Ontogenetic responses of physiological fitness in Spodoptera frugiperda (Lepidoptera: Noctuidae) in response to repeated cold exposure.

In this era of global climate change, intrinsic rapid and evolutionary responses of invasive agricultural pests to thermal variability are of concern given the potential implications on their biogeography and dire consequences on human food security. For insects, chill coma recovery time (CCRT) and critical thermal minima (CTmin), the point at which neuromuscular coordination is lost following cold exposure, remain good indices for cold tolerance. Using laboratory-reared Spodoptera frugiperda (Lepidoptera: Noctuidae), we explored cold tolerance repeated exposure across life stages of this invasive insect pest. Specifically, we measured their CTmin and CCRT across four consecutive assays, each 24 h apart. In addition, we assessed body water content (BWC) and body lipid content (BLC) of the life stages. Our results showed that CTmin improved with repeated exposure in 5th instar larvae, virgin males and females while CCRT improved in 4th, 5th and 6th instar larvae following repeated cold exposure. In addition, the results revealed evidence of cold hardening in this invasive insect pest. However, there was no correlation between cold tolerance and BWC as well as BLC. Our results show capacity for cold hardening and population persistence of S. frugiperda in cooler environments. This suggests potential of fall armyworm (FAW) to withstand considerable harsh winter environments typical of its recently invaded geographic range in sub-Saharan Africa.

Thermal plasticity in the invasive south American tomato pinworm Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae).

South American tomato pinworm, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) is a devastating invasive global insect pest of tomato, Solanum lycopersicum (Solanaceae). In nature, pests face multiple overlapping environmental stressors, which may significantly influence survival. To cope with rapidly changing environments, insects often employ a suite of mechanisms at both acute and chronic time-scales, thereby improving fitness at sub-optimal thermal environments. For T. absoluta, physiological responses to transient thermal variability remain under explored. Moreso, environmental effects and physiological responses may differ across insect life stages and this can have implications for population dynamics. Against this background, we investigated short and long term plastic responses to temperature of T. absoluta larvae (4th instar) and adults (24-48 h old) from field populations. We measured traits of temperature tolerance vis critical thermal limits [critical thermal minima (CTmin) and maxima (CTmax)], heat knockdown time (HKDT), chill coma recovery time (CCRT) and supercooling points (SCP). Our results showed that at the larval stage, Rapid Cold Hardening (RCH) significantly improved CTmin and HKDT but impaired SCP and CCRT. Heat hardening in larvae impaired CTmin, CCRT, SCP, CTmax but not HKDT. In adults, both heat and cold hardening generally impaired CTmin and CTmax, but had no effects on HKDT, SCP and CCRT. Low temperature acclimation significantly improved CTmin and HKDT while marginally compromising CCRT and CTmax, whereas high temperature acclimation had no significant effects on any traits except for HKDT in larvae. Similarly, low and high temperature acclimation had no effects on CTmin, SCPs and CTmax, while high temperature acclimation significantly compromised adult CCRT. Our results show that larvae are more thermally plastic than adults and can shift their thermal tolerance in short and long timescales. The larval plasticity reported here could be advantageous in new envirnments, suggesting an asymmetrical ecological role of larva relative to adults in facilitating T. absoluta invasion.

Life-stage related responses to combined effects of acclimation temperature and humidity on the thermal tolerance of Chilo partellus (Swinhoe) (Lepidoptera: Crambidae).

Adaptive thermal plasticity plays a key role in mitigating the effects of seasonal and diurnal thermal fluctuations among ectotherms at various life-stages. While the role of thermal history in conferring such plasticity is widely documented, its interaction with relative humidity (RH), another important driver of ectotherm survival and activity, is relatively underexplored. Yet the potential responses to these combinational stressors across ontogeny remain largely neglected. Against this background, we used a full-factorial design to test the combined acclimation effects of RH (45%, 65% and 85%) and temperature (23, 28 and 33 °C) on various indices of thermal sensitivity of laboratory reared spotted stemborer, Chilo partellus (Swinhoe) (Lepidoptera: Crambidae) following acclimation beginning at larval, pupal and adult life-stages. Traits measured included critical thermal limits (CTLs), supercooling points (SCPs), chill coma recovery time (CCRT) and heat knockdown time (HKDT). Larval acclimation at 23 °C; 85% RH recorded the lowest critical thermal minima (CTmin) whereas adult acclimation at 28 °C; 45% RH recorded the highest critical thermal maxima (CTmax). There were no significant differences (P > 0.05) in SCPs across all temperature × RH acclimations. Larval and pupal acclimations at 23 °C; 85% RH and adult acclimation at 23 °C; 45% RH significantly improved CCRT. Similarly, commencing acclimation at larval, pupal and adult stages at 28 °C; 85% RH improved HKDT whereas larval and pupal acclimations at 33 °C; 45% RH impaired it. Our results indicate that combinational interactions of temperature and RH have significant thermal fitness costs and benefits and are dependent on the life-stage acclimation timing. Results also imply that both the vulnerability and adaptive potential of C. partellus populations under rapid climate variability varies with ontogeny. This therefore calls for the consideration of the role of ontogeny and multi-factors in better understanding the impact of environmental stress on ectotherms.

Context-dependent integrated stress resistance promotes a global invasive pest.

