Predicting Habitat Suitability of Coptotermes Gestroi (Isoptera: Rhinotermitidae) with Species Distribution Models

HOUSEHOLD AND STRUCTURAL INSECTS Predicting Habitat Suitability of Coptotermes gestroi (Isoptera: Rhinotermitidae) With Species Distribution Models

1,2 3 1 HOU-FENG LI, IKUKO FUJISAKI, AND NAN-YAO SU

J. Econ. Entomol. 106(1): 311Ð321 (2013); DOI: http://dx.doi.org/10.1603/EC12309 ABSTRACT Coptotermes gestroi (Wasmann) is an important structural pest reported from Asia, PaciÞc islands, North America, Caribbean islands, South America, and Indian Ocean islands. This study summarized previous records of C. gestroi and its synonyms, presenting 184 infested counties from 24 countries. Based on the geo-references occurrence locations and global raster data of climate, geography, and human population, C. gestroi were found most commonly in warm, high precipitation, low altitude, and human populated areas. By using species distribution models, we predicted its current infested area (model 1), habitat suitability (model 2), and probability of introduction (model 3) on a global scale. The results showed its recorded locations and the predicted distribution of the present day are similar, but the suitable habitat is larger than its current distribution. The patterns of the introduction frequency (model 3) and habitat suitability (model 2) are inconsistent. Temperate cities with high introduction risk are located in Europe, United Sates, northeastern China, and Japan where habitat suitability is low and hence successful colonization is unlikely. In tropics and subtropics, habitat suitability of C. gestroi is high. We speculate that continuous urbanization and increasing human population will increase its introduction frequency and cause further extension in fast developing tropical and subtropical countries.

KEY WORDS invasive species, species distribution model, urban pest, subterranean termite

Urban environments are characterized by manmade (King and Spink 1969, Messenger et al. 2005). Only a construction and designed landscape but are also few termite species reach cosmopolitan distribution shaped by natural climate and geography. Some ar- (Gay 1967, Evans 2010). Their peridomestic habitat is thropods adapted to urban habitats could reproduce in affected by outdoor climatic and geographic factors large numbers, resulting in esthetic damage, economic that probably limit their colonization and further ex- loss, and human health threats (Robinson 2005). Do- tension in introduced area. mestic pests, such as Germen cockroach (Appel 1995), In tropical and subtropical areas, the genus, Cop- Pharaoh ant (Wheeler 1910), and stored food beetles totermes, is the most signiÞcant group, including Ϸ70 (Hill 2002) complete their life cycles indoors with described species (Vargo and Husseneder 2009, Con- limited food, water, and harborage, and have been stantino 2011) and one third of which considered pests spread around the world through commerce. Subter- (Edwards and Mill 1986, Su and Scheffrahn 2000). Six ranean termites (Rhinotermitidae) are important ur- Coptotermes species have been recorded as invasive ban pests. The most damaging subterranean species pests, and Coptotermes gestroi (Wasmann) and Cop- occur in three genera, Coptotermes, Heterotermes, and, totermes formosanus Shiraki, have the largest distribu- Reticulitermes (Edwards and Mill 1986), with a com- tion (Evans 2010), and are the most often occurring bined global economic impact of $40 billion annually in tropical and temperate areas, respectively (Su (Rust and Su 2012). In urban environments, subter- 2003). The distribution of C. formosanus had been well ranean termites live in the peridomestic area and usu- documented (Tamashiro and Su 1987). However, no ally nest in soil. Their subterranean gallery system and global distribution of C. gestroi has been available aboveground mud tubes could extend over a hundred because of the long-standing confusion of its taxon- meters connecting underground nests and food omy. C. gestroi was Þrst described from Myanmar, and sources such as tree stumps, dead branches of living then several synonyms were created from other Asian tree, gardening wood, and wooded constructions countries, such as C. heimi (Wasmann 1902) and C. parvulus Holmgren 1913a from India, C. havilandi Hol- 1 Department of Entomology and Nematology, Fort Lauderdale mgren 1911a from Malaysia, C. vastator Light 1929 Research and Education Center, University of Florida, 3205 College from the Philippines, C. paciﬁcus Light 1932 from In- Ave., Ft. Lauderdale, FL 33314. donesia, and C. obliquus Xia and He 1986 and C. yax- 2 Department of Wildlife Ecology and Conservation, Fort Lauder- ianensis Li 1986 from China. In the 20th century, C. dale Research and Education Center, University of Florida, 3205 College Ave., Ft. Lauderdale, FL 33314. gestroi was introduced to other geographic areas in- 3 Corresponding author, e-mail: houfeng@uß.edu. cluding PaciÞc islands, North America, Caribbean is-

