Survival analyses of Diaphorina citri immatures on young citrus orchard in São Paulo, Brazil

Análises de sobrevivência de imaturos de Diaphorina citri em pomar jovem de citros em São Paulo, Brasil

Paulo Eduardo Branco Paiva Pedro Takao Yamamoto About the authors

ABSTRACT

The survival of eggs and nymphs of Diaphorina citri Kuwayama (Hemiptera: Liviidae) was estimated on young plants (< 1 year) of Citrus sinensis (cultivar Valencia) grafted on Citrus limonia in 3 seasons (Winter and Spring 2013; and Autumn 2014) in Ribeirão Preto, São Paulo State, Brazil. Young shoots with eggs were selected from natural or artificial infestations. Eggs, small nymphs (1st to 3rd instar), and large nymphs (4th and 5th instar) were counted every 3 days. Shoots with large nymphs were caged until the emergence of the adults. The lowest eggs and nymph survival were observed during Winter (0.0%), and Autumn (0.4%); the highest survival rates were recorded during Spring (12.2%). The biotic factor of mortality identified was the parasitism of large nymphs by Tamarixia radiata Waterston (Hymenoptera: Eulophidae), observed in all seasons. Air temperatures (minimum and maximum), and air relative humidity (minimum) could not explain the immature survival differences between Spring (12.2%) and Autumn (0.4%). Rainfall during Spring (165 mm) was higher than during Autumn (48 mm) and may have favored the survival of D. citri in the Spring. Adverse abiotic factors seem to be more important on immature D. citri survival than the biotic factor (parasitism).

KEYWORDS
Asian citrus psyllid; HLB; natural mortality; ecological life table; Tamarixia radiata

RESUMO

A sobrevivência de ovos e ninfas de Diaphorina citri Kuwayama (Hemiptera: Liviidae) foi estimada em plantas jovens (< 1 ano) de Citrus sinensis (cultivar Valencia) enxertadas em Citrus limonia em 3 estações (inverno e primavera de 2013, e outono de 2014) em Ribeirão Preto, estado de São Paulo, Brasil. Ramos novos com ovos foram selecionados a partir de infestações naturais ou artificiais. Ovos, ninfas pequenas (ínstar 1 ao 3) e ninfas grandes (ínstar 4 e 5) foram contados a cada 3 dias. Ramos com ninfas grandes foram colocados em gaiolas até a emergência dos adultos. As menores sobrevivências de ovos e ninfas foram observadas no inverno (0,0%) e no outono (0,4%), e a maior sobrevivência ocorreu na primavera (12,2%). O principal fator biótico de mortalidade identificado foi o parasitismo de ninfas grandes por Tamarixia radiata Waterston (Hymenoptera: Eulophidae), observado em todas as estações. As temperaturas (mínima e máxima) e umidade relativa (mínima) do ar não explicaram as diferenças nas sobrevivências de imaturos entre a primavera (12,2%) e o outono (0,4%). As chuvas na primavera (165 mm) foram maiores que no outono (48 mm) e podem ter favorecido a sobrevivência de D. citri na primavera. Fatores abióticos adversos parecem ser mais importantes na sobrevivência de imaturos de D. citri que o fator biótico (parasitismo).

PALAVRAS-CHAVE
psilídeo asiático dos citros; HLB; mortalidade natural; tabela de vida ecológica; Tamarixia radiata

INTRODUCTION

The Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Liviidae), was reported in Brazil in the early 1940s (LIMA, 1942LIMA, A.M.C. Insetos do Brasil: Homópteros. Rio de Janeiro: Escola Nacional de Agronomia, 1942. 111p.); however, it only became a citrus major pest after Huanglongbing (HLB) was reported, in 2004. This psyllid is the only known insect vector of the bacteria associated to plants with the disease symptoms, “Candidatus Liberibacter asiaticus”, and “Ca. L. americanus” (BOVÉ, 2014BOVÉ, J.M. Huanglongbing or yellow shoot, a disease of Gondwanan origin: Will it destroy citrus worldwide? Phytoparasitica, v.42, n.5, p.579-583, 2014. http://dx.doi.org/10.1007/s12600-014-0415-4
http://dx.doi.org/10.1007/s12600-014-041...
), which causes the early fall and reduction of fruit size (BASSANEZI et al., 2011BASSANEZI, R.B.; MONTESINO, L.H.; GASPAROTO, M.C.G.; BERGAMIN FILHO, A.; AMORIM, L. Yield loss caused by huanglongbing in different sweet orange cultivars in São Paulo, Brazil. European Journal of Plant Pathology, v.130, n.4, p.577-586, 2011. http://dx.doi.org/10.1007/s10658-011-9779-1
http://dx.doi.org/10.1007/s10658-011-977...
). In addition to the severe loss in fruit production, it leads to an increase in production costs with the adoption of recommended mitigation measures (STANSLY et al., 2014STANSLY, P.A.; AREVALO, H.A.; QURESHI, J.A.; JONES, M.M.; HENDRICKS, K.; ROBERTS, P.D.; ROKA, F.M. Vector control and foliar nutrition to maintain economic sustainability of bearing citrus in Florida groves affected by huanglongbing. Pest Management Science, v.70, n.3, p.415-426, 2014. https://doi.org/10.1002/ps.3577
https://doi.org/10.1002/ps.3577...
).

