Research Article Received: 29 September 2013

Revised: 3 December 2013

Accepted article published: 24 December 2013

Published online in Wiley Online Library: 17 February 2014

(wileyonlinelibrary.com) DOI 10.1002/ps.3716

Host suitability comparison between the MEAM1 and AsiaII 1 cryptic species of Bemisia tabaci in cotton-growing zones of Pakistan Muhammad Z Ahmed,a,b∗ Muhammad Naveed,c Muhammad Noor ul Ane,d Shun-Xiang Ren,a Paul De Barroe and Bao-Li Qiua∗ Abstract BACKGROUND: Bemisia tabaci is a cryptic species complex. In Pakistan, members of the complex, MEAM1 and AsiaII 1, are the predominant species infesting cotton. The biology of the two on cotton, collard, cucumber and tomato was studied. RESULTS: In all cases there were significant interactions between species and host. MEAM1 developmental periods did not differ significantly across hosts, whereas AsiaII 1 developed more slowly on vegetables than on cotton. MEAM1 survival was highest on tomato (53.5 ± 1.1%), while AsiaII 1 survived best on cotton (67.3 ± 11.6%). MEAM1 longevity and fecundity were highest on tomato (14.7 ± 1.7 days and 82.4 ± 9.9 eggs), while AsiaII 1 longevity and fecundity were highest on cotton (23.7 ± 2.5 days and 135.2 ± 13.6 eggs). The MEAM1 intrinsic rates of increase (rm ) on cotton and vegetable were similar (0.08–0.10), whereas the AsiaII 1 rm on cotton (0.15) was higher than on vegetables (0.11–0.13). The biology of MEAM1 from Pakistan was compared with published studies; it had a consistently slower rate of development, lower percentage survival, lower adult longevity, longer generation time, lower net reproductive rate and lower rm . CONCLUSIONS: MEAM1 performed similarly across all hosts, whereas AsiaII 1 performed better on cotton. The comparison between the Pakistani MEAM1 with published studies suggests that the invasive MEAM1 may have higher performance. c 2013 Society of Chemical Industry  Keywords: Bemisia tabaci; host plant; life table; vegetable; cotton; Pakistan

1

INTRODUCTION

Pest Manag Sci 2014; 70: 1531–1537



Correspondence to: Muhammad Z Ahmed, Florida Museum of Natural History, University of Florida, Gainesville, FL 32611, USA; and Bao-Li Qiu, Department of Entomology, South China Agricultural University, Guangzhou, China. E-mails: [email protected] and [email protected]

a Department of Entomology, South China Agricultural University, Guangzhou, China b Florida Museum of Natural History, University of Florida, Gainesville, FL, USA c Central Cotton Research Institute, Multan, Pakistan d Department of Agricultural Entomology, University of Agriculture Faisalabad, Punjab, Pakistan e CSIRO Ecosystem Sciences, Brisbane, Queensland, Australia

www.soci.org

c 2013 Society of Chemical Industry 

1531

The whitefly pest, Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae), has a global distribution1 and is capable of causing extensive damage to vegetable, grain legume and fibre crops.2 It is a cryptic species complex, composed of numerous morphologically indistinguishable3 but genetically distinct groups.1,4,5 Molecular5,6 and biological data7,8 support their status as different species.9 In the past three decades, two members of the complex, Middle East–Asia Minor 1 (MEAM1, commonly known as biotypes B and B2) and Mediterranean (commonly known as biotype Q), have spread well beyond their home ranges via trade in ornamentals.10,11 In Pakistan, so far, 229 hosts of B. tabaci have been recorded.12 Among these host plants, cotton, Gossypium hirsutum L., is one of the most important economic crops; cotton and cotton products are major exports, and Pakistan is the fifth largest producer of cotton and the third largest exporter of raw cotton in the world.13,14 Cotton leaf curl disease (CLCuD) is caused by a complex of begomovirus species, all of which induce similar symptoms in cotton and are transmitted by B. tabaci.15 Three species, Asia1, AsiaII 1 and MEAM1, have been recorded in the cotton zone of Pakistan.16,17 While MEAM1 has invaded numerous countries, the population in Pakistan is more likely to be indigenous as it is genetically distinct from the invasive

