Understanding the potential impact of climate change on cassava-colonising whitefly, Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae)

Oluwatosin Zacheus Aregbesola

Abstract

Cassava has been described as a “super-crop” for its role as food crop, cash crop and industrial raw material. Its production is vital to the well-being of more than 700 million people globally. Cassava viruses and their vector (B. tabaci) are one of the greatest constraints to cassava production. Among the insect pests of cassava, B. tabaci stands out as an economically important pest, causing direct damage to a wide range of crops by producing sooty moulds and transmitting plant viruses. B. tabaci is a species complex consisting of more than 34 morphologically indistinguishable species. B. tabaci is known to vector over 100 plant viruses, including at least 11 viruses of cassava, driving disease epidemics across cassava production systems globally. Cassava farmers across Africa incur annual losses of over 1 billion USD due to viruses transmitted by B. tabaci. Even though cassava is expected to be resilient to climate change, at the moment, there is a dearth of information on temperature-dependence, and the potential impact of climate change on an African population of cassava-colonising B. tabaci. To fill this knowledge gap, this study was initiated to: evaluate the effects of temperature on the developmental characteristics of cassava-colonising B. tabaci, evaluate the effects of temperature on the reproductive performance of cassava-colonising B. tabaci, review the potential impact of climate change on whiteflies, model the distribution and abundance of cassava-colonising B. tabaci under climate change scenarios, and investigate strategies for adapting to cassava whitefly and virus disease under climate change scenarios. To provide a solid foundation for the study, potential impact of climate change on whiteflies and the viruses they vector was reviewed. These included the possible impacts on: life history traits (immature development time and survival, adult longevity and fecundity of adult female), movement and distribution, population dynamics, efficacy of management strategies, and implications for vectored plant viruses. The identity and purity of the B. tabaci colonies used for the experiments was confirmed by sequencing a fragment of the mitochondria cytochrome oxidase 1. The B. tabaci used was confirmed to be sub-Saharan Africa 1 Sub Group 3 (SSA1-SG3). Data on life history traits were collected from both laboratory and field experiments to facilitate model development and validation. To achieve this, a comprehensive study of the biology of the whiteflies was initiated. Data on longevity of newly emerged adults (males and females), and fecundity of adult females were collected under both field and laboratory conditions. For a better understanding of temperaturedependence, and the potential impact of climate change on the distribution and abundance of B. tabaci SSA1-SG3, data from the constant temperature experiments were used for phenology model building, while data from the field experiments were used for model validation. Cassava whiteflies are a threat to cassava production, and their populations may increase with climate change in some cassava-growing areas. Against this backdrop, a survey of smallholder farmers was carried out to understand their production characteristics, challenges and adaptive capacity to the potential impact of climate change on cassava whiteflies and associated viruses. Expert judgement of 20 whitefly and/cassava virus experts was then used to identify possible adaptation strategies and ways to enhance the adaptive capacity of the farmers. The review of climate change impacts on whiteflies suggests that temperature increase will likely reduce whitefly fecundity, longevity and development time, while elevated CO2 will lengthen development time but not likely affect fecundity and adult longevity of whiteflies. For most whitefly species living below their thermal optimum, temperature increase in both temperate and tropical zones will favour population increase. However, extreme temperatures will likely reduce whitefly populations. While climate change may alter levels of damages from whiteflies and plant viruses they transmit, the direction of change will be location specific and also depend on host-vector-virus interactions. The immature development time from egg to adult significantly differed at the six constant temperatures tested under laboratory conditions. Immature development time decreased with temperature up to 28 °C, it was slowest at 16 °C where it lasted 59.3 days and fastest at 28 °C lasting only 16.3 days. Additionally, immature development time at 32 °C was slower than at 28 °C, but faster than at other temperatures. Eggs did not successfully developed to adults at 36 °C. In climatic chambers, whiteflies oviposition peaked at temperatures from 20 °C to 28 °C and the number of eggs laid dropped outside these range of temperatures. The maximum number of eggs laid by an individual whitefly was 387 eggs, observed at 20 °C. Peak oviposition of 117.5 eggs per female was also recorded at 20 °C. Longevity was highest (19.7 days) at 24 °C for females and at 20 °C for males (11.0 days). The maximum longevity of an individual whitefly was 47 days (observed in both 20 °C and 24 °C treatments). Adult longevity at extreme temperatures was relatively lower. At 16 °C, longevity was 12.4 and 7.0 days for females and males respectively. At a high