Journal of Science, (2018) 18(5): 7; 1–10 doi: 10.1093/jisesa/iey092 Research

Presence and Distribution of dorsalis Hood (Thysanoptera: ) in Colombia

Everth Ebratt Ravelo,1,2 Jessica U. Vaca,1 Emilio P. Arévalo,2 Luis Delgado,2 María F. Díaz,2 Laura Piñeros,2 Ángela P. Castro,2 Helena Brochero,1 and Arturo Goldarazena3,4

1Universidad Nacional de Colombia, Bogotà, Colombia, 2Instituto Colombiano Agropecuario ICA, Bogotà, Colombia, 3Biodiversity, Earth and Life Institute – ELIB, Université catholique de Louvain, Louvain La Neuve, Belgium, and 4Corresponding author, e-mail: [email protected]

Subject Editor: Norman Leppla

Received 8 June 2018; Editorial decision 31 August 2018

Abstract The presence and distribution of Scirtothrips dorsalis was reported in Colombia in the Andean, Caribbean, and Orinoquia regions, from 0 to 1,200 meters of altitude (MASL) in the warm climate zone, with less than 2,000 mm rainfall per year and a temperature above 24°C, which corresponds to the tropical dry forest life zone (TDF). Larvae and adults of S. dorsalis were found on 13 plant species belonging to 12 genera in 12 families, of 181 plant species sampled from 129 genera in 47 families sampled. The botanical species with S. dorsalis presence included cotton (Gossypium hirsutum) L., mango () L., chili pepper (Capsicum frutescens) L., bell pepper (Capsicum annuum) L., orange ( sinensis) L., jasmine orange (Murraya paniculata) L., rose (Rosa sp.), and the weeds Sesbania exaltata (Mill.), Phyllanthus niruri L., Ludwigia hyssopifolia Vahl, Euphorbia hypericifolia L., Echinochloa colona L., and Amaranthus spinosus (L.). S. dorsalis prefers young leaves and floral structures, but in cotton it was also associated with squares. The low number of host plants is evident, far from the extensive lists obtained by other authors in other latitudes. S. dorsalis invaded Colombia only in recent years, and this is the first study of the presence and distribution of this in the area.

Key words: distribution, host plant, niche, trips

Resumen Se reportó la presencia y distribución de Scirtothrips dorsalis en Colombia, en las regiones Andina, Caribe y Orinoquia, desde los 0 hasta los 1200 metros de altitud (msnm), en el piso térmico cálido, con precipitación inferior a los 2000 mm anuales y temperatura superior a los 24°C, en correspondencia con la zona de vida bosque seco tropical (bs-T). Se encontraron larvas y adultos de S. dorsalis en 13 especies botánicas, 12 géneros y 12 familias, de las 181 especies botánicas, 129 géneros y 47 familias muestreadas. Las especies botánicas con presencia de S. dorsalis incluyeron el algodón (Gossypium hirsutum) L., mango (Mangifera indica) L., ají (Capsicum frutescens) L., pimentón (Capsicum annuum) L., naranja (Citrus sinensis) L., mirto (Murraya paniculata) L., rosa (Rosa sp.) y las arvenses Sesbania exaltata (Mill.), Phyllanthus niruri L., Ludwigia hyssopifolia Vahl, Euphorbia hypericifolia L., Echinochloa colona y (L.) Amaranthus spinosus (L.). En todas las especies muestreadas, a excepción del algodón, las preferencias por las estructuras vegetales se orientaron por las hojas jóvenes y estructuras florales, en algodón también se asoció a capsulas. Se evidencia el bajo número de plantas hospedantes, distante de los extensos listados obtenidos por otros autores en otras latitudes. El estudio presentado aquí es el primero en Colombia que examina la presencia y distribución de S. dorsalis en áreas que ha invadido en los últimos años.

Palabras clave: distribución, hospedante, nicho, trips

The family Thripidae (Thysanoptera) includes important pests of a abortion of floral structures, flowers, and fruits. In addition, they wide number of cultivated plant species, and much direct damage is can cause indirect damage, such as the transmission of viruses that attributed to them including: distortion of leaves, defoliation, and can affect yield and quality of crops (EFSA 2014). In the global

© The Author(s) 2018. Published by Oxford University Press on behalf of Entomological Society of America. This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs licence (http://creativecommons. 1 org/licenses/by-nc-nd/4.0/), which permits non-commercial reproduction and distribution of the work, in any medium, provided the original work is not altered or transformed in any way, and that the work is properly cited. For commercial re-use, please contact [email protected] 2 Journal of Insect Science, 2018, Vol. 18, No. 5

