An Integrated Disease Management of Oil Palms Affected by Bud Rot Results in Shorter Recovery Times

Bud rot is a limiting disease that affects most oil palm crops destroying thousands of hectares in Latin America. Bud rot (BR) is caused by the oomycete Phytophthora palmivora (Butler). Integrated disease management (IDM) technology has been used to control the disease, which slows down the progress of the disease, allowing palm recovery. However, the effect of this technology on the recovery speed of treated palms is not well known. We studied the time taken for palm recovery from BR under the integrated management approach. The study was carried out on 21 oil palm commercial cultivars dura × pisifera (D × P) and O × G hybrids affected by BR in the Colombian oil palm Central Zone. The analysis included different recovery times (RT), the severity degree, time of the year (wet or dry season), number of reinfections, and cultivar. The RT of bud rot-affected palms ranges from 103 to 315 days, with an average of 202.8 days when an IDM is used. RT was lower than that reported in the diseased palms without IDM (540 days). According to the severity degree, the RT lasted 202 days for severity degree 1, 198 days for severity degree 2, and 222 with severity degree 3 and 4. In comparison, there was no significant difference between dry and rainy seasons in RT. Differences between cultivars were found; however, under IDM, all cultivars showed low RT. The IDM has a positive impact in reducing the RT to BR. Low RT has indirect effects minimizing potential yield losses, improving the number of successfully recovered palms, and reducing the risk of disease dissemination.


Introduction
Bud rot (BR) is a disease that affects oil palms in several countries [1], and it is one of the most devastating diseases for the crop [2]. The disease has affected oil palm plantations in Congo [3], Suriname [4], Ecuador [5], Brazil [6], and different countries of Central America [7]. However, it has economic importance in some countries of Latin America due to large areas vanished by the disease. In Colombia, it was first reported in "The Arenosa" plantation [8], and during the last three decades, more than 95,000 hectares have been lost because of the disease [9].
Colombia has four oil palm regions; BR disease is present in all of them. In the Colombian Eastern Plains (CEP), oil palms affected by BR may recover spontaneously [10]. Gil et al. [11] found, analyzing several isolates collected in Colombia, that genetic diversity in the pathogen affects BR incidence and severity, which is especially true with the isolates from the CEP. Thus, the recovery of the palms in that region is strongly influenced by the genetic background of the isolates. However, despite the recovery in the CEP, BR significantly impacts productivity depending on the severity of the disease and the length of the recovery time. For instance, in cultivars from Southeast Asia evaluated in the CEP,

Data Collected
Eight years of records (2009-2016) of palms affected by BR with IDM were used as data input to the study. The IDM recommended by Cenipalma included the following activities: early detection of the disease, removal of infected tissue (surgery), implementation of phytosanitary rounds that consists of the application and rotation of oomycetes fungicides in the affected palms, elimination of palms beyond severity degree 4 or the ones that after two surgeries have not shown signs of recovery. Additionally, proper drainage management systems and adequate nutrition of the palm were implemented. After the BR diagnosis was recorded, the palms were intervened, and the recovery process was monitored. Then, a final decision was taken on whether the palm had fully recovered. When the palm did not show signs of adequate recovery, it was eliminated, cutting it down and removing/burning the tissues affected by BR, avoiding possible dispersion of the disease to the surrounding palms. This methodology made it possible to trace the progression of the BR disease for each of the palms evaluated. Total of 1680 palms in total were monitored from the 21 cultivars.

Data Analysis
The monitoring of each palm included three stages: (i) Management stage or diagnosis, where the palms were classified according to the degree of severity (degree 1 to degree 5); the severity was assessed based on the lesions found in the youngest leaves of each palm, using the scale developed by Cenipalma [18]. (ii) Monitoring, where the palms intervened with the IDM were followed up on the recovery process, and (iii) decision, where the palms were classified either as healthy to be released or eradicated after not showing signs of recovery after IDM. Table 2 shows the diseases categories according to the stage of the disease management process. Disease monitoring

BR-Released
The surgery treatment palm shows at least six healthy functional leaves and a healthy spear leaf package. Decision The palm is considered healthy and is no longer under disease monitoring in the IDM procedure

BR-Eradication
Removal of the palm after the two surgery treatments, the new growth still shows signs of the disease.

Eradicate
The recovery time (RT) was defined as the difference in the number of days a palm takes from removing the diseased tissue (FD) to the time removed from the monitoring and treatment management program. To be removed from the program, the plant must be declared vegetative recovered (FA), implying that it does not present signs of the disease and has at least six healthy and complete leaves [19]. The following equation shows the variables used to calculate the RT Equation (1).
Agronomy 2021, 11, 1995 5 of 13 Moreover, it was verified that each palm in the management cycle had one diagnosis, one decision record, and intermediate management records. It was also considered that some palms might have multiple disease cycles or reinfections.