haplotypes.1 AsiaII 1 (also referred to as biotypes K, P, PCG-1, PK1, SY and ZHJ2) has only been recorded on cotton plants in the Punjab, whereas Asia1 (also referred to as biotypes H, M, NA and PCG-2) has been found in both Sindh and Punjab. MEAM11 has been found only in Sindh.16,17 Given the genetic differences between MEAM1 in Punjab and those that have invaded, the authors were interested in answering two questions. Did the performance of MEAM1 on crop hosts differ from that of AsiaII

www.soci.org 1, and was there evidence to suggest a difference between the biology of MEAM1 from Pakistan (hereafter H2 MEAM1) and the biology of MEAM1 (hereafter H1 MEAM1) that had invaded. It was hypothesised that either H2 MEAM1 in Pakistan has different biological characteristics from those of the invasive H1 MEAM1 or AsiaII 1 performs better than H2 MEAM1 on cotton. There are no published comparisons of the biology of AsiaII 1 and H2 MEAM1. Based on previous results,16,17 it is tempting to suggest that AsiaII 1, which is dominant only in Punjab, and H2 MEAM1, which is only dominant in Sindh, may differ in biology. To begin to explore this, the authors compared the biological performance of AsiaII 1 and H2 MEAM1 on cotton and three vegetable hosts (collard, cucumber and tomato).

2

MATERIALS AND METHODS

Whitefly adults in Punjab and Sindh were collected in 2010 from cotton plants and reared at the University of Faisalabad, Pakistan, and the Central Cotton Research Institute, Multan. Their genetic identities were identified using mitochondrial COI (mtCOI) sequencing according to the procedure described by Ahmed et al.17 2.1 Host plants The host plants were tomato (Lycospersicum esculentum), cucumber (Cucumis sativus), collard (Brassica oleracea) and cotton (Gossypium hirsutum). Host plants were grown in pots of 12 cm diameter and used in experiments at the 6–9-leaf stage. All experiments were conducted in cages under the same conditions as Qiu et al.18 2.2 The development and survivorship of B. tabaci The development and survivorship of B. tabaci juveniles were investigated using the methods described by Qiu et al.18 In brief, 30 pairs of newly emerged MEAM1 and AsiaII 1 adults were taken from stock colonies and introduced into clip-on cages (3 cm in diameter and 1.5 cm in height) on the undersurface of the leaf. After 6 h of oviposition, adults and all eggs bar 50 were removed from the leaf. The test plants were then placed into cages (60 × 60 × 60 cm, referred to as ‘plant cages’) under conditions of 25 ± 1 ◦ C, 75 ± 5% RH and 14:10 L:D (light from 08:00 to 20:00 h). One plant per cage was used, and five leaf cages were applied on that plant in each plant cage. The developmental period and survivorship of the different stages (egg and first, second, third and fourth instars) were noted daily until all adults had emerged. Experiments were replicated 3 times on each of the host species. In each replicate, five leaf cages per plant per plant cage were used. 2.3 Sex ratios of B. tabaci adults The F1 adults were collected cage by cage and their sex was identified.19 There were three replicates.

1532

2.4 Longevity and fecundity of B. tabaci adults For each species, five pairs of newly emerged adults ( tomato (H2 MEAM1) > collard (H2 MEAM1) = tomato (AsiaII 1) = cucumber (AsiaII 1) = collard (AsiaII 1) > cotton (AsiaII 1).