temperature extreme of 36 °C, it was 8.5 days (females) and 6.0 days (males). The maximum longevity of a single individual during the field experiment was 28 and 31 days for males and females respectively. However, mean longevity for males was 9.2 days and 13.1 days for females. The maximum number of eggs laid by an individual B. tabaci outdoor was 287 eggs, although the mean fecundity per female was 94.5 eggs. Results from field experiments also show that immature development time decreased with increasing average temperature across B. tabaci generations. Development duration varied from 18 days in April (average temperature of 28.3 °C, and average relative humidity of 86.1%) to 25 days in July (average temperature of 25.6 °C and average relative humidity of 77.4%). It took an average of 21.3 days from egg to adult emergence under field conditions in Dar es Salaam, Tanzania where the average temperature and relative humidity were 28 °C and 78% respectively. For the climatic chamber experiment, peak survival (62.5%) was recorded at 24 °C, while least survival (14.9%) was observed at 16 °C. Host plant effects in form of leaf drying and dropping accounted for additional mortality of B. tabaci on cassava at 16 °C because cassava being a tropical crop could not tolerate the constant 16 °C treatment. Survival of immature stages under field conditions were also greatly affected by natural enemies and survival varied from 0.69% to 18.0%. Under laboratory conditions, third instars had lower development threshold (To) temperature of 2.2 °C, which was lower than for other instars, while pupa stage had the highest (To = 11.6 °C). Lower development threshold temperature for egg to adult emergence was 4.3 °C under laboratory conditions. Degree-days requirement varied from 504.4 at 28 °C to 695.8 at 16 °C under laboratory conditions. Similarly, results from field experiments suggest that pupa stage had the highest lower development threshold temperature (12.8 °C), and lower threshold temperature required for egg to adult emergence is 3.1 °C. The average degree-day requirement (egg – adult emergence) for field populations of B. tabaci in Dar es Salaam, Tanzania was 523. Several models describing temperature-dependence of insects were fitted to life history data, and an overall phenology model was developed for this pest using ILCYM® software. Immature development time was best described by the log-logistic model. A combination of Sharpe & DeMichele 12 and Logan’s Tb model provided an excellent description of temperature-dependent development rate of immature stages. Temperature-dependent mortality of immature stages was well described by Wang 2, Wang 3 and quadratic models. The longevity of adult females and oviposition time was best described by the Weibull distribution. The established phenology model predicted maximum population growth between 22 and 24 °C, and an optimum temperature for total fecundity per female to be 21.4 °C. The estimated establishment risk index based on the established phenology model suggests a decrease in distribution of B. tabaci SSA1-SG3 with climate change in North and West Africa, and a southward range expansion in southern Africa. The distribution of B. tabaci SSA1-SG3 is predicted not to significantly change in East Africa. In West Africa, the number of generations is predicted to increase with climate change based on generation index. However, activity index (a more reliable estimate of population growth) indicates a decrease in population growth with climate change. Climate change is predicted to cause a decrease in population growth potential in North Africa, parts of Central Africa Republic, southern region of Sudan, eastern regions of Ethiopia, Kenya and Somalia. Both the estimated generation and activity index agree with an increase in the number of generations and population growth potential in most parts of East and Southern Africa. Cassava-colonising B. tabaci SSA1-SG3 will continue to pose significant threat in cassava-growing countries across Africa. An interview study with 320 cassava farmers in Tanzania showed that most farmers produce cassava primarily for food. Some of the challenges of cassava production were diseases, insect pests, drought, finance, market access, planting materials among others. Farmers rely mainly on their friends and their own farms for cassava planting materials. Adaptive capacity was found to be moderate for most farmers, and some farmers apply simple methods to control cassava viruses and whiteflies. The 20 whitefly and/cassava virus expert interviewed recommended an integrated pest management approach, phytosanitation, novel vector management techniques and biocontrol of whiteflies as good adaptatation strategies; and that enhancing adaptive capacity of the farmers could be achieved with capacity building through level specific training of stakeholders. This is the first comprehensive study on temperature-dependence of life history traits of a cassava-colonising and endemic African population of B. tabaci (combining field and laboratory experiments). This is also the first study that described the potential impact of climate change on a cassava-colonising and endemic African population of B. tabaci. The findings will be useful for climate change adaptation planning and phytosanitary risk assessments.
Original languageEnglish
PublisherDepartment of Plant and Environmental Sciences, Faculty of Science, University of Copenhagen
Publication statusPublished - 2018

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