The Potential Distribution of an Invasive Mealybug Phenacoccus Solenopsis and Its Threat to Cotton in Asia

Agricultural and Forest Entomology (2010), 12, 403–416 DOI: 10.1111/j.1461-9563.2010.00490.x The potential distribution of an invasive mealybug Phenacoccus solenopsis and its threat to cotton in Asia

Yanping Wang∗, Gillian W. Watson† and Runzhi Zhang‡ CAS Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, No 1 Beichen West Rd., Chaoyang, Beijing 100101, China, ∗Graduate University of Chinese Academy of Sciences, Beijing 100049, China, †California Department of Food and Agriculture, Plant Pest Diagnostic Center, 3294 Meadowview Road, Sacramento, CA 95832, U.S.A. and ‡State Key Laboratory of Integrated Management of Pest Insects and Rodents in Agriculture, Beijing 100101, China

Abstract 1 In recent years, an invasive mealybug Phenacoccus solenopsis Tinsley (Hemiptera: Pseudococcidae) has attacked cotton (Gossypium hirsutum L.) in Pakistan and India, causing severe economic losses. This polyphagous pest was probably introduced accidentally from North America. Infestations have broken out suddenly and spread rapidly. 2 Seasonal and annual population growth data of P. solenopsis from nine locations in its native range in the U.S.A., and the distribution of the mealybug worldwide, were analyzed using the CLIMEX model. This indicated that tropical regions worldwide were highly suitable for P. solenopsis. 3 Its potential distribution was limited by cold in high latitudes and altitudes, and dryness in northern Africa, inland Australia and parts of the Middle East. CLIMEX wasusedtopredictwhereP. solenopsis might establish, and to estimate the potential threat to cotton yield in Asia. The key limiting factors were low precipitation as well as minimum temperatures in northern areas. 4 When irrigation was factored into the simulation, the potential distribution of P. solenopsis expanded dramatically, indicating that P. solenopsis presents a great economic threat to cotton in Asia and other parts of the world. Keywords Asia, CLIMEX, cotton, economic losses, Hemiptera Pseudococcidae, Phenacoccus solenopsis, potential distribution.

Introduction The first record of P. solenopsis damaging a crop was made by Fuchs et al. (1991), who reported it on cultivated The problem cotton in Texas, U.S.A. Other crops have been damaged in The solenopsis mealybug, Phenacoccus solenopsis (Hemiptera: Chile, on Solanum muricatum (Ait.), Solanaceae (Larraín, Sternorrhyncha: Coccoidea: Pseudococcidae) was described 2002), and Brazil, on Solanum lycopersicum L., Solanaceae by Tinsley (1898) from weed roots in a nest of the ant (Culik & Gullan, 2005). Granara de Willink (2003) recorded Solenopsis geminata Fabricius in New Mexico, U.S.A. This it from Argentina on false ragweed, Ambrosia tenuifolia highly polyphagous mealybug attacks numerous crops, weeds, Spreng. (Asteraceae). Initially, P. solenopsis was recorded only from the U.S.A., ornamentals and medicinal plants (Hodgson et al., 2008; Arif suggesting that it is native there. The first records made outside et al., 2009). Cotton (Gossypium hirsutum L., Malvaceae) is the continental U.S.A. were from Hawaii in 1966 (Kumashiro one of its most favoured hosts, and P. solenopsis attacks both et al., 2001), then from Mexico in 1978, South America from Bt and non-Bt cultivars (Dutt, 2007). It infests the leaves, fruit, 1985 onwards, and the Caribbean Islands and Central America branches, main stems, trunks and roots, feeding on phloem sap from 1986 onwards (Williams & Granara de Willink, 1992; and egesting copious, sugary honeydew. Watson & Chandler, 2000; Hodgson et al., 2008). Phenacoccus solenopsis was first found in Asia (Pakistan) in Correspondence: Runzhi Zhang. Tel: +86 10 64807270; fax: +86 2005 (Abbas et al., 2005; Zaka et al., 2006); it was recorded 10 64807099; e-mail: [email protected] from India soon afterwards (Yousuf et al., 2007). Hodgson