1 0.63 0.72

Fecundity

1 0.8

Sex ratio

1

on tomato and cucumber were similar, while the survivorship on cotton was significantly higher than the survivorships on the other plants (Fig. 1B). There is a significant interaction between host plants and whitefly species (F 3,100 = 12.93, P = 0.0001). The generational survivorship of H2 MEAM1 and AsiaII 1 was significantly different on cotton (F 1,4 = 1681.00, P tomato (AsiaII 1) = cucumber (AsiaII 1) = collard (AsiaII 1) = tomato (H2 MEAM1) = collard (H2 MEAM1) > cotton (H2 MEAM1) = cucumber (H2 MEAM1). 3.4 Longevity of B. tabaci adults The results for longevity of H2 MEAM1 and AsiaII 1 females are shown in Fig. 1C. The female adults of H2 MEAM1 and AsiaII 1 varied significantly when compared with each other (F 1,110 = 695.27, P < 0.0001) and also varied when compared across the different host plant species (F 3,110 = 16.47, P = 0.0001). The female adults of H2 MEAM1 had no significant difference in longevity across the four hosts (Fig. 1C). The longest longevity of AsiaII 1 females was on cotton (23.8 ± 0.5 days). This was significantly longer than for the other three host plant species (F 3,8 = 40.30, P < 0.0001) and was followed by tomato and then collard (20.33 ± 0.2 and 19.6 ± 0.3 days). There was significant interaction between host plant species and whitefly species (F 3,100 = 62.40, P < 0.0001). The H2 MEAM1 females showed significantly shorter longevity than AsiaII 1 on all four host plants, but especially on cotton (cotton: F 1,4 = 364.15, P < 0.0001; tomato: F 1,4 = 134.36, P = 0.0003; cucumber: F 1,4 = 9.29, P = 0.0381; collard: F 1,4 = 66.66, P = 0.0012) (Fig. 1C). Overall, longevity for both species on all four host plant species can be arranged in the following order: cotton (AsiaII 1) > tomato (AsiaII 1) > collard (AsiaII 1) > cucumber (AsiaII 1) > cucumber (H2 MEAM1) > tomato (H2 MEAM1) = collard (H2 MEAM1) > cotton (H2 MEAM1). 3.5 Fecundity of B. tabaci adults The fecundities of H2 MEAM1 and AsiaII 1 females varied significantly (F 1,110 = 1761.68, P < 0.0001) and also varied when

c 2013 Society of Chemical Industry 

wileyonlinelibrary.com/journal/ps

1533

3.3 Survivorship of the B. tabaci immatures The rank of the survivorships of H2 MEAM1 and AsiaII 1 varied significantly (F 1,110 = 57.24, P < 0.0001) and also varied when compared across the four host plant species (F 3,110 = 4.98, P = 0.001). The survivorships of H2 MEAM1 ranked as follows: tomato > collard > cotton and cucumber (53.3 ± 3.5%, 40 ± 2.0% and 40 ± 0.0% respectively). The survivorships on cotton and tomato were the same and were significantly different when compared with cucumber and collard (F 3,8 = 7.33, P = 0.0110) (Fig. 1B). The highest survivorship for AsiaII 1 was on cotton (67.33 ± 0.67%), followed by that on collard, tomato and cucumber (55.3 ± 2.9%, 53.3 ± 1.7% and 52 ± 4.1% respectively). The survivorships Pest Manag Sci 2014; 70: 1531–1537

Longevity

www.soci.org

30

** b

20

65

a

25

** a

75

**

a

MZ Ahmed et al.

c

c

c

c

b

b

b

b

55 45

d

*

*

bc c

c

35

15

25 10

15 5

5 Cotton

A

Tomato

Cucumber

Collard

Host plants: F1,110 = 279.72, P < 0.0001; Species: F3,110 = 11.46, P < 0.0001; Interactions: F3,100 = 64.58, P < 0.0001; LSD = 1.276

**

30

a

25

e

B

*

de

c

155

d

de

10

55 5

5 Cucumber

*

* 105

Tomato

Collard

bc

15

Cotton

Cucumber

** a

205

*

*

Tomato

Host plants: F3,20 = F1,110 = 57.24, P < 0.0001; Species: F3,110 = 4.98, P = 0.001; Interactions: F3,100 = 12.93, P = 0.0001; LSD = 1.016

255

b 20

Cotton

Collard

C

c

b

d e

Cotton

Tomato

c c

e

Cucumber

Collard

D H2 MEAM1 Host plants: F1,110 = 695.27, P < 0.0001; Species: F3,110 = 16.47, P = 0.0001; Interactions: 62.40, P < 0.0001; LSD = 1.205

AsiaII 1 Host plants: F1,110 = 1761.68, P < 0.0001; Species: F3,110 = 200.65, P < 0.0001; Interactions: F3,100 = 1539.32, P < 0.0001; LSD = 4.74

Figure 1. Comparison of the biology of H2 MEAM1 and AsiaII 1 on three vegetables and cotton: (A) developmental periods (egg to adult); (B) generation survivorship; (C) longevity; (D) fecundity. An asterisk above a column indicates a significant difference between the AsiaII 1 and MEAM1 on the same host species. Columns with the same letter indicate no significant differences when the same whitefly species is compared across different plant species.