D. citri adults may occur in any period or season; however, eggs and nymphs are observed when there are new flushes and leaves in citrus (HALL et al., 2008HALL, D. G.; HENTZ, M. G.; ADAIR Jr., R. Population ecology and phenology of Diaphorina citri (Hemiptera: Psyllidae) in two Florida citrus groves. Environmental Entomology, v.37, n.4, p.914-924, 2008. https://doi.org/10.1093/ee/37.4.914
https://doi.org/10.1093/ee/37.4.914...
). In São Paulo State, before it became the target of management programs, the largest adult populations of D. citri occurred during Spring and Summer (YAMAMOTO et al., 2001YAMAMOTO, P. T.; PAIVA, P. E. B.; GRAVENA, S. Flutuação populacional de Diaphorina citri Kuwayama (Hemiptera: Psyllidae) em pomares de citros na região Norte do Estado de São Paulo. Neotropical Entomology, v.30, n.1, p.165-170, 2001. http://dx.doi.org/10.1590/S1519-566X2001000100025
http://dx.doi.org/10.1590/S1519-566X2001...
). The frequent presence of new flushes in young plants may favor the survival of D. citri, and an early HLB infection (HALBERT; MANJUNATH, 2004HALBERT, S.E.; MANJUNATH, K.L. Asian citrus psyllids (Sternorryncha: Psyllidae) and greening disease of citrus: A literature review and assessment of risk in Florida. Florida Entomologist, v.87, n.3, p.330-353, 2004. https://doi.org/10.1653/0015-4040(2004)087[0330:ACPSPA]2.0.CO;2
https://doi.org/10.1653/0015-4040(2004)0...
). Therefore, newly planted citrus trees have been protected with long acting systemic insecticides (QURESHI et al., 2014QURESHI, J.A.; KOSTYK, B.C.; STANSLY, P.A. Insecticidal suppression of Asian citrus psyllid Diaphorina citri (Hemiptera: Liviidae) vector of huanglongbing pathogens. PLOS ONE, v.9, n.12, p.1-22, 2014. https://doi.org/10.1371/journal.pone.0112331
https://doi.org/10.1371/journal.pone.011...
), and techniques that avoid the access of insects to citrus plants have been adopted (CROXTON; STANSLY, 2014CROXTON, S.D.; STANSLY, P.A. Metalized polyethylene mulch to repel Asian citrus psyllid, slow spread of huanglongbing and improve growth of new citrus plantings. Pest Management Science, v.70, n.2, p.318-323, 2014. http://dx.doi.org/10.1002/ps.3566
http://dx.doi.org/10.1002/ps.3566...
; MIRANDA et al., 2015MIRANDA, M.P.; SANTOS, F.L.D.O.S.; FELIPPE, M.R.; MORENO, A.; FERERES, A. Effect of UV-blocking plastic films on take-off and host plant finding ability of Diaphorina citri (Hemiptera: Liviidae). Journal of Economic Entomology, v.108, n.1, p.245-251, 2015. http://dx.doi.org/10.1093/jee/tou036
http://dx.doi.org/10.1093/jee/tou036...
).