© 2010 The Authors Agricultural and Forest Entomology © 2010 The Royal Entomological Society 404 Y. Wang et al. et al. (2008) recorded it from Thailand and Taiwan in 2006. and four stress indices (cold, wet, hot and dry) to reflect Most of the published data on the economic impact of limited growth in the unfavourable period. The growth index P. solenopsis in Asia are from Pakistan and India because these is a combination of the temperature (TI) and moisture (MI) countries have been infested for the longest time; from 2005 indices; interactive stress indices (e.g. cold–dry) can be fitted onward, there have been many damaging outbreaks, severely if necessary. All of the indices are calculated weekly, then affecting their cotton industries. In the cotton-producing belt combined into an annual value; the subscripts ‘W’ and ‘A’ of Pakistan (totalling 3 237 485 ha in Punjab and Sindh), are used to indicate the weekly and annual values respectively. over 60 700 ha have been seriously damaged by P. solenopsis. There is a constraint on the minimum number of degree- Reportedly 12% of the crop was lost in 2006 and, in 2007, days of thermal accumulation above the development threshold almost 40% of the cotton in Punjab was damaged (Kakakhel, temperature to complete a generation (PDD; for an explanation, 2007). In 2007, up to US$121.4 million was spent on pesticides see Materials and methods). The weekly growth (GIW)and in the Punjab in only 2 months aiming to control the mealybug stress indices are integrated together as an annual index of (Dutt, 2007). The cost of insecticides and Bt cotton seed climatic suitability, the ecoclimatic index (EI), which is in the made cotton production by poor farmers almost unprofitable range 0–100. Locations with an EI value of 0 are unsuitable (Abdullah et al., 2007). In India, P. solenopsis was reported for propagation and persistence of the species; 0 < EI < 10 from all nine cotton-growing states in 2006. Severe economic indicates marginal conditions; 10 < EI < 20 represents suitable damage (estimated at US$400 000–500 000) was reported in conditions and EI > 20 indicates highly suitable habitat for Punjab and Hayana in 2007, and a more severe attack was colonization and reproduction (Sutherst & Maywald, 1985; anticipated in 2008–2009 (ICAC, 2008; Nagrare et al., 2009). Sutherst et al., 2004, 2007). Cotton production and consumption are becoming concen- When using CLIMEX, it is essential to ensure a close match trated in Asia; in 2008–2009, 75% of the world crop was with the species’ native and introduced ranges (Sutherst et al., produced in Asia, and this is expected to account for 84% of 2007). In the present study, the ‘Compare Location’ option world cotton mill use (ICAC, 2008). The economic impact of in CLIMEX and DYMEX, version 3.0 (Sutherst et al., 2007) P. solenopsis has become a major problem for Asian countries, was used in conjunction the native and introduced distributions and such severe damage suggests that it presents a significant of P. solenopsis to infer its climatic responses. The model threat to cotton production worldwide. The mealybug shows was used: (i) to predict the potential distribution and relative considerable plasticity in its morphology and ability to live abundance of P. solenopsis worldwide; (ii) to analyze the risk under a wide variety of environmental conditions (Hodgson of colonization of Asian cotton fields by P. solenopsis;and(iii) et al., 2008); effectively, it is pre-adapted to be an agricul- to estimate the resultant likely economic impact. tural pest. Phenacoccus solenopsis has become an aggressively A species’ climatic requirements can be inferred from invasive species on agricultural and ornamental plants, and has its geographical distribution and seasonal phenology, or spread rapidly between countries. Movement of the pest on from information derived from laboratory cultures, such fresh produce is likely to facilitate its dispersal in Asia and as the minimum, maximum and optimum temperatures for beyond, threatening the world cotton industry and other crops. development (Vanhanen et al., 2008). Although biological data from the laboratory can be used to parameterize the CLIMEX model, it is considered preferable to use geographical distribution because laboratory data do not reflect the more Application of the CLIMEX model to the mealybug problem complex outdoor environment (Vera et al., 2002; Kriticos et al., The earlier that a new invasive pest is recognized, the better 2003a, b; Sutherst, 2003; Ulrichs & Hopper, 2008). The strategic plans for control and administration can be made native range of an organism normally comprises the most (Maelzer & Zalucki, 2000). Eco-climatic models are often useful and reliable data for CLIMEX analyses (Kriticos et al., used early in a pest invasion, when little information on the 2003a, 2007). Usually, the iterative fitting process matched invader is available (Sutherst & Maywald, 2005). CLIMEX with the current geographical distribution can provide one is one of the most important ecoclimatic models used to or more simulations of the potential distribution (Sutherst, predict the potential distribution of an invader, mostly based 2003). However, the known distribution often does not provide on the climates of its native and introduced ranges (Sutherst & sufficient data for parameter-fitting (Stephens et al., 2007), in Maywald, 1985; Sutherst et al., 2007). It has been extensively which case laboratory data may be used as the initial parameter developed to forecast the potential ranges of pests, weeds and values (Migeon et al., 2009). If detailed biological data are biological control agents (Hughes & Maywald, 1990; Sutherst unavailable, fitting model parameters should ‘listen to the & Maywald, 2005; Pattison & Mack, 2008). known geographical distribution’, especially its boundaries. The ‘Compare Locations’ function of CLIMEX is primarily In CLIMEX, soil moisture values for a phytophagous insect used for forecasting the potential distribution of a species are usually adjusted to reflect the requirements of the host as determined by climate; nonclimatic factors are excluded plants. The lower soil moisture limit for development is usually (Sutherst & Maywald, 1985). It assumes that, in 1 year, an set to 0.1 (the permanent wilting point), which is normally organism at any location usually experiences two sets of at approximately 10% of soil moisture (Scott & Yeoh, 1999; conditions: one favourable for population growth, and the Kriticos et al., 2007; Stephens et al., 2007). In drought-stressed other unfavourable, in which population growth is limited. circumstances, the survival and growth of phytophagous insects CLIMEX uses an annual growth index (GIA) to describe the are often improved, and insect outbreaks may become more potential for population growth during the favourable period, frequent and more severe (Mattson & Haack, 1987; Fleming