1534

compared across hosts (F 3,110 = 200.65, P < 0.0001) (Fig. 1D). H2 MEAM1 females laid more eggs on cotton and collard (cotton: 79.3 ± 1.9; collard: 81.67 ± 4.4 eggs), followed by tomato (71.67 ± 1.6 eggs). The lowest fecundity was found on cucumber (48.33 ± 1.6 eggs female−1 ). AsiaII 1 females laid significantly more eggs on cotton (188 ± 3.8 eggs; F 3,8 = 408.6, P < 0.0001). This is twice as many as the numbers laid on cucumber (88 ± 3.0 eggs) and collard (80.67 ± 1.6 eggs) and more than 3 times the number laid on tomato (48 ± 3.0 eggs). There is significant interaction between host plant species and whitefly species (F 3,100 =1539.32, P < 0.0001). The highest fecundity for an individual female was on cotton, while the lowest was on tomato. However, when the fecundities of H2 MEAM1 and AsiaII 1 were compared, there was a significant difference in relation to cotton (F 1,4 = 655.01, P < 0.0001), tomato (F 1,4 = 46.25, P = 0.0024) and cucumber (F 1,4 = 129.92, P = 0.0003) (Fig. 1 D), but no difference for collard (F 1,4 = 0.05, P = 0.8424). Overall, fecundity of both species on all four host plant species can be arranged in the following order: cotton (AsiaII 1) > cucumber (AsiaII 1) > collard (AsiaII 1) = cotton (H2 MEAM1) = collard (H2 MEAM1) > tomato (H2 MEAM1) > cucumber (H2 MEAM1) = tomato (AsiaII 1).

wileyonlinelibrary.com/journal/ps

3.6 Sex ratios The sex ratios of H2 MEAM1 and AsiaII 1 on the four host plant species are detailed in Table 3. In all cases, female adults were always the dominant sex. The host plant did influence the degree of dominance. The sex ratio varied significantly among host plant species (F 3,110 = 51.70, P < 0.0001) and between whitefly species (F 1,110 = 96.27, P < 0.0001), and there was a significant interaction between host plant species and whitefly species (F 3,100 = 20.73, P < 0.0001). The sex ratio between the two whitefly species was significantly different on cotton (F 1,4 = 46.63, P = 0.0024), cucumber (F 1,4 = 248.80, P < 0.0001) and collard (F 1,4 = 21.69, P = 0.0096), but not on tomato (F 1,4 = 0.08, P = 0.7893) (Table 1). Overall, the sex ratio for both whitefly species across all four host plant species can be arranged in the following order: cotton (AsiaII 1) > tomato (AsiaII 1) = tomato (H2 MEAM1) > collard (AsiaII 1) = cucumber (AsiaII 1) = cotton (H2 MEAM1) > collard (H2 MEAM1) > cucumber (H2 MEAM1). 3.7 Life table of H2 MEAM1 and AsiaII 1 on three vegetable plants and cotton host Life table statistics for H2 MEAM1 and AsiaII 1 on the four host plant species are shown in Table 4. Female AsiaII 1 reared on

c 2013 Society of Chemical Industry 

Pest Manag Sci 2014; 70: 1531–1537

Host suitability for B. tabaci species in cotton-growing zones of Pakistan

Table 3. Sex ratios of H2 MEAM1 and AsiaII 1 on each host planta Sex ratio (♀/♂) Plants

H2 MEAM1

AsiaII 1

1.15 ± 0.005 bc 1.20 ± 0.004 b 1.01 ± 0.006 d 1.10 ± 0.011 c

Cotton Tomato Cucumber Collard

1.39 ± 0.035 a 1.20 ± 0.016 b 1.15 ± 0.005 bc 1.17 ± 0.01 bc

Host plants: F 1,110 = 96.27, P < 0.0001; species: F 3,110 = 51.70, P < 0.0001; interactions: F 3,100 = 20.73, P < 0.0001; LSD = 0.073.