0022-0493/13/0311Ð0321$04.00/0 ᭧ 2013 Entomological Society of America 312 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 106, no. 1 lands, South American, and Indian Ocean islands (Gay Materials and Methods 1967). The synonyms of C. gestroi were adopted in- Locations Sampled. Published literature containing dividually at different geographic areas for many de- collection records of C. gestroi and its synonyms were cades. In light of recent taxonomic studies (Roonwal reviewed. The Þrst documented year in each country, and Chhotani 1962; Gay 1967; Kirton and Brown 2003; recorded species name, identiÞed material, and ref- Yeap et al. 2007, 2010; Li et al. 2011), the C. parvulus, erences were tabulated (Table 1). To establish a reg- C. paciﬁcus, C. havilandi, C. vastator, C. heimi, C. ular resolution database for worldwide distribution obliquus, and C. yaxianensis were proven to be junior simulation, only county records or smaller adminis- synonyms of C. gestroi. Currently, C. gestroi is consid- trative regions were used for current study. If multiple ered the most destructive structural pest in South- locations were documented in a county, we randomly east Asia (Kirton and Azmi 2005, Lee et al. 2007), selected one location. If no speciÞc location was men- India (Roonwal and Chhotani 1989, referred as C. tioned in a county, physical middle point was chosen. heimi), and Brazil (Constantino 2002, referred as C. In total, 184 county records of 24 countries were ob- havilandi). C. gestroi continually extended its infes- tained from 66 publications (Table 1). Coordinates of tation in newly invaded areas, including Taiwan (Li the 184 observation points were estimated by using et al. 2009) and Florida (Su et al. 1997, Scheffrahn Google Earth software. In addition, background ref- and Su 2005). erence points were selected at 0.5 degree interval, In addition to the taxonomic confusion, obtaining a which approximately correspond to a county size, on global distribution map through Þeld survey is always terrestrial area between 40 degrees north and south time-consuming and Þnancially challenging. Previous latitude where most termite species were found (Egg- termite surveys were geographically scattered and de- leton 2000). In total, 30,385 background reference pendant on work of few scientists. Sampling bias points were obtained. caused by different investigators and different original Environmental Factors. To describe ecological research purposes remain uncorrected because of niche of C. gestroi and to predict its current distribu- sparse information on previous sampling methods. We tion area, habitat suitability, and possibility of intro- have no idea if many of the areas that show an absence duction in worldwide scale, publicly available global of C. gestroi truly lack this species or just have not been raster data of environmental factors were used. properly surveyed yet. To overcome these limitations, Monthly minimum and maximum temperatures, pre- the current study reviews published literature with cipitation and altitude, which were representative of several hundreds of collection records of C. gestroi 1950Ð2000 (Hijimas et al. 2005), were obtained from (Table 1) to obtain its recorded occurrence locations WorldClim (2010). From monthly minimum and (Fig. 1A), and by using species distribution models to maximum temperatures and precipitation, we de- predict its current areas of infestation (Fig. 1B). Spe- rived annual minimum and maximum temperatures cies distribution models or ecological niche models and precipitation. Moderate Resolution Imaging are frequently used to predict the potential range of Spectroradiometer (MODIS)/terra land cover type exotic species (Peterson and Vieglais 2001, Welk et al. 2007 data with the International Geosphere-Biosphere 2002) to assess invasion potential. A common ap- Programme (IGBP) vegetation classiÞcation scheme, proach is to parameterize models based on the native which differentiates 16 land cover classes (Friedl et al. 2002), were obtained from NASA the Warehouse In- range of species and use the deÞned environmental ventory Search Tool (2010). Gridded Population of correlates to predict the adventive range (Welk et al. the World (GPW) version three (Center for Interna- 2002, Richardson and Thuiller 2007). Various methods tional Earth Science Information Network [CIESIN] have been developed that allow predictions using ex- 2005), which depicts the human population density in isting species occurrence data to understand the 2010, was obtained from Web site of the Center for mechanism of speciesÕ arrange shifts in the face of International Earth Science Information Network of global-scale ecological changes (Elith et al. 2011). the Earth Institute at Columbia University. Raster data Climate variables, such as temperature and precipita- of MODIS land cover type, and human population tion, are often seen as primary driving factors among were resampled with nearest neighbor assignment to environmental variables. Previous laboratory studies match 30 arc-seconds grid of temperature, precipita- have shown C. gestroiÕs foraging and nesting behavior tion, and altitude data using ArcGIS 9.3. Values of are affected by environmental factors such as temper- environmental raster data at each sample point were ature, soil moisture, and soil type (Arab and CostaÐ extracted using ArcGIS 9.3 Spatial Analyst. PearsonÕs Leonardo 2005, Arab et al. 2005, Lima et al. 2006). correlation coefÞcient between every paired environ- Additional variables, such as land cover type, are used mental factor, except for categorical land cover type, to further reÞne the model (Pearson et al. 2004, Brad- was calculated and tested under a hypothesis of no ley and Mustard 2006). In the current study, we de- correlation using SAS CORR procedure (SAS Institute scribe the ecological niche of C. gestroi based on the 1985). The difference between recorded sites and climatic and geographic data of the recorded locations regular selected locations on the six environmental (Fig. 2). By using species distribution models, we factors, excluding land cover type, was tested by Wil- further predicted its habitat suitability (Fig. 1C) and coxon rank sum test using SAS NPAR1WAY proce- probability of introduction globally (Fig. 1D). dure (SAS Institute 1985). February 2013 LIETAL:HABITAT SUITABILITY OF Coptotermes gestroi 313

