Nietschke et al.: Potential for Scirtothrips dorsalis Establishment in US 79

CLIMATOLOGICAL POTENTIAL FOR SCIRTOTHRIPS DORSALIS (THYSANOPTERA: THRIPIDAE) ESTABLISHMENT IN THE UNITED STATES

BRETT S. NIETSCHKE1, DANIEL M. BORCHERT2, ROGER D. MAGAREY1,2,4 AND MATTHEW A. CIOMPERLIK3 1Center for Integrated Pest Management, North Carolina State University, 1730 Varsity Drive, Suite 110 Raleigh, NC 27606

2United States Department of Agriculture, Center for Plant Health Science and Technology, 1730 Varsity Drive, Suite 300/400 Raleigh, NC 27606

3United States Department of Agriculture, Center for Plant Health Science and Technology, Pest Detection and Diagnostics Laboratory, Edinburg, TX 78539

4E-mail address: [email protected]

ABSTRACT

Scirtothrips dorsalis is a serious exotic pest that has recently become established in the con- tinental United States. It is of major concern to regulatory agencies because it has a wide host range and high reproductive potential. A weather-based mapping tool, NAPPFAST, was used to predict potential establishment of S. dorsalis in North America. The analysis was based on a degree-day model and cold temperature survival of S. dorsalis. The results demonstrated that S. dorsalis could potentially produce up to 18 generations and was likely to survive in the southern and western coastal plains of the United States. It is concluded that S. dorsalis is likely to be a serious economic pest in the southern United States. Addi- tional maps and information are available at the web site (http://www.nappfast.org).

Key Words: exotic species, insect development, temperature, risk mapping, Scirtothrips dor- salis

RESUMEN

Scirtothrips dorsalis es una importante plaga exotica que se ha establecido recientemente en el continente de los Estados Unidos. La presencia de este insecto es preocupante para las agencias que se encargan de la proteccion fitosanitaria debido a que esta especie tiene una lista amplia de plantas hospederas y un alto potencial reproductivo. Utilizamos el programa de mapeo NAPPFAST (que se basa en temperatura) para predecir las posibles areas de es- tablecimiento de S. dorsalis en Norte America. El analisis se baso en un modelo de grados dia y en la supervivencia de S. dorsalis a temperaturas bajas. Los resultados demuestran que S. Dorsalis potencialmente podria producir hasta 18 generaciones por año y que es pro- bable que sobreviva en las planicies costeras del sur y el oeste de los Estados Unidos. Con- cluimos que S. dorsalisprobablemente se convertira en una plaga economica seria para el sur de los Estados Unidos.

Translation provided by the authors.

The chilli thrips, Scirtothrips dorsalis Hood Trinidad and Tobago, Puerto Rico (Ciomperlik (Thysanoptera: Thripidae) is a serious exotic pest unpublished data), and in South America in Suri- that has recently become established in the conti- name (Ciomperlik et al. 2005b) and Venezuela nental United States. It is a highly polyphagous (M. Quiros, pers. comm.). In late 2005, S. dorsalis species with over 100 plant species cited as host was reported in Florida (Hodges et al. 2005) and plants (Meissner et al. 2005). Scirtothrips dorsa- has been detected 70 times in 16 Florida counties lis occurs throughout Asia, Australasia, and the (Holtz 2006). In 2004, APHIS began a compre- Pacific Islands (CABI 2005) and in 2003 was in- hensive risk assessment of the potential intro- tercepted at the port of Miami, Florida, on a ship- duction and establishment of S. dorsalis (Meiss- ment of peppers (Capsicum sp.) originating from ner et al. 2005). the Caribbean island of St. Vincent (Skarlinsky Scirtothrips dorsalis is estimated to produce 2003). It was subsequently confirmed in St. Vin- up to 8 generations annually in Japan (Tatara cent, St. Lucia (Skarlinsky 2003; Ciomperlik & 1994); however, its generational potential in the Seal 2004), Barbados (Ciomperlik et al. 2005a), United States is unknown. Although S. dorsalis