The populations of D. citri are regulated by ecological factors of biotic nature: competition, natural enemies and host plant, and abiotic nature: environmental conditions (YANG et al., 2006YANG, Y.; HUANG, M.; C. BEATTIE, G. A.; XIA, Y.; OUYANG, G.; XIONG, J. Distribution, biology, ecology and control of the psyllid Diaphorina citri Kuwayama, a major pest of citrus: A status report for China. International Journal of Pest Management, v.52, n.4, p.343-352, 2006. http://dx.doi.org/10.1080/09670870600872994
http://dx.doi.org/10.1080/09670870600872...
). Among the natural enemies of D. citri, the parasitoid Tamarixia radiata Waterston (Hymenoptera: Eulophidae) was reported as the most important biological control agent (PLUKE et al., 2008PLUKE, R.W.H.; QURESHI, J.A.; STANSLY, P.A. Citrus flushing patterns, Diaphorina citri (Hemiptera: Psyllidae) populations and parasitism by Tamarixia radiata (Hymenoptera: Eulophidae) in Puerto Rico. Florida Entomologist, v.91, n.1, p.36-42, 2008. https://doi.org/10.1653/0015-4040(2008)091[0036:CFPDCH]2.0.CO;2
https://doi.org/10.1653/0015-4040(2008)0...
), and it was the only natural enemy observed in citrus areas of São Paulo (PAIVA; PARRA, 2012aPAIVA, P.E.B.; PARRA, J.R.P. Life table analysis of Diaphorina citri (Hemiptera: Psyllidae) infesting sweet orange (Citrus sinensis) in São Paulo. Florida Entomologist, v.95, n.2, p.278-284, 2012a. https://doi.org/10.1653/024.095.0206
https://doi.org/10.1653/024.095.0206...
). Although predators are important in the control of immature D. citri in other citrus areas (MICHAUD, 2004MICHAUD, J.P. Natural mortality of Asian citrus psyllid (Homoptera: Psyllidae) in central Florida. Biological Control, v.29, n.2, p.260-269, 2004. http://dx.doi.org/10.1016/S1049-9644(03)00161-0
http://dx.doi.org/10.1016/S1049-9644(03)...
; QURESHI; STANSLY, 2009QURESHI, J.A.; STANSLY, P. A. Exclusion techniques reveal significant biotic mortality suffered by Asian citrus psyllid Diaphorina citri (Hemiptera: Psyllidae) populations in Florida citrus. Biological Control, v.50, n.2, p.129-136, 2009. http://dx.doi.org/10.1016/j.biocontrol.2009.04.001
http://dx.doi.org/10.1016/j.biocontrol.2...
), there is no evidence that they are important in Brazil (São Paulo state).

In contrast to what occurs under artificial conditions, where immature individuals of D. citri have high survival rates (> 70%) (NAVA et al., 2007NAVA, D.E.; TORRES, M.L.G.; RODRIGUES, M.D.L.; BENTO, J.M.S.; PARRA, J.R.P. Biology of Diaphorina citri (Hem., Psyllidae) on different hosts and at different temperatures. Journal of Applied Entomology, v.131, n.9-10, p.709-715, 2007. http://dx.doi.org/10.1111/j.1439-0418.2007.01230.x
http://dx.doi.org/10.1111/j.1439-0418.20...
), these immatures have presented low survivals rates in citrus under natural conditions; less than 10% in Florida, USA, (MICHAUD, 2004MICHAUD, J.P. Natural mortality of Asian citrus psyllid (Homoptera: Psyllidae) in central Florida. Biological Control, v.29, n.2, p.260-269, 2004. http://dx.doi.org/10.1016/S1049-9644(03)00161-0
http://dx.doi.org/10.1016/S1049-9644(03)...
), and less than 20% in São Paulo, Brazil (PAIVA; PARRA, 2012aPAIVA, P.E.B.; PARRA, J.R.P. Life table analysis of Diaphorina citri (Hemiptera: Psyllidae) infesting sweet orange (Citrus sinensis) in São Paulo. Florida Entomologist, v.95, n.2, p.278-284, 2012a. https://doi.org/10.1653/024.095.0206
https://doi.org/10.1653/024.095.0206...
). A high mortality of D. citri was observed under adverse artificial conditions by the combination of high temperatures and low air relative humidity (MCFARLAND; HOY, 2001MCFARLAND, C.D.; HOY, M.A. Survival of Diaphorina citri (Homoptera: Psyllidae), and its two parasitoids, Tamarixia radiata (Hymenoptera: Eulophidae) and Diaphorencyrtus aligarhensis (Hymenoptera: Encyrtidae), under different relative humidities and temperature regimes. Florida Entomologist, v.84, n.2, p.227-233, 2001.), or in unsuitable host plants (BORGONI et al., 2014BORGONI, P.C.; VENDRAMIM, J.D.; LOURENÇÃO, A.L.; MACHADO, M.A. Resistance of Citrus and Related Genera to Diaphorina citri Kuwayama (Hemiptera: Liviidae). Neotropical Entomology, v.43, n.5, p.465-469, 2014. http://dx.doi.org/10.1007/s13744-014-0230-0
http://dx.doi.org/10.1007/s13744-014-023...
; HALL et al., 2015HALL, D. G.; GEORGE, J.; LAPOINTE, S. L. Further investigations on colonization of Poncirus trifoliata by the Asian citrus psyllid. Crop Protection, v.72, p.112-118, 2015. http://dx.doi.org/10.1016/j.cropro.2015.03.010
http://dx.doi.org/10.1016/j.cropro.2015....
). Considering new planted citrus trees are highly attractive to D. citri adults due to the constant emission of new flushes, and are also susceptible to HLB infection, the survival of immature D. citri was estimated and compared in different seasons.