a

cotton had a higher intrinsic rate of increase (0.149) and a higher net reproductive rate (45.18) than those reared on the other vegetable hosts. The generation times for AsiaII 1 ranged from 30.49 days on cucumber to 38.89 days on cotton; however, the finite rate of increases ranged from 1.11 on cucumber to 1.16 on cotton and collard. Female H2 MEAM1 had the highest rm (0.104) and R0 (34.44) on cotton and the lowest rm (0.087) and R0 (25.62) on cucumber. For H2 MEAM1, the mean generation time ranged from 28.48 on cucumber to 31.03 on cotton, while the finite rate of increase ranged from 1.09 on cucumber to 1.11 on cotton. 3.8 Comparison of Pakistan H2 MEAM1 with invasive H1 MEAM1 H2 MEAM1 took longer to develop on all vegetables compared with H1 MEAM1 (Table 5). H2 MEAM1 had a consistently slower rate of development compared with H1 MEAM1 (Table 5). H2 MEAM1 survival was lower on cucumber and collard compared with H1 MEAM1 (Table 3). Female adult H2 MEAM1 had lower longevities compared with H1 MEAM1 on all vegetable hosts across all studies (Table 5). H2 MEAM1 fecundity was substantially lower than that found in all previous studies (Table 5). The intrinsic rate of increase, the finite rate of increase and the mean generation time of H1 MEAM1 was higher than that observed for H2 MEAM1 on all three vegetable hosts (Table 5). The net reproductive rate of H1 MEAM1 was also higher than that observed for H2 MEAM1 (Table 5).

4

DISCUSSION

Ahmed et al.16,17 found that AsiaII 1 was the predominant member of the B. tabaci species complex in the Punjab cotton zone, and its abundance was associated with a high incidence of CLCuD. It was suggested that AsiaII 1 may be a more efficient vector of CLCuD compared with MEAM1, which was absent from Punjab but present in the Sindh cotton zone where CLCuD had a lower

www.soci.org

incidence. The present study revealed that AsiaII 1 performed better on cotton than on vegetables, while H2 MEAM1 performed similarly across the range of hosts tested. Previous studies have shown that the interaction of invading MEAM1 with indigenous species can lead to displacement and extinction of the indigenous species.32 – 34 In Pakistan, AsiaII 1 and MEAM1 occupy different but adjacent geographic regions, and, while it is not yet known why this separation is occurring, it is interesting to note that there are high levels of agricultural trade between them, suggesting that isolation is unlikely to be a factor,16,17 as one would imagine there is plenty of opportunity for human-assisted spread. What is known is that the H2 MEAM1 in Pakistan is genetically distinct from the haplotypes that have invaded globally. Further, a comparison with published studies provides evidence that strongly hints at Pakistan H2 MEAM1 being biologically inferior to that which has invaded elsewhere and so may lack the same ability to be invasive. The present study compares a range of biological traits, but the comparison of rm is perhaps the most critical. Although previously published studies vary in terms of experimental design and conditions, the present comparison with published data (Table 5) shows that H2 MEAM1 has the lowest of all published rates of increase and consistently underperforms for all other traits. Other explanations such as relative abundance17,35 or a synergistic relationship with CLCuD17,36 are also possible. Relative abundance, though, does not seem to be a factor, as invasive MEAM1 is able readily to displace less competitive members of the complex, even when at a lower abundance relative to the indigenous population.32,37 Thus, while the global experience of invasive populations of MEAM1 clearly shows its capacity to displace indigenous competitors, the authors suggest that the reason this does not appear to be occurring in Pakistan is that the MEAM1 found in Pakistan is not invasive in the way MEAM1 that has spread beyond its home range is. It is interesting that genetically different haplotypes under the same species actually have different biological characteristics. De Barro and Ahmed1 have already shown that not all haplotypes under the same species have the same potential to invade. Assuming that H2 MEAM1 and H1 MEAM1 are all the same species, it would be interesting to undertake a comparative genomic analysis to determine whether invasive genotypes possess traits that facilitate invasiveness that are lacking in the population in Pakistan. This would help further to clarify the reasons why some B. tabaci are invasive and others are not.

ACKNOWLEDGEMENTS The authors thank the anonymous reviewers for their constructive comments on the manuscript and Anne Bourne for help with the

Table 4. Life table parameters of H2 MEAM1 and AsiaII 1 on various vegetables and cotton hosta R0 Plants Cotton Tomato Cucumber Collard

34.44 29.98 25.62 33.59

AsiaII 1 45.18 42.82 33.86 39.75

H2 MEAM1 0.1043 0.0984 0.0872 0.1034

T AsiaII 1 0.1499 0.1311 0.1048 0.1125

H2 MEAM1 31.03 27.17 23.48 30.29

λ AsiaII 1 38.89 37.56 30.49 35.52

H2 MEAM1 1.11 1.10 1.09 1.11

AsiaII 1 1.16 1.14 1.11 1.12

R0 – net reproductive rate; rm –intrinsic rate of increase; T – mean generation time; λ – finite rate of increase.

