Potential Distribution in Mexico of Diaphorina citri
Contents
1. EE oo 20 20 0 400 SS _ erre Hos Kilometers Fig 4 Climatic suitability map for Diaphorina citri growth as a function of temperature in Mexico Quijano et al Potential distribution of Diaphorina citri in Mexico 43 Index of favorable temperatures for vector oviposition IFTVO 7 state division E Hl 0 01 GH 01 02 HM 02 03 E 03 0 4 5 0 4 0 5 05 06 E os 0 7 E 07 08 0 8 0 9 400 200 o 400 a A aa 09 1 Kilometers Fig 5 Climatic suitability map for Diaphorina citri oviposition as a function of temperature in Mexico Index of potential generations for the asian citrus psyllid INPGV state division Ho EE 0 01 MA o 0 gt WM 02 03 03 04 04 05 05 06 os o 7 HI 07 08 HE 08 09 MN O Fig 6 Climatic suitability map showing the different numbers of generations of Diaphorina citri in various areas of Mexico The number of generations are depicted as follows purple 0 blue 3 blue green 5 dark green 8 medium green 10 light green 13 yellow 16 orange 19 pink 22 red 25 and brown 27 44 Florida Entomologist 96 1 Index of climatic suitability i for the asian citrus psyllid ics __ state division E HM 0 0 GM 01 02 HM 02 03 0 3 0 4 04 05 E 05 06 EJ os 0 7 E 07 08 MA os 0 9 400 200 o EE 09 1 March 2013 400 EA Kilometers Fig 7 Climatic suitability map for Diaphorina citri and citrus as a2. perform the analysis Mapping Procedure Maps were created using the software Arc Map ver 10 1 Every factor considered to affect March 2013 the D citri potential distribution was treated as an independent information layer or shape In the case of host availability data consisted on planted area with citrus species at the municipality level This shape was overlaid with the land use layer to acquire the agricultural land where citrus is present Data were interpolated using the inverse distance weighted procedure Shepard 1968 Weather data were analyzed at a daily level and the different indexes were calculated for ev ery yr of the time series for every weather sta tion The curve of probability of exceedance was calculated for every station and the values of the indexes corresponding to the 80 of probability were used to elaborate the maps To analyze the plausibility of the proposed re gionalization the actual distribution of HLB was considered as a reference Fig 1 and Suppl Fig 1 show the sites with HLB detections in Mexico from Mar 2009 to Dec 2011 The Yucatan Penin sula and the Middle Western coast of the Pacific Ocean with a tropical climate are the most af fected areas by HLB In some other areas Clas positive psyllids have been found but not infected trees RESULTS AND DISCUSSION The results of the 56 810 simulations for the 4 criteria analyzed and the integrated index are shown in Table 1 The comparis
3. 3 different criteria the index of favorable temperatures for D citri de velopment IFTVD the index of favorable tem peratures for D citri oviposition FTVO and an index of potential generations of the insect in a yr INPGV The first 2 indices represent the frac tion of the yr with favorable temperatures for the insect s development and oviposition respective ly The third index represents the proportion of the maximum number of generations estimated for D citri in the country for every yr and was considered as an indicator of the probability of high developmental rates for this insect The cal culation of these indexes was as follows IFTVD No of days with mean daily temperature ranging in the vector threshold during the yr No of days of the yr 40 Florida Entomologist 96 1 IFTVO No of days with mean daily temperature ranging in the vector s oviposition thresh old during the yr No of days of the yr INPGV number of potential generations of D citri in a yr Maximum number of Poten tial Generations obtained Temperatures of 10 C and 33 C were consid ered as the minimum and maximum thresholds for the development of this insect Liu amp Tsai 2000 meanwhile 16 C and 41 6 C were used to represent the minimum and maximum oviposi tion threshold temperatures respectively Hall et al 2011 A thermal requirement of 250 3 Degree Days DD to complete the life cycle from egg to adult Liu amp
4. D 2011 A comparison of methods for combining maps in pest risk assessment application to Di abrotica virgifera virgifera EPPO Bull 41 217 225 EsQUIVEL CH VEZ F VALDOVINOS PONCE G Mora Acu ILERA G GOMEZ JAIMES R VELAZQUEZ MONREAL J MAnzaNILLA RaM REZ M A FLORES S NCHEZ J L AND L PEZ ARROYO J I 2012 An lisis histol gico en c tricos agrios y naranja dulce asociados a s ntomas ocasionados por Candidatus Liberibacter asiaticus Agrociencia Submitted Foop AND AGRICULTURAL ORGANIZATION 1996 Agro eco logical zoning guidelines FAO Soils Bull 73 Soil Resources Management and Conservation Service FAO Land and Water Development Division GUTIERREZ A P AND Ponti L 2011 Assessing the in vasive potential of the Mediterranean fruit fly in California and Italy Biol Invasions 13 1387 1402 Hatt D G AND ALBRIGO L G 2007 Estimating the relative abundance of flush shoots in citrus with implications on monitoring insects associated with flush HortScience 42 364 368 Hatt D G Lapointe S L AND WENNINGER E K 2007 Effects of particle film on biology and behavior of Di aphorina citri Hemiptera Psyllidae and its infesta tions in citrus J Econ Entomol 100 847 854 Hatt D G WENNINGER E J AND Hentz M G 2011 Temperature studies with the Asian citrus psyllid Diaphorina citri Cold hardiness and temperature thresholds for oviposition J Insect Sci 83 1 15 Har