& Volney, 1995). However, for sap-sucking insects such as geographical distribution with the known distribution of mealybugs, soil moisture is usually not a key limiting factor P. solenopsis. ◦ for reproduction and population growth. The choice of 11.5 C for the lower temperature limit for The stress indices in CLIMEX are set to determine the growth (DV0) was determined from the northern distribution geographical distribution (Sutherst et al., 2007). In practice, the of P. solenopsis in Nevada and Idaho (U.S.A.), although no boundaries of the distribution are used to conﬁrm the threshold winter collection records are known from these states (prob- values for survival and the weekly stress accumulation rates, ably as a result of the lack of collecting). January collection using an iterative ﬁtting process (Sutherst & Maywald, 2005). records from El Centro in southern California showed that the adult mealybug could successfully overwinter there. The lower and upper optimum temperatures (DV1 and DV2) were ◦ Materials and methods set at 20 and 30 C respectively, which was within the range The present distribution of P. solenopsis reported for other mealybug species. Hodgson et al. (2008) considered that P. solenopsis and Phenacoccus solani Ferris The distribution of P. solenopsis (Figs 1 and 2) was based on might be environmentally induced variants of a single species. previous studies (Ben-Dov, 2009; Hodgson et al., 2008); spec- The optimal temperature for population growth of P. solani, ◦ imens in the U.S. National Museum of Natural History and however, was 20–25 C (Nakahira & Arakawa, 2006), and California State Collection of Arthropods; literature cited in the P. solani is found in higher latitudes including Italy (Mazzeo Results section below; searches of the Internet; and on obser- et al., 1999) and Canada (British Columbia) (Ben-Dov, 2005). vations of internationally recognized mealybug experts [Drs By contrast, P. solenopsis is mostly present in tropical and sub- D. R. Miller (USDA-ARS, retired), M. Kosztarab (Virginia tropical areas (Fig. 2), so the optimum temperature for growth Tech, Blacksburg, Virginia, retired), and P. J. Gullan, Univer- of P. solenopsis was higher than that of P. solani. The upper sity of California, Davis, U.S.A.) personal communication; and temperature limit for growth (DV3) for P. solenopsis was set G.W.W.]. Records from glasshouses were not included.

Table 1 CLIMEX parameter values for Phenacoccus solenopsis CLIMEX parameter value selection Growth indices Parameters Values CLIMEX, version 3.0, includes weather data (monthly long- Moisturea Lower limit of soil moisture necessary 0.05 term average maximum and minimum temperatures, rainfall for growth (SM0) and relative humidity) from a database of 2218 meteorological Lower limit of optimal soil moisture for 0.30 stations located worldwide for 1931–1960. To overcome the ◦ growth (SM1) spatial limitation of the limited meteorological database, a 0.5 Upper limit of optimal soil moisture for 1.50 grid of long-term average climate surface variables for the growth (SM2) world terrain was used (after New et al., 1999). Upper limit of soil moisture necessary 2.00 Iterative parameter-ﬁtting was used to develop the CLIMEX for growth (SM3) ◦ model for P. solenopsis. The native range, relative abundance Temperature ( C) Lower temperature threshold for 11.50 and seasonal phenology in the U.S.A. were used to infer its growth (DV0) climatic requirements. The adjusted parameter values were then Lower limit of optimal temperature for 20.00 growth (DV1) visually validated against the reported invasive distribution Upper limit of optimal temperature for 30.00 of P. solenopsis around the world. During this process, the growth (DV2) parameter values compared favourably with the observed native Upper temperature threshold for 35.00 distribution. These values are summarized in Table 1. Several growth (DV3) other parameters possible in CLIMEX were not utilized in the Degree-day threshold above DV0 370.00 ◦ present study. (11.50 C) to complete one generation (PDD) Stress indices Cold stress temperature threshold 1.50 ◦ Growth indices. The growth indices (on a scale from 0–100) (TTCS) ( C) indicate how favourable each location is for population growth; Weekly rate of cold stress −0.0004 they were calculated weekly and annually after Sutherst and accumulation (THCS) Maywald (1985). Heat stress temperature threshold 38.00 ◦ (TTHS) ( C) Weekly rate of heat stress 0.00007 Temperature. In the absence of any published biological data accumulation (THHS) for P. solenopsis, the temperature parameter values were Dry stress threshold (SMDS) 0.05 initially inferred from data available for other mealybug Weekly rate of dry stress accumulation −0.01 species, particularly other members of the genus Phenacoccus (HDS) Wet stress threshold (SMWS) 2 00 [on Phenacoccus herreni Cox & Williams (Herrera et al., . Weekly rate of accumulation of wet 0.05 1989); on Phenacoccus manihoti Matile-Ferrero (Lema & stress (HWS) Herren, 1985); on Phenacoccus madeirensis Green (Chong et al., 2003); and on Maconellicoccus hirsutus (Green) (Chong aMoisture parameters were in units measuring the proportion of soil et al., 2008)] before being reﬁned by matching the simulated moisture-holding capacity.