context, the most important species of Thysanoptera for agricultural species has been recorded in Huila, Tolima, and Vichada departments production are grouped in the genera Caliothrips Daniel, Retithrips (ICA 2012). S. dorsalis is successful in expanding its geographical Marchal, Sericothrips Haliday, Thrips Linneaeus, Frankliniella distribution range due to passive transport through human activi- Karny, and Scirtothrips Shull (Leigh 1995, Mailhot et al. 2007). The ties, new sites to colonize derived by climate change, and the lack of genus Scirtothrips has 100 described species (ThripsWiki 2017), predators or specific plant defenses in its host that restrict its colon- distributed in the tropical and subtropical areas of the world, with ization (Kumar et al. 2013). This could be considered a biological relevant species considered of economic importance for world agri- invasion, as it is a nonnatural distribution process caused by human culture such as Scirtothrips aurantii, Scirtothrips citri, Scirtothrips commercial activity (Gutiérrez 2006). Rodríguez (2006) and Kenis perseae, Scirtothrips inermis, Scirtothrips longipennis, Scirtothrips et al. (2008), recognize that the invasion of ecosystems by introduced mangiferae, Scirtothrips oligochaetus, and Scirtothrips dorsalis species is one of the greatest threats to biodiversity and the structure (Hoddle and Mound 2003, EPPO 2005). of communities, with direct negative impacts of nonnative species on S. dorsalis Hood has been associated with young leaves, flow- the native biota, with effects on predation, hybridization, generation ers, and terminal shoots in more than 200 species of dicotyledonous of changes in ecosystem processes, loss of biodiversity, population plants, in about 40 botanical families (Hoddle and Mound 2003). It imbalances, and competition for habitats. preferentially feeds on the epidermis, and occasionally, on palisade In order to update the status of this economically important spe- tissues in young leaves and tissues of the apex of young fruits, espe- cies in Colombia, the purpose of this study was to determine the cially when they are still hidden under the calyx. In many hosts, it geographical distribution and identification of plants associated can feed on upper surfaces of leaves when the levels of infestation are and nonassociated with S. dorsalis in three ecological regions of high. Larvae and adults are often located toward the main central Colombia where main agricultural crops are established. vein of young leaves or near the damaged area of leaf tissues. Pupae can be found in the leaf litter on the soil, in the axils of the leaves, in Materials and Methods curled leaves or under the calyx (Kumar et al. 2013). The feeding damage of S. dorsalis is characterized by bronzed Geographic Location and Sampling scars on the leaves, petals, and epidermis of fruits. A concentric ring This study was carried out between 2013 and 2016 and is part of is often formed in the scarred tissue around the apex, fruit distor- the doctoral thesis project: Diversity and geographical distribution tion, and premature leaf senescence (Kumar et al. 2013). In add- of Thysanoptera: Tripinae with emphasis on Frankliniella Karny in ition, it has the capacity to transmit phytopathogenic viral particles Colombia. Samples were collected covering ranges of 500 meters of of Tospovirus (= Bunyavirales: Tospoviridae: Orthotospoviruses) altitude from 0 to 3,000 meters above sea level (MASL), in several (Jones 2005, Adams et al. 2017) that cause considerable losses in life zones such as tropical dry forest, lower montane dry forest, lower yields, profitability, and may lead to the implementation of excessive montane moist forest, tropical moist forest, premontane moist for- and restrictive control measures in export markets (Riley et al. 2011, est, premontane very moist forest, premontane pluvial forest, lower Ebratt et al. 2013). montane very moist forest, tropical very dry forest, and premontane S. dorsalis is native to tropical Asia (Dev 1964, Mound and Palmer transitional moist forest in the Andean region; tropical dry forest, 1981) but it currently occurs in , the Solomon Islands, tropical very dry forest, tropical moist forest, premontane dry for- Israel, the Caribbean region (Kumar et al. 2013), North America est, premontane moist forest, tropical thorn forest in the Caribbean (Nietschke et al. 2008) and South America in Surinam, Venezuela region and, the tropical dry forest and the tropical rain forest zone (Cermeli et al. 2009), and Colombia (ICA 2012). In Colombia, this of the Orinoquia region (Holdridge 1967, IAvH 2014) in different

Fig. 1. Presence of S. dorsalis in Colombia: A. Total distribution of sampling points (N = 1,227). B. Points with presence of S. dorsalis in Colombia (N = 169). Table 1. Plants host of S. dorsalis in Colombia in the tropical dry forest (TDF) life zone Journal ofInsectScience, 2018, Vol. 18, No.5

Plant Species Family Region Department Municipality Altitude Latitude Longitude System Number of moni- Number of Number of Number of tored plants occurrence adults larvae

Amaranthus spinosus Amaranthaceae Caribbean Cesar Bosconia 114 10,05258 −73,86875 Weed 4 1 1 6 Capsicum annuum Solanaceae Andean Huila Pital 960 2,18815 −75,81784 Crop 10 1 2 3 Tolima Coello 486 4,27647 −75,01584 10 1 5 5 Capsicum sp Solanaceae Caribbean Bolivar San Jacinto 265 9,82972 −75,13525 Crop 10 1 2 1 Carmen de Bolívar 369 9,73939 −75,23635 10 1 2 1 Citrus sp Rutaceae Caribbean Magdalena Zona Bananera 40 10,76546 −74,14754 Crop 10 1 1 12 Andean Tolima Espinal 318 4,20598 −74,88172 10 1 7 4 Echinochloa colona Poaceae Andean Tolima Espinal 388 4,12716 −74,84169 Weed 3 1 4 5 Euphorbia hypericifolia Euphorbiaceae Andean Huila Villavieja 387 3,19616 −75,22933 Weed 3 1 5 4 Gossypium hirsutum Malvaceae Andean Tolima Armero 312 5,01427 −74,90511 Crop 10 2 5 1 368 5,11144 −74,89405 10 2 6 1 Espinal 318 4,15219 −74,85444 Crop 10 4 74 23 356 4,17713 −74,92647 10 1 3 1 319 4,13430 −74,84708 10 2 27 9 342 4,15691 −74,94863 10 2 4 5 Natagaima 348 3,49755 −75,13863 Crop 10 4 33 7 347 3,50275 −75,14116 10 4 22 2 348 3,50591 −75,13522 10 2 17 2 344 3,48452 −75,13911 10 2 10 8 347 3,49030 −75,13186 10 2 9 4 333 3,68419 −75,10452 10 3 18 9 333 3,67433 −75,10672 10 4 54 2 329 3,67652 −75,10160 10 4 17 4 Coello 263 4,42388 −74,83913 10 1 8 10 Huila Villavieja 374 3,38175 −75,17119 Crop 10 1 3 3 373 3,37544 −75,17169 10 3 6 2 387 3,20475 −75,23777 10 1 1 16 402 3,21501 −75,23422 10 2 7 1 387 3,21638 −75,23098 10 1 9 1 383 3,21877 −75,23001 10 2 7 1 386 3,21363 −75,22788 10 2 29 1 376 3,35444 −75,19886 10 3 15 3 377 3,35588 −75,23041 10 3 12 6 365 3,33069 −75,18863 10 1 2 9 364 3,34506 −75,17505 10 1 3 13 361 3,34829 −75,18559 10 1 4 3 361 3,34933 −75,18137 10 2 6 1 362 3,34813 −75,18202 10 1 5 5 366 3,34512 −75,17342 10 1 4 4 Campoalegre 519 2,69927 −75,35213 Crop 10 4 25 2 518 2,69986 −75,35522 10 3 7 2 509 2,70352 −75,35644 10 2 4 5 498 2,70513 −75,35086 10 3 19 2