5. Entomologist 96 1 March 2013 POTENTIAL DISTRIBUTION IN MEXICO OF DIAPHORINA CITRI HEMIPTERA PSYLLIDAE VECTOR OF HUANGLONGBING PATHOGEN I Torres Pacueco J I L PEZ ARROYO J A AGUIRRE G MEZ R G GUEVARA GONZALEZ R YANEZ LOPEz M I HerN NDEZ ZUL AND J A QUIJANO CARRANZA Cuerpo Acad mico Ingenier a de Biosistemas Divisi n de Investigaci n y Postgrado Facultad de Ingenier a Universidad Aut noma de Quer taro M xico Campo Experimental General Ter n Instituto Nacional de Investigaciones Forestales Agr colas y Pecuarias M xico Campo Experimental Baj o Instituto Nacional de Investigaciones Forestales Agr colas y Pecuarias M xico Corresponding author E mail juanangelquijano prodigy net mx A pdf file with supplementary material for this article in Florida Entomologist 96 1 2013 is online at http purl fcla edu fela entomologist browse ABSTRACT Huanglongbing HLB the citrus disease associated with the bacteria Candidatus Liberi bacter asiaticus is the most important threat of the Mexican citrus industry Since 2009 this bacterium has been detected in 11 out of 23 citrus producing states of the country al though with a limited distribution in each state The Asian citrus psyllid Diaphorina citri Kuwayama Hemiptera Psyllidae is the vector of this bacterium the insect is distributed in all the citrus growing zones of Mexico Presently the lime production zone in the Mexic
6. acter spp y el ps lido asi tico de los c tricos Diapho rina citri Hermosillo Sonora Mexico http www calcitrusquality org wp content uploads 2009 05 Ep idemiology of HLB and its implications on disease management Bassanezi 2010 pdf BarooL A IrTIkHAR Y MuGuHat S M Kuan M M JASKANI M J ABBAS M AND Han I A 2007 Citrus greening disease a major cause of citrus decline in the world A review Hort Sci Prague 34 159 166 Beppow J M Kriticos D ParDEY P G AND SUTHERST R W 2010 Potential Global Crop Pest Distribu tions Using CLIMEX HarvestChoice Applications Working Paper 27 pp http harvestchoice org sites default files downloads publications Beddowetal 2010HCPotentialGlobalCropPestDistributionsUs ingCLIMEX 3 pdf Bove J M 2006 Huanglongbing A destructive new ly emerging century old disease of citrus J Plant Pathol 88 1 7 37 Bove J M AND GARNIER M 2002 Phloem and xylem restricted plant pathogenic bacteria Plant Science 163 1083 1098 Bussy J R 1991 BIOCLIM A bioclimatic analysis and prediction system pp 64 68 In C R Margules and M P Austin eds Nature Conservation Cost Effec tive Biological Surveys and Data Analysis CSIRO Canberra Curti Diaz S A D az ZoRRILLA U LOREDO SALAZAR R X SANDOVAL J A PASTRANA L AND RODR GUEZ M 1998 Manual de producci n de naranja para Vera cruz y Tabasco Libro T cnico No 2 INIFAP Ce
7. availability of susceptible hosts was de limited by considering the total area of planted citrus in Mexico including sweet orange Mexi can lime tangerine Citrus reticulata Blanco and pummelo Citrus maxima Burm Merr Data of areas planted were obtained from the Agricultural and Fishery Information System of Mexico Servicio de informaci n Agropecuaria y Pesquera SIAP Citrus zones were classified according to the probability of occurrence of fa vorable temperatures for vegetative bud growth of citrus i e shoots or flushes The range of temperatures of 13 35 C was considered Hardy amp Khurshid 2007 to be generally operative for growth and development of citrus species Two indexes were calculated to estimate the period of the yr with suitable conditions for the produc tion of vegetative shoots i the index of favor able temperatures for citrus growing IFTCG and ii the index of the length of the growing N STATE Baja California Sur Campeche Chiapas S Colima Hidalgo Jalisco Michoac n Nayarit Nuevo Le n Quintana Roo San Luis Potos Sinaloa Tamaulipas Veracruz Yucat n Fig 1 Distribution of HLB detections in Mexico in December 2011 Quijano et al Potential distribution of Diaphorina citri in Mexico 39 wm Index of favorable temperatures for citrus growing IFTCG state division e HM 0 0 HE 01 02 HM 02 03 03 04 04 05 0 5 06 NJ os o 7 MA 07 os
8. function of the Integrated Indexes insect almost throughout the yr Fig 4 In the case of oviposition JFTVO the temperature con ditions are more restrictive for the vector with all the northern states getting a medium to low risk classification Southern states present favor able conditions of temperature for oviposition in a great proportion of the yr especially Michoacan Guerrero Oaxaca Veracruz Tabasco Campeche Yucatan Quintana Roo and Chiapas Fig 5 With respect to the number of generations of D citri the areas with the highest risk to reach the maximum number are distributed within the states of Colima Jalisco Michoac n Nayarit Sinaloa Tabasco Veracruz and Yucat n This map is coincident with the reports of high popula tions of D citri and HLB detections Ur as L pez et al 2011 Vel zquez Monreal et al 2011 www senasica gob mx Considering the states where the disease has been undetected the northern zone of Veracruz and southern Tamaulipas present the most favor able conditions for the insect and where it can develop more than 11 generations per yr Fig 6 This indicates the constant threat of the arrival and development of Clas carrying psyllids The citrus zone of Nuevo Leon reaches a medium risk classification with 6 generations per yr Fig 6 The distribution of the Integrated Index of Ag roclimatic risk for D citri in the citrus zones of Mexico JCS is shown in Fig 7 This inde
