Management of Banana Bunchy Top in Hawaii
The objective of our work is to study the ecology and epidemiology of an important virus (Banana bunchy top virus) and its associated vector the banana aphid (Pentalonia nigronervosa). Banana bunchy top virus is currently the most economically important disease of bananas in Hawaii. The ultimate goal is to develop integrated disease management practices for mananging this virus.
Objectives of the project include:
i) obtaining a better understanding of the banana aphid’s biology and ecology,
ii) studying the pattern of banana bunchy top virus spread in commercial fields, and
iii) determining disease parameters that are important to the development of virus management practices
Monitoring of pest densities allows for informed decision-making regarding the judicious use of pesticides. Prior to the start of this project, there were no sampling plans available for monitoring population densities of P. nigronervosa on banana. Thus, field surveys were conducted to develop a sampling plan for this pest. Based on these surveys, a sequential binomial sampling plan has been developed. Further, it was determined that the within-plant distribution of P. nigronervosa is an important factor to consider when sampling for this pest. Specifically, aphids were found more frequently near the base of banana plants, followed by the newest unfurled leaf at the top of the plant. Aphids were least likely to be located on leaves in between the top and bottom of the plant. In the past it was widely accepted among banana growers in Hawaii that banana aphid occurs preferentially on the cigar leaf (newest unfurled leaf). During this study, it was determined that sampling the cigar leaf for aphid presence is not a reliable technique because in 50% of the cases this provides a false negative for their presence This sampling plan is currently assisting in the development of sustainable management practices for banana production and the results from this study were recently published in a manuscript entitled “Within-Plant Distribution and Binomial Sampling of Pentalonia nigronervosa (Hemiptera: Aphididae) on Banana” Journal of Economic Entomology, 99(6): 2185-2190 authored by Robson et al., 2006. Future research needs include evaluating this sampling plan with insecticides and cultural management tactics such as roughing for the further development of disease management strategies.
Few studies have been conducted on the biology and ecology of P. nigronervosa. Thus, studies were carried out to determine the effect of temperature and rearing methods on P. nigronervosa biology. Data on population growth, longevity, and fecundity of P. nigronervosa at different temperatures are useful for developing prediction models for aphid population dynamics under field conditions. During these studies, aphids were evaluated at three temperatures (20, 25, and 30º C). These temperatures represent the temperature range of banana growing areas in the Hawaiian Islands. Banana aphids were reared on six different types of banana leaf cuttings. i) mature leaf >1 m in length, ii) young leaf < 0.5m in length, iii) leaf petiole, iv) leaf midrib, (v) symptomatic BBTV leaf, and vi) cigar leaf (newest unfurled leaf). It was found that the banana aphid performed better when not confined on plantlets, followed by leaf midrib cuttings. Further, their intrinsic rate of increase (r), net reproductive rate (Ro), doubling time (DT), nymphal mortality, and mean offspring per female all showed maximal rates at 25ºC. The r was greater when aphids were reared on intact banana plantlets than on plant cuttings. The results showed that it is important to conduct whole plant experiments when evaluating banana aphid growth features because various growth parameters may be underestimated if various plant cuttings are used. This further implicates the importance of comparing insect rearing methods for studies such as life tables.
Results of this experiment may help predict at what temperatures banana aphid populations will build to greater numbers, assisting in the development of management practices aimed to control the banana aphid and BBTD. Future studies need to examine the population thresholds that induce the production of alate (winged) banana aphids because the alates are most responsible for spreading the virus. Additional, studies are also needed for determining biotic and abiotic factors affecting banana aphid population growth in the field. The findings from this study were published under the title “Biology of Pentalonia nigronervosa (Hemiptera: Aphididae) on Banana Using Different Rearing Methods” Environmental Entomology 36(1): 46-52 authored by Robson et al. 2007.