Figure 1 The native distribution of Phenacoccus solenopsis in the U.S.A. , Areas where P. solenopsis is widely distributed (Kosztarab, 1996; Miller et al., 2005, Hodgson et al., 2008; California State Collection of Arthropods; U.S. National Museum of Natural History; and Dr D. R. Miller, personal communication); , areas where P. solenopsis is probably present (Dr D. R. Miller, personal communication); , areas where the P. solenopsis distribution is limited by cold winters (Kosztarab, 1996; Hodgson et al., 2008).

Figure 2 The world distribution of Phenacoccus solenopsis outdoors. , Recorded locality points; , widely distributed areas. The rectangle contains numerous small countries where the mealybug is present.

◦ at 35 C, to fit the warmer parts of its native and introduced the genus Phenacoccus (Lema & Herren, 1985; Herrera et al., ranges. 1989; Chong et al., 2003, 2008), and were tuned by iterative matching with the driest and wettest distribution records of P. solenopsis in the U.S.A. Threshold heat sum (PDD). The minimum thermal accumula- Soil moisture parameters in CLIMEX are calculated pro- tion necessary to complete a generation (the sum of degree- portionally from the plant-available water capacity within the days above DV0) was set at 370 degree-days for P. solenopsis, effective rooting zone. The lower soil moisture limit for devel- adjusted by matching with the northern limit and high alti- opment (SM0) was set at 0.05, indicating the low moisture tude distribution records (e.g. La Tinaja, Veracruz Province and requirements of host plants living in the semi-desert region Mexico), respectively. of the western U.S.A. The lower and upper limits for optimal growth (SM1 and SM2) were liberally set to 0.3 and 1.5, Moisture. In the present study, the moisture parameter was respectively, to reflect the rapid population growth and repro- not simply accorded to the routine requirement of the host duction of P. solenopsis in slightly low and high precipitation plants. It was preferable to determine whether the mealybug regions of the southern and eastern U.S.A. The upper limit for favoured dry or wet conditions, based on the relative abundance development (SM3) was set at 2.0, based on reports that the and seasonal phenology of P. solenopsis in field conditions. population growth of the closely-related mealybug P. manihoti Next, the moisture values were compared with the available was limited during the rainy season but become explosive dur- literature on other mealybugs, particularly other members of ing the dry season (Lema & Herren, 1985).

The irrigation function in CLIMEX was used to provide Wet stress. The wet stress threshold was set to equal SM3, and the most realistic projections of the potential distribution the weekly rate of wet stress accumulation was 0.05, adjusted of P. solenopsis in agricultural areas. Where weekly rainfall to ensure the inclusion of high-precipitation sites in Florida and was <25 mm during the growing season (1 March to 30 parts of Mexico and South-East Asia. September), it was topped up to 25 mm to allow for irrigation. When rainfall exceeded 25 mm, irrigation was withdrawn. CLIMEX model matching Stress indices. The stress indices are used to reflect the limited Nine representative locations were selected to reflect the population growth during unfavourable seasonal conditions. range of natural climatic conditions that suit the survival of The annual stress values, on a scale from 0 (no stress) to P. solenopsis in its native range: Guttenberg (north-east New 100 (lethal conditions), were calculated by the weekly value Jersey) with an extremely cold winter; Vicksburg (western multiplied by the number of weeks subsequent to the stress Mississippi) and Miami (southeast Florida) represented areas first exceeding zero (Sutherst et al., 2007). with substantial precipitation in the southern U.S.A.; Hidalgo (southern Texas), Las Cruces (southern New Mexico), Yuma (western Arizona) and Keene (in the middle of California) Cold stress. Phenacoccus solenopsis can survive in temper- ◦ represented western areas with extremely dry, hot summers; atures as low as 0 C in the field (NCIPM, 2008). For the ◦ and Esmeralda (Nevada) and Elmore (Idaho) represented the long-term average effect, the cold stress factor was set at 1.5 C northern limit of the distribution of P. solenopsis. The values with a stress accumulation rate of −0.0004. This rate fitted the of CLIMEX indices for the selected locations in the U.S.A. are northern limit sites of Esmeralda (Nevada) and Elmore (Idaho) given in Table 2. in the U.S.A. Four important cotton-cultivating locations outside the U.S.A. were chosen to analyze the climatic suitability of Asian cotton fields for P. solenopsis: Multan (Punjab) in Heat stress. Phenacoccus solenopsis can thrive in temperatures ◦ Pakistan; Bathinda (Punjab) and Hisar (Haryana) in India; above 40 C in the field (NCIPM, 2008). The heat stress ◦ and Akesu (Xinjiang) in north-western China. The values of temperature threshold was set at 38 C to account for the CLIMEX indices for the selected locations in Asia are given averaging effect of climate. The weekly rate of heat stress in Table 2. accumulation value was 0.00007, which was adjusted low enough to account for the persistence of P. solenopsis in warmer places such as New Mexico and Arizona (U.S.A.). Results and Discussion The present distribution of P. solenopsis Dry stress. The dry stress threshold was set at the same level as SM0. The weekly rate of dry stress accumulation was set In the U.S.A., P. solenopsis is fairly widespread (McKenzie, at −0.01, tuned down to barely allow for the persistence of 1967; Kosztarab, 1996; Hodgson et al., 2008) and it is common P. solenopsis in the low-rainfall regions of the western U.S.A. in the south-eastern states (Miller, 2005). It has been recorded