9. high risk for the occurrence of suitable temperatures for D citri development are distributed throughout the country with the only exception of the states of Baja California and Sonora Fig 4 In the states of Campeche Chiapas Quintana Roo Tabasco Yucat n some parts of Guerrero and the region named La Huasteca where the states of Hidalgo San Luis Potos Tamaulipas and Veracruz converge the temperature conditions are favorable for this Citrus tree IFTCG 0 92 0 45 0 24 Days with favorable temperature 0 365 98 55 146 3index of favorable temperatures for D citri development 4index of favorable temperatures for D citri oviposition 5index of potential generations of D citri in a year lindex of favorable temperatures for citrus growing Integrated Index of Climatic Suitability for D citri index of length of the growing period for citrus Parameter Min Max Mean Std dev 42 Florida Entomologist 96 1 March 2013 Index of length of the growing period for citrus ILGPC __ State division io E o o E 0 1 0 2 E 02 03 103 04 J04 05 05 06 E 0 6 0 7 E 0 7 0 8 gt BN MMH 08 09 Eoo Fig 3 Climatic suitability map for Citrus growth as a function of soil moisture conditions in Mexico Index of favorable temperatures for vector development IFTVD E a state division E HM oo GE 01 02 HM 02 03 03 04 7 0 4 0 5 Jos 08 EJ os 0 7 MA 07 08
10. 0 SIMULATIONS PERFORMED FOR THE 4 AGRO CLIMATIC CRITERIA ANALYZED IN RELATION TO DISTRIBUTION OF THE ASIAN CITRUS PSYLLID AND CITRUS PHENOLOGY Quijano et al Potential distribution of Diaphorina citri in Mexico 41 tudes In the states of Campeche Chiapas Quin tana Roo southern Veracruz Tabasco Yucatan and the coastal zones of Colima Guerrero and Michoacan the maximum suitability of tempera tures for citrus growing is present as indicated by the red color This implies that during the whole yr the temperature is favorable for the produc tion of vegetative shoots and therefore for the de velopment and continuous increase of the D citri population Liu amp Tsai 2000 Tsai et al 2002 Hall et al 2007 2011 With respect to the growing period there is a remarkable contrast between the southern and northern regions In the south of the country humidity is available for growth throughout the yr In comparison the states of northern Mexico like Baja California Nuevo Le n Sinaloa So nora and Tamaulipas the period with at least minimally sufficient soil moisture covers 10 or less of the yr Such contrasts could have deter mined the pattern in the Mexican citrus industry distribution with the presence of irrigated cit rus groves mainly in the northern states of the country and with the concentration of Mexican and Persian lime production in southern Mexico www siap gob mx These contrasts also help to understand
11. E o oo 400 200 0 et A a Kilometers ee Fig 2 Climatic suitability map for Citrus growth as a function of temperature in Mexico period for citrus ILGPC which estimates the number of days with sufficient soil moisture for vegetative growth The formulas for these index es are shown below IFTCG No of days with mean daily temperature ranging in the citrus threshold during the yr No of days of the yr ILGPC No of days with available humidity for citrus growing during the yr No of days of the yr The length of the growing period was calcu lated on a daily basis through a simple water balance in which rainfall P is compared with potential evapotranspiration PET following the method proposed by the Food and Agricultural Organization FAO 1996 When P exceeds half PET the growing period is considered to start and residual moisture storage is calculated as a function of soil physical properties The growing period ends when residual moisture is completely exhausted Under these considerations days of the yr are counted as favorable for growing of citrus when some residual humidity is available P PET gt 0 and non favorable when there is not any residual humidity Irrigation was not includ ed in the water balance considering that the in the case of sweet orange more than 70 of the cultivated area is under rainfed conditions The suitability of climatic conditions for D citri was analyzed with
12. Mexico in 2008 began a monitoring program of the bacterium that included sam pling insects and citrus vegetative material In 2009 Clas was detected first in the municipalities of Tizimin state of Yucatan and Lazaro Carde nas state of Quintana Roo and then in plant and psyillid samples in the states of Jalisco and Nayarit In 2010 HLB was found in Campeche Colima and Sinaloa Trujillo Arriaga 2010 At the end of 2011 the bacteria had been detected in the states of Baja California Sur Michoacan Chi apas and Hidalgo for a total of 11 afflicted states SENASICA 2012 Mexican lime Citrus aurantifolia Swingle is the citrus species predominantly affected by HLB in Mexico Robles Gonz lez et al 2011 This is the second most widely planted citrus species in the country with 166 580 ha planted but sweet orange Citrus x sinensis L Osbeck is the most important with 335 471 ha planted Presently more than 10 000 ha of commercial groves have been reported as infected with Clas SENASICA 2012 Histological studies developed by Esquiv el Chavez et al 2012 showed that Mexican lime was the more susceptible to Clas and developed symptoms more rapidly than sweet orange and Persian lime Citrus x latifolia Tanaka The com mercial groves of Mexican lime are distributed mainly in the states of Colima and Michoacan at the southern coast of the Pacific Ocean The most important commercial groves of sweet orange are established in a reg