MATERIAL AND METHODS

Survival analyzes were carried out on orange trees younger than 1 year old (Citrus sinensis), cultivar Valencia, grafted on Citrus limonia. These trees were planted in June 2013, among orange trees (4 years old), cultivar Pera, in Ribeirão Preto, São Paulo state, Brazil (21°12’17”S, and 47°52’17”W). The citrus area was located at 630 m above sea level, in an eutrophic latosol with clay texture; and the climate, according to the classification by Köppen, was type Aw — tropical, with warm and humid Summers, and mild Winters with severe droughts.

Observations occurred in three periods: from July 1st to July 25th (Winter season); from October 18th to November 22nd (Spring season), 2013; and from March 23rd to April 18th (Autumn season), 2014. The trees were irrigated with 3 mm of water (drip system) in a daily basis, in dry periods. At the beginning of the experiments, the plants were pruned and fertilized (50 g of calcium nitrate per plant), and pesticides were not applied during the study.

In July 2013 (Winter), D. citri eggs were not observed, and new flushes were artificially infested. In each young flush, 5 adults of D. citri were caged for 2 days. The insects were reared in Murraya paniculata, at the facility of Escola Superior de Agricultura “Luiz de Queiroz” da Universidade de São Paulo (ESALQ-USP), in Piracicaba City, São Paulo. Fifty-seven flushes of 24 orange trees were infested during Winter. In October (Spring), in 13 orange trees, 52 flushes were naturally infested, and 30, artificially infested. In March of 2014 (Autumn), in 8 orange trees, 42 flushes with eggs were selected after a natural infestation.

Infested flushes were marked with a white line and a numbered label. Live eggs and nymphs were counted with a magnifying glass aid (10 ×) every 3 days. Small nymphs were considered from the 1st to 3rd instars, and large nymphs were those from the 4th and 5th instars. Branches with large nymphs received a cage, a voile tissue bag of 30 × 50 cm, until adult emergence. Emerged adults were withdrawn and counted. Nymphs parasitized by T. radiata were identified by characteristic mummification.

Daily data of maximum and minimum temperatures, air relative humidity (ARH) at 3 p.m., and rainfall were obtained in an automatic meteorological station located at 200 m from the citrus area. For all seasons, the number of days with:

  1. minimum temperature below 13.5°C, a lower base temperature, estimated by NAVA et al. (2007)NAVA, D.E.; TORRES, M.L.G.; RODRIGUES, M.D.L.; BENTO, J.M.S.; PARRA, J.R.P. Biology of Diaphorina citri (Hem., Psyllidae) on different hosts and at different temperatures. Journal of Applied Entomology, v.131, n.9-10, p.709-715, 2007. http://dx.doi.org/10.1111/j.1439-0418.2007.01230.x
    http://dx.doi.org/10.1111/j.1439-0418.20...
    ;

  2. maximum temperature above 32.0°C, temperature unsuitable to development of D. citri immatures (NAVA et al., 2007NAVA, D.E.; TORRES, M.L.G.; RODRIGUES, M.D.L.; BENTO, J.M.S.; PARRA, J.R.P. Biology of Diaphorina citri (Hem., Psyllidae) on different hosts and at different temperatures. Journal of Applied Entomology, v.131, n.9-10, p.709-715, 2007. http://dx.doi.org/10.1111/j.1439-0418.2007.01230.x
    http://dx.doi.org/10.1111/j.1439-0418.20...
    ); and

  3. ARH less than 30%, a condition in which the survival of nymphs is very low (PARRA et al., 2010PARRA, J.R.P.; LOPES, J.R.S.; TORRES, M.L.G.; NAVA, D.E.; PAIVA, P.E.B. Bioecologia do vetor Diaphorina citri e transmissão de bactérias associadas ao huanglongbing. Citrus Research & Technology, v.31, n.1, p.37-51, 2010. http://dx.doi.org/10.5935/2236-3122.20100004
    http://dx.doi.org/10.5935/2236-3122.2010...
    ) were calculated.