Statistical Analysis
Descriptive statistics, data normality, and confidence interval at 95% were used to analyze recovery times per palm, using the R package, version 3.4.0. [27]. Data normality was assessed by the Kolmogorov Smirnov test. To establish differences according to the dependence that the recovery time may have with other variables, separate analyses were carried out regarding the degree of disease severity, type of cultivar, number of reinfections in the year, and the season when the treatment took place.

Results
Out of the 1680 palms included in this study, 261 palms developed the disease during the observation period. They had an accumulated incidence of 15%. The RT of the infected palms ranged from 103 to 315 days, with an average of 202.8 days and a standard deviation of 39.7 days. Figure 1 shows the distribution of RT, where 90% of palms exhibited a RT ranging from 163 to 242 days. takes from removing the diseased tissue (FD) to the time removed from the monitoring and treatment management program. To be removed from the program, the plant must be declared vegetative recovered (FA), implying that it does not present signs of the disease and has at least six healthy and complete leaves [19]. The following equation shows the variables used to calculate the RT Equation (1).
Moreover, it was verified that each palm in the management cycle had one diagnosis, one decision record, and intermediate management records. It was also considered that some palms might have multiple disease cycles or reinfections.

Statistical Analysis
Descriptive statistics, data normality, and confidence interval at 95% were used to analyze recovery times per palm, using the R package, version 3.4.0. [27]. Data normality was assessed by the Kolmogorov Smirnov test. To establish differences according to the dependence that the recovery time may have with other variables, separate analyses were carried out regarding the degree of disease severity, type of cultivar, number of reinfections in the year, and the season when the treatment took place.

Results
Out of the 1680 palms included in this study, 261 palms developed the disease during the observation period. They had an accumulated incidence of 15%. The RT of the infected palms ranged from 103 to 315 days, with an average of 202.8 days and a standard deviation of 39.7 days. Figure 1 shows the distribution of RT, where 90% of palms exhibited a RT ranging from 163 to 242 days.

Recovery Times according to BR Severity Degree
The RT was analyzed according to the severity degree found in palms treated with the IDM of BR. One hundred ninety-six cases were treated with severity degree 1, 48 cases with severity degree 2, and only 17 palms with severity degree of 3 and 4 were intervened. The recovery time for palms with severity degree 1 was on average 202 days, 198 days for severity degree 2, and in the palms with severity degree 3 and 4 was slightly over 222 days ( Figure 2).

Recovery Times According to BR Severity Degree
The RT was analyzed according to the severity degree found in palms treated with the IDM of BR. One hundred ninety-six cases were treated with severity degree 1, 48 cases with severity degree 2, and only 17 palms with severity degree of 3 and 4 were intervened. The recovery time for palms with severity degree 1 was on average 202 days, 198 days for severity degree 2, and in the palms with severity degree 3 and 4 was slightly over 222 days ( Figure 2). Data normality was assessed by the Kolmogorov Smirnov test, obtaining a p-value of <2.2 for severity degrees 1 and 2. However, the collected records for grades 3 and 4 were not enough (n = 17) to measure the normality of the data, as the IDM was focused on early detection. The confidence interval for palms detected with severity degree 1 was between 197 and 206 days, with a probability of 95%, while the confidence interval for palms detected with severity degree 2 was between 185 and 211 days (Table 3). Agronomy 2021, 11, x FOR PEER REVIEW 6 of 13 Data normality was assessed by the Kolmogorov Smirnov test, obtaining a p-value of <2.2 for severity degrees 1 and 2. However, the collected records for grades 3 and 4 were not enough (n = 17) to measure the normality of the data, as the IDM was focused on early detection. The confidence interval for palms detected with severity degree 1 was between 197 and 206 days, with a probability of 95%, while the confidence interval for palms detected with severity degree 2 was between 185 and 211 days (Table 3).

Recovery Times according to the Year of the Evaluation
Descriptive statistics of the RT according to the year in which the disease was detected is presented ( Table 4). The RT for each year showed that 2015 recorded the lowest values, with 183 days of recovery time, while 2013 recorded the highest value, with an average of 214 days of RT. Although for these years, the rainfall pattern shows a 600 mm of difference, for 2015, the total amount of rainfall recorded was 2406 mm, and for 2013 total rainfall was 3069 mm, taking into account this rainfall pattern recorded it is likely that the high relative humidity favored the development of the disease. The RT that occurred in the different severity degrees across the years of evaluations was similar in palms affected by BR with severity degrees of 1 and 2 ( Figure 3). Few palms found with severity degree 3 that began after the first two years of the evaluation showed BR again in 2013.

