Mechanisms of population establishment in invasive South American tomato pinworm Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae)

Global insect pest invasions have dramatically increased over the past decades, posing significant

biosecurity threats to natural and managed ecosystems. As such, the mechanisms of spread and

rapid establishment of invasive species have been a key issue for agricultural stakeholders.

Similarly, while availability of suitable plant hosts is key to establishment, the eco-physiological

mechanisms facilitating invasion amongst most invasive species are unclear. The South American

tomato pinworm, Tuta absoluta (Meyrick, 1917) (Lepidoptera: Gelechiidae) is a devastating

invasive global insect pest of tomato, Solanum lycopersicum L. (Solanaceae) accounting for ~80-

100% yield losses. It has aggressively invaded the African continent since its first detection in

North Africa in Morocco and Tunisia in 2008. Despite its economic importance and global pest

status, little is known on eco-physiological mechanisms likely aiding its rapid establishment and

spread. In addition, although diapause has not been reported in the pest’s Mediterranean invaded

areas, no studies have looked at its overwintering survival in sub-Saharan Africa. Against this

background, this study assessed the role of eco-physiology in explaining part of the observed

invasion success of this insect. Specifically, I investigated (i) the natural and low risk T. absoluta

control strategies including scoping the native natural enemy guild of the pest insect in Botswana

(Chapter 2) (ii) short- and long- term plastic responses to temperature (Chapter 3), (iii) basal cold

hardiness and made inferences on overwintering strategy (Chapter 4), (iv) basal water balance and

desiccation resistance (Chapter 5), and (v) integrated stress resistance (cross tolerance) to various

abiotic co-occurring stressors as a potential survival mechanisms for this species (Chapter 6).

Natural substances (NSs) vis pesticidal plant extracts, naturally occurring antagonists and related

substances (e.g., biological control agents) for T. absoluta were reviewed and considered more

environmentally friendly, bio-based and sustainable alternatives for management that can be used

in combination with other low risk substances in a holistic way for successful pest control. Focus

was also taken on the enabling and limiting factors that influence farmers in embracing the use of

these NSs in an integrated approach. A scoping of the local natural enemy guild for T. absoluta

showed a limited range of natural enemies that can be used for biocontrol of T. absoluta in

integrated management systems. Chapter 2 also revealed that (i) different physiological

mechanisms facilitating population establishment of T. absoluta in novel environments under

rapidly changing environments and (ii) different natural- and low-risk substances and local natural

enemies can be used to sustainably manage T. absoluta in agroecosystems. Results for the potential

plastic responses to both short- and long-term acclimation showed that larvae are more thermally

plastic than adults and can shift their thermal tolerance in short- and long- timescales. Larval

plasticity advantage over adults reported here suggest asymmetrical ecological role of the larvae

relative to adults in facilitating T. absoluta invasion. Empirical study on T. absoluta’s cold

tolerance showed that larval lower lethal temperatures ranged from -1˚C to -17˚C for 0.5-4h

durations and were more cold hardy than adults. Adults showed lower temperature activity limits

than larvae albeit freeze strategy experiments showed neither life stages survived internal freezing

indicating that both larvae and adults were chill-susceptible. In addition, fasting and dehydration

pre-treatment depressed supercooling points (SCPs), although asymmetrically, conferring more

negative SCPs for larvae while ramping rates and inoculative freezing also affected SCPs (Chapter

4). An investigation of water balance and desiccation tolerance showed body water content

(BWC), body lipid content (BLC) and water loss rates (WLRs) significantly varied across life

stages. Second instars recorded the lowest while 4th instars exhibited the highest BWC and BLC

while they also had lowest WLRs. Desiccation resistance assays were consistent, showing that 2nd

instars were the most vulnerable while 4th instar larvae and adults were the most desiccation

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tolerant. This showed that T. absoluta 4

th instar larvae were the most resilient developmental stage

and potentially contribute the most to the invasion success of the pest in arid and semi-arid

environments (Chapter 5). Integrated resistance assays showed context dependent (type of stress

x developmental stage) integrated stress resistance that may heighten invasiveness in T. absoluta.

Indeed, fasted individuals had a significantly higher desiccation resistance while desiccation

acclimation improved starvation resistance. This cross tolerance indicates potential shared co evolutionary mechanisms across divergent stressors and may help facilitate survival for invasive

species under heterogeneous but stressful environments (Chapter 6). Unravelling such factors

associated with successful invasion provide a basis for mitigating the introduction, establishment

and spread of the pest species, especially when key life stages e.g., larvae and adults are targeted

for experiments that inform early warning systems. This information is also important in modelling

pest risk status, allows temporal life-stage specific targeting of management strategies and for

developing early-warning system predictive models. Incorporation of these species-specific eco physiological traits in predictive models can help refine invasive species potential spread and may

help predict biogeographic patterns under changing climates