507 2,71088 −75,33585 10 2 18 6 3 4 Table 1. Continued

Plant Species Family Region Department Municipality Altitude Latitude Longitude System Number of moni- Number of Number of Number of tored plants occurrence adults larvae

547 2,72230 −75,31708 10 4 17 2 526 2,68813 −75,36094 10 4 32 1 527 2,69208 −75,36188 10 4 17 1 525 2,69238 −75,36008 10 3 15 1 532 2,68472 −75,36677 10 2 7 1 Aipe 371 3,23345 −75,22752 10 1 5 5 Cundinamarca Ricaurte 302 4,28602 −74,74352 Crop 10 2 38 8 301 4,28497 −74,74219 10 2 41 15 301 4,28397 −74,74088 10 2 28 3 305 4,29211 −74,73677 10 2 33 7 311 4,28941 −74,73402 10 2 16 5 345 4,29247 −74,73575 10 1 18 9 283 4,29747 −74,74183 10 4 36 2 291 4,30775 −74,74889 10 3 48 5 297 4,30355 −74,74436 10 1 1 3 290 4,28083 −74,73419 10 1 4 3 Orinoquia Vichada Puerto Carreño 47 6,19768 −67,46557 Crop 10 1 5 3 49 6,19682 −67,46499 10 1 1 1 56 6,25074 −67,53278 10 1 10 1 48 6,19769 −67,46581 10 1 4 3 48 6,19735 −67,46611 10 1 5 5 55 6,25124 −67,53229 10 1 1 5 55 6,25148 −67,53225 10 1 2 10 52 6,19699 −67,46453 10 1 1 1 58 6,25049 −67,53239 10 1 4 4 49 6,19704 −67,46591 10 1 7 2 42 6,19589 −67,46559 10 3 15 7 46 6,20784 −67,48207 10 2 5 1 Journal ofInsectScience, 2018, Vol. 18, No.5 Caribbean Cesar Bosconia-Copey 114 10,05258 −73,86875 Crop 10 1 8 6 Sucre Sampués 111 9,12620 −75,25859 Crop 10 1 0 9 Cordoba Montería 17 8,77209 −75,88448 Crop 10 3 11 3 12 8,74107 −75,80349 10 8 170 1 11 8,78275 −75,85408 10 7 84 7 Ludwigia hyssopifolia Onagraceae Andean Tolima Espinal 388 4,12716 −74,84169 Weed 5 1 3 4 Mangifera indica Anacardiaceae Caribbean Magdalena Zona Bananera 40 10,76546 −74,14754 Crop 10 1 29 2 Andean Tolima Coello 486 4,27647 −75,01584 10 1 3 5 Murraya paniculata Rutaceae Caribbean Magdalena Zona Bananera 40 10,76546 −74,14754 Backyard 10 1 1 5 Phyllanthus niruri Euphorbiaceae Andean Tolima Armero 368 4,68061 −74,90861 Weed 3 1 4 3 Rosa sp Rosaceae Caribbean Bolivar Carmen de Bolívar 310 9,73419 −75,22069 Backyard, 4 1 3 13 Andean Tolima Flandes 302 4,23245 −74,86134 Garden 5 1 4 21 Guamo 303 4,01634 −74,92001 5 1 2 14 Sesbania exaltata Fabaceae Andean Huila Villavieja 383 3,21127 −75,22466 Weed 1 1 7 2

TOTAL 809 169 1267 424 Journal of Insect Science, 2018, Vol. 18, No. 5 5 agro-ecosystems of the Andean, Caribbean, and Orinoquia regions identified. The specimens were cleared in cold 5% KOH, followed of Colombia (Fig. 1A). by washing with distilled water. Subsequently, larvae and adults For the development of the monitoring activities, we conducted were mounted in Hoyer’s medium in slides, and dried in the oven collection tours to each geographical region and in different agricul- for 48 h at 35–40°C, according to Mound and Marullo (1996). Few tural areas of 23 departments in Colombia. Six agricultural crops specimens of each species were mounted in Canada Balsam for the were selected, 10 plants per hectare were sampled and in each plant permanent collection according to Mound and Marullo (1996). three structures. For the weeds and wild plants one to five plants The taxonomic determination of adults was carried out based on were sampled. In total, 11,590 of entomological samples were col- morphological characters according to available keys (Hoddle and lected in 4,555 monitoring points; 674 entomological samples cor- Mound 2003, Kumar et al. 2013) and larvae were identified based responded to cotton, 33 to chili pepper, 33 to bell pepper, 221 to on Vierbergen et al. (2010) with the help of a Leica ZOOM 2000 mango crops, 75 to orange, 225 to rose flower, 608 for weeds, and stereoscope and a Nikon morphological type-119YS2-T microscope. 9,721 to other plant species. Samples were collected by beating of leaves, floral structures, and Identification of Plants fruits in different agricultural production systems, in weeds, back- Taxonomic keys of the Flora of Colombia were used (Gentry 1996, yard, and wild plants using a 000 caliber brush moistened with 70% Bernal et al. 2015) and comparisons were made with the herbarium ethanol, and white plastic plates were used to collect the individu- of the Institute of Natural Sciences of the National University of als. Finally, the specimens were deposited in 1.5 ml Eppendorf tubes Colombia. with 70% ethanol. Each sample was assigned with a unique identi- fication code. Data Analysis The association of S. dorsalis with the plants according to the Treatment of the Sample botanical family, genus, species, and plant structure was also deter- From the specimens obtained, the larval stages were separated from mined. Based on the abundance of adults in plant structures (young the adults. The thrips were sorted by morphotypes and they were leaf, floral bud, flower, and fruit), the similarity among them was

10 11 9 8 9 e e 7 6 7 5 5 Abundanc

Abundanc 4 3 3 2 1 1 1001000 1001000 Altitude (masl) Precipitation(mL)

Correlations ValidSpearmant(N-2)p-level 20 Altude/Abundance295 -0.8003-22.850, 00001 Abundance/Temperature 2950.778821.25 0, 00001 Abundance/Precipitaon295 -0.4553-8.75 0, 00001

Abundance Abundance/Altude 295-0.8003 -22.85 0, 00001

1 35 30 25 20 15 Temperature °C

Fig. 2. Abundance of S. dorsalis in correlation with altitude (MASL), average annual temperature (°C), and average annual precipitation in Colombia.