Pest Manag Sci 2014; 70: 1531–1537

c 2013 Society of Chemical Industry 

wileyonlinelibrary.com/journal/ps

1535

a

H2 MEAM1

rm

www.soci.org

MZ Ahmed et al.

Table 5. Comparison of the biology of H1 MEAM1 from all studies published since 1995 with H2 MEAM1 on various host plants

Host

Temperature (◦ C)

Development period (days)

Survival (%)

Adult longevity (days) 20.3 19.1 20.3 22.7

Fecundity (eggs ♀−1 )

T

R0

rm

λ

References Zang et al. (2006)25 Guo et al. (2013)20 Guo et al. (2013) 20 Guo et al. (2013) 20 Jiao et al. (2012)22 H2 MEAM1 in present study

Cotton Cotton Cotton Cotton Cotton Cotton

28 27 27 27 25 25

23.5 19.4 19.5 21.1 19.0 24.4

86.2 56.7 65.9 78.3 65 40

14.8

79.3

31.0 34.44 0.10 1.11

Tomato Tomato Tomato Tomato Tomato Tomato

25 25 25 26 25 25

18.0

60.2

20.6

222.0

27.2 64.30 0.15 1.17 0.12 1.13

17.8 17.8 19.4 21.3

70.0 63.1 54.6 53.3

21.4 25.2 15.8

120.0 71.7

27.7 51.33 0.12 1.15 27.2 29.98 0.09 1.10

Tsai and Wang (1996)28 Van Giessen et al. (1995)29 Zhang and Wan (2012)21 Zhang and Wan (2012) 21 Qiu et al. (2011)18 H2 MEAM1 in present study

Cucumber Cucumber Cucumber

25 25 25

19.3 19.6 23.3

46.4 46.3 40.0

9.9 21.1 16.7

76.0 98.2 48.3

23.2 19.80 0.13 1.14 27.9 24.32 0.11 1.13 23.5 25.62 0.08 1.09

Tsai and Wang (1996)28 Qiu et al. (2011)18 H2 MEAM1 in present study

Collard Collard Collard

25 25 25

18.6 19.7

68.5 46.7

21.1 15.8

143.0 81.7

0.14 1.15 31.7 34.53 0.13 1.14 30.3 33.59 0.10 1.11

Van Giessen et al. (1995)29 Qiu et al. (2011)18 H2 MEAM1 in present study

Meana

26

19.4

63.4

20.2

128.8

27.5 34.74 0.13 1.14

Meanb

26

20.6

63.7

14.5

141.1

26.0 45.6 0.15 1.24

Meanc

25

22.2

45.0

15.8

70.3

28.0 30.91 0.09 1.10

Guo et al. (2013);20 Jiao et al. (2012);22 Zhang and Wan (2012);21 Qiu et al. (2011);18 Zang et al. (2006);25 Tsai and Wang (1996);28 Van Giessen et al. (1995)29 Guo et al. (2013);20 Zhang and Wan (2012);21 Jiao et al. (2012);22 Qiu et al. (2011);18 Feng et al. (2009);23 Mansaray and Sundufu (2009);24 Zang et al. (2006);25 Musa and Ren (2005);26 Liu and Stansly (1998);27 Tsai and Wang (1996);28 Van Giessen et al. (1995)29 H2 MEAM1 in present study

99.2 117.4 154.4

25.14 28.18 30.28

a

Average of published studies above with the same host without H2 MEAM1. Average of all published studies across all hosts without H2 MEAM1. c Average for H2 MEAM1. b

statistical analysis. This research forms part of the postdoctoral fellowship of MZA at South China Agricultural University. The authors would like to acknowledge the Central Cotton Research Institute, Sakrand, Sindh, and the Central Cotton Research Institute, Multan, Punjab, Pakistan. This research was supported by funding from the National Basic Research Program of China (2013CB127604), New Century Excellent Talents in University (NCET-11-0917) and the National Department Public Benefit Research Foundation (201303019).