There are ongoing studies to learn more about the biology and ecology of the banana aphid, but much of the attention is now focused on how this relates to their ability to transmit BBTV to healthy banana plants. Although, previous research (Robson et al., 2007) indicates that various growth parameters of the banana aphid are significantly reduced on plant cuttings compared to whole plants, we learned that their efficiency in obtaining and transmitting BBTV to healthy banana plants is similar whether they feed on whole plant or leaf cuttings infected with BBTV, respectively (Figure 1).
In controlled experiments, it was also found that BBTV is transmitted by the banana aphid between 20 and 28 hours after feeding on an infected plant (acquisition) including the 12 hour acquisition access time. In two trials, the transmission efficiency for the 28 hour treatment period was 50 and 60%, respectively. Their transmission efficiency for the 36 hour time period was 90 and 100% for trials 1 and 2, respectively (Table 1).
The minimum latent period (i.e., length of time after a plant has been inoculated with a virus that an aphid can acquire and transmit the virus from that plant) of BBTV within banana plants was investigated. The inoculation efficiency was 0 and approximately 75% at the 15 and 20 day test periods, respectively (Figure 2). This indicates that the minimum latent period is somewhere between 15 and 20 days following virus inoculation. These studies are among a few that have been conducted to examine BBTV’s transmission efficiency.
Data on the ability of the banana aphids to transmit BBTV at different temperatures are useful for understanding their transmission biology. Banana aphids were evaluated at three temperatures (20, 25, and 30º C) for their ability to transmit BBTV to healthy banana plants. Additionally, studies were conducted to compare the efficiency of adult and nymphs in transmitting BBTV. During these investigations, it was determined that adults can transmit the virus at all three temperatures but they have low efficiency at 20ºC. Nymphs did not do as well compared to adults and could not transmit BBTV to healthy plants when exposed to 20ºC (Figure 3). It was also noted that banana aphids were more settled on the leaves at 25 compared to 30ºC.
An effective management strategy for BBTV is dependent on rapid detection of symptomatic plants so that potential source plants of BBTV can be destroyed promptly. Thus, field studies were also conducted in Oahu, Hawaii to identify features of banana bunchy top disease (BBTD) that could be used as pre-symptomatic indicators of BBTV infection. The growth and morphology of banana plants infected with BBTV and healthy controls were investigated. The time interval between aphid inoculation of BBTV and the initial appearance of visual disease symptoms (i.e. incubation period) was also determined. Plants infected with BBTV showed a significant reduction in petiole morphology, plant canopy and height, leaf area, pseudostem diameter and chlorophyll content compared with control plants. Growth differences between virus-infected and control plants were not observed until 40 to 50 days after the plants were inoculated with viruliferous aphids. Other growth parameters such as petiole width and leaf production were not statistically different between infected and control plants. The results show that banana growth parameters may not be suitable as pre-symptomatic indicators of BBTV infection and that PCR assays can provide earlier detection (5 to 10 days in advance) of BBTV in banana plants compared to visual symptoms. It was also found that the initial appearance of observable BBTV symptoms ranged from 25 to 85 days after viruliferous aphid inoculation (Figure 4). The results of this study have been submitted to a peer review journal for publication.
To learn more about the epidemiology of BBTV, GPS units were used to track the movement pattern of the virus in two commercial banana orchards. Monthly data from these farms were initiated in January 2005 and completed in January 2007. Farm 1 used known disease-free plants (micro-propagated banana plants) for planting material, and farm 2 used banana suckers removed from various fields within the farm as planting material. From the data collected from farm 1, it was determined that the virus movement was influenced by wind direction and that the spread pattern was clustered. Additionally, it was found that the virus moved approximately 30 meters per month (Figure 5). Data from farm 2 are still being analyzed but results from the initial analysis indicate that the spread pattern is random and further suggest that field-to-field spread of BBTV from farm 2 is mostly influenced by the planting of infected plant material throughout the farm. We have established a small field of known disease-free banana plantlets on farm 2 and are now monitoring the spread of BBTV in that field. An additional 1 acre field was established at the Poamoho research station and the pattern of BBTV spread is being monitored at that site.
