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© 2011 Plant Management Network.
Accepted for publication 27 June 2011. Published 3 October 2011.


A Review of Huanglongbing (Citrus Greening) Management in Citrus Using Nutritional Approaches in China


Yulu Xia, Assistant Director, Center for Integrated Pest Management, North Carolina State University, Raleigh, NC 27606; Gecheng Ouyang, Associate Professor, Guangdong Entomological Institute, Guangzhou, China; Ronald A. Sequeira, National Science Program Leader, Yu Takeuchi, Pest Risk Analyst, and Ignacio Baez, National Program Staff Scientist, USDA-APHIS Center for Plant Health Science and Technology, Raleigh, NC 27606; Jianchi Chen, Research Plant Pathologist, UDSA-ARS Crop Diseases, Pests and Genetics, Parlier, CA 93648


Corresponding author: Yulu Xia. Yulu_xia@ncsu.edu


Xia, Y., Ouyang, G., Sequeira, R. A., Takeuchi, Y., Baez, I., and Chen, J. 2011. A review of huanglongbing (citrus greening) management in citrus using nutritional approaches in China. Online. Plant Health Progress doi:10.1094/PHP-2010-1003-01-RV.


Abstract

The Asian form of huanglongbing (HLB) is caused by ‘Candidatus Liberibacter asiaticus (Las),’ a phloem-limited bacterium transmitted by the Asian citrus psyllid, Diaphorina citri Kuwayama. Nutrient management, together with other cultural practices such as pruning and irrigation, for mitigation of the disease has been practiced in China for many years. Our literature review, field survey, and interviews with Chinese scientists and growers indicate that these cultural practices were generally ineffective for the disease management. However, a nutritional approach in conjunction with other cultural practices such as irrigation can maintain grove productivity for a certain time depending on the type of citrus species/cultivars, the age of the trees, the propagation method of the plants, the Asian citrus psyllid (ACP) (Diaphorina citri Kuwayama) population, and other factors. Symptomatic mature pommelo (Citrus maxima Merr) and sweet orange (C. sinensis L. Osbeck) plants can commonly survive and maintain a certain level of productivity for an additional 4 to 5 years, even longer assuming vigorous ACP control.


HLB in China and Studies on Nutritional Approach for HLB Management

Huanglongbing (HLB) is caused by ‘Candidatus Liberibacter asiaticus (Las),’ a phloem-limited bacterium transmitted by the Asian citrus psyllid, Diaphorina citri Kuwayama. Although HLB was first reported in China early in the past century (1,4,21), the disease might have occurred in Guangdong province in the late 1800s (14,20). HLB was already a major citrus disease in Chaoshan, Guangdong province, in the 1930s (3,7,20). The disease spread to neighboring citrus-producing provinces from Guangdong, although it remains questionable whether Chaoshan is the sole source of early HLB infestation in China (X. Y. Zhao, personal communication). The disease reportedly occurs in a total of 11 provinces and is still the number one threat to citrus production in Guangdong, Guangxi, and Fujian provinces (Fig. 1).


Fig. 1. Citrus producing regions and HLB occurrence in China.


In the early days, lack of nutrition and/or other cultural factors such as insufficient soil moisture were believed to cause the disease (2,3,7,8,9,10,19). Scientific studies regarding the role of micronutrients and fertilizers on disease progress and citrus production in infected groves were conducted fairly early in China. The first comprehensive study was implemented from 1937 to 1941 (14). The main purpose of this study was a more etiological consideration of HLB than disease management. The study was conducted at what was then Lingnan University; the agricultural division of the university that later became the present-day South China Agricultural University (SCAU) in the capital of Guangdong province. The study was divided into a series of independent field experiments. The main objective of this study was HLB etiology, e.g., whether malnutrition was the cause of the disease. The results of this 5-year study were published in four reports. Here, we selectively present experiments from the study and their results.