Table 1. First record of Coptotermes gestroi at each infested country, identiﬁcation method, and references

Geographic First ID d area Country/area record Recorded species name methodsc Reference Additional references Asia Myanmar 1895 Termes gestroi Wasmanna S Wasmann 1896 Haviland 1898, Holmgren 1913b, Coptotermes gestroi (Wasmann) S Holmgren 1911a Kirton and Brown 2003 Malaysia/Sarawak 1898 T. gestroi S Haviland 1898 Jenkins et al. 2007 C. gestroi S Holmgren 1911a Malaysia/Peninsula C. havilandi Holmgren A Holmgren 1913b C. travians (ϭ C. gestroi)b S Tho 1992 (Kirton and Brown 2003) C. gestroi S, mt gene Yeap et al. 2007 Singapore 1898 T. gestroi S Haviland 1898 Jenkins et al. 2007 C. gestroi S Holmgren 1911a C. gestroi S, mt gene Yeap et al. 2007 India 1902 Arrhinotermes heimi Wasmanna A Wasmann 1902 Silvestri 1923, Roonwal and A. heimi Wasmann A, S Holmgren 1913b Chhotani 1962, Roonwal and C. parvulus Holmgrena S Holmgren 1913a Bose 1964, Chatterjee and C. gestroi Thakur 1967, Amir 1975, S Holmgren and Holmgren Roonwal and Chhotani 1989 1917 Taiwan 1910 C. gestroi A, S Oshima 1910a Oshima 1910b C. havilandi ? Holmgren 1912 C. gestroi S Tsai and Chen 2003 C. gestroi A, S, mt Li et al. 2009 gene Thailand 1911 C. havilandi Holmgrena ? Holmgren 1911a Holmgren 1911b, Harris 1968, C. havilandi A Holmgren 1913b Roonwal and Chhotani 1989, C. havilandi S Ahmad 1965 Jenkins et al. 2007 C. gestroi S, mt gene Yeap et al. 2007 Indonesia 1911 C. gestroi S Holmgren 1911a Roonwal and Chhotani 1962, Kirton C. javanicus Kemnera A, S Kemner 1934 and Brown 2003 C. parvulus S Kemner 1934 C. heimi S Amir 1975 C. gestroi S, mt gene Yeap et al. 2007 Pakistan 1916 C. heimi S Ahmad 1955 Roonwal and Chhotani 1962, Khan C. heimi A, S Chaudhry and Ahmad 1972 and Ahmad 1955 C. gestroi S, mt gene Yeap et al. 2010 Philippines 1917 C. formosanus (ϭ C. vastator)b S Oshima 1920 (Light 1929) C. travians (ϭC. vastator)b S Oshima 1920 (Light 1929) C. vastator Lighta A, S Light 1929 China 1963 C. yaxianensis Lia A, S Li 1986 Li 2000 C. obliquus Xia et Hea S Xia and He 1986 C. gestroi S Xia and He 1986 Bangladesh 1968 C. heimi A, S Chaudhry and Ahmad 1972 Amir 1975, Roonwal and Chhotani 1989 PaciÞc Ocean French Polynesia 1932 C. pacificus Lighta A Light 1932 Guam (U.S.) 1970 C. formosanus (ϭ C. vastator)b ? Hromada 1970 (Su and Yudin 2002 Scheffrahn 1998) C. vastator A, S Su and Scheffrahn 1998 U.S./Hawaii 1963 C. vastator A Weesner 1965 C. vastator A, S Woodrow et al. 2001 C. vastator mt gene Yeap et al. 2007 Japan/Marcus Island 2000 C. vastator A, S Morimoto and Ishii 2000 North America Mexico 1994 C. havilandi S Ferraz and MendezÐMontiel 2004 U.S./Florida 1996 C. havilandi A, S Su et al. 1997 Scheffrahn 2004, Jenkins et al. 2007 C. gestroi A, S Scheffrahn and Su 2005 C. gestroi mt gene Li et al. 2009 Caribbean Barbados 1936 C. havilandi ? Adamson 1938 Ocean C. havilandi A Tucker 1939a Jamaica 1939 C. javanicus ? Tucker 1939b Snyder 1956 C. havilandi ? Adamson 1948 Cuba 1990 C. havilandi A, S Hernańdez 1994 Scheffrahn et al. 1994, J. Krecek presonal communication British West Indies 1990 C. havilandi S Scheffrahn et al. 1990 Scheffrahn et al. 1994 C. gestroi mt gene Scheffrahn et al. 2004 Antigua and Barbuda 1994 C. havilandi ? Scheffrahn et al. 1994 Scheffrahn et al. 2003 C. gestroi mt gene Scheffrahn et al. 2004 Montserrat (U.K.) 1994 C. havilandi ? Scheffrahn et al. 1994 Saint Kitts and Nevis 1997 C. gestroi S Scheffrahn et al. 2004 Puerto Rico (U.S.) 2002 C. havilandi S Scheffrahn et al. 2003 C. gestroi mt gene Jenkins et al. 2007 South America Brazil 1923 C. havilandi ? Araujo 1958 Menezes et al. 1998, Fontes and C. havilandi A, S CostaÐLeonardo et al. 1999 Veiga 1998, Constantino 2002, Ferraz and MendezÐMontiel C. gestroi mt gene Martins et al. 2010 2004 Paraguay 1998 C. havilandi ? Fontes and Milano 2002 Indian Ocean Mauritius 1936 Coptotermes sp. A, S Moutia 1936 C. havilandi A, S Snyder 1949 French Reúnion 1957 C. havilandi ? Paulian 1957