1 0.40

0.8 0.30 y

y 0.6

0.4 0.20 Probabilit Probabilit 0.2 0.10 0 51015202530 -0.2 0.00 01000200030004000 Temperature °C Altitude (m)

Fig. 3. Estimated probability of the presence of S. dorsalis in Colombia, at different temperatures (°C) (N = 1,057; r2 = 0.8462; area under the curve (AUC) = 0.760; P < 0.0001) and altitudinal gradient in meters (N = 1057; r2 = 0.9987; AUC = 0.685; P = 0.001). 6 Journal of Insect Science, 2018, Vol. 18, No. 5 determined by means of Bray–Curtis similarity index (Ramirez S. dorsalis prefers young leaves (38.46%, n = 65 occurrence), fol- 2006, Pulido et al. 2015). The presence of S. dorsalis was correlated lowed by flowers (22.48%, n = 38 occurrence), fruits (21.89%, with the climatic variables temperature (°C—annual average), pre- n = 37 occurrence in cotton squares), and flower buds (17.16%, cipitation (mL—annual average), and altitude (MASL) by means of n = 29 occurrence). The Bray–Curtis similarity index showed that Spearman ranges; in addition, the probability of encounter based on S. dorsalis preferred young leaves and buds, compared with the other the climatic variables was determined through logistic regressions. structures of the host plants (Fig. 4). The software ArcGIS 10.1 (ArcMap version 10.1), and the programs In this study, S. dorsalis is nonhost in 175 botanical species in STATISTICA v10, InfoStat v2008, Past v3, and SAS v9.2 were used. 119 genera (Table 2).

Results Presence of S. dorsalis in Colombia Discussion The presence of larvae and adults of S. dorsalis was recorded in 169 Presence of S. dorsalis in Colombia (13.77%) of 1227 sampled sites (Fig. 1A). One hundred and thirty S. dorsalis is a nonnative polyphagous species of recent report in two sampled sites (78.24%) in the Andean region, especially in the Colombia (Seal et al. 2010, ICA 2012) with a high capacity to warm valley of the upper Magdalena (departments of Tolima, Huila, occupy large areas and geographic distribution. It is also a species and Cundinamarca); 27 (15.88%) in the Caribbean region in the with a high degree of environmental and phytosanitary risk since departments of Córdoba, Sucre, Bolívar, Magdalena, and Cesar; it could generate negative effects on the native flora and on the and 10 (5.88%) in the Orinoquia region, in the natural savannah expected yields in cultivated plants of economic interest for the agri- of the municipality of Puerto Carreño, northeast of the department culture of Colombia. It is evident that the introduction and establish- of Vichada (Fig. 1B). All samples of S. dorsalis were collected in the ment of species such as S. dorsalis would be able to affect existing tropical dry forest life zone (TDF). trophic networks and could alter processes of population dynamics that allow the regulation of species (Morse and Hoddle 2006). Geographic and Altitudinal Distribution The presence of S. dorsalis in the warm climate zone of the Andean, S. dorsalis was reported in the Andean, Caribbean, and Orinoquia Caribbean, and Orinoquia regions of Colombia, in tropical dry forest regions with an estimated altitudinal distribution from 0 to 1,200 areas (TDF) (Holdridge 1967), coincides with the results obtained by meters (n = 295; r = −0.8003; P = 0.00001), average annual tem- other authors (Cermeli et al. 2009) and could provide elements to char- peratures higher than 24.4°C (n = 295; r = 0.7789; P = 0.00001), acterize and potentially delimit the occupation and invasion areas, by and average annual precipitation less than 1683.4 ml (n = 295; recognizing the optimal climatic variables of its ecological niche. In r = −0.4554; P = 0.00001) (Table 1, Fig. 2). The logistic regres- Colombia, tropical dry forests correspond to a plant formation that presents a continuous, nondense forest cover. They are distributed sion model adjusted for the variable temperature (P (S. dorsalis) = 1/1 + e−(−31.798 + 1.237)) suggests that there is a probability ≥50% between 0 and 1,000 MASL, with one or two periods of drought per (r2 = 0.8462, area under the curve (AUC) = 0.760; P < 0.001) of absence of S. dorsalis in areas with temperature ≤20°C, and altitud- −(−0.813 − 0.002) inal ranges above ≥1,200 MASL (P (S. dorsalis) = 1/1 + e ) (r2 = 0.9987; AUC = 0.685; P = 0.001) (Fig. 3).

Distribution According to the Life Zone One hundred percent (100%) of the positive reports of S. dorsalis were located in the TDF in the Andean, Caribbean, and Orinoquia regions (Table 1).