80 Florida Entomologist 91(1) March 2008

has colonized parts of Florida, the areas where it modeling system (Borchert & Magarey 2005; could potentially survive and establish remain Magarey et al. 2007). The system was built and undefined. A predicted establishment map was maintained by a commercial weather company developed by Venette & Davis (2004) based on a (ZedX, Inc., Bellefonte, PA) with experience in biome matching technique (Olsen et al. 2001). pest modeling and site-specific weather data The study predicts that potential establishment (Russo 1999). The NAPPFAST system links daily in the eastern United States would not include climate and historical weather data with biologi- the coastal plain, with the exception of a small cal models that contain a series of interactive ‘fill- area of southern Florida. On the west coast, po- in-the-blanks’ templates (Borchert & Magarey tential establishment was limited to the Wil- 2005). The model template was based on one de- lamette Valley in Oregon. veloped for European corn borer (Dillehay et al. The biome approach used by Venette & Davis 2005) that uses daily weather and climate data (2004) is an example of an inductive risk mapping from approximately 2000 weather stations across technique where the predicted distribution is North America. Individual station values are in- based on a climate or habitat match (Baker 2002). terpolated to a 10 km2 by using the Barnes Inductive risk maps based on climate and host method (Barnes 1964). The NAPPFAST system distribution have been used widely to predict po- has been validated for Japanese beetle (Popillia tential pest establishment (Sutherst & Maywald japonica) (Magarey et al. 2005), Diaprepes abbre- 1985; McKenney et al. 2003; Hoddle 2004). Risk viatus (Lapointe et al. 2007) and numerous inter- maps also are created with deductive techniques nal APHIS pests risk assessments (Magarey et al. that use experimental data to create biological 2005). As NAPPFAST lacks international models that predict a pathogen’s distribution weather data (outside of North America), valida- from weather or climate data (Baker 2002). One tion of the model was limited to the Caribbean. deductive approach useful for predicting estab- Based upon the insect development template lishment of exotic insect pests is phenology mod- in NAPPFAST, generation potential maps were els (Baker 1991; Jarvis & Baker 2001; Baker created for S. dorsalis from 10 years (1994-2004) 2002). Another approach is to exclude areas of the North American climate database. To deter- where cold or hot temperatures result in pest mine the potential number of generations S. dor- mortality (Magarey et al. 2007). The comparison salis could complete in a year, the developmental of deductive and inductive approaches for the model used parameters of 9.7°C as the base devel- same pest provides additional evidence for deci- opmental temperature and cumulative degree- sion makers. day (DD) requirement from oviposition to oviposi- Recently, site-specific weather technologies tion of 281°C DD (Tatara 1994). These require- have made it easier to apply pest phenology and ments were similar to those Shibao (1996) used weather-based risk models to risk prediction on a for S. dorsalis on grape (Vitis vinifera). To illus- regional or national scale. The technology uses trate the influence of climate on generation poten- spatial interpolations and numerical models to tial, probability maps were developed displaying create simulated observations (Russo 1999; Ma- the frequency of occurrence of 1 to 5 generations. garey et al. 2001). Site-specific weather technolo- Although S. dorsalis will most likely develop more gies have successfully been used to deploy pheno- than 5 generations in many areas of the United logical models at the scale of individual farms or States, it was assumed that 5 generations repre- at a regional scale for many insects including, ap- sented the biological impact sufficiently. Data ple (Malus domestica) pests, gypsy moth (Lyman- which occurred less than 2 out of 10 years were tria dispar), root weevils (Diaprepes abbreviatus), excluded from the maps and the remaining data Monarch butterfly (Danaus plexippus), and Euro- reclassified (with ArcGIS 8.3, ESRI, Redlands pean corn borer (Ostrinia nubilalis) (Russo et al. USA) into a single representative class to demon- 1993; Felland et al. 1997; Dively et al. 2004; Dille- strate the generational potential of S. dorsalis. hay et al. 2005; Lapointe et al. 2007). In this Ten-year probability maps for generations 1 to 5 study, a web-based modeling system was used to were added and divided by 5 to maintain a 10- create potential weather-based pest establish- class scale. A value of 1 represents low occurrence ment maps in the United States for S. dorsalis. of multiple S. dorsalis generations, while a value of 10 indicates S. dorsalis has the degree-days re- METHODS quired to complete 5 generations. To define areas in the United States where S. Risk maps for S. dorsalis were created by using dorsalis may potentially establish, maps showing the standardized procedure for 50 exotic pests a cold temperature exclusion boundary were cre- listed as priorities by the Cooperative Agricul- ated with the 10-year North American climate da- tural Pest Survey program (Borchert & Margo- tabase in NAPPFAST. The cold temperature ex- sian, unpublished). Climate risk maps were pro- clusion model was developed for when the mini- duced based on the North Carolina State Univer- mum daily temperature reaches -4°C or below for sity-APHIS Plant Pest Forecast (NAPPFAST) 5 or more days in a year. These parameters were