13. Potential Production of Crops which 38 Florida Entomologist 96 1 integrates a daily weather database a national database of soil profiles and models to simulate the growth and development of crops and pests For insects SIMPEC includes a simple algorithm to calculate the number of generations based on the degree days approach and a routine to esti mate the probability of favorable conditions for an organism This study proposes a deductive mapping approach based on the analysis of the climatic conditions to delimit the most suitable zones for the development and growth of Asian citrus psyllid populations These zones are considered to be at the highest risk of developing new in fections of Clas the apparent cause of HLB in citrus trees MATERIALS AND METHODS The data generated in this study are displayed in black and white in Figs 1 6 These figures are reproduced in color in the online supplementary document at http purl fcla edu fcla entomolo gist browse The figures in the supplementary document are referred to below as Suppl Fig 1 Suppl Fig 2 etc __ state division HA HLB detection citrus planted area March 2013 Factors Affecting Distribution of Diaphorina citri The potential distribution of D citri was con sidered to be determined by 2 main factors a the availability of susceptible hosts and b the suit ability of climatic conditions for the development of D citri The
14. Tsai 2000 was utilized to calculate the number of potential generations of D citri To estimate daily DD the residual method was ap plied which has the following formula Daily DD Tmax Tmin 2 Lower threshold temperature The number of potential generations NPG of D citri in a yr was calculated as follows NPG Accumulated DD in a yr DD required to complete one generation Finally an Integrated Index of Climatic Suit ability IICS for D citri was calculated com bining the different indexes following a similar procedure as Moschini et al 2010 A simple av erage was used for combining them IICS IFTCG ILGPC IFTVD IFTVO IN PGV 5 Climatic Database Daily data of the meteorological variables rainfall rain mm maximum temperature Tmax C and minimum temperature Tmin C were utilized from 2985 weather stations of the National Weather Service SMN of Mexico Observed values of these variables represent se ries from 1950 through 2010 Data quality con trol was performed through an exhaustive visual inspection of yearly graphics for each variable After the elimination of invalid or illogical val ues data from 2 470 weather stations with a time series of at least 18 yr in the period of 1967 to 2008 were considered The average time series of the finally selected weather stations was 23 yr The weather database was saved as a text format files and incorporated to the SIMPEC structure to
15. a en cada estado El ps lido asi tico de los c tricos Diaphorina citri Kuwayama Hemiptera Psyllidae es el vector de la bacteria y actualmente se encuentra distribuido en todas las zonas productoras de c tricos del pa s Hasta ahora la mayor afectaci n por esta enfermedad corresponde a la zona comercial de producci n de lim n mexicano en los estados de Colima Jalisco Michoac n Nayarit y Si naloa en la costa del Oc ano Pac fico Una de las estrategias que se han implementado para la contenci n de esta enfermedad es el manejo regional de poblaciones del ps lido Para con tribuir a sustentar esta estrategia analizamos las series hist ricas diarias de temperatura y precipitaci n de todo el pa s y clasificamos las zonas citr colas con base en la probabilidad de presentar condiciones favorables para la reproducci n continua y acelerada del ps lido Los resultados indican que de las regiones m s importantes de producci n de naranja dulce en el pa s la parte sur de Veracruz y la regi n denominada La Huasteca donde convergen los estados de Veracruz Tamaulipas San Luis Potosi e Hidalgo presentan el riesgo m s alto para la reproducci n acelerada del ps lido Actualmente esta regi n se encuentra libre de este pat geno y se considera de la m s alta prioridad para el manejo de las poblaciones del ps lido a fin de evitar el ingreso y establecimiento del HLB Palabras Clave an lisis de riesgo d as grado mapeo deductiv
16. amp Albrigo 2007 Hall et al 2007 2011 S tamou et al 2008 Modeling techniques have been used to esti mate the potential distribution of pests at the first stages of invasions and model outputs are needed to support the planning of surveys and implementation of eradication measures Rafos 2003 Magarey et al 2007 Arambout et al 2009 Lad nyi Horv th 2010 Rosa et al 2011 Guti errez amp Ponti 2011 Computer systems based on models of pest behavior have been developed to estimate potential pest distribution and to cre ate pest risk maps as in the case of NAPPFAST North Carolina State University APHIS Plant Pest Forecasting System an internet based sys tem to develop risk maps of plant pests Magarey et al 2007 The system has a daily based climate database and a biological template to create sim ple models Similarly CLIMEX Climatic Index is a computer system that estimates the climatic re gions that a species could potentially occupy when there are no limiting factors other than climate Sutherst et al 1999 Sutherst 2004 Beddow et al 2010 In addition BIOCLIM Bioclimatic Analysis And Prediction System created by Busby 1991 and MAXENT Maximum Entropy Method developed by Phillips et al 2006 have been used to estimate spread patterns of plant pests Dupin et al 2011 Kriticos et al 2012 Qui jano et al 2011 developed a computer system named SIMPEC Information System to Assess Ecological