The egg-adult duration was calculated by the weighted mean, considering the number of emerged adults and the period (days) between egg stage and adult emergence. To build the life table, the model proposed by SOUTHWOOD (1978)SOUTHWOOD, T.R.E. Ecological methods: with particular reference to the study of insect populations. London: Chapman and Hall, 1978. 524p. was adopted. The number of dead insects (dx) at each stage was obtained by the difference between the number of live insects (lx) of the stage and the number of live insects in the next stage (lx1). Mortality was obtained through the relation between dead and living insects at each stage (dx / lx), and survival, through their difference (Sx = 1 - dx / lx). The parasitism of D. citri nymphs by T. radiata was calculated by the ratio (%) between mummified nymphs and large nymphs.

RESULTS

The survival of D. citri eggs was low in the 2013 Winter. After artificial infestations, 567 eggs were obtained, of which only 15 nymphs (2.6%) hatched (Table 1). Inviable eggs, initially of a light-yellow color, became dark in 2 or 3 days. The survival of small nymphs was 20%, and no large nymphs were observed in this season. Thus, with a mean minimum temperature of 12.7°C and maximum of 26.0°C, and 42.8% ARH at 3 p.m., no D. citri adults emerged during Winter (Table 2 and Fig. 1).

Table 1.
Life table for Diaphorina citri immatures on young trees (< 1 year old) of Citrus sinensis cultivar Valencia, during July 2013 and April 2014, in Ribeirão Preto City, São Paulo state, Brazil.
Table 2.
Climatic variables of seasons, survival of Diaphorina citri immatures in young trees (< 1 year old) of Citrus sinensis cultivar Valencia, and parasitism of nymphs of D. citri by Tamarixia radiata in Ribeirão Preto, São Paulo state, Brazil.
Figure 1.
Daily data: rainfall (mm) (blue bar), maximum temperature (°C) (gray line), minimum temperature (°C) (purple line), air relative humidity (%) at 3 p.m. (blue line), during all seasons in Ribeirão Preto City, São Paulo state, Brazil.

In the Spring of 2013, with minimum and maximum temperatures of 17.8 and 30.5°C, and minimum ARH of 41.6% (Table 2 and Fig. 1), the survival of D. citri immatures was higher than in the Winter of 2013, and in the Autumn of 2014 (Tables 1 and 2). From 705 eggs obtained in 82 branches (30 artificially and 52 naturally infested), 268 nymphs hatched (38.0%) (Table 1). From 705 eggs, 86 D. citri adults were obtained (12.2%) (Table 1). From oviposition, that occurred for one week, there was an emergence of adults in two weeks. The estimated egg-adult duration was 18.8 days in the Spring of 2013. In this season, egg-adult survival rates varied among the 13 citrus trees, and in six of them there was no emergence of adults (Table 3). The presence of large nymphs did not guarantee T. radiata parasitism, observed in 4 out of 9 citrus trees. D. citri parasitism rates, by T. radiata during Spring, was 9.9% (20/202), and 25% (6/24) during Autumn, despite the lower large nymph density in this season (Tables 1 and 3).

Table 3.
Number and survival of Diaphorina citri immatures during spring of 2013, and parasitism by Tamarixia radiata in 13 individual young trees (< 1 year old) of Citrus sinensis cultivar Valencia in Ribeirão Preto, São Paulo state, Brazil.

In the Autumn of 2014, with temperatures similar to those of the Spring of 2013, and slightly higher ARH (45.9%) (Table 2), the survival of D. citri immatures was low (Table 1). From 487 eggs, only 2 adults (0.4%) emerged. Despite similar temperatures and ARHs in Spring and Autumn, rainfall was higher and more frequent in the Spring of 2013 (165 mm) than in the Autumnof 2014 (48 mm) (Table 2 and Fig. 1). D. citri eggs survival was higher during Spring than Winter and Autumn (Tables 1 and 2). The survival of small nymphs was similar during Winter (20%) and Autumn (21%) (Table 1), and the survival of large nymphs was higher during Spring (47.3%) than Winter (0.0%) and Autumn (11.1%) (Table 1). Only during 2 days of Winter, the minimum temperature was below the base temperature (13.5°C) estimated for this specie. In Spring and Autumn, during most of the study period, maximum temperatures were above 32.0°C (Table 2), a thermal condition that would limit immature development.

DISCUSSION

Under natural conditions with thermal and hydric variations, which directly influence the insect and the host plant, the survival of D. citri eggs and nymphs was low in this study. In a 4 years old Valencia sweet orange trees, PAIVA; PARRA (2012a)PAIVA, P.E.B.; PARRA, J.R.P. Life table analysis of Diaphorina citri (Hemiptera: Psyllidae) infesting sweet orange (Citrus sinensis) in São Paulo. Florida Entomologist, v.95, n.2, p.278-284, 2012a. https://doi.org/10.1653/024.095.0206
https://doi.org/10.1653/024.095.0206...
reported survival variation of D. citri immatures from 10% in Spring (2006) and Autumn (2007) to 20% in Summer and late Autumn (2007). The mortality of eggs and small nymphs was the key phase for the population growth of this insect.

