production by reducing tree vigor due to sap losses and sooty mold and negatively affects harvest productivity (Yamashita and Hayashida 2006). It is an invasive pest in Japan that was first detected in tea plantations in Uji, Kyoto Prefecture, in 2004 (Yamashita and Hayashida 2006) and in almost all the main areas of tea production by 2010, mainly due to human-mediated migration (Kasai et al. 2010; Ozawa et al. 2015). The non-native parasitoid wasp Encarsia smithi (Silvestri) was reported to suppress the Japanese population of A. camelliae (Yamashita and Hayashida 2006; Kishida et al. 2010; Ozawa and Uchiyama 2013). E. smithi is widely known as an excellent agent for the biological control of the citrus spiny whitefly Aleurocanthus spiniferus (Quaintance) (Flanders 1969). The Japanese population of E. smithi was generated from 20 individuals collected in China and released to control citrus spiny whitefly in a citrus orchard in 1925 (Kuwana 1934). Then, the population was bred and released in additional affected areas, following an initiative of the Japanese government. As a result, A. spiniferus was almost completely eliminated, except for occasional outbreaks in a limited number of regions (Ohgushi 1969). E. smithi was also introduced in Micronesia (Nafus 1988; Marutani and Muniappan 1991; Muniappan et al. 1992), Hawaii (Nakao and Funasaki 1979), and southern Africa (van den Berg and Greenland 1997) and effectively controlled the populations of A. spiniferus. E. smithi can parasitize different species of the genus Aleurocanthus (Schauff et al. 1996; Heraty et al. 2007; Dubey and Ko 2012) such as the citrus blackfly Aleurocanthus woglumi Ashby in Mexico (Flanders 1969). The population density of A. camelliae often decreases at high parasitism rates of E. smithi (Yamashita, personal communication); therefore, the latter is a potential agent for the biological control of camellia spiny whitefly. E. smithi was not detected in tea plantations prior to the invasion of A. camelliae in Japan (Takagi 1974); thus, its migration probably occurred either concurrently or immediately after the invasion of whiteflies. Since an artificial release of E. smithi was not implemented in Japanese tea plantations, E. smithi either migrated from citrus spiny whitefly to camellia spiny whitefly, or it was newly immigrated to tea plantations, following the invasion of camellia spiny whitefly. A molecular study using base sequences of mitochondrial DNA suggested that the second assumption is more plausible (Uesugi et al. 2016). In either case, the ability of E. smithi to quickly disperse and locate whiteflies makes it a very effective agent of biological control in the early stages of invasion. If the migration and dispersal of E. smithi to tea plantations were slow, whitefly outbreaks would often occur (Torchin et al. 2003). In this study, we surveyed 27 tea plantation sites in Shizuoka Prefecture, Japan to identify any changes in the population densities of A. camelliae 1–3 years after the initial detection in 2010 and also to estimate the parasitism rates of E. smithi. Based on the obtained data, we discussed the dispersal of E. smithi and the field mortality rates A. camelliae due to parasitism during the early stages of invasion. 2
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Materials and methods Study sites
A total of 26 tea plantation sites (ID1–ID26) was surveyed in this study, located within a 3.86 km radius from the site (ID0; 34.784°N, 138.131°E) where A. camelliae was first detected in Shizuoka Prefecture, Japan in October 2010 (Ozawa et al. 2015; Fig. 1). A. camelliae invaded this area in October 2008 from Mie Prefecture, due to human-mediated migration. ID5 was located in an organic tea plantation, whereas all the other tea plantations were under conventional pest control management with the regular application of insecticides. Population density and parasitism rate