a Original descriptions of C. gestroi and its synonyms. b Specimen was Þrst misidentiÞed as other species (not synonyms), which was later changed into C. gestroi or its synonyms. c IdentiÞcation methods: S, soldier morphology; A, alate morphology; mt gene, mitochondria DNA gene sequences; ?, unmentioned method. d References presented additional collection localities for the country. 314 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 106, no. 1

Fig. 1. Coptotermes gestroi distribution and invasion simulation in global wide scale. According to previous studies, on total 184 counties of 24 countries were infested (A). Based on the distribution records and global raster data of climate, geography, and human population, C. gestroi infestation of the present day (B, model 1), habitat suitability (C, model 2), and probability of introduction (D, model 3) were predicted by using species distribution model. February 2013 LIETAL:HABITAT SUITABILITY OF Coptotermes gestroi 315

Fig. 2. Comparison of six environmental factors between C. gestroi recorded locations and background reference points at overall terrestrial domain between north and south 40 degree. Environmental factors included: annual minimum and maximum temperature (A, B); annual minimum and maximum precipitation in driest and wettest month (C, D); altitude (E); human population density (F). In total, 184 records of C. gestroi was showed by columns and right vertical axis. Background reference points were selected at 0.5 degree interval, which approximately correspond to a county size, on terrestrial area between 40 degrees north and south latitude. In total, 30,385 regular points was presented by lines and left vertical axis. The difference between recorded sites and regular selected locations on each environmental factor was tested by Wilcoxon rank sum test. Z and p value were shown in each subÞgure.