Nietschke et al.: Potential for Scirtothrips dorsalis Establishment in US 81

based on a study of a similar thrips species, TABLE 1. HOST SPECIES FOR SIRTOTHRIPS DORSALIS Thrips palmi (McDonald et al. 2000) because the (CABI 2005). temperature that is lethal to S. dorsalis is un- Host Status known. McDonald et al. (2000) presented LD90 mortality lethal time data for 3 temperatures; 0°C, -5°C, and -10°C. A threshold of -4°C was used Almonds (Prunus dulcis) because -10°C occurs infrequently in the southern Apples (Malus spp.) Asparagus (Asparagus spp.) Primary United States and the LD90 at 0°C was over 170 h. Both S. dorsalis and T. palmi occur frequently as Barley (Hordeum spp.) mixed populations in the field (M. Ciomperlik, un- Beans (Phaseolus spp.) Primary published data; Chu et al. 2006). A 10-year fre- Broccoli (Brassica oleracea) quency map showing the cold temperature exclu- Cantaloupes (Cucumis spp.) Primary sion boundary was created in NAPPFAST and im- Carrots (Daucus carota) Primary ported into the GIS. Data were excluded from the Celery (Apium graveolens) maps which occurred less than 8 out of 10 years Citrus (Citrus spp.) Secondary and the remaining data reclassified into a single Corn (Zea spp.) Primary representative class. Cotton (Gossypium spp.) Secondary Mortality of S. dorsalis at temperatures above Cucumbers (Cucumis spp.) Primary 33°C has been observed, with the mortality rate Grapes (Vitis spp.) Primary at 100% after 3 d exposure to 38°C (Tatara 1994). Lettuce (Lactuca spp.) However, constant high temperatures of this Oats (Avena spp.) magnitude and duration are not generally found Onions (Allium spp.) Secondary in the United States, so a high temperature exclu- Peaches (Prunus persica) Primary sion boundary was not included. The final climate Peanuts (Arachis spp.) Secondary risk map for S. dorsalis was created by overlaying Pears (Pyrus spp.) Primary the generation potential map with the cold tem- Potatoes (Solanum spp.) Primary perature exclusion boundary. Rice (Oryza spp.) The density of host crops also determines Sorghum (Sorghum spp.) where insects may potentially establish. Host Soybeans (Glycine spp.) Primary density risk maps for the United States were cre- Strawberries (Fragaria spp.) Primary ated in ArcGIS from county acreage data (USDA Sunflower (Helianthus spp.) Primary NASS 2002). The analysis was restricted to the Tomatoes (Lycopersicon spp.) Secondary top 30 agricultural commodities by value. Host Wheat (Triticum spp.) determination and host status (primary versus Pine (Pinus spp.) secondary) (Table 1) was obtained from informa- Other Softwood Trees tion in the APHIS Global Pest Disease Database, Soft Hardwood Trees Primary which was primarily sourced from the CABI Crop Hardwood Trees Primary Compendium (CABI 2005). Total primary and secondary host acres were divided by the total acres per county, re-classed into 10 classes based lis could potentially establish or has already on the classification scheme in Table 2 and com- established, the major host crops of peppers (Cap- bined in a 2 (primary):1 (secondary) weighted sicum annum), eggplant (Solanum melongena), analysis. The scale of 1 to 10 describes the propor- tion of total host acreage per county: for example a rank of 1 indicates no host acreage, while a score of 10 indicates that 75-100% of the acres in the TABLE 2. RECLASSIFICATION SCHEME FOR HOST PROPOR- county contains suitable hosts for the pest. TION DATA. A final risk map representing the influence of both climate and host was created in the GIS. The Proportion of host acres Host reclassification host risk map (Fig. 1) and the climate risk map per county value (Fig. 2) were multiplied by 0.34 and 0.66, respec- 01 tively, and added together to obtain a final risk 0-0.01 2 map (Fig. 3). These values were selected to give 0.01-0.025 3 greater importance to the host layer. 0.025-0.05 4 0.05-0.075 5 RESULTS 0.075-0.1 6 0.1-0.25 7 The greatest density of susceptible hosts in- 0.25-0.5 8 cludes the Gulf Coast of Texas, southern Florida, 0.5-0.75 9 the lower Mississippi valley, and the central val- 0.75-1 10 ley of California (Fig. 1). In areas where S. dorsa- 82 Florida Entomologist 91(1) March 2008