1. Application of micronutrients such as zinc sulphate (ZnSO4), copper sulphate (CuSO4), boron (H3BO3), calcium sulphate (CaSO4), ferric sulphate (FeSO4), and potassium hydrophosphate (KH2PO4) by trunk injection and soil drench appeared to have no impact on disease progress.

a. Injection. This experiment was conducted on 0.05 ha of 6- to 7-year-old Tankan mandarin grove. The citrus trees were infected with HLB for one to two years. Micronutrients were applied manually to a drilled hole 30 cm (about 1 foot) from the ground on the trunk. The treatments and doses are listed in Table 1. Each treatment was replicated six times (six trees), with one untreated tree having a drilled hole, another without.


Table 1. Micronutrients applied by trunk drilling (20 August 1937-July 1938) [Chen 1943 (1)].

Nutrients ZnSo4 CuSo4 H3BO3 CaSo4 KHPo4 MgSo4 Dose
(g/tree)
Dose (g/tree) 0.5 0.2 0.1 1.5 1.0 0.2
Treatment I + + + + + + 3.5
II + + + + +    3.3
III + + + +       2.3
IV + + +          0.8
V + +             0.7
VI +                0.5

b. Soil drench. This experiment was conducted on 0.10 ha of 3- to 9-year-old Tankan mandarin grove. The citrus trees were infected with HLB, based on symptomatic expression, for anywhere from several months to several years. Micronutrient solutions were applied to the soil surrounding the trunk base. The top surface soil near the trunk base was removed before application and the treated areas were covered with rice straw after the application. The treatments and doses are listed in Table 2.


Table 2. Micronutrients applied by soil application (20 August 1937-July 1938).

Micronutrient ZnSO4 CuSO4 H3BO3 CaSO4 KHPO4 MgSO4 Dose
(liter/
tree)
Concentration (%) 10% 5% 4% 15% 6% 3%
Treatment I + + + + + + 5
II + + + + +    5
III + + + +       4
IV + + +          4
V + +             3
VI +                3

The results of this experiment are listed in Table 3. All 5 to 6 trees receiving each treatment were reported dead or deteriorated, with the exception of one tree receiving trunk injection (treatment II) and three trees receiving trunk injection of ZnSO4 (treatment VI) only. However, in the latter case, the symptomatic untreated control tree also did not die or deteriorate. Notably, none of the initially asymptomatic trees developed symptoms during the year-long experiment.


Table 3. Results of trunk and soil applications of micronutrients on infected citrus plants (20 August 1937-July 1938) (1 plant/rep) [Chen 1943 (1)].

Replicates Performance of treated plantsx Ctrlx Ctrly
1 2 3 4 5 6
Treat-
ments
I Trunk filling D D D D D D D N
Soil trench X X D D X    D N
II Trunk filling X X D O X X X N
Soil trench D D D D X   X N
III Trunk filling X X D D D D N N
Soil trench X D X D X   X N
IV Trunk filling D D D X D D D N
Soil trench X X X X D    X N
V Trunk filling N D D D D D D N
Soil trench O X X D X    D N
VI Trunk filling D N N D D N N N
Soil trench X X X X X    O N

Abbreviations: X = deteriorated, N = no change, D = dead, O = renew growth.

 x Started as symptomatic plants.

 y No symptoms on plants.


2. Application of micronutrients such as zinc sulphate (ZnSO4), copper sulphate (CuSO4), boron (H3BO3), calcium sulphate (CaSO4), ferric sulphate (FeSO4), potassium hydrophosphate (KH2PO4) by leaf spray and trunk painting resulted in no reduction in disease progress.

3. Several field trials were conducted to investigate the impact of foliar applications with micronutrients on disease progress. These studies were carried out on different citrus species and/or cultivars in different locations across Guangdong over a 3-year period. The outcomes from these studies showed no difference in the treated and untreated trees in terms of number of dead trees and visual disease progress by the end of the experiment. Table 4 gives the details for one of these trials. This study was conducted at a 4-year-old Ponkan mandarin (Citrus reticulata Blanco cv. 'Ponkan') grove. The infected trees were in the early stages of symptomatic disease expression.