Habitat Suitability Simulation. We used the maxi- 2007), following to a number of preceding studies that mum entropy (Maxent) algorithm (Phillips et al. 2006, predicted potential distribution of exotic species in Elith et al. 2011), a machine-learning robust species their adventive range (e.g., Elith et al. 2010, 2011). distribution modeling method with presence only data Using geo-referenced presence data, randomly se- (Elith et al. 2006, Hernandez et al. 2006, Guisan et al. lected pseudo-absences data, and environmental fea- 316 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 106, no. 1

Table 2. Correlation analysis of the six environmental factors (SAS, CORR procedure)

Environmental factors MinT MaxT MinP MaxP Alt Pop Min temp (MinT) Ϫ0.39 0.44 0.29 Ϫ0.47 0.14 Max temp (MaxT) Ͻ0.001 Ϫ0.46 Ϫ0.29 Ϫ0.36 Ϫ0.09 Min precipitation (MinP) Ͻ0.001 Ͻ0.001 0.01 Ϫ0.04 0.02 Max precipitation (MaxP) Ͻ0.001 Ͻ0.001 0.92 Ϫ0.06 0.13 Altitude (Alt) Ͻ0.001 Ͻ0.001 0.59 0.47 Ϫ0.11 Population (Pop) 0.06 0.25 0.78 0.09 0.16

r, above diagonal; p value, below diagonal. tures, Maxent establishes species-environmental rela- cover type, 84 records were in urban area, 28 in crop- tionship, and uses the relationship to deÞne a spatially lands, 16 in evergreen broadleaf forest, 15 in mosaic explicit probability distribution of the environmental area of cropland and natural vegetation, 12 in woody suitability for the modeled species. We assessed the savanna, 9Ð10 in open shrub lands or permanent wet- performance of the model prediction by using the area lands, and 1Ð3 in closed shrub land, evergreen needle under the receiver operating characteristic curve leaf forest, deciduous broadleaf forest, mixed forests, (area under the curve, AUC), a threshold-indepen- or grasslands. There were Ϸ69% (127/184) records dent measure of model performance that measures the found in human modiÞed areas including urban area, degree to which predicted probabilities at random cropland, and mosaic area of cropland and natural occupied points exceed those at random background vegetation. Of the 184 observation locations, annual points (Fielding and Bell 1997). We randomly split the minimum and maximum temperatures were nega- data into training and testing subsets, with 75% of the tively correlated (p Ͻ 0.001; Table 2). Annual mini- presence data to train models and the remaining 25% mum and maximum temperatures were strongly cor- as test cases to calculate AUC. The simulation model related with minimum and maximum precipitation, with all seven environmental factors mentioned above and altitude (p Ͻ 0.001; Table 2). The other environ- was generated Þrst. mental factor pairs did not show a correlation. The Because the Þrst model showed the two anthropo- human population was not correlated with any other genic factors, human population and land cover type, factors (p Ͼ 0.05). Of the seven environmental factors, were dominant, to reveal the habitat suitability with annual minimum and maximum temperatures, mini- limited human inßuence, the second model was gen- mum and maximum precipitation, and altitude are erated with the other Þve climatic and geographic mostly correlated and we considered them as natural factors. For comparison, the third model was gener- factors. Because most termites were found in human ated with the two anthropogenic factors alone. The populated areas, we considered land cover type and reasons why land cover type was categorized as an- human population are anthropogenic factors in this thropogenic factor in current study were further dis- study. cussed in results and discussion section. Model Simulation. All three models resulted in high AUC (0.978, 0.936, and 0.968 for models 1, 2, and 3), suggesting that the predicted probability of habitat Results suitability at observed locations was greater than at Ecological Niche Description. C. gestroi distributed random background points. Predicted current areas of between north and south 35 degree latitude, and over infestation with model 1 (Fig. 1B), which included 88% (163/184) observation locations were at northern seven environmental factors, highly matched the cur- hemisphere (Fig. 1A). Comparison of the six environ- rent observed distribution of C. gestroi (Fig. 1A) with mental factors between the observation points and few exceptions such as southeastern China (Guang- background reference points showed C. gestroi was dong province), Vietnam, Sri Lanka, and Western not homogeneously distributed at terrestrial domain Africa (northern coast of Gulf of Guinea). According (p Ͻ 0.001, SAS NPAR1WAY) (Fig. 2). Most C. gestroi to model 2 (Fig. 1C), which included Þve climatic and was found at warmer areas where the annual minimum geographic factors, the area of suitable habits for C. and maximum temperature were 13.2 Ϯ 6.2 (mean Ϯ gestroi is much larger than its current known distri- SD) and 34.8 Ϯ 4.7ЊC (Fig. 2A,B). These areas were bution (Fig. 1A). Most Southeast Asia, South Asian, recorded with high annual precipitation, 1477.3 Ϯ northern Australia, surrounding areas of Gulf of Mex- 813.4 mm, and the minimum and maximum precipi- ico, Central America, northeast of South America tation in the driest and wettest month were 23.4 Ϯ 33.3 (northeast of Andes Mountains), central and south- mm (Fig. 2C) and 309.4 Ϯ 182.6 mm (Fig. 2D), re- eastern Africa, and Madagascar are suitable habits for spectively. Most records (87%, 160/184) located at low C. gestroi. The prediction with model 3 (Fig. 1D), land areas (Ͻ500 m altitude; Fig. 2E). Over 80% of C. which included only anthropogenic factors such as gestroi records (147/ 183) were found at human pop- human population and land cover type, reconÞrmed ulated areas with over 200 people per square kilome- that the current distribution of C. gestroi is human ter. However, in overall terrestrial domain between mediated. Many developed areas including metropol- north and south 40 degree, only 8% area contains such itan areas in eastern United States, central Europe, high human population density (Fig. 2 F). For land Japan, and northeastern China were under high risk of February 2013 LIETAL:HABITAT SUITABILITY OF Coptotermes gestroi 317