Host Botanical Species and Preferences for Structures Of the 184 botanical species sampled, which were grouped into 131 genera and 44 families, S. dorsalis was found in 13 species of 12 gen- era and 10 botanical families, all angiosperms. The 13 botanical spe- cies were related to agricultural systems in cotton, orange, bell pepper, chili pepper, and mango crops; the presence in plants of Rosa spp. It was also evidenced in gardens and backyards in the municipalities of Carmen de Bolívar (Department of Bolívar, Caribbean region), Flandes, and Guamo (Department of Tolima, Andean region). All plant species with presence of S. dorsalis corresponded to true host plants due to the report of larvae stages and suggest a first list of host plants for the presence in the botanical families Malvaceae, Anacardiaceae, Solanaceae, Rutaceae, Poaceae, Amaranthaceae, Euphorbiaceae, Onagraceae, Rosaceae, and Fabaceae (Table 1). Larvae and adult stages of S. dorsalis were found in leaves, flower buds, and squares of cotton (Gossypium hirsutum); in leaves Fig. 4. Preferences for plant structures, using the Bray–Curtis similarity and inflorescences of mango (Mangifera indica) crop; in leaves and index in 13 botanical species associated with S. dorsalis in three geographic flowers of orange (Citrus sinensis), and in leaves and flowers of bell regions of Colombia (N = 169; Cophenetic corr. = 0.948; read cases = 169; pepper and chili pepper (Capsicum annuum, Capsicum frutescens). omitted cases = 0; P < 0.05). Journal ofInsectScience, 2018, Vol. 18, No.5 Table 2. Species and botanical families sampled and nonhost with S. dorsalis in the Andean (A), Caribbean (C), and Orinoquia (O) regions

Plant species Family Region Number of Plant species Family Region Number of Plant species Family Region Number of monitored plants monitored plants monitored plants

Acacia sp Fabaceae A 2 Emilia sp Asteraceae A,O 2 Pisum sativum Fabaceae A 5 Ageratum sp Asteraceae C 1 Euphorbia catinifolia Euphorbiaceae C,O 2 Pithecellobium A 1 guachapele Allium cepa Amaryllidaceae A 4 Euphorbia C 1 Priva lappulacea Verbenaceae A 1 heterophylla Allium fistulosum A 1 Euphorbia hirta A 5 Prunus domestica Rosaceae A 2 Allium sativum A 3 Euphorbia postrata A 1 Prunus persica A 3 Amaranthus sp A 1 Fragaria ananassa Rosaceae A 1 Prunus sp A 1 Amaranthus dubius A 5 Funastrum clausum Apocynaceae C 1 Psidium guajava Myrtaceae O 9 Anthurium sp Araceae A 1 Furcraea andina Asparagaceae A 4 Pyrus communis Rosaceae A 1 Arachis pintoi Fabaceae A, C 4 Furcraea sp A 1 Quercus sp Fabaceae C 2 Asparagus Asparagaceae A 1 Galinsoga parviflora Asteraceae A 1 Raphanus Brassicaceae A 7 officinalis raphanistrum Baccharis prunifolia Asteraceae A 1 Galinsoga sp A 1 Raphanus sp A 5 Bauhinia forficata Fabaceae C 1 Gliricidia sepium Fabaceae A,C,O 9 Rhynchosia minima Fabaceae A,C 7 Bidens pilosa Asteraceae A 1 Hedychium Zingiberaceae A 1 Ricinus communis Euphorbiaceae A 1 coronarium Bixa orellana Bixaceae A 10 Helianthus annuus Asteraceae A 1 Rubus glaucus Rosaceae A 26 Boerhavia Nyctaginaceae A 1 Heliotropium Boraginaceae A,C 3 Rubus sp A 1 decumbens angiospermum Boerhavia erecta A 1 Heliotropium indicum C 1 Ruellia tuberosa Acanthaceae A 1 Borreria capitata Rubiaceae C 2 Heliotropium sp A 1 Ruta sp Rutaceae A 1 Borreria laevis A 1 Hemigraphis alternata Acanthaceae C 1 Sambucus sp Adoxaceae O 1 Brassica rapa Brassicaceae A 1 Hevea brasiliensis Euphorbiaceae O 5 Sarcostemma Apocynaceae A 1 clausum Caesalpinia coriaria Fabaceae C 1 Holcus lanatus Poaceae A 1 Saurauia scabra Actinidiaceae A 1 Caesalpinia sp C 1 Hypochaeris radicata Asteraceae A 1 Scoparia dulcis Scrophylariaceae A 1

Calliandra C 1 Hyptis mutabilis Lamiaceae C 1 Senna occidentallis Fabaceae A 1 surinamensis Calliandra trinervia C 1 Inga densiflora Fabaceae C 1 Senna sp A,C 7 Calotropis gigantea Apocynaceae C 2 Inga edulis A 2 Senna viarum A 1 Canna indica Cannaceae A 1 Ipomoea pes-caprae Convolvulaceae O 3 Sida acuta Malvaceae A 1 Cannabis sp Cannabaceae A 1 Ipomoea sp A 1 Sida parviflora A 1 Cassia Fabaceae A 1 Kallstroemia maxima Zygophyllaceae A 2 Sida rhombifolia A 2 aeschynomene Cassia fistula C 1 Lachemilla orbiculata Rosaceae A 1 Silybum marianum Asteraceae A 1 Centrosema A 2 Lactuca sativa Asteraceae A 1 Solanum tuberosum Solanaceae A 8 acutifolium Chamaecrista sp C 1 Lagascea mollis A 2 Solanum A 1 crotonifolium Chrysanthemum sp Asteraceae A 2 Lantana camara Verbenaceae A 3 Solanum A 5 lycopersicum 7 Table 2. Continued 8

Plant species Family Region Number of Plant species Family Region Number of Plant species Family Region Number of monitored plants monitored plants monitored plants