The population density of A. camelliae and parasitism rate of E. smithi were estimated from surveys that carried out in 2011–2013. In 2011, two surveys were conducted in 15 and 24 sites, whereas in 2012 and 2013, four surveys each year were conducted in all 27 sites (Table 1). Due to the four discontinuous generations of A. camelliae per year in this region (Ozawa et al. 2013), leaf sampling was performed in May, July, September, and November in accordance with each generation, a few days after the peak of adult whitefly emergence when many of the hosts and parasitoids also emerge (Table 1). A total of 100 tea leaves was collected from five tea beds (i.e., 20 leaves per tea bed) in each site; however, the sampling number was decreased to 50, 30, 20, or 10 with the increasing density of A. camelliae population. We collected the fourth to sixth leaves from the top of a shoot, in order to assure that most nymphs were of the current generation. Fourth instar nymphs were counted on each leaf under a stereomicroscope in the laboratory. Broken nymph shells or shells without marginal wax were excluded from count data. The emergence of A. camelliae was distinguished from that of E. smithi by the shape of exit holes on the shells. The holes caused by the emergence of whiteflies are T-shaped, whereas those caused by wasps are circular. We considered that all the circular holes were caused by E. smithi, since no other parasitoid wasps were ever recorded in Japan; in addition, we did not observe any other wasps emerged from A. camelliae. The rate of parasitism was calculated based on the number of holes as follows: p/(h + p), where h is the number of emerged whiteflies, and p is the number of emerged wasps. The 95% confidence intervals (CIs) of the population density of A. camelliae and parasitism rate of E. smithi were calculated using 1,000 resampling iterations for the data obtained from each leaf. Data analysis
The contribution of E. smithi to the field mortality rate of A. camelliae was evaluated by the relationship between the growth rate of A. camelliae population and the parasitism rate of E. smithi. The growth rate per generation in each site (r, i.e, the ratio of population density of the next generation to the current generation) was calculated as follows: = (1 − )(1 − ), (1) 3
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where rmax is the maximum growth rate of A. camelliae population per generation; mp is the mortality rate due to parasitism per generation (i.e., the rate of parasitism); mo is the unknown mortality rate due to other factors than parasitism, including pesticides, other natural enemies, low temperature in winter, mechanical injury by wind or raindrop, and leaf pruning. In this study, the maximum growth rate of A. camelliae population per generation (rmax) was calculated using the intrinsic rate of natural increase (0.056 d-1) and the development time (45.9 d) of A. camelliae at 25°C (Kasai et al. 2012) and estimated to be 13.07. From equation (1), we obtained the following: = + , (2) where K = –log(r/rmax); kp = –log(1 – mp); and ko = –log(1 – mo). The effects of the surveyed site, year, and month on kp and ko (i.e., K – kp) were evaluated by keyfactor/key-stage analysis (Yamamura 1999; Yamamura 2012) as described by Yamamura (2014) using R 3.2.2 (R Core Team, Vienna, Austria). Population densities of less than 0.5 nymphs per leaf were excluded, since they were too low to estimate the rate of parasitism. Regression analysis was implemented as follows: = + , (3) where K and kp are the response and predictor variables, respectively. If the slope (α) is equal to 1, the intercept (β) is equal to ko. To calculate the slope and the intercept of the regression line, we used the linear mixed model (LMM), in which the surveyed site, year, and month were random effects. The regression analysis was performed using the lme4 package (Bates et al. 2016) in R 3.2.2. The 95% Wald CIs of estimates were calculated by the confint function in R 3.2.2. Population densities of less than 0.5 nymphs per leaf were excluded. We also evaluated the effect of distance from site ID0 and the surveyed generation of whiteflies on population density and parasitism rate using the generalized linear mixed model (GLMM), in which the surveyed year, and month were random effects. The analysis was performed using the lme4 package in R 3.2.2.