Table 2 CLIMEX index values for selected locations of the United States and Asia, to analyze the climatic suitability for Phenacoccus solenopsis

Location Longitude, latitude Degree-days TIA MIA GIA CS HS DS EI

U.S.A. Elmore −115.7, 43.1 1125 32 58 (97) 4 (31) 63 0 1 (0) 2 (12) Esmeralda −117.2, 37.7 1697 27 9 (62) 0 (22) 65 0 5 (0) 0 (8) Keene −118.6, 35.2 1109 36 59 (98) 7 (35) 5 0 1 (0) 7 (33) Yuma −114.6, 32.7 3993 38 0 (52) 0 (16) 0 1 28 (1) 0 (16) Las Cruces −106.8, 32.3 1930 43 20 (70) 9 (39) 39 0 2 (0) 6 (24) Hidalgo −98.3, 26.1 4285 54 52 (86) 30 (45) 0 0 0 30 (45) Miami −80.3, 25.8 4535 95 100 (100) 95 (95) 0 0 0 95 (95) Vicksburg −90.9, 32.3 2883 57 100 (100) 57 (57) 0 0 0 57 (57) Guttenberg −74.0, 40.8 1498 42 100 (100) 42 (42) 26 0 0 31 (31) China Akesu 80.4, 40.7 1850 42 0 (61) 0 (39) 68 0 12 (2) 0 (12) Pakistan Multan 71.5, 30.2 5175 29 2 (53) 0 (8) 0 3 19 (4) 0 (8) India Bathinda 74.8, 30.3 4990 32 25 (57) 1 (9) 0 1 2 (2) 1 (9) Hisar 75.8, 29.3 4938 35 27 (57) 2 (11) 0 0 2 (2) 2 (11)

Numbers in parentheses represent the parameter values under irrigated conditions. CLIMEX indices: TIA, annual temperature index; MIA, annual moisture index; GIA, annual growth index; CS, cold stress; HS, heat stress; DS, dry stress; EI, ecoclimatic index.

© 2010 The Authors Agricultural and Forest Entomology © 2010 The Royal Entomological Society, Agricultural and Forest Entomology, 12, 403–416 408 Y. Wang et al. from 14 states: Arizona, California, District of Colombia, The documented global distribution of P. solenopsis is Florida, Illinois, Maryland, Michigan, Mississippi, New Jersey, shown in Fig. 2. The first records from outside the U.S.A. were New Mexico, New York, Ohio, Texas and Virginia (Halbert, from the Hawaiian Islands in 1966 (Kumashiro et al., 2001), 1998, 2008; Miller, 2005; Ben-Dov, 2009) (Fig. 1). The lack Mexico (1978), South America (Ecuador) from 1985 onwards, of records from some states reflects a lack of collection and and the Caribbean Islands (Cuba and the Dominican Republic) preservation of museum specimens (D. R. Miller, personal and Central America (Panama) from 1985 onwards (Williams communication). & Granara de Willink, 1992). Watson and Chandler (2000) Phenacoccus solenopsis has been extending its distribution recorded it from Barbados and Jamaica, and Hodgson et al. outside the U.S.A.; by July 2009, it had been recorded from 24 (2008) recorded it from the Cayman Islands. The mealybug was countries on five continents, as detailed below. The publication first recorded in the Galapagos Islands in 2001 (Causton et al., of ten new country records subsequent to 2008 indicates that 2006), and was reported from Chile (Larraín, 2002), Argentina its distribution has expanded rapidly. (Granara de Willink, 2003), Brazil (in Espírito Santo state;

(a)

(b)

Figure 3 CLIMEX model showing the potential geographical distribution of Phenacoccus solenopsis in the U.S.A., as shown by the ecoclimatic index (a) with natural rainfall and (b) with irrigation during the growing season. The darker the shading, the more favourable the conditions are for the survival of P. solenopsis. Localities are marked as follows: G. Guttenberg (New Jersey); V, Vicksburg (Mississippi); M, Miami (Florida); H, Hidalgo (Texas); C, Las Cruces (New Mexico); Y, Yuma (Arizona); K, Keene (California); E, Esmeralda (Nevada); and L, Elmore (Idaho).