Chrysobalanus Chrysobalanaceae A, C 2 Lantana sp A 1 Solanum melongena A,C 6 icaco Cissus verticillata Vitaceae A 1 Leptochloa scabra Poaceae A 11 Sorghum bicolor Poaceae C 1 Citrullus lanatus Cucurbitaceae O 1 Licania sp Chrysobalanaceae C 1 Sphagneticola Asteraceae A 2 trilobata Citrus aurantifolia Rutaceae A 6 Ludwigia sp Onagraceae A 1 Spinacia oleracea Amaranthaceae A 1 Citrus latifolia A,C,O 8 Malus sylvestris Rosaceae A 1 Tabebuia rosea Bignoniaceae C 1 Citrus limon A 2 Malus domestica A 1 Tachigali guianensis Fabaceae A,O 4 Citrus reticulata A,O 5 Malvastrum Malvaceae A 3 Talinum fruticosum Portulacaceae A 2 americanum Citrus sinensis A,C,O 35 Malvaviscus A 1 Talinum paniculatum A 1 concinnus Cleome affinis Cleomaceae A 1 Manihot esculenta Euphorbiaceae A,C,O 50 Tamarindus indica Fabaceae C 1 Cleome spinosa C 1 Melochia parvifolia Malvaceae A 6 Taraxacum officinale Asteraceae A 5 Cleoserrata sp A 1 Melochia pyramidata A 2 Taraxacum sp A 1 Cnidoscolus urens Euphorbiaceae A 1 Momordica charantia Cucurbitaceae A 2 Tecoma stans Bignoniaceae A 2 Coffea arabica Rubiaceae A,C 31 Musa paradisiaca Musaceae A,C,O 65 Tephrosia sp Fabaceae A 1 Cordia alliodora Boraginaceae A 1 Musa sp C,O 2 Thevetia peruviana Apocynaceae A 1 Cordia dentata C 7 Nicotiana tabacum Solanaceae A,C 2 Tithonia diversifolia Asteraceae A,O 4 Coriandrum Apiaceae A 3 Parthenium Asteraceae A 1 Tithonia sp A,O 2 sativum hysterophorus Crescentia cujete Bignoniaceae C 1 Passiflora edulis Passifloraceae A,C,O 39 Tridax procumbens A,C 6 f. flavicarpa Crotalaria juncea Fabaceae A 1 Passiflora edulis Sims A 2 Trifolium pratense Fabaceae A 3 Croton leptostachys Euphorbiaceae A 1 Passiflora ligularis A 4 Trifolium repens A 4 Cyathula Amaranthaceae A 1 Passiflora maliformis O 2 Trifolium sp A 5

achyranthoides Journal ofInsectScience, 2018, Vol. 18, No.5 Dahlia sp Asteraceae A 3 Passiflora O 1 Turnera ulmifolia A 1 quadrangularis Daucus carota Apiaceae A 1 Passiflora tarminiana A 3 Vicia faba A 6 Delechampia Euphorbiaceae A 1 Pavonia sepium Malvaceae A 1 Zantedeschia Araceae A 2 scandens aethiopica Dioclea sp Fabaceae A 2 Persea americana Lauraceae A,C,O 151 Zea mays Poaceae A,C,O 48 Eclipta alba Asteraceae A 1 Phaseolus vulgaris Fabaceae A,C 19 Emilia sonchifolia A,C,O 12 Physalis sp Solanaceae A 1 Journal of Insect Science, 2018, Vol. 18, No. 5 9 year; they consist of 8,146,000 hectares, which correspond to 11.3% Alves-Silva et al. 2013, Burckhardt et al. 2014). Our results are of the territory of Colombia and have distinctive floristic and faunal far less diverse than the reports of CABI (2018) and USDA-APHIS affinities compared to other life zones (IAVH 2014). According to (2006), since S. dorsalis infests a wide variety of host plants Hernández (1990), this formation is also known as moist temperate belonging to more than 100 plant taxa among 40 families (Mound forest, tropical deciduous forest, or drought-deciduous tropical low- and Palmer 1981). These records does not necessarily make them land forest in other classification systems. These forests are currently true host plants, without the evidence of immature states present under a high degree of intervention, degradation, use, and extensive in them. The above is relevant, considering that Colombia is the over exploitation for agricultural and livestock production. second country with the highest plant biodiversity in the world, with heterogeneous local habitats and isolations, which histori- Geographic and Altitudinal Distribution cally have favored high rates of speciation and endemism in many Taking into account the objective sampling area that was included taxa, benefited by the of climates, floristic mosaics, and biogeo- in this study and that the first report for Colombia was in the year graphical overlaps between the Andean, Orinoquia, Guyanese, 2012, it was determined that S. dorsalis is not widely distributed, Caribbean, Pacific, and Amazonia regions (Gentry 1988, Josse possibly due to the negative influence of climatic conditions and the et al. 2012). presence of different geographic barriers. S. dorsalis showed preferences for young leaves and flower Temperature is important for the developmental rate of S. dor- buds of different crops, weeds, and wild plants. The preferences for salis with a critical threshold between 9.7 and 32°C with an opti- structures were oriented toward young leaves and flower buds in mal generation rate of 25°C (Tatara 1994, Shibao 1996). In this chili pepper, bell pepper, mango, jasmine orange, orange, and rose. study, this species was found in an average temperature of 24.4°C In cotton crops, it was reported in the young leaves, flower buds, in all ecological regions, which means an advantageous condition and fruits. This agrees with Seal et al. (2006) and this species pre- for its establishment. Additionally, S. dorsalis density has been pos- fers to feed on tender tissues in young leaves in some plant