17. an states of Colima Jalisco Michoacan Nayarit and Sinaloa near to the Pacific Ocean coast is the most affected by this disease One of the main strategies to retard or stop the advance of HLB consists in the regional management of the psyllid populations In order to contribute to the support of this strategy we analyzed the daily courses of temperature and rainfall all over the country to classify the citrus zones according to the probability of occurrence of favorable conditions for rapid and continuous psyllid reproduction The results indicate that one of the most important regions of sweet orange production of Mexico southern Veracruz and the region named La Huasteca where the states of Veracruz Tamaulipas San Luis Potosi and Hidalgo converge represent the zones with the highest risk for an accelerated reproduction of the psyllid At present these regions remain free of the bacterium and are considered of highest priority for the management of psyllid populations and for preventing the entry and establishment of HLB Key Words risk analysis degree days deductive mapping agro ecological indexes RESUMEN El Huanglongbing HLB la enfermedad causada por la bacteria Candidatus Liberibac ter asiaticus es la amenaza m s importante para la prevalencia de la industria citr cola mexicana Desde 2009 el pat geno ha sido detectado en 11 de los 23 estados productores de c tricos del pa s aunque con una distribuci n limitad
18. e are only 2 veg etative flushes during the yr Our study could contribute substantially to planning the regional approach intended for the management of D citri in Mexico ACKNOWLEDGMENTS The authors acknowledge The Consejo Nacional de Ciencia y Tecnologia of Mexico for fellowship support of Juan Angel Quijano Carranza and for providing the financing for the project Manejo de la enfermedad Huanglongbing HLB mediante el control de poblacio nes del vector Diaphorina citri Hemiptera Psyllidae el psilido asi tico de los c tricos 108591 from which this work was derived REFERENCES CITED ALDAMA AGUILERA C OLVERA VARGAS L A AND GALIN po Menpoza M A 2011 Reportes epidemiol gicos de HLB pp 122 127 En Memoria del 2 Simposio Nacional sobre investigaci n para el manejo del Ps lido Asi tico de los C tricos y el Huanglongbing en M xico Texcoco M xico https sites google com site diaphorina hlb2simpnal ARAMBOUT J P FinLay K J Luck J AND BEATTIE G A C 2009 A concept model to estimate the potential distribution of the Asiatic citrus psyllid Diaphorina citri Kuwayama in Australia under climate change A means for assessing biosecurity risk Ecological Modelling 220 2512 2524 Bassanezi R B 2008 Epidemiology of huanglongbing and its implications on disease management pp 37 43 In Memoria del 2 Taller Internacional sobre Huanglongbing de los c tricos Candidatus Liberib
19. es for biological control of Diapho rina citri Hemiptera Psyllidae in Mexico pp 329 330 In T R Gottwald and J H Graham eds Proc March 2013 Intl Res Conf Huanglongbing 1 5 Dec 2008 Or lando Florida Macarey R D Fow er G A BorcHERT D M SUTTON T B Cotunca Garcia M AND SIMPSON J A 2007 NAPPFAST An internet system for the weather based mapping of plant pathogens Plant Disease 91 336 345 MEDINA UrrurIa V M RogLes Gonz Lez M M BECE RRA RODR GUEZ S OROZCO ROMERO J OROZCO SAN tos M Garza L prez J G Ovanpo Cruz M E AND CH VEZ CONTRERAS X 2008 El cultivo de lim n Mexicano Libro T cnico N m 1 Campo Experimen tal Tecom n INIFAP SAGARPA M xico 188 pp MIRANDA SALCEDO M A AND L PEZ ARROYO J I 2010 Fluctuaci n poblacional del ps lido asi tico de los c tricos Diaphorina citri Kuwayama Hemiptera Psy llidae y de sus enemigos naturales en Michoac n En Memoria del ler Simp Nac sobre investigaci n para el manejo del Ps lido Asi tico de los Cr ticos y el Huanglongbing en M xico https sites google com site diaphorina hlb2simpnal ORTEGA ARENAS L D VILLEGAS MONTER A ORDU O Cruz N VEGA CH VEZ J LOMEL FLORES J R AND Ronr cuEz Leyva E 2010 Fluctuaci n poblacional de Diaphortina citri y enemigos naturales asociados a especies de c tricos en Cazones Veracruz M xico pp 56 63 Memoria del ler Simposio Nacional s
20. ion near the northern coast of the Gulf of Mexico with 258 546 h 77 of total distributed in the states of Veracruz Tamaulipas San Luis Potos and Nuevo Le n according to da ta from the Agricultural and Fishery Information System of Mexico www siap gob mx 2012 The last inspections in these states have not detected the presence of the bacterium SENASICA 2012 Some studies have estimated the risk associ ated with D citri and with the HLB dispersal for different regions of Mexico D az et al 2010 Al dama Aguilera et al 2011 These studies classify almost all the important citrus zones of the coun try as being at high risk of Clas infection This is so because these authors assign a similar weight to the area planted with citrus and to agrome teorological requirements of the establishment of D citri Our goal was to test the hypothesis that differences in agroclimatic conditions of cit rus growing zones determine the rates of psyllid population growth The importance of pest host climate interac tions in the progress of infections with Clas in citrus trees have been noted by several authors Zhao 2010 and Bassanezi 2008 related the increasing in infection rates with the presence of high populations of the psyllid On the other hand the population dynamics of D citri are strongly dependent on citrus phenology because vegetative flushes must be available for the ovi position of the psyllid Tsai et al 2002 Hall