The results obtained under field conditions differ from those obtained under ideal conditions for insect development (25°C, and 60 – 80% ARH, constants). Under controlled conditions, the host plant did not affect the survival of D. citri eggs and nymphs; 75% of the immature D. citri survived in M. paniculata plants, which originated from seeds (LIU; TSAI, 2000LIU, H.; TSAI, J.H. Effects of temperature on biology and life table parameters of the Asian citrus psyllid, Diaphorina citri Kuwayama (Homoptera: Psyllidae). Annals of Applied Biology, v.137, n.3, p.201-206, 2000. https://doi.org/10.1111/j.1744-7348.2000.tb00060.x
https://doi.org/10.1111/j.1744-7348.2000...
). As to C. limonia, the immatures survival was of 72% (NAVA et al., 2007NAVA, D.E.; TORRES, M.L.G.; RODRIGUES, M.D.L.; BENTO, J.M.S.; PARRA, J.R.P. Biology of Diaphorina citri (Hem., Psyllidae) on different hosts and at different temperatures. Journal of Applied Entomology, v.131, n.9-10, p.709-715, 2007. http://dx.doi.org/10.1111/j.1439-0418.2007.01230.x
http://dx.doi.org/10.1111/j.1439-0418.20...
). Similarly, in Valencia sweet orange grafted on C. limonia, the survival rate was 66% (ALVES et al., 2014ALVES, G.R.; DINIZ, A.J.F.; PARRA, J.R.P. Biology of the Huanglongbing vector Diaphorina citri (Hemiptera: Liviidae) on different host plants. Journal of Economic Entomology, v.107, n.2, p.691-696, 2014. http://dx.doi.org/10.1603/Ec13339
http://dx.doi.org/10.1603/Ec13339...
), and greater than 60% in Pera and Natal oranges (NAVA et al., 2010NAVA, D.E.; GOMEZ-TORRES, M.L.; RODRIGUES, M.D.; BENTO, J.M.S.; HADDAD, M.L.; PARRA, J.R.P. The effects of host, geographic origin, and gender on the thermal requirements of Diaphorina citri (Hemiptera: Psyllidae). Environmental Entomology, v.39, n.2, p.678-684, 2010. http://dx.doi.org/10.1603/EN09252
http://dx.doi.org/10.1603/EN09252...
; BORGONI et al., 2014BORGONI, P.C.; VENDRAMIM, J.D.; LOURENÇÃO, A.L.; MACHADO, M.A. Resistance of Citrus and Related Genera to Diaphorina citri Kuwayama (Hemiptera: Liviidae). Neotropical Entomology, v.43, n.5, p.465-469, 2014. http://dx.doi.org/10.1007/s13744-014-0230-0
http://dx.doi.org/10.1007/s13744-014-023...
). In our study, in the field, for C. sinensis trees younger than 1 year old, grafted on C. limonia, there was no immature survival of D. citri in the Winter of 2013, and only 0.4% of them reached their adult life in the Autumn of 2014.

The higher survival of eggs and nymphs may explain the higher population density and population peaks of D. citri during Spring and Summer (YANG et al., 2006YANG, Y.; HUANG, M.; C. BEATTIE, G. A.; XIA, Y.; OUYANG, G.; XIONG, J. Distribution, biology, ecology and control of the psyllid Diaphorina citri Kuwayama, a major pest of citrus: A status report for China. International Journal of Pest Management, v.52, n.4, p.343-352, 2006. http://dx.doi.org/10.1080/09670870600872994
http://dx.doi.org/10.1080/09670870600872...
; YAMAMOTO et al., 2001YAMAMOTO, P. T.; PAIVA, P. E. B.; GRAVENA, S. Flutuação populacional de Diaphorina citri Kuwayama (Hemiptera: Psyllidae) em pomares de citros na região Norte do Estado de São Paulo. Neotropical Entomology, v.30, n.1, p.165-170, 2001. http://dx.doi.org/10.1590/S1519-566X2001000100025
http://dx.doi.org/10.1590/S1519-566X2001...
). During Autumn and Winter, the population was reduced, probably due to ecological factors, such as competition, natural enemies, host plants, and abiotic nature (YANG et al., 2006YANG, Y.; HUANG, M.; C. BEATTIE, G. A.; XIA, Y.; OUYANG, G.; XIONG, J. Distribution, biology, ecology and control of the psyllid Diaphorina citri Kuwayama, a major pest of citrus: A status report for China. International Journal of Pest Management, v.52, n.4, p.343-352, 2006. http://dx.doi.org/10.1080/09670870600872994
http://dx.doi.org/10.1080/09670870600872...
). Although D. citri adults occur at any period and season, eggs and nymphs were only observed when there were citrus flushes. Moreover, population outbreaks can occur if environmental conditions are favorable and new shoots are available (HALL et al., 2008HALL, D. G.; HENTZ, M. G.; ADAIR Jr., R. Population ecology and phenology of Diaphorina citri (Hemiptera: Psyllidae) in two Florida citrus groves. Environmental Entomology, v.37, n.4, p.914-924, 2008. https://doi.org/10.1093/ee/37.4.914
https://doi.org/10.1093/ee/37.4.914...
).