Culik & Gullan, 2005), Guatemala (Hodgson et al., 2008) and from Colombia (Kondo et al., 2008). In Africa, P. solenopsis has been recorded from Sierra Leone (EPPO, 2001), Nigeria, Benin and Cameroon in West Africa (Akintola et al., 2008; Hodgson et al., 2008). In Asia, P. solenopsis was first recorded from Pakistan in 2005 (Abbas et al., 2005) under the nomen nudum Phenacoccus gossypiphilous (Hodgson et al., 2008). It was found in India soon afterwards (Yousuf et al., 2007). Records from Thailand and Taiwan were provided by Hodgson et al. (2008); from Vietnam by Nguyenˆ˜ and Huynh` (2008); and from inland China (Guangzhou) by Wang et al. (2009) and Wu and Zhang (2009); it has been identified in Hong Kong (Dr P. J. Gullan, personal communication) and also in Sri Lanka (Vinobaba & Prishanthini, 2009). It was also recorded in the Pacific Region from New Caledonia by Hodgson et al. (2008).

CLIMEX model match with the native distribution The CLIMEX parameters in Table 1 were used to simulate the potential distribution of P. solenopsis in the U.S.A. (Fig. 3a). There was close agreement between the predicted (Fig. 3a) and the known (Fig. 1) distributions. Moisture was not a limiting factor at Guttenberg (New Jersey) and Vicksburg (Mississippi) (Fig. 4a, b) as a result of abundant rainfall. At these localities, the population growth of P. solenopsis was mainly affected by temperature; the variation of GIW corresponded with TIW (the weekly temperature index), particularly with a marked cold stress value of 26 in winter in Guttenberg (Table 2). The variation in TIW and MIW (the weekly moisture index) at Miami (Florida) (Fig. 4c) suggested that high summer temperatures and excessive moisture in autumn were likely to restrict population growth, indicating that areas with extremely high rainfall were unfavourable for serious infestation by P. solenopsis. In the western and southern U.S.A., there is usually only a little, asymmetrical natural rainfall each year, so that temperature and soil moisture together affected the seasonal population growth of P. solenopsis (Fig. 4d, e). The annual moisture index (MIA) values at Hidalgo (Texas) and Keene (California) were 52 and 59, respectively, and dropped to 20 and 0 at Las Cruces (New Mexico) and Yuma (Arizona), respectively (Table 2). In the western U.S.A., high summer temperatures are usually accompanied by little or no natural rainfall. Yuma (Arizona) is an extremely dry area so dry stress was the most important stress factor, and there was also some degree of heat stress in midsummer. At Las Cruces (New Mexico), low MIA accompanied by a cold stress value of 39 limited the population growth of P. solenopsis (Table 2). In the northwestern U.S.A., restricted natural rainfall and an extremely cold winter limited growth and reproduction of the mealybug. In Esmeralda (Nevada) and Elmore (Idaho), the cold stress values were as high as 65 and 63, respectively (Table 2). Cold winters and lack of soil moisture were key factors Figure 4 Seasonal values of CLIMEX indices at ﬁve representative sites determining the potential colonization and reproduction of in the U.S.A. under natural rainfall: (a) Guttenberg, New Jersey; (b) P. solenopsis in the U.S.A. Under natural precipitation, dry Vicksburg, Mississippi; (c) Miami, Florida; (d) Hidalgo, Texas; (e) Las stress constrained the climatic suitability in the western states Cruces, New Mexico. Top: , average maximum temperature; , (Fig. 5) and, presumably, cold stress prevented the survival of average minimum temperature; , rainfall. Bottom: , weekly growth P. solenopsis in northern parts of the U.S.A. (Fig. 6). Records index; , weekly temperature index; , weekly moisture index. from the western U.S.A. (Arizona, California and Texas) on

Figure 5 CLIMEX model simulation of dry stress for Phenacoccus solenopsis in the U.S.A. The darker the shading, the less favourable the conditions areforthesurvivalofP. solenopsis.