Recovery Times According to the Year of the Evaluation
Descriptive statistics of the RT according to the year in which the disease was detected is presented ( Table 4). The RT for each year showed that 2015 recorded the lowest values, with 183 days of recovery time, while 2013 recorded the highest value, with an average of 214 days of RT. Although for these years, the rainfall pattern shows a 600 mm of difference, for 2015, the total amount of rainfall recorded was 2406 mm, and for 2013 total rainfall was 3069 mm, taking into account this rainfall pattern recorded it is likely that the high relative humidity favored the development of the disease. The RT that occurred in the different severity degrees across the years of evaluations was similar in palms affected by BR with severity degrees of 1 and 2 ( Figure 3). Few palms found with severity degree 3 that began after the first two years of the evaluation showed BR again in 2013.  2009  111  107  188  216  205  218  315  197-213  2010  57  103  195  212  209  233  291  200-218  2011  37  112  176  190  191  204  299  179-202  2012  5  171  188  195  198  202  234  169-226  2013  9  105  214  222  214  243  282  175-253  2014  29  126  167  196  200  231  274  184-215  2015  13  108  146  186  183  214  274 153-213    The data analyzed correspond to seven years of rainfall ( Table 5). The average RT of palms affected by BR during the dry season was 199 days, with a confidence interval between 183 and 215 days (95% probability). The average RT during the rainy season was  The data analyzed correspond to seven years of rainfall ( Table 5). The average RT of palms affected by BR during the dry season was 199 days, with a confidence interval between 183 and 215 days (95% probability). The average RT during the rainy season was 203 days, with a confidence interval between 198 and 208 days (95% probability). No statistically significant differences were found in the recovery time between the dry and the rainy seasons. Figure 4A shows the average RT for each season of the year, where the RT difference between dry and rainy seasons was only four days. Figure 4B shows the RT for the dry and rainy seasons across the severity degrees of infection. RT ranged from 103 to 315 with an average of 202 days, independent of the season or the BR severity degree.  Figure 4A shows the average RT for each season of the year, where the RT difference between dry and rainy seasons was only four days. Figure 4B shows the RT for the dry and rainy seasons across the severity degrees of infection. RT ranged from 103 to 315 with an average of 202 days, independent of the season or the BR severity degree.

Recovery Times According to the Number of Infections
The palms affected by BR in this study were classified according to the number of times they were infected. The results show that 210 palms presented a single infection, 43 palms had two infections, and seven palms had three infections. Only one palm was Agronomy 2021, 11, 1995 9 of 13 registered with four infections. The average recovery time was around 200 days for all palms, regardless of BR infections on the same palm ( Figure 5).
the year's season and the severity degrees of BR in 21 cultivars of E. guineensis and interspecific O×G hybrids under integrated disease management. G: severity degree of BR disease. The horizontal line represents the median of the data.

Recovery Times according to the Number of Infections
The palms affected by BR in this study were classified according to the number of times they were infected. The results show that 210 palms presented a single infection, 43 palms had two infections, and seven palms had three infections. Only one palm was registered with four infections. The average recovery time was around 200 days for all palms, regardless of BR infections on the same palm ( Figure 5).

Figure 5.
Recovery time of palms infected one (I1), two (I2), or more times (I3, I4) with bud rot under integrated disease management. The horizontal line represents the median of the data. The palms must have been released from the integrated disease management (total recovery) before the disease was detected again to be considered separated infections.

Recovery Time according to the Type of Cultivar
In general, the recovery time for palms affected by BR in the 21 commercial cultivars ranged between 162 and 233 days, with 202 days on average ( Figure 6). Cultivars (Djongo × Ekona) × Yangambi (T17) and Deli × AVROS (T3) showed the lowest RT in the study, with 161 and 163 days, respectively. The O×G hybrid "Coari × La Mé" (T15) and Deli × AVROS cultivars T9 and T4 had the highest recovery time: 230, 232, and 233 days, respectively.