The frequent presence of flushes in young plants may favor the survival of D. citri and an early HLB infection (HALBERT; MANJUNATH, 2004HALBERT, S.E.; MANJUNATH, K.L. Asian citrus psyllids (Sternorryncha: Psyllidae) and greening disease of citrus: A literature review and assessment of risk in Florida. Florida Entomologist, v.87, n.3, p.330-353, 2004. https://doi.org/10.1653/0015-4040(2004)087[0330:ACPSPA]2.0.CO;2
https://doi.org/10.1653/0015-4040(2004)0...
). Therefore, in new plantations, young trees are rigorously protected with systemic insecticides of long residual action (QURESHI et al., 2014QURESHI, J.A.; KOSTYK, B.C.; STANSLY, P.A. Insecticidal suppression of Asian citrus psyllid Diaphorina citri (Hemiptera: Liviidae) vector of huanglongbing pathogens. PLOS ONE, v.9, n.12, p.1-22, 2014. https://doi.org/10.1371/journal.pone.0112331
https://doi.org/10.1371/journal.pone.011...
), or foliar insecticide sprays, based on a fixed schedule (BELASQUE JUNIOR et al., 2010BELASQUE JUNIOR, J.; BASSANEZI, R.B.; YAMAMOTO, P.T.; AYRES, A.J.; TACHIBANA, A.; VIOLANTE, A.R.; TANK JUNIOR, A.; DI GIORGI, F.; TERSI, F.E.A.; MENEZES, G.M.; DRAGONE, J.; JANK, JR, R.H.; BOVÉ, J.M. Lessons from huanglongbing management in São Paulo State, Brazil. Journal of Plant Pathology, v.92, n.2, p.285-302, 2010. http://dx.doi.org/10.4454/jpp.v92i2.171
http://dx.doi.org/10.4454/jpp.v92i2.171...
). Additionally, methods that prevent insect access to plants may be adopted (CROXTON; STANSLY, 2014CROXTON, S.D.; STANSLY, P.A. Metalized polyethylene mulch to repel Asian citrus psyllid, slow spread of huanglongbing and improve growth of new citrus plantings. Pest Management Science, v.70, n.2, p.318-323, 2014. http://dx.doi.org/10.1002/ps.3566
http://dx.doi.org/10.1002/ps.3566...
; MIRANDA et al., 2015MIRANDA, M.P.; SANTOS, F.L.D.O.S.; FELIPPE, M.R.; MORENO, A.; FERERES, A. Effect of UV-blocking plastic films on take-off and host plant finding ability of Diaphorina citri (Hemiptera: Liviidae). Journal of Economic Entomology, v.108, n.1, p.245-251, 2015. http://dx.doi.org/10.1093/jee/tou036
http://dx.doi.org/10.1093/jee/tou036...
).