21. itri Homoptera Psyllidae in southern Florida Florida Entomol 85 446 451 Ur as L rEz M A HERN NDEZ FUENTES L M L PEZ Arroyo J I AND GARC A ALVAREZ N C 2011 Dis tribuci n temporal y densidades de poblacion del ps lido asi tico de los c tricos Hemiptera Psyllidae en Nayarit M xico pp 156 162 In J I L pez Arroyo and V W Gonz lez Lauck Comp 2 Simp Nac so bre Investigaci n para el Manejo del Ps lido Asi tico de los C tricos y el Huanglongbing en M xico Mon tecillo Edo de M xico M xico 5 y 6 de diciembre 2011 ISBN 978 607 425 680 2 424 pp VEL ZQUEZ MONREAL J J RoBLES GONZ LEZ M M MANZANILLA RAMiREZ M A CARRILLO MEDRANO S H AND Orozco Santos M 2011 Din mica pobla cional de Diaphorina citri Kuwayama Hemiptera Psyllidae en el estado de Colima pp 161 168 In J I L pez Arroyo and V W Gonz lez Lauck Comp 2 Simp Nac sobre Investigaci n para el Manejo del Ps lido Asi tico de los C tricos y el Huanglongbing en M xico Montecillo Edo de M xico M xico 5 y 6 de diciembre 2011 ISBN 978 607 425 680 2 424 pp ZHAO X 2010 Background current situation and man agement of the HLB and its vector in China pp 44 52 In Memoria del 2 Taller Intl sobre Huanglong bing de los c tricos Candidatus Liberibacter spp y el ps lido asi tico de los c tricos Diaphorina citri Hermosillo Sonora Mexico
22. ntro de Investigaci n Regional Golfo Centro Campos Ex perimentales Ixtacuaco y Huimanguillo Veracruz y Tabasco M xico 175 pp Curti Diaz S A LOREDO SALAZAR R X D AZ ZORRILLA U SANDOVAL J A AND HERN NDEZ J 1996 Manual de producci n de lim n Persa Folleto T cnico 14 INIFAP Centro de Investigaci n Regional Golfo Centro Campo Experimental Ixtacuaco Tlapa coy n Ver M xico 145 pp Da Graca J V 1991 Citrus greening disease Annu Rev Phytopathol 29 109 136 Da Graca J V AND KorsTEN L 2004 Citrus huan glongbing Review present status and future strate gies pp 229 245 In S A M H Naqvi ed Diseases of fruits and vegetables Vol 1 Kluwer Academic Publishers The Netherlands Da Graca J V 2008 Biology history and world status of huanglongbing I Taller Intl sobre Huanglong bing de los c tricos Candidatus Liberibacter spp y el ps lido asi tico de los c tricos Diaphorina citri Hermosillo Sonora M xico http www concitver com huanglongbingYPsilidoAsiatico MemorC3ADa 1Graca pdf 46 Florida Entomologist 96 1 D az P G Mora A G L PEZ A J I GUAJARDO P R AND S NCHEZ C I 2010 Modelaci n espacial de zonas de riesgo agroclim tico para el desarrollo de Diapho rina citri en zonas citr colas del estado de Veracruz Caso de estudio naranja En Memorias del XIV Simp Intl SELPER Dupin M BRUNEL S BAKER R EYRE D AnD MAkows KI
23. o ndices agroecol gicos Quijano et al Potential distribution of Diaphorina citri in Mexico 37 Since the beginning of this century the Ameri can Continent has been under the invasion by the phloem limited bacterium Candidatus Liberib acter asiaticus Clas which is associated with one of the most destructive citrus diseases Huan glongbing HLB or citrus greening da Graca 1991 da Graca amp Korsten 2004 Bov amp Garnier 2002 Bov 2006 Clas which still cannot be cul tured in vitro can be transmitted by grafts and by the psyllid vectors Trioza erytreae Del Guerico in Africa and Diaphorina citri Kuwayama in Asia and now in American countries Batool et al 2007 da Graca 2008 In the Americas HLB was reported for the first time in Brazil in 2004 da Graca 1991 In Mexico this disease was first reported in 2009 and its distribution in the coun try is still limited The Mexican Government through the General Direction for Plant Health SAGARPA SENASICA DGSV is on constant alert in an attempt to maintain the most impor tant production zones of citrus Sapindales Ru taceae free of HLB Trujillo Arriaga et al 2008 The threat that this disease represents is greatly exacerbated by the wide distribution in Mexico of its effective vector the Asian citrus psyllid Di aphorina citri Kuwayama L pez Arroyo et al 2009 Trujillo Arriaga 2010 Because of the presence of HLB in Brazil and in the USA
24. obre investigaci n para el manejo del Ps lido Asi tico de los Cr ticos y el Huanglongbing en M xico Moschin1 R C Herr G E Contr H A CAZENAVE G AND CoRrTESE P L 2010 Riesgo agroclim tico de las reas citr colas de Argentina en relaci n a la abundancia de Diaphorina citri Informe de enero 2010 Programa Nac de prevenci n del Huanglong bing Ministerio de Agricultura Ganader a y Pesca Presidencia de la naci n Buenos Aires Argentina 14 pp ORTEGA ARENAS L D VILLEGAS MONTER A ORDUNO Cruz N VEGA CH VEZ J LOMEL FLORES J R AND Ronr cuEz Leyva E 2011 Abundancia estacional de Diaphortina citri y enemigos naturales asociados a especies de c tricos en Cazones Veracruz M xico Memoria del 20 Simposio Nac sobre investigaci n para el manejo del Ps lido Asi tico de los Cr ticos y el Huanglongbing en M xico https sites google com site diaphorina hlb2simpnal QUIJANO CARRANZA J A ROocHA RODR GUEZ R AND AGUI RRE G MEZ J A 2011 Sistema de Informaci n para el Monitoreo del Potencial Ecol gico de los Cultivos SIMPEC INIFAP SAGARPA M xico Publ t cnica no 2 32 pp Raros T 2003 Spatial stochastic simulation offers po tential as a quantitative method for pest risk analy sis Risk Analysis 23 651 661 RobLes GoNz LEz M M VELAZQUEZ MONREAL J J MaAnzaANILLa RAM REZ M A Orozco Santos M FLoREs VIRGEN R AND MEDINA URRUTIA V M 2011 El HLB en