Fig. 1. Host density map risk map for S. dorsalis. and tomatoes (S. lycopersicum) predominately are DISCUSSION grown in California and southern Florida. Based on the NAPPFAST analysis, S. dorsalis The development of risk maps to predict the has a high generation potential throughout the establishment areas in the United States of S. United States (Fig. 2). In the southern states of dorsalis demonstrates how NAPPFAST can be South Carolina, Georgia, Florida, Alabama, Mis- used to aid pest risk assessment. The analysis sissippi, Louisiana, and Texas, S. dorsalis may suggests that if S. dorsalis were to establish in the produce 12 or more generations annually. Con- United States, it will have a high generational po- versely, 4 to 10 generations were predicted on the tential and could potentially produce up to 18 West Coast of the United States, with increased generations in regions where cold temperatures potential in southern California, Nevada, and are predicted not to preclude S. dorsalis establish- Arizona. ment. However, the model does not account for en- The final risk map incorporates host density, vironmental factors such as shorter day length, generation potential, and cold temperature exclu- which could induce diapauses response and there- sion (Fig. 3). Due to its exclusion from cold climate fore reduce the generational ability of S. dorsalis. areas (where minimum daily temperature The model also does not account for seasonal reaches -4°C or below on at least 5 d per year), migration and greenhouse production that could analysis suggests that S. dorsalis would probably make it a pest beyond the northern boundary of only establish in the southern United States and establishment. along the west coast. Areas of the Caribbean Alternative issues relating to the prediction of where S. dorsalis has been reported; St. Vincent, pest establishment based on phenology models St. Lucia, Barbados, Trinidad and Tobago, Puerto also need to be considered. For example, the NAP- Rico (Skarlinsky 2003; Ciomperlik & Seal 2004; PFAST model does not include any latitudinal ad- Ciomperlik et al. 2005a, b; Ciomperlik, unpub- justments that would account for increased devel- lished data), all had favorable DD accumulations opment rates at higher temperatures (Rock et al. (18 generations or more) and no cold climate ar- 1993). The model also assumes that the thresh- eas (results not shown). olds published in the literature are correct. Rock Nietschke et al.: Potential for Scirtothrips dorsalis Establishment in US 83

Fig. 2 Ten-year climate risk map for S. dorsalis based upon the average frequency of 1-5 generations. et al. (1993) raise the question that laboratory de- humidity (~20%) also will be deleterious to S. dor- rived thresholds may under-estimate generation salis populations (as occur in the Imperial Valley potential in the field due to microclimate differ- of southern California). This effect has been docu- ences. Although the thresholds used for S. dorsa- mented on western flower thrips (Frankliniella lis were field derived (Tatara 1994), the exact tim- occidentalis) in the Arava Valley of Israel (Chyzik ing of phenological events is not critical for pre- & Orna-Ucko 2002), but was complicated by the dicting pest establishment, but rather the rela- influence of irrigation and cropping systems. tive totals. A high generation potential does not The generation potential of S. dorsalis coupled guarantee that a pest will reach high population with the wide distribution of host crops increases levels; rather it indicates that temperature accu- the likelihood of S. dorsalis establishment and its mulation is not a limiting factor. potential to cause economic damage in the United Other environmental factors such as rainfall States. Additionally, its major host crops of pep- also may affect the generational potential of S. pers, eggplant, and tomatoes predominately are dorsalis, based on studies from India (Varadhara- grown in California and southern Florida, regions jan & Veeravel 1995; Lingeri et al. 1998) that sug- where S. dorsalis are predicted to produce a high gest populations may be reduced in high or in- (10 to 18) number of generations annually. Scirto- tense rainfall regions. The level or intensity of thrips species including S. dorsalis particularly rainfall required to reduce populations and the cause economic damage to crops when tempera- subsequent affect on the generational potential of tures are high over summer (Hoddle 2002). Be- S. dorsalis is unclear. Nevertheless, it is antici- cause S. dorsalis has a short life cycle of 15-20 d pated that S. dorsalis will mainly achieve pest (CABI 2005) and is a known pest problem in Ja- status during periods of low rainfall (Mound & pan where it produces up to 8 generations annu- Palmer 1981) and thrive under hot, dry condi- ally (Tatara 1994), it may be assumed that crop tions. This confirms the assumption that that regions where S. dorsalis completes 8 or more high temperature mortality will probably not be generations face a reasonable chance of sustain- important in the United States. It is unclear if low ing economic damage. This includes regions 84 Florida Entomologist 91(1) March 2008