species, itively correlated with temperature but negatively correlated with and could be limited by the adverse conditions to low temperatures relative humidity and precipitation (Mannion et al. 2014). Because and high rainfall. In general, young leaves infested by thrips have the Andean and Caribbean regions are characterized by a bimodal high contents in soluble protein and total nitrogen (Paine 1992). precipitation regimen with changing seasonal average temperatures, Schoonhoven et al. (2005) propose that high concentrations of sec- but Orinoquia regions have a monomodal rain regime between April ondary metabolites support the direct defense of the plant, which is and November with more constant average temperature throughout effective against several species of herbivores, so insect populations the year (Pacheco and León-Aristizabal 2001), we expect that geo- must develop efficient strategies for detoxification or regulation of graphical dispersion and establishment of S. dorsalis will be differ- their intake. ential for these three regions. It is evident that S. dorsalis does not adapt to cold environments Acknowledgments with minimum daily temperatures of −4°C for at least 5 d a year; however, in subtropical and tropical environments with warm cli- We thank the officials of the Colombian Agricultural Institute in the differ- mate and prolonged droughts, 18 generations can be obtained per ent departmental sections, the Faculty of Agricultural Sciences, Bogotá at the National University of Colombia, Bogotá headquarters, the company year with high population densities (Nietschke et al. 2008, Kumar BIOQUALITY AGRO, and the growers in all the regions visited, for the sup- et al. 2013). Seal et al. (2010) determined that, under the influence of port during the field activities necessary to the development of this work. We subtropical environmental conditions, S. dorsalis could reach a gen- thank to Prof. Dr. Thierry Hance for a critical review of the manuscript and eration every 27 d, at temperatures >20°C with food sources pref- provide funds for publishing. erably based on young tissue of host plants such as jalapeño pepper and rose. This circumstance makes the arrival of S. dorsalis, like the Literature Cited arrival of any other invasive organism, reach a level of important phytosanitary risk, given the difficulty to evaluate the impacts gener- Adams, M., E. Lefkowitz, A. King, B. Harrach, R. Harrison, N. Knowles, ated on natural, intervened, and agricultural ecosystems. A. Kropinski, M. Krupovic, J. Kuhn, A. Mushegian, et al. 2017. Changes to and the international code of virus classification and nomen- Climatic conditions, which could restrict the presence and estab- clature ratified by the International Committee on Taxonomy of Viruses lishment of populations of S. dorsalis in the geography of Colombia, (2017). Arch. Virol. 162: 2505–2538. have to do with average annual temperatures below 24°C, rain- Alves-Silva, E., P. K. Maruyama, A. Cavalleri, and K. Del-Claro. 2013. fall above 2,000 mm per year and interactions related to the alti- Flower stage and host plant preference by floral herbivore thrips (Insecta: tude-temperature at altitudes above 1,200 MASL. These conditions Thysanoptera: Frankliniella) in a Brazilian savanna. Stud. Neotrop. Fauna could negatively influence the biology and behavior of the insect and Environ. 48: 25–31. become a natural environmental limit for the distribution, estab- Bernal, R., S. R. Gradstein, and M. Celis. (eds.). 2015. Catálogo de plantas lishment, and reproduction of the species, since they become unfa- y líquenes de Colombia. Instituto de Ciencias Naturales, Universidad vorable habitats (Nietschke et al. 2008). According to Pulido et al. Nacional de Colombia, Bogotá. http://catalogoplantasdecolombia.unal. (2015), to determine these habitats, it is necessary to make predic- edu.co. Burckhardt, D., D. Ouvrard, D. Queiroz, amd D. Percy. 2014. Psyllid host- tive models to recognize the distribution according to the ecological plants (Hemiptera: Psylloidea): resolving a semantic problem. Fla. niches and potential occupation areas of S. dorsalis. Entomol. 97: 242–246. CABI. 2018. Scirtothrips dorsalis (chilli thrips). In Invasive species compen- Host Botanical Species and Preferences for dium. CAB International, Wallingford, UK. www.cabi.org/isc. Cermeli, M., J. Perozo, and L. Piñango. 2009. Scirtothrips dorsalis Hood Structures (Thysanoptera, Thripidae) nuevo insecto plaga del algodonero (Gossypium The larval stages of S. dorsalis were found in 13 plant species that hirsutum L.) en Venezuela. Entomotropica 24: 85–88. constitute a true hosts (Table 1), where S. dorsalis can develop and Dev, H. 1964. Preliminary studies on the biology of the assam thrips, complete its life cycle (Mound and Marullo 1996, Marullo 2004, Scirtothrips dorsalis Hood, on tea. Indian J. Entomol. 26: 184–194. 10 Journal of Insect Science, 2018, Vol. 18, No. 5