C. gestroi invasion because of high human activity ing C. gestroi, share three biological characteristics: (Fig. 1D, model 3); however, climatic and other geo- feeding on sound wood, nesting in wood, and high graphic conditions of these areas are not suitable for generating supplementary reproductive (Evans its colonization (Fig. 1C, model 2). 2010), which ease their dispersion through anthropogenic transportation and colonization in human mod- Discussion iÞed environment. Sound wood is the common material used for boat and house construction, cargo The historical collection records (Table 1, and cited container, pallet, and furniture. With proper water references) reßect that C. gestroi and its synonymic supply, termite species feeding and nesting in these species had already widely distributed in South Asia wood material and wood products can survive long and Southeast Asia when they were Þrst described distance transportation. Boats and vessel infested by C. between 1895 and 1934. So far, most records (144 of gestroi have been reported from Florida (Scheffrahn 184 counties) are observations made in Asia. Genetic and Su 2005) and from Italy (Ghesini et al. 2011). studies showed C. gestroi collected from non-Asian These boats may be infested through cargos, or during countries could be linked to Asian populations (Jen- termite dispersal ßight seasons, alates might have been kins et al. 2007, Martins et al. 2010), which also sup- attracted by light radiating from boats and then ported the suggestion that Asia is the origin of the formed incipient colonies on boats. After several species. The putative native populations could be fur- years, following generation of alates produced by ma- ther divided into several geographic groups such as ture colonies could ßy out from the boats to another Philippines, Malay Peninsula, Indonesia, and India (Li port. Infested marine hubs have been reported as the et al. 2009; Yeap et al. 2009a, 2010, 2011). However, not source of further dispersion of invasive termite species all currently infested Asian countries are in its native on land (Hochmair and Scheffrahn 2010). In addition, range. Phylogeographic studies using mitochondrial shipping infested wood and wood products are an- gene sequences and microsatellite markers demon- other introduction pathway across natural barriers. strated that C. gestroi invaded Taiwan recently from Termites could forage out of infested woods and ex- the Philippines (Li et al. 2009, Yeap et al. 2011). To tend its territory from wood to soil. Orphaning colony further deÞne the endemic range of C. gestroi, genetic of C. gestroi could produce supplementary reproduc- studies including samples collected from Pakistan in tive caste within a few months (CostaÐLeonardo et al. the west to the Philippines in the east would be nec- 2004), which increases survival rate of introduced essary. The simulation models of the current study colonies. showed C. gestroi may have already occurred in south- A biological invasion event generally included two ern Myanmar, Cambodia, southern Vietnam, and major steps: 1) introduction by human vectors and 2) southern China (Fig. 1B), hence, Þeld survey in these naturalization at nonendemic area (FalkÐPetersen et areas would be crucial for determining its endemic range. al. 2006). In the current study, we could divide the Outside of Asia, C. gestroi was Þrst recorded in Brazil seven environmental factors into two groups for sim- of South America in 1923 and then found at islands of ulating the two steps of its invasion. Human population Caribbean Ocean, Indian Ocean, and PaciÞc Ocean in is related to anthropogenic transportation and hence 1930s. North America is the latest continent inhabited, it is an introduction factor. For the land cover type, reporting invasion in 1990s. Jekins et al. (2007) and most of records (127/184, 69%) were in human de- Martins et al. (2010) attempted to trace the source of veloped area. Based on the observation in newly in- the intercepted or invaded populations of United vaded area, Taiwan (Li et al. 2009), C. gestroi nested States, Australia, Puerto Rico, and Brazil by using in tree trunks and stumps were commonly found not mitochondrial gene sequences. In these two studies, only in urban area but also in nondisturbed environ- only endemic populations from Malay Peninsula were ment that indicates human modiÞed environment is included, hence, other possible sources, such as the not the required factor for its survival. Wood con- Philippines, Indonesia, and India, were excluded. For struction and wood production in urban and devel- further studies, including more native population sam- oped areas were more likely the initial food source for ples and adopting molecular markers with high reso- their early colonization. Observation frequency on lution of population structure such as microsatellite land cover types should represent more on frequency markers (Yeap et al. 2009b) would facilitate our un- of introduction than habitat suitability for establish- derstanding of its historical dispersal route. ment. Model 3 that included human population and The natural dispersal of termite population relies on land cover type predicted introduction frequency of dispersal ßights of the alate caste produced by mature C. gestroi worldwide. However, minimum and maxi- colonies. Compared with other insects, termite alates mum temperature and precipitation, and altitude are are weak ßiers. Most of observed termite species ßew crucial environmental factors for its establishment. less than several hundred meters and only ßy once in Model 2 including the Þve climatic and geographic their life time (Nutting 1969). Hence, it is not easy for factors predicted the habitat suitability for its natu- termites to cross natural barriers, which limited the ralization. Model 1 including all seven anthropogenic, size of their endemic area. To date, only 26 of the climatic, and geographic factors predicts its current around three thousands termite species (Ͻ1%) are infestation in both endemic and invaded area based on invasive species (Evans 2010). These termites, includ- introduction possibility and habitat suitability. 318 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 106, no. 1