Table 4. Micronutrient treatments by foliar application.

Nutrients ZnSO4 CuSO4 H3BO3 CaSO4 KH2(PO4) MgSO4 Dose
(g/liter)
Solution (g/liter)

25

12.5 10 37.5 15 17.5
Treatment I + + + + + + 117.5
II + + + + +   100.0
III + + + +        85.0
IV + + +       47.5
V + +         37.5
VI +           25.0
Control (infested)             No trt
Control (healthy)             Trt

Other trials that included application of micronutrients for HLB prevention also yielded negative outcomes (i.e., no disease regression).

Above we highlighted a few results from the extensive, data-packed publication by Chen (1). We have translated key sections into English and interested readers can contact the senior author for more information. It is worth noting that the number of trees in some of the experiments was small. In addition, no systematic statistical analysis was conducted throughout the study, and the interactions of various factors (micronutrients here) were not considered when designing the field experiments. These shortfalls were common in early field research. Additionally, some of the experiments were conducted in relatively young trees (3 to 4 years old). As we will point out later, young infected citrus trees generally do not perform as well as mature trees under a nutritional program or other cultural practices such as irrigation. We also note that yield was not specifically reported in these studies. Nevertheless, those observations may be considered to provide empirical baselines.

Gao and Zheng (2) conducted a series of field studies at Liufeng Village in Fujian province. This study demonstrated the different responses among orange species/cultivars to nutrient applications. Following are some relevant trials:

1. Foliar applications of micronutrients plus other cultural management in mature (9 to 11 years) Ponkan mandarins. A cocktail of micronutrients (Co, Mg, Zn, Ca, Mn, Mo, etc.) was applied by leaf spray at every "flush" in 1960. The total number of treated trees in the grove was 100; 15 of them had HLB symptoms. When results were checked in December 1961, the disease incidence had increased rapidly and there were few fruits on the infected trees. Insect pests, including psyllids, were managed in the grove.

2. Nutritional management plus cultural management program in young Ponkan mandarins (the exact age of the trees was not given). A total 87 seedlings were used − 45 as treated, 42 as untreated controls − and planted in the spring of 1960. Best management practices [e.g., fertilizer application (no mention of fertilizer type) every two months plus other production measures such as irrigation] were also used in the treated trees. By the end of 1961, the disease incidence in the treated and untreated trees reached 42.2% and 42.5%, respectively. All seedlings were soon dead. These seedlings were air-layered plants from the "healthy plants" (though they were obviously not). It was not clear whether micronutrients were applied in the plot.

3. Nutritional management plus cultural management program in mature sweet oranges and tangerines. The trial was conducted in a plot of sweet orange (Citrus sinensis Osbeck ‘kinkunembo’) and tangerines (Citrus tangerina hort. ex Tanaka) (20-year-old). The trial was initiated in 1962 and results were recorded in December 1963. The objective was to compare the disease progress and fruit yield under the local management program to a "best management practices" (including, optimized fertilization and irrigation) program. This trial yielded some interesting results. Under the best practices management program, 1) the disease progress seemed halted (sweet orange) or progressed more slowly (tangerine); 2) symptomatic plants renewed some growth; and 3) yield increased compared to the previous year for C. tangerina hort. ex Tanaka (Table 5).


Table 5. Disease progress and fruit yield of HLB-infected trees (20 years old).

Species/
cultivar
Treatment #
trees
%
infected
(1962)
%
infected
(1963)
%
 infection
increase
% yield
increase
/tree
Av treatedx 97 49.7 50.5 0.8 22.2
Av untreatedy 27 66.6 92.5 25.9 0
Bw treatedx 113 24.7 30.9 6.2 35.4z

 v A: C. sinensis Osbeck forma kinkunembo.

 w B: Citrus tangerina hort. ex Tanaka.

 x best management program.

 y local management program.

 z compared to previous year (1962).


         Although the author did not specify the specific details of the best management program, our interviews with other scientists who conducted similar tests in China at the time indicated that the program included leaf spray micronutrients, more frequent fertilization, regular irrigation, and pruning diseased branches (but no pruning was conducted in this trial, as the author clearly stated in the paper).