Figure 6 CLIMEX model simulation of cold stress for Phenacoccus solenopsis in the U.S.A. The darker the shading, the less favourable the conditions areforthegrowthandsurvivalofP. solenopsis. desert plants such as Atriplex canescens, Tribulus terrestris Topping up the precipitation to 25 mm per week in the and Atriplex canescens (Hodgson et al., 2008) suggest that growing season (i.e. to simulate irrigation) increased climatic P. solenopsis is extremely drought-resistant. It could survive in suitability for P. solenopsis in the western U.S.A. (Fig. 3b). At areas where annual precipitation is mostly less than 500 mm, if Yuma, one of the hottest places in the U.S.A., irrigation raised host plants are available. The mealybug can colonize different the value of MIA from 0 to 52. Correspondingly, the GIA and microhabitats on the plants to ensure its survival. It can occur EI values were both enhanced to 16 (Table 2). For the other on the roots or the crown of its host, so avoiding very hot and locations in the western U.S.A., application of irrigation also dry and/or very cold conditions to some extent. Lack of soil increased all these indices to a great extent. Irrigation during the moisture might directly impact this mealybug if it is restricted growing season overcame the limiting factor of lack of rainfall, to roots in the upper layer of soil. making such areas a suitable habitat for P. solenopsis.

The threat presented by P. solenopsis and Punjab, Pakistan (NCIPM, 2008). During 2006, the mealybug caused 40–50% yield losses in several parts of The potential global range of P. solenopsis was predicted Gujarat, India (Nagrare et al., 2009), and approximately 40% using the CLIMEX model (Fig. 7). When the distribution of cotton yield was lost in Punjab, Pakistan, in 2007 (Abdullah in natural rainfall (Fig. 7a) was compared with the known et al., 2007). global distribution (Fig. 2), all the reported occurrences of Estimated targets for 2008–2009 cotton production in the mealybug outside the U.S.A. fell within the predicted Pakistan, India and China are given in Table 3, based on distribution. Climatic conditions throughout the pantropical Townsend (2008); the same source estimated 2008–2009 cotton regions were predicted to be very suitable for P. solenopsis. production in the U.S.A. at approximately 3.5 million tons. Areas with high invasion risk included the Caribbean region, Cotton production in China is mainly focused in the Huang- Central and South America, sub-Saharan Africa, southern Asia Huai-Hai regions (including Henan, Shandong, Hebei, Shanxi and coastal Queensland in Australia. Europe and New Zealand and Shaanxi provinces), Xinjiang Uygur Autonomous Region showed sub-optimal suitability for P. solenopsis colonization. and Changjiang River areas (mainly including Jiangsu, Hubei, Cold stress was the primary limiting factor in higher latitudes Anhui, Hunan, Sichuan, Jiangxi and Zhejiang provinces), and in high altitude areas. Heat and dry stress were predicted to which produce 40%, 32% and 26% of the total production, prevent the establishment of P. solenopsis in the Sahara, inland respectively (Zhai et al., 2008). Australia and in parts of the Middle East. Using CLIMEX, it was conservatively predicted that in Simulation of irrigation greatly extended the areas suited to ‘highly suitable’ habitat (EI > 20), P. solenopsis would cause P. solenopsis colonization in dry climate zones (Fig. 7b). It a cotton production loss of 20%. Proportionally, the yield loss expanded the suitable areas in North and South Africa, southern would be 13.3% in ‘suitable’ habitats (10 < EI < 20) and 6.7% Mediterranean Europe, the Middle East and southern Australia. in ‘marginal’ habitats (EI < 10). CLIMEX modelling indicated that the polyphagous mealybug With irrigation, the EI values of Multan (Pakistan), Bathinda P. solenopsis presents a significant threat to agriculture and and Hisar (India) were 8, 9 and 11, respectively (Table 2), horticulture in many tropical and subtropical countries. scoring as plausible ‘marginal’ habitat for P. solenopsis.All three localities have recorded severe damage by the pest, however, so these places proved to be ‘highly suitable’ habitat The threat to cotton-cultivating countries in Asia for the mealybug, despite their low EI values. The mealybug Four cotton-cultivating locations were used to analyze the would probably show large annual fluctuations in numbers in climatic suitability for P. solenopsis in Asian cotton fields: these localities (Sutherst, 2003). Similarly, the cotton-growing Multan (Pakistan), Bathinda and Hisar (India) and Akesu land of Akesu (Xinjiang, China) had an EI value of 12 (Table 2) (China). CLIMEX was used to predict the potential distribution under irrigation, with cold stress in the winter being the main of P. solenopsis in Asia, without and with irrigation (Fig. 8a, limiting factor for P. solenopsis. With such a low EI value, the location probably experiences large annual fluctuations in b). Under natural rainfall conditions, the MIA values for Bathinda and Hisar (India) and Multan (Pakistan) were 25, 27 mealybug numbers. During the growing season, however, the population growth would not be restricted by cold stress. The and 2, respectively. The MIA value at Akesu was 0, with a high cold stress value of 68. Irrigation in the growing season greatly large cotton-growing areas in Xinjiang therefore are potentially ‘suitable’ habitat for P. solenopsis colonization. increased the MIA value of these places, especially in Multan and Akesu (Table 2). The other large cotton-growing areas in China (Huang-Huai- As was found for the U.S.A., the combination of low Hai regions and Changjiang River areas), and the cotton- precipitation and cold temperatures reduced the potential growing areas of Pakistan and India, were all identified by survival and colonization of P. solenopsis in Asia [dry stress CLIMEX as ‘highly suitable’ habitat for P. solenopsis.The (Fig. 9) and cold stress (Fig. 10)]. areas in Pakistan and India are already infested (Muhammad, Simulation of irrigation considerably increased the extent to 2007; Nagrare et al., 2009) but not the areas in China (Wang which P. solenopsis could colonize dry cotton lands in Asia. et al., 2009). With the mealybug established in all these It expanded the potential range of P. solenopsis in Akesu, areas, the forecast losses in cotton yield in 2008/2009 would an important cotton-producing area in China, by increasing be 1.4 million tons in China, 1.12 million tons in India and 0.48 million tons in Pakistan (Table 3). the GIA and EI values for Akesu from 0 to 39, and 0 to 12, respectively (Table 2). Cotton production in the Xinjiang Uygur Autonomous Region, China, might be seriously reduced if P. solenopsis became established there. Under irrigation, Concluding remarks the marginally suitable habitats in southern Pakistan, northern India and parts of the Middle East also became suitable for Phillips et al. (2006) and Ortega-Huerta et al. (2008) found P. solenopsis colonization and establishment (Fig. 8b). that the Genetic Algorithm for Rule-set Prediction (GARP) (Stockwell & Peters, 1999) predicted a relatively extensive potential distribution for the objective species. A comparison of the predicted result of CLIMEX (Fig. 7a) with the previous Predicted cotton yield losses in Asia analysis of P. solenopsis potential distribution using GARP Phenacoccus solenopsis on cotton has caused heavy economic (Wang et al., 2009) demonstrated that the two models agreed damage in severely affected regions such as Gujarat, India, on the core areas in which P. solenopsis was most likely