Fig. 3. Risk map for S. dorsalis based on generation potential, minimum temperature exclusion, and host den- sity. where S. dorsalis occurs, but may not perma- to vegetable, ornamental and fruit crops, and to nently establish. native plants in natural ecosystems. This is cur- Comparisons may be drawn between S. dorsa- rently the case in southern Florida, where S. dor- lis and T. palmi through this study. This is rele- salis is causing significant damage in ornamental vant since T. palmi has established in Florida, but landscapes (Lance Osborne, pers comm.). In addi- has not been reported in other U.S. states (CABI tion, S. dorsalis has recently been found in dam- 2005). Both T. palmi and S. dorsalis have a simi- aging population levels in Barbados on sea island lar geographical distribution and attack many of cotton (Gossypium barbadense), which suggests the same host plants, although S. dorsalis has a that it could become a serious pest of cotton (G. wider host range than T. palmi. Thrips palmi has hirsutum) in North America. Another concern is a similar base and DD requirement (10.1°C, that S. dorsalis is a vector of Tomato Spotted Wilt 197°C DD, McDonald et al. 2000) to S. dorsalis Virus, which is a serious disease with a large host (9.7°C, 281°C DD, Tatara 1994). Because the de- range (Venette & Davis 2004). velopmental biology of both species is similar, Due to NAPPFAST’s lack of international their restriction to Florida suggests this study weather daily data, the phenology or cold temper- over estimates the potential establishment range ature exclusion model could not be generated out- for S. dorsalis. However, it cannot be assumed side of North America. With the exception of Ja- that T. palmi has reached its full establishment pan and Korea, S. dorsalis is mostly reported in potential or that S. dorsalis will follow a similar tropical countries (CABI 2005), making valida- establishment pattern. Scirtothrips dorsalis ap- tion difficult unless geographic locations of S. dor- pears to be a more aggressive pest than T. palmi salis observations are known. in Caribbean field studies (Ciomperlik, unpub- The results of this study differs from Venette & lished data), causing increased feeding damage to Davis (2004), who used an inductive biome ap- several host crops. Moreover, S. dorsalis is likely proach (Olson et al. 2001) to predict establish- to be more damaging than T. palmi with respect ment of S. dorsalis in the north-east and Great Nietschke et al.: Potential for Scirtothrips dorsalis Establishment in US 85

Lakes, but not on the coastal plain of the U.S. Ven- DILLEHAY, B. L., D. D. CALVIN, G. W. ROTH, J. A. HYDE, ette & Ragsdale (2004) used a biome approach to G. A. KULDAU, R. J. KRATOCHVIL, J. M. RUSSO, AND predict the distribution of soybean aphid (Aphis D. G. VOIGHT. 2005. Verification of a European corn glycines) in the United States Their results pro- borer (Lepidoptera: Crambidae) loss equation in the vided a good first estimate but did not forecast the major corn production region of the Northeastern United States. J. Econ. Entomol. 98: 103-112. establishment of soybean aphid in central and DIVELY, G. P., R. ROSE, M. K. SEARS, R. L. HELLMICH, D. northern Illinois, the Dakotas and Nebraska. The E. STANLEY HORN, D. D. CALVIN, J. M. RUSSO, AND advantage of the Olson technique is that it is eco- P. L. ANDERSON. 2004. Effects on monarch butterfly logically based rather than only using tempera- larvae (Lepidoptera: Danaidae) after continuous ex- ture as in our study. 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