REFERENCES

1536

1 De Barro P and Ahmed MZ, Genetic networking of the Bemisia tabaci cryptic species complex reveals pattern of biological invasions. PLoS ONE 6(10):e25579 (2011). 2 Oliveira MRV, Henneberry TJ and Anderson NP, History, current status, and collaborative research projects for Bemisia tabaci. Crop Prot 20:709–723 (2001).

wileyonlinelibrary.com/journal/ps

3 Rosell RC, Bedford ID, Frohlich DR, Gill RJ, Brown JK and Markham PG, Analysis of morphological variation in distinct populations of Bemisia tabaci (Homoptera: Aleyrodidae). Ann Entomol Soc Am 90:575–589 (1997). 4 Boykin LM, Shatters RG, Rosell RC, McKenzie CL, Bagnall RA, De Barro P, et al. Global relationships of Bemisia tabaci (Hemiptera: Aleyrodidae) revealed using Bayesian analysis of mitochondrial COI DNA sequences. Mol Phyl Evol 44:1306–1319 (2007). 5 Dinsdale A, Cook L, Riginos C, Buckley YM and Barro PD, Refined global analysis of Bemisiatabaci (Hemiptera: Sternorrhyncha: Aleyrodoidea: Aleyrodidae) mitochondrial cytochrome oxidase 1 to identify species level genetic boundaries. Ann Entomol Soc Am 103:196–208 (2010). 6 Boykin LM, Armstrong KF, Kubatko L and De Barro P, Species delimitation and global biosecurity. Evol Bioinform 8:1–37 (2012). 7 Xu J, De Barro PJ and Liu SS, Reproductive incompatibility among genetic groups of Bemisia tabaci supports the proposition that the whitefly is a cryptic species complex. Bull Entomol Res 100:359–366 (2010). 8 Liu SS, Colvin J and De Barro PJ, Species concepts as applied to the whitefly Bemisia tabaci systematics: how many species are there? J Integ Agric 11:176–186 (2013).

c 2013 Society of Chemical Industry 

Pest Manag Sci 2014; 70: 1531–1537

Host suitability for B. tabaci species in cotton-growing zones of Pakistan 9 De Barro PJ, Liu SS, Boykin LM and Dinsdale AB, Bemisia tabaci: a statement of species status. Annu Rev Entomol 56:1–19 (2011). 10 Cheek S and MacDonald O, Management of Bemisia tabaci. Pestic Sci 42:135–137 (1994). 11 Dalton R, The Christmas invasion. Nature 443:898–900 (2006). 12 Attique MR, Rafiq M, Ghaffar A, Ahmad Z and Mohyuddin AI, Hosts of Bemisia tabaci (Genn.) (Homoptera: Aleyrodidae) in cotton areas of Punjab, Pakistan. Crop Prot 22:715–720 (2003). 13 National Cotton Council of America – Rankings. [Online]. USDA Foreign Agriculture Service (2013). Available: http://www.cotton. org/econ/cropinfo/cropdata/rankings.cfm [16 January 2014]. 14 Ali G, Cotton innovation: developing cotton quality innovation analysis tool. CABI Ref. FR/CABI-PK/CR60014/2010, CABI, South Asia (2010). 15 Geering ADW, Cotton Leaf Curl (Cotton Leaf Curl Multan Virus and Others). [Online]. Pest and Diseases Image Library (2010). Available: http://www.padil.gov.au/pests-and-diseases/Pest/Main/136662 [16 January 2014]. 16 Ahmed MZ, Ren SX, Mandour NS, Maruthi MN, Naveed M and Qiu BL, Phylogenetic analysis of Bemisia tabaci (Hemiptera: Aleyrodidae) populations from cotton plants in Pakistan, China, and Egypt. J Pest Sci 83:135–141 (2009). 17 Ahmed MZ, De Barro PJ, Greeff JM, Ren S-X, Naveed M and Qiu BL, Genetic identity of the Bemisia tabaci species complex and association with high cotton leaf curl disease (CLCuD) incidence in Pakistan. Pest Manag Sci 67:307–317(2011). 18 Qiu BL, Dang F, Li SJ, Ahmed MZ, Jin FL, Ren SX, et al. Comparison of biological parameters between the invasive B biotype and a new defined Cv biotype of Bemisia tabaci (Hemiptera: Aleyradidae) in China. J Pest Sci 84:419–427 (2011). 19 Gill RJ, The morphology of whiteflies, in Whiteflies: their Bionomics, Pest Status and Management, ed. by Gerling D. Intercept, Andover, Hants, UK, pp. 13–46 (1990). 20 Guo JY, Wu G and Wan FH, Effects of high-gossypol cotton on the development and reproduction of Bemisia tabaci (Hemiptera: Aleyrodidae) MEAM1 cryptic species. J Ecol Entomol 106:1379–1385 (2013). 21 Zhang GF and Wan FH, Suitability changes with host leaf age for Bemisia tabaci B biotype and Trialeurodes vaporariorum. Environ Entomol 10:1125–1130 (2012). 22 Jiao X, Xie W, Wang S, Wu Q, Zhou L, Pan H, et al. Host preference and nymph performance of B and Q putative species of Bemisia tabaci on three host plants. J Pest Sci 85:423–430 (2012). 23 Feng YT, Wu QJ, Xu BY, Chang XL, Xie W and Zhang YJ, Fitness costs and morphological change of laboratory-selected thiamethoxam resistance in the B-type Bemisia tabaci (Hemiptera: Aleyrodidae). J Appl Entomol 133:466–472 (2009).