Results
Changes in the population density of A. camelliae fourth instar nymphs and the parasitism rate of E. smithi in each site are shown in Fig. 2. In ID0, the population density of A. camelliae was severely high when first detected in October 2010, and heavy sooty mold was observed on the entire surface of tea leaves (Ozawa et al. 2015). In 2011, the population densities were less than 10 nymphs per leaf, i.e., 4.80 (95% CI: 2.87–7.15) nymphs per leaf in May, 6.22 (95% CI: 2.92–8.93) nymphs per leaf in July, 8.04 (95% CI: 6.34–10.20) nymphs per leaf in September, and 3.04 (95% CI: 2.29–3.85) nymphs per leaf in November, and sooty mold was limited only to a few parts of the tea plantation. In September and November 2012 and in 2013, the population density was less than one nymph per leaf. In ID0, parasitism by E. smithi was observed after the first survey in May 2011, and the rate of parasitism was 54.3% (95% CI: 36.2%–72.1%) in September 2012. The patterns of change in the population density of A. camelliae were different between the sites. The highest population densities were observed in ID1, ID6, ID10, and ID15, which were 123 (95% CI: 88.0–176) nymphs per leaf in September 2012, 29.7 (95% CI: 21.3–39.3) nymphs per leaf in November 2013, 120 (95% CI: 82.6–160) nymphs per leaf in November 2013, and 40.5 (95% CI: 4
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28.8–54.7) nymphs per leaf in November 2013, respectively, whereas they were less than 10 nymphs per leaf in ID2–ID4, ID7–ID9, ID11–ID14, and ID16–ID26 almost throughout the survey period. In ID5, the population density remained high throughout the survey period, reaching the highest rate of 68.8 (95% CI: 46.5– 101) nymphs per leaf in November 2013. Parasitism by E. smithi was detected in ID1, ID3, and ID6, which were the nearest sites to ID0, in November 2011 and in almost all the sites in 2012 and 2013. In some sites (i.e., ID6, ID10, and ID15), the rate of parasitism tended to remain at low levels or declined with increasing population density of A. camelliae. For example, in ID10, the population density of A. camelliae rapidly increased from 5.08 (95% CI: 3.66–6.81) nymphs per leaf in May 2013 to 120 (95% CI: 82.6–160) nymphs per leaf in November 2013, while the parasitism rate of E. smithi decreased from 3.43% (95% CI: 0%–8.54%) to 0.137% (95% CI: 0%–0.302%), respectively. Key-factor/key-stage analysis showed that ko was more important (92.5%) than kp (7.53%) (Table 2). The total survival rate was strongly affected by the surveyed site and month (21.5% and 19.7%, respectively), but not as much by the surveyed year (2.70%) (Table 2). Significant differences were observed among the effects of different surveyed months on the total survival rate (P = 0.000521, Table 2). A significant correlation between K and kp was detected by regression analysis using LMM (P = 0.00682). The slope (α) and intercept (β) of the regression line were calculated to be 0.682 (95% CI: 0.175–1.17) and 0.978 (95% CI: 0.562–1.39), respectively. When the intercept (β) was assumed to be equal to ko, the mortality rate of A. camelliae due to other factors than parasitism (mo) was calculated to be 62.4% (95% CI: 42.9%–75.1%). When the rate of parasitism by E. smithi (mp) was zero, the population growth rate per generation (r) was calculated to be 4.91 (95% CI: 3.23–7.46). Regression analysis using GLMM suggested that the distance from ID0 had a significant negative effect on both the population density of A. camelliae (P < 0.0001) and the parasitism rate (P = 0.000174) (Table 3). The surveyed generation did not have a significant effect on the population density (P = 0.0598) or parasitism rate (P = 0.0910) (Table 3). However, there was a significant effect of the interaction of distance and generation on the population density (P = 0.00982) (Table 3).