Adults of D. citri exhibit a high tolerance to extreme temperatures, and can survive in low-temperature conditions (0 or 5°C for 1 day) (EL-SHESHENY et al., 2016EL-SHESHENY, I.; HIJAZ, F.; EL-HAWARY, I.; MESBAH, I.; KILLINY, N. Impact of different temperatures on survival and energy metabolism in the Asian citrus psyllid, Diaphorina citri Kuwayama. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, v.192, p.28-37, 2016. http://dx.doi.org/10.1016/j.cbpa.2015.11.013
http://dx.doi.org/10.1016/j.cbpa.2015.11...
), as well as oviposit in warm environments (35°C), depositing about 30 eggs within 48 hours (HALL et al., 2011HALL, D. G.; WENNINGER, E. J.; HENTZ, M. G. Temperature studies with the Asian citrus psyllid, Diaphorina citri: Cold hardiness and temperature thresholds for oviposition. Journal of Insect Science, v.11, n.83, p.1-15, 2011. https://doi:10.1673/031.011.8301
https://doi:10.1673/031.011.8301...
). Similarly, D. citri adults can survive in very dry environments (MCFARLAND; HOY, 2001MCFARLAND, C.D.; HOY, M.A. Survival of Diaphorina citri (Homoptera: Psyllidae), and its two parasitoids, Tamarixia radiata (Hymenoptera: Eulophidae) and Diaphorencyrtus aligarhensis (Hymenoptera: Encyrtidae), under different relative humidities and temperature regimes. Florida Entomologist, v.84, n.2, p.227-233, 2001.). This fact may explain the peak population of D. citri during late Winter and early Spring, as observed by YAMAMOTO et al. (2001)YAMAMOTO, P. T.; PAIVA, P. E. B.; GRAVENA, S. Flutuação populacional de Diaphorina citri Kuwayama (Hemiptera: Psyllidae) em pomares de citros na região Norte do Estado de São Paulo. Neotropical Entomology, v.30, n.1, p.165-170, 2001. http://dx.doi.org/10.1590/S1519-566X2001000100025
http://dx.doi.org/10.1590/S1519-566X2001...
for the conditions of São Paulo.

D. citri parasitism by T. radiata occurred in all seasons of the study, even in very low densities from the third to the fifth instar nymphs (2013 Winter, and 2014 Autumn). In previous research, the highest rates of parasitism were observed during Summer (25%) and Autumn (15%), and the lowest, during Spring (11%) and Winter (6%) (PAIVA; PARRA, 2012bPAIVA, P.E.B.; PARRA, J.R.P. Natural parasitism of Diaphorina citri Kuwayama (Hemiptera, Psyllidae) nymphs by Tamarixia radiata Waterston (Hymenoptera, Eulophidae) in São Paulo orange groves. Revista Brasileira de Entomologia, v.56, n.4, p.499-503, 2012b. http://dx.doi.org/10.1590/S0085-56262012000400016
http://dx.doi.org/10.1590/S0085-56262012...
). The data obtained in this study for Spring were similar to those obtained by these authors, indicating that this season is the most favorable to the development of D. citri, and that the lower parasitism by T. radiata may be one key factor for the greater population observed during Spring.

In addition to the parasitoids, the role of predators in the regulation of the D. citri population should be considered, mainly of nymphs, a stage with low mobility and restricted to new shoots. MICHAUD (2002)MICHAUD, J.P. Classical biological control: A critical review of recent programs against citrus pests in Florida. Annals of the Entomological Society of America, v.95, n.5, p.531-540, 2002. http://dx.doi.org/10.1603/0013-8746(2002)095[0531:CBCACR]2.0.CO;2
http://dx.doi.org/10.1603/0013-8746(2002...
considered the contribution of predators to the biological control of D. citri greater than that of T. radiata in Florida (USA), and suggested that parasitism could be overestimated, because mummified (parasitized) nymphs are not predated and remain longer in citrus leaves. The T. radiata parasitoid, as far as it is concerned, is the only natural enemy associated with D. citri in São Paulo (PAIVA; PARRA, 2012aPAIVA, P.E.B.; PARRA, J.R.P. Life table analysis of Diaphorina citri (Hemiptera: Psyllidae) infesting sweet orange (Citrus sinensis) in São Paulo. Florida Entomologist, v.95, n.2, p.278-284, 2012a. https://doi.org/10.1653/024.095.0206
https://doi.org/10.1653/024.095.0206...
).

The low survival of eggs and small nymphs, and additional parasitism of the fourth and fifth instars by T. radiata may limit the natural growth of D. citri population in citrus. Although abiotic factors are not enough to prevent the spreading of HLB pathogens, they play an important role in the natural mortality of eggs and small nymphs, preventing the insect from reaching high populations in São Paulo citrus orchards.

ACKNOWLEDGMENTS

We thank APTA Regional Leste for the assignment of the area for the experiment, the Integrated Pest Management Laboratory of ESALQ-USP for supplying the insects, and Instituto Agronômico de Campinas (IAC) for climatological data.

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Publication Dates

  • Publication in this collection
    14 Nov 2019
  • Date of issue
    2019

History

  • Received
    24 Nov 2018
  • Accepted
    01 Aug 2019
Instituto Biológico Av. Conselheiro Rodrigues Alves, 1252 - Vila Mariana - São Paulo - SP, 04014-002 - São Paulo - SP - Brazil
E-mail: arquivos@biologico.sp.gov.br