Discussion
The implementation of integrated disease management (IDM) on plants affected by BR positively impacted the reduction of RT with an average of 203 days from the time the disease was identified to the time the palms recovered. In contrast, without IDM, the RT was on average 540 days. Thus, the RT was 337 days shorter with IDM than without IDM [12]. The IDM also impacted how the palms reached the advanced stages of the disease. Without IDM, progressive destruction of the canopy was observed, with some palms losing up to 100% of the leaf area and reaching the highest disease severity degree called the crater state. Of the 540 days that an untreated palm took on average to fully recover, the first 270 days corresponded to the gradual process of the disease until reaching the crater state. The other 270 days went from the emergence of new healthy leaves until the canopy was fully developed [12]. Moreover, the palms had yield reductions without management, with a negative impact on average bunch weight, up to 8 kg. Additionally, the oil-to-bunch potential of palms affected by the BR may decrease by up to eight percentage points, due to low oil synthesis and poor bunch conformation, compared to bunches from healthy or recovered palms [28].
Our results showed that palms with severe degrees of the disease under IDM were sporadic and mostly happened during the first stages of the IDM implementation. Therefore, most of the cases treated early showed low RT, ranging from 161 to 233 days, with an overall average of 203 days. In this sense, in the last years of evaluations, only severity degrees 1 and 2 were detected due to different factors such as (i) the improvement of the process for identifying and monitoring BR disease under field conditions. (ii) The integrated disease management contributed to early detection of the disease, reducing inoculum sources. As a result, there were fewer cases of the disease, and more palms recovered.
Early detection under different scenarios such as years of evaluation and season of the year did not show statistical differences in RT, showing the benefits of early detection again. Additionally, even in heavy rainy seasons, the pattern of low RT was maintained, even though high rainfall and relative humidity favor the development of the disease. Thus, when an IDM program is implemented and carried out promptly when the plants are in the first degrees of severity, the loss of leaf area or canopy is mitigated, having enough canopy area to continue the physiological processes. Furthermore, the early detection and timely treatment of the disease minimizes FFB and oil extraction losses and reduces the risk of having high concentrations of potential inoculum in the field, reducing the risk of BR dissemination. In this sense, another successful experience in early detection is reported in Ganoderma boninense Pat. in Southeast Asia to reduce the risk of disease dissemination [29], supporting that early detection is a crucial strategy for mitigating the disease impact in oil palm.
According to Torres et al. [21], a palm affected by BR should undergo an IDM process instead of allowing the disease to continue until it reaches strong canopy and yields losses. When the IDM treatment is completed effectively, the palm shows continuous leaf growth and at least six healthy and complete leaves. At this point, the palm is considered healthy, and the canopy can support the new branches with normal development; however, it is important to highlight that reinfection could happen, although, in our research, low reinfection percentages of the initially affected palms were measured. Factors that enhance the disease development were considered and managed within the IDM, such as humidity, nutritional deficiencies, and excess water. These factors create a favorable environment for the development of P. palmivora to cause BR [17].
All cultivars evaluated in this study summarize the genetic basis of the commercial oil palm (E. guineensis, DxP) cultivars planted around the world [1]. Although they belong to different genetic backgrounds, they all respond positively to early BR management strategies in the Central Colombian region, showing low RT, even though they differ in the disease incidence. In the case of the evaluated O × G hybrids, BR was present. Previous reports showed that although they get sick, most of the time, the severity is low. For that reason, they are considered resistance cultivars against BR [10,13]. The hybrids also responded to IDM, showing similar RT to E. guineensis.
In this scenario of IDM, palms showed a positive response to the disease due to better agronomic and crop management practices [2]. However, early detection only works when the disease has low incidences, usually below 5%, and the IDM implementation protocol is rigorously followed [21]. Thus, the early detection strategy does not work in areas where the disease is epidemic, and severity reaches the worst degrees. As a result, the IDM does not impact palm recovery. For this reason, although genetic resistance has not yet been described in E. guineensis cultivars, it is the long-term way to ensure the sustainability of the crop in high-risk areas.
There is a learning curve in adopting the early treatment technology, which will determine the success of the management with a progressive reduction in the recovery times of the treated palms. The decrease in the recovery time not only depends on the early treatment with surgeries to remove the tissue affected by the disease, but also depends on multiple factors that make up the integrated agronomic management strategy. In time, IDM impacts the factors that limit crop productivity when BR is present, reducing yield and economic losses, showing the importance of timely management intervention [30].

Conclusions
Early detection is crucial for the integrated BR management in oil palm, positively impacting the RT. Low RT reduces yield losses and disease risk, and early identification improves the number of palms successfully recovered. Palms affected by BR and treated under an IDM can recover in less than seven months (202 days), far from the 18 months reported for non-treated palms (540 days). Although differences between cultivars were found, under IDM, all cultivars showed low RT. The reduction in RT occurs, regardless of the year, season, degree of severity, and the number of infections. However, IDM for BR just works under scenarios of low incidences of the disease and in non-epidemic regions.
Finally, early detection for BR management is one but not the only disease management strategy to ensure crop sustainability. It must be integrated with the best agronomic practices, chemical and biological control of the causal agent, and in the long-term, cultivars genetically resistant to the disease.

Data Availability Statement:
The data presented in this study are available on request from the corresponding author. The data are not publicly available due to privacy restrictions.