Discussion
E. smithi is well known as a unique parasitoid wasp of the invasive camellia spiny whitefly A. camelliae in Japan, since its recent migration to tea plantations (Kishida et al. 2010). In this study, parasitism by E. smithi was detected in almost all the surveyed sites in 2012 and 2013, reaching substantial rates in many cases. Regression analysis using GLMM suggested that the population density of A. camelliae did not significantly increase with generation progress (Table 3). As shown in Fig. 2, the population density was suppressed at less than 10 nymphs per leaf, except for that in ID1, ID5, ID6, ID10, and ID15. Regression analysis using LMM suggested that K was significantly correlated with kp. Indeed, the population of A. camelliae increased by 4.91 (95% CI: 3.23–7.46) times per generation in an average tea plantation when parasitism did not exist. Although key-factor/key-stage analysis revealed that the mortality rate due to other factors than parasitism was relatively high, parasitism by E. smithi considerably contributed to suppress the population density of A. camelliae during the early 5
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invasion stages. In addition, Kishida et al. (2010) reported that host-feeding behavior may also increase the mortality rates of A. camelliae; however, this effect was not evaluated in the present study. Overall, our data suggested that E. smithi is an effective agent for the biological control of A. camelliae. E. smithi is known to have high dispersal ability. For example, in Micronesia, parasitism by E. smithi was detected at distances of more than 1 km from the release site within a year after the introduction of only 24–67 individuals (Marutani and Muniappan 1991). In this study, parasitism by E. smithi was detected at distances of up to 3.86 km from ID0 without artificial release and migration, which could be explained either by the migration of E. smithi from citrus spiny whitefly to camellia spiny whitefly, or its immigration to tea plantations, following the invasion of camellia spiny whitefly. The plausible routes of migration are two; one is migration from an existent population in surrounding citrus orchards, and the other is migration from a population in the initial invasion site (ID0), which followed the invasion of whitefly. The second route would be more plausible, since regression analysis using GLMM suggested that the parasitism rate was significantly negatively correlated with the distance from ID0 (Table 3). The high regional rates of spread might be caused by frequent aerial dispersal. For example, the populations of the ash whitefly parasitoid Encarsia inaron (Walker) are dispersed at long distance by prevailing winds (Pickett and Pitchairn 1999). The population densities of A. camelliae were largely different between the surveyed sites. This trend has been also observed in other regions in the early invasion stages (Takewaka and Murai 2008; Ozawa et al. 2015). Key-factor/keystage analysis revealed that the total survival rate of A. camelliae was strongly influenced by the survival rate due to other factors than parasitism, and that differences between the surveyed sites substantially influenced the survival of A. camelliae (Table 2). A plausible explanation for the site effect on the mortality rate could be that the mortality rate was highly influenced by the different pest control management practices in each tea plantation. For example, the population density of A. camelliae remained high in ID5 located at organic tea plantation, despite the high parasitism rate of E. smithi, probably because the mortality rate of whiteflies due to pesticides was small. Key-factor/key-stage analysis also revealed that the surveyed month strongly influenced the mortality of A. camelliae (Table 2). It is possible that the annual leaf pruning in May after the first harvest might decrease the population density (K. Yamashita, personal communication) as well as the high mortality of egg and first instar nymph during the winter (Yamashita et al. 2016). Our results suggested that whitefly outbreaks were related to the low rates or decline of parasitism, which were probably caused by the use of broadspectrum insecticides. Bioassay studies demonstrated that organophosphorus, pyrethroid, nereistoxin, and neonicotinoid pesticides, which are used in tea plantations in Japan, are lethal to E. smithi (Fukuyama et al. 2011; Yamashita and Yakahi 2011). The high mortality rates of E. smithi due to insecticides might cause the resurgence of A. camelliae populations, because sessile nymphs are more protected on the underside of the leaves. However, the relationship between the application of broad-spectrum insecticides and the decline in the parasitism rates of E. smithi, in order to clarify the mechanism of A. camelliae resurgence, requires further investigation.
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References
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This study was supported in part by a grant from the Research and Development Projects for Application in Promoting New Policy of Agriculture, Forestry and Fisheries (no. 21002, MAFF). We would like to thank A. Ozawa, Y. Yumita, and T. Nakaichi for their guidance in field work. We also thank Z.-X. Luo for the assistance in this study.