© 2010 The Authors Agricultural and Forest Entomology © 2010 The Royal Entomological Society, Agricultural and Forest Entomology, 12, 403–416 412 Y. Wang et al. , as ﬁtted by the ecoclimatic index (a) with natural rainfall and (b) with irrigation in the growing season. . P. solenopsis Phenacoccus solenopsis (a) (b) CLIMEX model simulation of the potential global distribution of Figure 7 The darker the shading, the more favourable the conditions are for the survival of

(a)

(b)

Figure 8 Potential geographical distribution of Phenacoccus solenopsis in Asia, as shown by the ecoclimatic index (a) with natural rainfall and (b) with irrigation in the growing season. The darker the shading, the more favourable the conditions are for the survival of P. solenopsis. Localities are indicated as: ,Multan(Pakistan); , Bathinda; , Hisar (India); , Akesu (China).

Table 3 CLIMEX-predicted losses in cotton yield in 2008/2009 in China, India and Pakistan, as a result of Phenacoccus solenopsis infestation, based on estimated target ﬁgures from Townsend (2008)

Estimated production Climatic suitability for Predicted loss of Reduction of cotton Countries (regions) 2008/2009 (million tons) Phenacoccus solenopsis output (%) production (million tons)

China (HHH) 3.20 China Highly suitable 20.00 −0.64 China (XJ) 2.56 total Suitable 13.30 −0.34 total (CJR) 2.08 7.84 Highly suitable 20.00 −0.42 −1.40 India 5.60 Highly suitable 20.00 −1.12 Pakistan 2.40 Highly suitable 20.00 −0.48

HHH, Huang-Huai-Hai regions; XJ, Xinjiang Uygur Autonomous Region; CJR, Changjiang River areas.

Figure 9 Distribution map of dry stress for Phenacoccus solenopsis in Asia, simulated by the CLIMEX model. The darker the shading, the less favourable the conditions are for the survival of P. solenopsis.

Figure 10 Distribution map of cold stress for Phenacoccus solenopsis in Asia, simulated by the CLIMEX model. The darker the shading, the less favourable the conditions are for the survival of P. solenopsis. to be found, although GARP produced a broader and more tropical and subtropical countries. It is a severe threat to inclusive prediction. The GARP model, developed using all cotton production in Asia; the climate of much of these the speciﬁc occurrence records of P. solenopsis (both native cotton-producing areas is at least as suitable for P. solenopsis and invasive) indicated that the added use of exotic occurrence colonization and establishment as is its native territory in the records probably over-rated the potential distribution. In the U.S.A. In particular, the values of the EI in southern China inferential procedure of the ‘Compare Locations’ module of CLIMEX, however, climatic factors are mainly derived from were generally higher than those in the native territory of the the native range of the organism. mealybug. Careful quarantine inspection of imported planting CLIMEX modelling indicated that P. solenopsis presents material and fresh produce is recommended to slow the spread a signiﬁcant threat to agriculture and horticulture in many of this injurious pest.

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