25. on of the mean of days with favorable temperatures for citrus 98 55 and for the psyllid 211 7 indicates that this factor is more restrictive for the tree than for the insect In northern locations temperatures remain below the citrus requirements in the win ter This also indirectly affects the growth and development of the psyllid because of the lack of vegetative shoots in the winter The mean of days with favorable soil moisture for citrus was 200 75 The maximum number of potential psyl lid generations obtained was 27 with a mean value of 14 The values of the standard deviations for these factors are indicative of the great vari ability of the climatic conditions in the Mexican citrus zones Index of Susceptible Host Availability Figure 2 and Fig 3 and Suppl Figs 2 and 3 show the maps of 80 of probability of exceedance for the 2 indexes describing the susceptible host availability the days of the yr within the thermal thresholds for the citrus growing IFTCG Fig 2 and the period with available soil moisture for rainfed cultivation of citrus LGPC Fig 3 In both maps the dark red color in the scale repre sents the most suitable conditions for citrus grow ing In the case of temperature Fig 2 and Suppl Fig 2 a gradual decrease in the values of the index is evident from south towards northern lati Diaphorina citri Days with favorable temperature TABLE 1 BASIC STATISTICS OF THE RESULTS OF 56 81
26. py S AND KHURsHID T 2007 Calculating heat units for citrus Primefacts NSW department of primary industries Primefact 749 3 pp JASSO ARGUMEDO J LozANO CoNTRERAS M BARROSO AK H AND L PEZ ARROYO J I 2010 Abundancia estacional de Diaphorina citri Hemiptera Psylli dae y sus enemigos naturales en huertas de lim n persa en Yucat n M xico pp 311 318 In J I L pez Arroyo y V W Gonz lez Lauck Comp Memorias del Primer Simposio Nacional sobre Investigaci n para el Manejo del Ps lido Asi tico de los C tricos y el Huanglongbing y en M xico 8 9 Diciembre 2010 Monterrey N L M xico https sites google com site diaphorina simposiohlb1_050 001 Kriticos D J WEBBER B L LERICHE A Ora N Mac ADAM I BATHOLS J AND SCOTT J K 2012 CliMond global high resolution historical and future scenario climate surfaces for bioclimatic modelling Methods in Ecology and Evolution 3 53 64 Lap nyr M anD HorvAtu L 2010 A review of the po tential climate change impact on insect populations General and agricultural aspects Appl Ecol En viron Res 8 143 152 Liv Y H anp Tsar J H 2000 Effects of temperature on biology and life table parameters of the Asian citrus psyllid Diaphorina citri Kuwayama Homop tera Psyllidae Ann Appl Biol 137 201 206 Loprz Arroyo J I Jasso J Reyes M A LOERA GAL LARDO J CORTEZ MONDACA E AND MIRANDA M A 2009 Perspectiv
27. r pest monitoring and surveying Through this approach the design and operation of regional management strategies can be more efficient in tracking invasive pests using the available agro climatic information and saving human efforts and economic resources Current citrus zones with presence of HLB in Mexico meet the criteria of climatic suitability for a continuous production of vegetative shoots and high reproduction rates of D citri These areas have a humid tropical megathermal climate ac cording to the K ppen classification as well as the zones reported with HLB infections in Brazil Cuba and the state of Florida in USA Southern Veracruz and La Huasteca are the zones with the highest risk for D citri increasing populations due to its similarity in climate conditions with the currently HLB infected zones in Mexico see Figs 1 and 7 These zones are the most important of the country in terms of sweet orange production and should be considered as the highest priority in crop protection actions in order to suppress the psyllid populations and to prevent their spread throughout the commercial groves The state of Tamaulipas in its central part presents a me dium to high risk and should also be considered to be in serious danger Only Nuevo Leon Sonora and Baja California have climatic conditions that could greatly facilitate the management of the vector mainly because scarce populations of D citri are predictable since ther
28. rboles de lim n mexicano Citrus auran tifolia Christm Swingle su dispersi n y s ntomas en Colima M xico pp 43 53 In J I L pez Arroyo and V W Gonz lez Lauck Comp 2 Simposio Na cional sobre Investigaci n para el Manejo del Ps lido Asi tico de los C tricos y el Huanglongbing en M xico Montecillo Edo de M xico M xico l 5 y 6 de diciembre 2011 ISBN 978 607 425 680 2 424 pp Rocha M A AND PADR N J E eds 2009 El culti vo de los c tricos en el Estado de Nuevo Le n Libro cient fico no 1 Inst Nacl Invest Forestales Agr co Quijano et al Potential distribution of Diaphorina citri in Mexico 47 las y Pecuarias CIRNE Campo Experimental Gral Ter n M xico 474 pp Rosa G S Costa M I S CORRENTE J E SILVEIRA L V A anD Gopoy W A C 2011 Population dynam ics life stage and ecological modeling in Chrysomya albiceps Wiedemann Diptera Calliphoridae Neo trop Entomol 40 181 189 SENASICA Servicio NACIONAL DE SANIDAD INOCUIDAD Y CALIDAD AGROALIMENTARIA 2008 Manual t cnico para la detecci n del Huanglongbing de los c tricos Direcci n General de Sanidad Vegetal Direcci n de Protecci n Fitosanitaria SENASICA Servicio NACIONAL DE SANIDAD INOCUIDAD Y CALIDAD AGROALIMENTARIA 2012 Acciones contra el Huanglongbing y su vector en M xico Informe del 02 de enero al 30 de junio de 2012 Direcci n General de Sanidad Vegetal Direcci n de Protecci n Fito