4. A survey of citrus groves at the same village provided additional evidence that the addition of nutrients to certain symptomatic citrus trees might be helpful in maintaining citrus production. According to Gao and Zheng (2), the village first reported HLB occurrence in 1941. By 1957, the disease was found in most groves and the disease incidence increased steadily, reaching 42% symptomatic plants in 1963. An enhanced citrus management program, e.g., with the addition of nutrients and irrigation, was implemented in 1962. Total fruit yield for citrus from this village increased 32.4% and 41.2% in the years 1962 and 1963, respectively, compared to 1961. This result appears consistent with grower experiences in Florida (Phil Stansly, personal communication). Unfortunately, there were no records beyond 1963 in this early Chinese study.

Since the study conducted by Gao and Zheng (2) did not separate nutrition/fertilization from other cultural practices such as irrigation in the best practices management program, one could question which measure or combination of these measures played the key role in the observed yield increase and halted/slowed disease progress. Additionally, some citrus plants in the grove were grown directly from seeds (vs. grafted plants) and we do not know what role this factor may have played in the yield increase. We can speculate that additional nutrition/fertilization and irrigation can provide at least a short-term growth boost to diseased plants, especially if the grove was not optimally managed at the outset. Additionally, the age of the citrus trees likely played a key role here. It seems that older trees (>10-year) responded better to the increased nutrition and other cultural practices. It was especially true in mature sweet orange based on the results from this study and our interviews with leading Chinese scientists such as Professors Zhao Xue Yuan and Ke Chong which helped interpret research results. Clearly, the study indicated that disease progress subsided and fruit production improved under the best practices management program. Given the intriguing nature of these records, this publication (2) has been translated into English. Interested readers can contact the senior author for copies.

Dr. K. H. Lin, a world-renowned HLB scientist at SCAU, as well as other scientists in China conducted a number of field studies and surveys to evaluate the impact of nutrition/fertilization and other cultural practices on HLB-infected plants from the 1950s to 1970s. Unfortunately, detailed information on experimental design and treatment data for these studies is no longer available. Based on the summary reports and our interview with the scientists who conducted these studies, results of these studies did not show significant differences in terms of disease progress under different fertilization and nutrition conditions (2,6,9,16,17,18,19,23,24). Despite the overall trend of limited effectiveness of nutrition application for managing HLB-infected groves, Lin noted different performance among orange species/cultivars in response to nutrient application as well as other cultural management practices such as pruning and irrigation.

The former Guangxi HLB Research Team lead by Professor X. Y. Zhao conducted a series of field studies at Liuzhou Horticultural Farm, Liuzhou Citrus Farm, and Liuzhou Regional Agricultural Research Institutes during the 1960s to 1970s. The main goals of these tests were to evaluate whether cultural practices can cure the infected plants or prevent or reduce HLB infection. The cultural practices included removal of decayed roots in combination with extensive application of organic fertilizers, few or no synthetic fertilizers, pruning the diseased branches, and leaf surface fertilization. Although these practices resulted in strong spring flushing in the diseased plants, they did not reduce incidence or severity of HLB later in the year (23,24). However, the researchers observed that these diseased plants maintained good productivity for several years with enhanced nutritional programs, coupled with good irrigation and pruning. This was especially true for pommelo, sweet orange, and certain cultivars of mandarins.

One key difference in comparing these studies to current ongoing nutritional studies in Florida is that the early studies in China were predominantly soil applications of nutrients, fertilizers, or animal and human manure, whereas current studies in Florida emphasize foliar applications of micronutrients. Another important difference is that we do not know whether psyllids were effectively controlled in these early Chinese studies, or even considered at the time since the vector nature of ACP was not well understood. This makes it more difficult to compare the results to the outcomes in Florida where psyllid populations in the experimental and commercial groves are well controlled. However, even if the psyllid, or any insect, was not known to be the vector, psyllid populations might have been well managed if an insect pest management program was implemented at the test site. Organochloride insecticides or other broad-spectrum insecticides were widely used for citrus pest management during the time; the psyllid was likely often an unintentional target.