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Figure legends
Fig. 1 Tea plantation sites (ID 0–26) that surveyed for estimating the population density of the camellia spiny whitefly Aleurocanthus camelliae and the parasitism rate of the non-native parasitoid wasp Encarsia smithi in Shizuoka Prefecture, Japan. ID0 is the site where A. camelliae was initially detected in October 2010. ID1–ID27 are within a distance of 3.86 km from ID0.
Fig. 2 Changes in the population density of the camellia spiny whitefly Aleurocanthus camelliae (solid black line) and the parasitism rate of the nonnative parasitoid wasp Encarsia smithi (dotted gray line) in 27 tea plantation sites in Shizuoka Prefecture, Japan from 2011 to 2013. Numbers in round brackets are the site identification (ID) number. ID0 is the site where A. camelliae was initially detected in October 2010. ID1–ID27 are within a distance of 3.86 km from ID0. Open circles indicate the absence of fourth instar nymphs. Vertical bars show 95% confidence intervals estimated by 1,000 resampling iterations.
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Table 1. Date of leaf sampling and number of tea plantation sites (ID 0–26) that were surveyed for estimating the population density of the tea spiny whitefly Aleurocanthus camelliae and the parasitism rate of the non-native parasitoid wasp Encarsia smithi in Shizuoka Prefecture, Japan. Date of leaf sampling
No. of sites
Jul 07, 2011
24
Site identification (ID) number a
May 09, 2011
15
0–12, 15, 20, and 21
Sep 17, 2011
27
0–26
Nov 04, 2011
May 18, 2012 Jul 18, 2012
Sep 25, 2012
Nov 19, 2012
May 08, 2013 Jul 30, 2013
Sep 19, 2013
Nov 12, 2013
27 27 27 27
0–23 0–26 0–26 0–26
27
0–26 0–26
27
0–26
27 27 27
0–26 0–26 0–26
, ID0, the site that A. camelliae was initially detected in Shizuoka Prefecture, Japan in October 2010; ID1–ID27, sites within a distance of 3.86 km from ID0 a
Table 2. Effects of the surveyed site, years, and month on the mortality rate of Aleurocanthus camelliae due to parasitism or other factors as revealed by key-factor/key-stage analysis (Yamamura 1999). Factor
d. f.
Site
20
Year
2
Month
3
Unknown variability Totalc
58
kp
Stagea
ko
Totalb
F
P
–0.108 (–0.368%)
6.41 (21.9%)
6.29 (21.5%)
1.12
0.361
–0.269 (–0.919%)
6.04 (20.7%)
5.77 (19.7%)
1.40
0.255
6.81
0.000521
0.458 (1.57%) 2.12 (7.25%) 2.20 (7.53%)
0.332 (1.13%) 14.3 (48.8%) 27.0 (92.5%)
0.79 (2.70%) 16.4 (56.0%) 29.2 (100%)
Population densities of less than 0.5 nymphs per leaf were excluded from this analysis. a, kp = – log(1 – mp), where mp is the mortality rate due to parasitism per generation; ko = – log(1 – mo), where mo is the estimated mortality rate due to other factors than parasitism. b, key factor; c, key stage.
Table 3. Effects of the distance from ID0a and the surveyed generation on the population density of Aleurocanthus camelliae and the parasitism rate of Encarsia smithi as revealed by the generalized linear mixed model. Response variable
Model
Logarithmic Gaussian population density
Parasitism rate
Logistic
Predictor
P
(Intercept)
–0.400 (–1.02, 0.235)
0.279
Distance (km)
–0.996 (–0.461, –0.270)
< 0.0001
Generation
0.0907 (0.0106, 0.168)
0.0598
Distance × Generation
0.0727 (0.0341, 0.107)
< 0.0001
–2.18 (–4.03, –0.344)
0.00229
–0.343 (–0.523, –0.165)
0.000174
(Intercept) Distance (km) Generation Distance × Generation
a
Estimate (95% CI)
0.121 (–0.0163, 0.381)
0.0910
0.00982 (–0.00079, 0.0277)
0.279
, ID0, the site that A. camelliae was initially detected in Shizuoka Prefecture, Japan in October 2010.