29. sa nitaria S TAMOU M FLORES D FRENCH J V AND HALL D G 2008 Dispersion patterns and sampling plans for Diaphorina citri Hemiptera Psyllidae in citrus J Econ Entomol 101 4 1478 1487 SHEPARD D 1968 A two dimensional interpolation func tion for irregularly spaced data Proc 23rd Natl Conf Assoc Computing Machinery pp 517 524 Sutuerst R W 2004 Prediction of species geographical ranges A critical comment on M J Samways R Os burn H Hastings and V Hattingh 1999 Global cli mate change and accuracy of prediction of species geo graphical ranges establishment success of introduced ladybirds Coccinellidae Chilocorus spp worldwide J Biogeography 26 795 812 J Biogeogr 30 805 816 TRUJILLO ARRIAGA J SANCHEZ ANGUIANO H M AND Ro BLES GARCIA P L 2008 En Memoria del ler Taller Intl sobre Huanglongbing de los c tricos Candida tus Liberibacter spp y el ps lido asi tico de los c tri cos Diaphorina citri Hermosillo Sonora M xico http www concitver com huanglongbingY PsilidoA siatico Indice html TRUJILLO ARRIAGA J 2010 Situaci n actual regulaci n y manejo del HLB en M xico En Memoria del 2 Ta ller Intl sobre el Huanglongbing y el Ps lido Asi ti co de los C tricos M rida Yucat n Mexico https sites google com site diaphorina tallerhlb Tsar H T Wang J J anD Liu Y H 2002 Seasonal abundance of the Asian citrus psyllid Diaphorina c
30. the differences in the seasonality of citrus shoot production In southern Mexico veg etative growth occurs throughout the yr which is especially evident in the different lime species whereas in the northern states productive citrus trees mainly have shoot production during the fall and at the end of the winter Curti D az et al 1996 1998 Medina Urrutia et al 2008 SENA SICA 2008 Rocha Padr n 2009 As can be seen in Fig 1 and Suppl Fig 1 the zones where HLB is currently present in Mexico are coincident with the more suitable areas for citrus production Integrated TICS 0 0 84 0 51 0 18 INPGV 0 0 85 0 5 0 19 No of Gen 0 7 14 5 2 0 34 0 28 TFTVO 0 0 99 0 92 0 58 TFTVD 0 19 0 361 02 124 11 102 01 Ovipos Develop 335 8 211 7 69 35 0 27 ILGPC 0 1 0 4 335 8 200 75 87 6 Index of Climatic Suitability for D citri Development Days with favorable soil moisture 0 Figures 4 5 and 6 and Suppl Figs 4 5 and 6 show the maps of temperature conditions for the growth and development of D citri at a prob ability of exceedance of 80 The Index of days within the thermal thresholds for the insect de velopment IFTVD and oviposition are described in Fig 4 and Fig 5 and the number of genera tions that the psyllid can complete in a yr as a proportion of the maximum obtained INPGV are presented in Fig 5 For the first index UFTVD zones with medium to
31. x One Potential Distribution in Mexico of Diaphorina citri Hemiptera Psyllidae Vector of Huanglongbing Pathogen Author s I Torres Pacheco J I L pez Arroyo J A Aguirre G mez R G Guevara Gonz lez R Y nez L pez M I Hern ndez Zul and J A Quijano Carranza Source Florida Entomologist 96 1 36 47 2013 Published By Florida Entomological Society DOI http dx doi org 10 1653 024 096 0105 URL http www bioone org doi full 10 1653 024 096 0105 BioOne www bioone org is a nonprofit online aggregation of core research in the biological ecological and environmental sciences BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies associations museums institutions and presses Your use of this PDF the BioOne Web site and all posted and associated content indicates your acceptance of BioOne s Terms of Use available at www bioone org page terms_of_use Usage of BioOne content is strictly limited to personal educational and non commercial use Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors nonprofit publishers academic institutions research libraries and research funders in the common goal of maximizing access to critical research 36 Florida
32. x rep resents the average of the different criteria used in this approach summarizing the factors of sus ceptible host availability and favorable climate for the vector In the resulting map the highest risk 0 8 to 0 9 occurs in some regions of Chiapas Quintana Roo Tabasco Veracruz and Yucatan It implies that most of the yr in those zones there can be citrus trees with vegetative growth and favorable temperatures for the reproduction of the insect Studies about the abundance of D citri in Michoac n Veracruz and Yucatan Jasso Argumedo et al 2010 Miranda Salcedo amp L pez Arroyo 2011 Ortega Arenas et al 2011 confirm the results generated in this work In the region of La Huasteca Tamaulipas San Luis Potosi Hidalgo and Veracruz Guerrero Michoac n Co lima and scattered zones of Jalisco and Nayarit the risk of climatic suitability ranks from 0 7 to 0 8 Some zones of Jalisco Nayarit Central Tam aulipas and the state of Sinaloa register medium Quijano et al Potential distribution of Diaphorina citri in Mexico 45 values of this index 0 6 to 0 7 In Nuevo Le n Sonora great part of Jalisco northern Tamau lipas and Baja California the risk of favorable conditions for the development of D citri can be considered medium to low lt 0 5 Fig 7 Implications for the Management of D citri and HLB In general pest risk maps provide a scien tific basis to decide where to allocate resources fo
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