By comparing the simulation maps, we found in- tries with high introduction probability and high hab- consistent patterns of the introduction frequency itat suitability could take actions to develop quaran- (model 3) and habitat suitability (model 2). Their tine procedures and to implement construction overlapped areas for these two models include India, practice to reduce its potential damage in advance. Southeast Asian, part of Western Africa, southern China, and scattered spots in Central and South Amer- ica. Some temperate cities with high introduction risk Acknowledgments are located in Europe, United Sates, northeastern We thank our colleagues of Fort Lauderdale Research and China, and Japan. We speculated that if human create Education Center, University of Florid for translating liter- a favorable environment such as indoor heating, local ature and geo-referencing collection location including Ru- infestation may occur in these temperate zone, but dolf Scheffrahn and Dennis Zielstra (German), Natsumi further naturalization is unlikely. However, tropics Kanzaki (Japanese), Thomas Chouvenc (French), Maria Te- and subtropics are under higher risk of C. gestroi es- resa Ferreiar (Portuguese), Garima Kakkar (Indian), and tablishment. Model 2 (Fig. 1C) showed that the pre- Angelica Moncada (Spanish). The authors also thank the two dicted suitable habitat of C. gestroi is much larger than anonymous reviewers and Tonini Francesco and Paul Bar- dunias (University of Florida) reviewing the early version of its current distribution (model 1, Fig. 1B). Continuous this manuscript. This study was supported in part by a grant urbanization and increasing human population in from USDAÐAgriculture Research Services under the grant tropical and subtropical areas will increase its intro- agreement 58-6435-2-276. duction frequency. Once the introduced colonies es- tablished in tropical and subtropical urban area, climatic factors will be unlikely to further limit References Cited naturalization and expansion. Adamson, A. M. 1938. Notes on termites destructive to The congenerous temperate species, C. formosanus, buildings in the Lesser Antilles. Trop. Agric., Trinidad 15: is considered one of the 100 worst invasive species in 220Ð224. the world (Global Invasive Species Database 2010) Adamson, A. M. 1948. Notes on the termite fauna of the because of the substantial damage this species caused Lesser Antilles. Trop. Agric., Trinidad 25: 53Ð55. in the three fast developed and populated countries, Ahmad, M. 1955. Termites of West Pakistan. 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