Tea plantation N 34.80 ºN
24
3 km
2 km
Initial place of invasion 20
138.10 ºE
Fig. 1
12 1
3
15 17 18
4 50 2
10
Kikugawa
21
13
1 km
11
26
8
9
6
7
22
14 19 16
138.15 ºE
Shimada
Japan Tokyo
23
25
Makinohara
Shizuoka Prefecture
(0)
0 km
102
whitefly parasitism
100 103 (1)
100 103
80 102
80 102
0.35 km
100
(2)
0.38 km
80
10
60
10
60
10
60
1
40
1
40
1
40
10-1
20 10-1
20 10-1
20
10-2
0
0
0
103
102 10
10-2
100 103 (4)
(3)
0.39 km
100 103
80 102 0.45 km
1
10-2
80 102 60
10
40
1
40
1
40 20
20 10-1
10-2
0
0
102 10
10-2
100 103
0.90 km
1
10-2
100 103
(7)
10
60
10
40
1
40
1
40 20
10-2
0
0
Fig. 2
100
(8)
60
20 10-1
2013 Year
0
80 102
20 10-1
2012
60
80 102 0.92 km
10-1
2011
80
10
20 10-1
(6)
0.82 km
60
10-1 103
100
(5)
10-2
2011
2012
2013 Year
10-2
1.08 km
2011
Parasitism rate of E. smithi (%)
Population density of whitefly of A. camelliae (fourth instar nymphs / leaf)
103
80 60
2012
2013 Year
0
102
(9)
1.33 km
whitefly parasitism
100 103 80 102
100 103
(10)
1.54 km
100
(11)
1.65 80 102 km
80
10
60
10
60
10
60
1
40
1
40
1
40
10-1
20 10-1
20 10-1
20
10-2
0
0
0
103
102 10
10-2
100 103
(12)
1.90 km
80 102
1
60
10
40
1
10-2
100103
(13)
2.00 km
100
(14)
80 102 2.08 km
80
60
10
60
40
1
40
10-1
20 10-1
20 10-1
20
10-2
0
0
0
103
102
10-2
100 103
(15)
2.35 km
80 102
10-2
100103
(16)
2.38 km
80 102
(17)
100
2.40 km
80
10
60
10
60
10
60
1
40
1
40
1
40 20
10-1
20 10-1
20 10-1
10-2
0
0
2011
2012
Fig. 2 Continued.
2013 Year
10-2
2011
2012
2013 Year
10-2
2011
Parasitism rate of E. smithi (%)
Population density of whitefly of A. camelliae (fourth instar nymphs / leaf)
103
2012
2013 Year
0
102
10
whitefly parasitism
2.40 km
1
100 103 80 102 60
10
40
1
(19)
100 103
2.48 km
80 102
(20)
100
2.69 km
80
60
10
60
40
1
40
10-1
20 10-1
20 10-1
20
10-2
0
0
0
103
102 10
10-2
100 103
(21)
2.83 km
80 102
1
60
10
40
1
10-2
100 103
(22)
2.86 km
80 102 2.95 km
80
60
10
60
40
1
40 20
10-1
20 10-1
20 10-1
10-2
0
0
103
102 10
(24)
10-2
100 103
3.57 km
80 102
1
60
10
40
1
(25)
10-2
100 103
3.83 km
80 102
20
0
Fig.2 Continued.
2012
2013 Year
80
40
0
2011
3.86 km
1
10-2
2013 Year
100
40
20 10-1
2012
(26)
10
20 10-1
2011
0
60
10-1
10-2
100
(23)
10-2
2011
Parasitism rate of E. smithi (%)
Population density of whitefly of A. camelliae (fourth instar nymphs / leaf)
103 (18)
60
2012
2013 Year
0