We have started to promote the use of known disease-free planting material (tissue culture banana plantlets) to banana growers so that they can avoid the unintentional planting of infected banana plants throughout their farms. Workshops are ongoing to familiarize banana growers with tissue-cultured banana plants and discuss the benefits of using tissue culture banana plantlets as part of an integrated disease management program. We have noticed a significant jump in the number of growers interested in using tissue-cultured plants on their farms. We are now in the early stages of developing a tissue culture facility on campus to insure that disease-free plantlets are readily available to banana growers.
Molecular data (partial sequences of BBTV’s DNA genome) is being used to address specific questions regarding the introduction and spread of this pathogen in Hawaii. The results thus far are summarized in the following three figures.
Figure 6 illustrates the genetic placement of Hawaii BBTV isolates from different islands in relation to BBTV isolates from other regions of the world. It is important to note that Hawaii isolates form a monophyletic clade, suggesting there was only one introduction of this pathogen into the State of Hawaii. Although Hawaii’s BBTV could be grouped with isolates from the South Pacific, its original source could not be pin pointed because there are no BBTV sequences deposited in databases for comparison.
Figure 7 shows the placement of isolates collected from different Hawaiian islands. Interestingly, enough isolates from Maui and Hawaii (Big Island) form monophyletic clades, suggesting only one introduction into those islands. On the contrary, Kauai isolates are located at different branches in the tree, suggesting multiple introductions of BBTV were made into that island. Oahu isolates are present throughout the tree, suggesting that it served as the original BBTV source area for infections into other Hawaiian islands.
Figure 8 illustrates BBTV introduction and spread hypothesis and summarizes the results obtained with the use of molecular tools. It shows that BBTV was introduced into Oahu in 1989 (one introduction). It then spread to other islands, once into Maui and Hawaii (Big Island), respectively, and multiple times into Kauai.
Much of the data from this molecular work suggest that the spread of BBTV throughout Hawaii was greatly influenced by the movement of infected plant material throughout the islands. Similarly, we have determined that the within-farm spread of BBTV may be more influenced by the planting of infected banana suckers than aphid vectors. This further suggests the importance of using known disease-free banana plants as replant material.
In addition to the original goals, current research work includes determining how long banana plants remain virulent after a bananacide injection (i.e., herbicides that can be injected into banana plants for destruction of infected plants) and whether the two most important banana cultivars grown in Hawaii differ in their susceptibility to BBTV, and finally finding out how to incorporate the judicious use of insecticide into an integrated disease management program.
Impacts and Contributions/Outcomes
Our results are being disseminated to banana stakeholders through workshops, farm site visits, collaborative research projects, websites, conferences, and email action groups. Each year, we highlight relevant findings at the local banana conference and from stakeholders comments and questions determine additional research needs. In the past, Hawaii growers were given limited information regarding the virus and vector and thus relied on their own guesswork on how to best manage this virus. Thus, one of the leading constraints to greater adoption of IPM strategies for BBTV management in Hawaii was the availability of trustworthy information. Through our collaborative research and outreach efforts, we have been able to give stakeholders creditable information on the virus and its associated vector and have thus removed some of the questionable myths regarding banana bunchy top virus.
Since the start of the project, growers have gained a better understanding of the virus and are now changing their production practices in an effort to better manage the disease. We now expect to see a reversal in banana acreage lost because of this intrepid virus. In addition to accomplishing the original objectives of the project, we have instituted additional goals that we feel will substantially benefit the banana industry in Hawaii. Further, one graduate student received her Master of Science degree in May 2006 on research conducted in accomplishing the objectives of the project and another graduate student will complete her degree in August 2007 on research work related to this project. Research from this project has been highlighted in a USDA-CSREES movie and collaborators of this project have contributed to the design of a BBTV awareness poster. Two papers have been published in peer review journals and two additional manuscripts have been submitted for publication. Four slide presentations highlighting some of our work are posted online at http://www2.hawaii.edu/~snelson/HBIA/.
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