In summary, we highlight key studies in China that indicate:

1. Application of micronutrients either by soil and leaf surface application, together with other cultural practices, had limited effects on HLB disease progress and spread.

2. However, increased nutrition, coupled with other cultural practices such as irrigation, may have prolonged grove productivity for variable periods. It appears that important variables linked to production sustainability include:

a. Citrus species/cultivars. Pommelo and sweet orange generally have a better response than mandarin.

b. Age/size of trees at the time of infestation. Mature/full-grown infected trees (10 or more years old) can sustain productivity longer than younger trees, especially with a good nutritional program.

c. Propagation method. Plants grown from seeds or air-layering (not a current commercial practice in China or elsewhere) showed better response to nutritional programs.

Further study is urgently needed to clarify some of the knowledge gaps noted above.


Survey of Nutritional Approaches in the Field

Nutrition and other cultural practices for managing HLB have likely been in use as long as the disease has existed in China. This is especially true since it was believed that nutritional shortages might be one of the causes for the disease. Thus, adding homemade fertilizers such as plant residues and human and animal manure was a common practice in HLB-infected groves. Later, the infectious nature of the disease was preliminarily demonstrated in the late 1930s (1) and confirmed in the 1950s (9,19). The now well-known three-pronged approach to combating the disease was first elaborated by Dr. Lin. This three pronged disease management approach includes:

1. elimination of inoculum sources by removal of symptomatic trees;

2. insecticide treatments to minimize insect vector populations; and

3. use of pathogen-free seedlings for new plantings.

Additionally, a domestic quarantine measure was also proposed as a key step (12).

Disagreement and debates among scientists and government officials regarding the use of cultural approaches, including the use of micronutrients and fertilizers for managing HLB often took on political overtones in China during the 1950s to the 1980s. One group was led by Dr. Lin and a number of plant pathologists who were against using any cultural or nutritional approach for disease management and emphasized tree removal and the three-pronged approach. Another group, mainly made by government officials in charge of regulatory management, as well as horticulturists, plant physiologists, and entomologists did not believe in the three-pronged approach, but endorsed cultural management approach. This group believed that the disease could be effectively controlled by using cultural practices alone, denying the necessity of removal of infected trees as a source of inoculums. Their claim was supported by field observations or field visits rather than research or actual experiments (2,10,5,13,22). These pro-nutrition supporters believed that nutrition and other cultural practices could not only prolong grove productivity, but also control or even eradicate the disease. In this sense, the approach they advocated is fundamentally different from the nutritional approach being used in Florida that emphasizes foliar applications of both micronutrients and macronutrients, in addition to seeking a number of additional phytosanitary measures including the use of organic acids, SAR elicitors, Bacillus subtilis, hydrogen peroxide, potassium phosphate, together with vigorous ACP management program.

Fierce debates regarding the value of the nutritional approach and other cultural management practices were held in major scientific meetings such as the SCAU Scientific Forum and the meetings organized by the Ministry of Agriculture, top scientific journals such as Acta Phytopathologica Sinica, and even major public media (2,8,13,22,24,25).

Many field success stories of managing HLB by using nutrition together with other cultural practices were claimed in China; however, many of these stories were not scientifically verified. A typical case happened in the 1950s, when a number of influential citrus growers (so-called "Model Workers"), such as Mr. Guo Kun Chen in Fujian, claimed that by using nutrition (fertilization) together with other cultural measurements such as cutting the decayed roots, their infected citrus plants were "cured" and production restored. A few scientists joined in supporting the claim (5,10). This led to a massive "Grass-Root Movement of HLB Control" program in the large areas of Guangdong and Fujian, two provinces with the most severe HLB infestation in 1958, with the aim of eradicating the disease from the areas in a year or two (5,24). The main approach in the program included increasing fertilization and nutrition, cutting heavily infected branches only, and removing decayed roots. By the end of 1959, this very large government-organized program failed to produce results. HLB became even more serious. Dr. Lin investigated these "successfully cured" fields later and found that either the infected trees were dead already or claims were made that were found to be false (2,24).