www.soci.org

24 Mansaray A and Sundufu AJ, Oviposition, development and survivorship of the sweetpotato whitefly Bemisia tabaci on soybean, Glycine max, and the garden bean, Phaseolus vulgaris. J Insect Sci 9:1 (2009). 25 Zang LS, Chen WQ and Liu SS, Comparison of performance on different host plants between the B biotype and a non-B biotype of Bemisia tabaci from Zhejiang, China. Entomol Exp Appl 121:221–227 (2006). 26 Musa P and Ren SX, Development and reproduction of Bemisia tabaci (Homoptera: Aleyrodidae) on three bean species. Insect Sci 12:25–30 (2005). 27 Liu TX and Philip A, Life history of Bemisia argentifolii (Homoptera: Aleyrodidae) on Hibiscus rosa-sinensis (Malvaceae). Fl Entomol 81:437–445 (1998). 28 Tasi JH and Wang K, Development and reproduction of Bemisia argentifolii (Homoptera: Aleyrodidae) on five host plants. Environ Entomol 25:810–816 (1996). 29 Van Giessen WA, Mollema C and Elsey KD, Design and use a simulation model to evaluate germplasm for antibiotic resistance to the greenhouse whitefly (Trialeurodes vaporariorum) and the sweet potato whitefly (Bemisia tabaci). Entomol Exp Appl 76:271–286 (1995). 30 Birch LC, The intrinsic rate of natural increase in an insect population. J Anim Ecol 17:15–26 (1948). 31 Lin CS, The theory and experiment study of animal population change – the innate capacity for increase of Tribolium confusum (H.). Acta Zool Sin 16:323–328 (1964). 32 De Barro PJ and Hart PJ, Mating interactions between two biotypes of the whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae), in Australia. Bull Entomol Res 90:103–112 (2000). 33 Liu SS, DeBarro PJ, Xu J, Luan JB, Zang LS, Ruan YM, et al. Asymmetric mating interactions drive widespread invasion and displacement in a whitefly. Science 318:1769–1772 (2007). 34 Crowder DW, Horowitz AR, De Barro PJ, Liu SS, Showalter AM, Kontsedalov S, et al. Mating behavior, life history and adaptation to insecticides determine species exclusion between whiteflies. J Anim Ecol 79:563–570 (2010). 35 De Barro PJ, Bourne A, Khan SA and Brancatini VAL, Host plant and biotype density interactions – their role in the establishment of the invasive B biotype of Bemisia tabaci. Biol Inv 8:287–294 (2006). 36 Costa HS, Brown JK and Byrne DN, Life history traits of the whitefly, Bemisia tabaci (Homoptera: Aleyrodidae), on six virus-infected or healthy plant species. Environ Entomol 20:1102–1107 (1991). 37 De Barro P, Liu SS and Bourne A, Age-based differential host acceptability and human mediated disturbance prevent establishment of an invasive species and displacement of a native competitor. Biol Invasions 12:3429–3438 (2010).

1537

Pest Manag Sci 2014; 70: 1531–1537

c 2013 Society of Chemical Industry 

wileyonlinelibrary.com/journal/ps

Host suitability comparison between the MEAM1 and AsiaII 1 cryptic species of Bemisia tabaci in cotton-growing zones of Pakistan.

Bemisia tabaci is a cryptic species complex. In Pakistan, members of the complex, MEAM1 and AsiaII 1, are the predominant species infesting cotton. Th...
530KB Sizes 0 Downloads 0 Views