Ebratt, E., R. Acosta, O. Martínez, O. Guerrero, and W. Turizo. 2013. Tomato Mailhot, D. J., J. J. Marois, and D. L. Wright. 2007. Influence of flower thrips spotted wilt virus (TSWV), weeds and thrip vectors in the tomato (Solanum on Fusarium hardlock severity. Plant Dis. 91: 1423–1429. lycopersicum L.) in the Andean region of Cundinamarca (Colombia). Mannion, C., A. Derksen, D. Seal, L. Osborne, and C. Martin. 2014. Agronomía Colombiana. 31: 58–67. Population dynamics of Sirtotrhips dorsalis (Thysanoptera: Thripidae) EFSA. 2014. Scientific opinion on the pest categorisation of Scirtothrips dor- and other thrips species on two ornamental host plant species in Sourthen salis. EFSA panel on plant health (PLH). EFSA J. 12: 3915. Florida. Environ. Entomol. 43: 849–858. EPPO. 2005. Scirtothrips aurantii, S. citri, S. dorsalis. Bulletin OEPP/EPPO, Marullo, R. 2004. Host-plant range and relationships in the Italian thrips PM 7/56: 353–356. fauna. Acta Phytopathol. Entomol. Hung. 39: 243–254. Gentry, A. H. 1988. Changes in plants community diversity and floristic com- Morse, J. G., and M. S. Hoddle. 2006. Invasion biology of thrips. Annu. Rev. position on environmental and geographical gradients. Ann. Missouri Bot. Entomol. 51: 67–89. Gard. 75: 1–34. Mound, L. A., and R. Marullo. 1996. The thrips of Central and South America: Gentry, A. 1996. A field guide to the families and genera of woody plants of an introduction. Memoirs on Entomology, International, Gainesville, FL. North West South America: (Colombia, Ecuador, Peru with Supplementary pp. 6, 488. Notes Herbaceous Taxa). The University of Chicago Press. pp. 920. Mound, L. A., and J. M. Palmer. 1981. Phylogenetic relationships between Gutiérrez, F. 2006. Estado de conocimiento de especies invasoras. Propuesta some genera of Thripidae (Thysanoptera). Entomol. Scand. 15: 153–617. de lineamientos para el control de los impactos. Instituto de Investigación Nietschke, B. S., D. M. Borchert, R. D. Magarey, and M. A. Ciomperlik. de Recursos Biológicos Alexander von Humboldt, Bogotá D.C., Colombia. 2008. Climatological potential for Scirtothrips dorsalis (Thysanoptera: pp. 158. Thripidae) establishment in the United States. Fla. Entomol. 91: 79–86. Hernández, C. 1990. La selva en Colombia, pp. 13–40. In C. Hernández and Pacheco, Y., and G. León-Aristizabal. 2001. Clasificación climática de la J. Carrizosa (eds.), Selva y futuro. Sello Editorial, Bogotá. Orinoquia Colombiana a partir de los patrones de circulación atmosférica. Hoddle, M. S., J. M. Heraty, P. F. Rugman-Jones, L. A. Mound, and Meteorol. Colomb. 4: 117–120. R. Stouthamer. 2008. Relationships among species of Scirtothrips Paine, T. 1992. Cuban laurel thrips (Thysanoptera: Phlaeothripidae) biology in (Thysanoptera: Thripidae, ) using molecular and morphological Southern California: seasonal abundance, temperature dependent develop- data. Ann. Entomol. Soc. Am. 101: 491–500. ment, leaf suitability, and predation. Ann. Entomol. Soc. Am. 85: 164–172. Holdridge, L. R. 1967. Life zone ecology. In: Instituto Geográfico Agustin Pulido, H. L., A. A. Rudas, J. A. Betancourt, W. E. Grant, and S. J. Vilchez. Codazi, 2004. Tropical Science Center, San José, Costa Rica. http://www. 2015. Distribución inusual y potencial de la garrapata común del ganado, igac.gov.co/igac. Rhipicephalus (Boophilus) microplus, en zonas tropicales de alta montaña IAvH. 2014. El bosque seco tropical en Colombia, p. 349. In C. Pizano and de los Andes colombianos. Biota Colombiana. 16: 75–95. H. García (ed.). El bosque tropical seco en Colombia, memoria técnica Ramirez, G. A. 2006. Ecología: Métodos de muestreo y análisis de pobla- para la verificacion en campo del mapa del bosque seco tropical en ciones y comunidades. Editorial Pontificia Universidad Javeriana, Bogotá, Colombia Escala 1:100.000. Bogotá, Colombia. http://www.humboldt. Colombia. pp. 273. org.co/images/documentos/pdf/investigacion/gonzalez-m-et-al-2014-me- Riley, D. G., V. J. Shimat, R. Srinivasan, and S. Diffie. 2011. Thrips vectors of moria-tecnica-verificacion.pdf tospoviruses. J. Integr. Pest Manag. 2: 1–10. ICA. 2012. Situación actual del trips amarillo del ají Scirtothrips dor- Rodríguez, L. F. 2006. Can invasive species facilitate native species? Evidence salis (Hood) (Thripidae:Thripinae) en Colombia. Boletin epidemi- of how, when, and why these impacts occur. Biol. Invasions 8: 927–939. ológico. ICA. Bogotà, Colombia. https://www.ica.gov.co/Areas/Agricola/ Schoonhoven, L. M., J. van Loon, and M. Dicke. 2005. Insect plant biology. Servicios/Epidemiologia-agricola/BOLETINES/Nacionales/2012/B_N_ Oxford University Press, UK. pp. 421. SDORSALIS_DIC_2012.aspx. Seal, D. R., M. Ciomperlik, M. L. Richards, and W. Klassen. 2006. Distribution Jones, D. R. 2005. Plant viruses transmitted by thrips. Eur. J. Plant Pathol. of chilli thrips, Scirtothrips dorsalis (Thysanoptera: Thripidae), in pepper 113: 119–157. fields and pepper plants on st. Vincent. Fla. Entomol. 89: 311–320. Josse, C., F. Cuesta, G. Navarro, V. Barrena, M. Becerra, E. Cabrera, Seal, D. R., W. Klassen, and V. Kumar. 2010. Biological parameters of E. Chacón-Moreno, W. Ferreira, M. Peralvo, J. Saito, et al. 2012. Scirtothrips dorsalis (Thysanoptera: Thripidae) on selected hosts. Environ. Physical geography and ecosystems in the tropical andes. Chapter 10, Entomol. 39: 1389–1398. pp. 152–169. In Sebastian K. Herzog Rodney Martinez, Peter M. Shibao, M. 1996. Effects of temperature on development of the chili thrips, Jørgensen, Holm Tiessen (eds.), Climate Change and Biodiversity in Scirtothrips dorsalis Hood (Thysanoptera: Thripidae), on grape. Appl. the Tropical Andes. http://www.infobosques.com/descargas/biblio- Entomol. Zool. 31: 81–86. teca/214.pdf Tatara, A. 1994. Effect of temperature and host plant on the development, Kenis, M., M. A. Auger-Rozenberg, A. Roques, L. Timms, C. Péré, M. J. Cock, fertility and longevity of Scirtothrips dorsalis Hood (Thysanoptera: J. Settele, S. Augustin, and C. Lopez-Vaamonde. 2008. Ecological effects Thripidae). Appl. Entomol. Zool. 29: 31–37. of invasive alien . Biol. Invasions 11: 21–45. ThripsWiki. 2017. Thripidae. http://thrips.info/w/index.php?title= Kumar, V., G. Kakkar, C. Mckenzie, D. R. Seal, and L. S. Osborne. 2013. An Thripidae&oldid=33251. overview of chilli thrips, Scirtothrips dorsalis (Thysanoptera: Thripidae) USDA-APHIS. 2006. Scirtothrips dorsalis Hood: chilli thrips Thysanoptera/ biology, distribution and management, pp. 53–77. In S. Soloneski and M. Thripidae. NEW PEST ADVISORY GROUP (NPAG) Plant Epidemiology Larramendy (ed.), Weed and pest control - Conventional and new chal- and Risk Analysis Laboratory Center for Plant Health Science & lenges. Intech, Rijeka, Croatia. Technology, North Carolina, United States. pp. 1–7. Leigh, T. F. 1995. Bionomics of cotton thrips: a review, pp. 61–70. In B. Vierbergen, G. B., H. Kucharczyk, and W. D. J. Kirk. 2010. A key to the L. Parker, M. Skinner and T. Lewis (eds.), Thrips biology and management. second instar larvae of the Thripidae of the Western Palaearctic región Springer Science & Business Media, New York. (Thysanoptera). Tijdschr. Entomol. 153: 99–160.