Currently, few growers emphasize the role of nutrition in HLB management program in China. Rather, nutritional management is used as a part of an overall integrated citrus production system. This is especially true in large-scale commercial production. Micronutrient products such as those shown in Figure 2 continue to be commonly used.


   

Fig. 2. Micronutrient product (containing boron, zinc, magnesium, selenium, and calcium) used in a plantation in Gong Cheng county, Guangxi province.

 

Discussion

Overall, our survey in China has not found consistent evidence to support the nutritional approach as an effective means of maintaining grove productivity or slowing disease progress in HLB-infected plants. Nor is there evidence of widespread current use of a nutritional-only approach for HLB management in China. However, our field surveys and interviews with Chinese scientists and growers point to strong evidence that the infected grown citrus plants can remain productive for years under a good nutritional program combined with other cultural practices such as good irrigation. It is particularly evident that mature pommelo and sweet orange plants can maintain productivity for 4 to 5 years, even longer under a good nutrition program after HLB symptoms become apparent. Our recent investigation in a citrus farm in southern Fujian province where HLB has been severe since 1940s reveals even more intriguing facts. In spite of repeated HLB outbreaks at the farm, a total of 410 old Ponkan and Jiaogan mandarins (Citrus reticulata Blanco ‘Jiaogan’), mostly planted in 1967 and 1974, remain productive with foliar application of a cocktail of micronutrients twice a year and other cultural practices such as pruning and irrigation, together with vigorous ACP management. Among them, 123 (30%) plants are HLB symptomatic. Evidence indicates that these plants were infected with the disease from 2001 to 2003. This means that infected plants survive and maintain certain level productivity for about eight years. The fact that Ponkan and Jiaogan mandarins are known as the most susceptible cultivars to HLB makes observation very unusual. We do not think this is due to plant resistance to HLB because a large number of infected trees of same cultivars had been removed from the groves. Rather, the effective psyllid control after the initial infection, mature plant size at the time of infection, pruning, nutritional approach, among others, might play key role here.

Although a majority of well-managed groves today, such as the large commercial production areas in Guangxi province, adopt the three-pronged approach, there is a wide discrepancy in timing of removal of HLB infected plants. Generally speaking, few groves remove grown trees at the first appearance of symptoms. In a few special cases, infected mature trees may survive and maintain productivity for a prolonged period even under conventional practices. Further studies are underway to investigate and monitor the infection rate and titer change of these infected but productive old trees.

Although the results from field studies and large commercial applications of the nutritional approach in China are valuable in providing perspective, these studies were conducted with specific conditions and limited knowledge several decades ago. The objectives, application methods, and citrus production system were markedly different from current studies. For example, there were likely no psyllid-focused control programs implemented in most of the studies, since psyllids were not known to be disease vectors until early 1970s in China. This alone can lead to different outcomes. In addition, nutrient materials and application methods used at the time can have different results from those used today.

The main objective of nutritional approaches, as we stated in the beginning, is to prolong citrus production under HLB infestation, as an alternative to immediate removal of trees at the first signs of infection, especially in the mature groves. Since nutritional approach have not been shown to cure or slow HLB progress, these infected plants may eventually lose productivity, even under the best nutritional scenarios. The essence of the argument might not be about whether or not we should remove infected trees, but when. A balanced approach that considers short-term survival of the industry and long-term prospects, scientific principle and the economic reality, is needed.


Acknowledgements

The authors wish to thank Professor Zhao Xue Yuan, Citrus Research Institute, Chinese Academy of Agricultural Science, and many our colleagues in China and the United States for helping us with this survey, data collection, and reviewing the article. This article is a joint effort by the United States Department of Agricultural, Animal and Plant Health Inspection Service, Plant Protection and Quarantine, Center for Plant Health Science and Technology and North Carolina State University.


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