In nature, insects concurrently face multiple environmental stressors, a scenario likely increasing with climate change. Integrated stress resistance (ISR) thus often improves fitness and could drive invasiveness, but how physiological mechanisms influence invasion has lacked examination. Here, we investigated cross-tolerance to abiotic stress factors which may influence range limits in the South American tomato pinworm-a global invader that is an ecologically and socially damaging crop pest. Specifically, we tested the effects of prior rapid cold- and heat-hardening (RCH and RHH), fasting, and desiccation on cold and heat tolerance traits, as well as starvation and desiccation survivability between T. absoluta life stages. Acclimation effects on critical thermal minima (CTmin ) and maxima (CTmax ) were inconsistent, showing significantly deleterious effects of RCH on adult CTmax and CTmin and, conversely, beneficial acclimation effects of RCH on larval CTmin . While no beneficial effects of desiccation acclimation were recorded for desiccation tolerance, fasted individuals had significantly higher survival in adults, whereas fasting negatively affected larval tolerances. Furthermore, fasted and desiccation acclimated adults had significantly higher starvation tolerance, showing strong evidence for cross-tolerance. Our results show context-dependent ISR traits that may promote T. absoluta fitness and competitiveness. Given the frequent overlapping occurrence of these divergent stressors, ISR reported here may thus partly elucidate the observed rapid global spread of T. absoluta into more stressful environments than expected. This information is vital in determining the underpinnings of multistressor responses, which are fundamental in forecasting species responses to changing environments and management responses.

Biogeography of cereal stemborers and their natural enemies: forecasting pest management efficacy under changing climate.

BACKGROUND: Climate warming presents physiological challenges to insects, manifesting as loss of key life-history fitness traits and survival. For interacting host-parasitoid species, physiological responses to heat stress may vary, thereby potentially uncoupling trophic ecological relationships. Here, we assessed heat tolerance traits and sensitivity to prevailing and future maximum temperatures for the cereal stemborer pests, Chilo partellus, Busseola fusca and Sesamia calamistis and their endo-parasitoids, Cotesia sesamiae and Cotesia flavipes. We further used the machine learning algorithm, Maximum Entropy (MaxEnt), to model current and potential distribution of these species. RESULTS: The mean critical thermal maxima (CTmax ) ranged from 39.5 ± 0.9°C to 44.6 ± 0.6°C and from 46.8 ± 0.7°C to 48.5 ± 0.9°C for parasitoids and stemborers, with C. sesamiae and Ch. partellus exhibiting the lowest and highest CTmax respectively. From the current climate to the 2050s scenario, parasitoids recorded a significant reduction in warming tolerance compared with their hosts. Habitat suitability for all stemborer-parasitoid species was spatially heterogeneous under current and future climatic scenarios. Cotesia sesamiae C. flavipes and B. fusca exhibited significant habitat loss, whereas Ch. partellus and S. calamistis showed a significant habitat gain under future 2050s predictions. Model metrics based on mean area under the curve ranged from 0.72 to 0.84 for all species, indicating a good predictive performance of the models. CONCLUSION: These results suggest C. sesamiae and C. flavipes may face survival constraints or extirpation compared with their pest hosts when environmental temperature reaches their upper thermal limits earlier, likely reducing pest regulation through density-mediated effects. The results demonstrate potential destabilization of stemborer-parasitoid trophic systems potentially compromising biocontrol efficacy under climate warming. © 2022 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Geographic dispersion of invasive crop pests: the role of basal, plastic climate stress tolerance and other complementary traits in the tropics.

Global pest invasions have significantly increased in recent years. These invasions together with climate warming directly impact agriculture. Tropical climates feature extreme weather events, including high temperatures and seasonal droughts. Thus, successful invasive pests in tropics have to adapt to these extreme climate features. The intrinsic factors relevant to tropical invasion of insects have been explored in many studies, but the knowledge is rather dispersed in contemporary literature. Here, we reviewed the potential biophysical characters of successful invasive pests' adaption to tropical environments including [1] inherent high basal stress tolerance and advanced life-history performances [2], phenotypic plasticity [3], rapid evolution to environmental stress, polyphagy, diverse reproductive strategies and high fecundity. We summarised how these traits and their interactive effects enhance pest invasions in the tropics. Comprehensive understanding of how these characters facilitate invasion improves models for predicting ecological consequences of climate change on invasive pest species for improved pest management.

Cold hardiness of the South American tomato pinworm Tuta absoluta (Lepidoptera: Gelechiidae): both larvae and adults are chill-susceptible.

BACKGROUND: For many insects, including invasive species, overwintering survival is achieved behaviourally (e.g. through migration) or physiologically by entering diapause, a state of arrested physiological development that may be accompanied with depressed supercooling points (SCPs). Diapause allows in situ adaptation to adverse environmental conditions, providing sufficient parent propagules for insect pest proliferation when optimal conditions resurface. This phenomenon has however not been observed in the invasive South American tomato pinworm Tuta absoluta in its Mediterranean invaded areas. Moreover, no studies have looked at its overwintering survival in sub-Saharan Africa. Here, we thus investigated the cold hardiness of Tuta absoluta larvae and adults to better explain its local overwintering adaptation strategy. RESULTS: Larval lower lethal temperatures ranged from -1 to -17 °C for 0.5 to 4 h durations. Adults showed lower temperature activity limits than larvae albeit freeze strategy experiments showed neither survived internal freezing. Fasting and dehydration pre-treatment generally depressed SCPs, although asymmetrically, conferring more negative SCPs for larvae. Ramping rates, synonymic to diurnal temperature changes also significantly affected SCPs while, inoculative freezing significantly compromised freezing temperatures in both larvae and adults. CONCLUSION: Our results suggest that (i) Tuta absoluta larvae and adults are chill-susceptible and may successfully overwinter, (ii) larvae appear more cold hardy than adults and (iii) ecological factors e.g. inoculative freezing, cooling rates, feeding- and hydration-status may affect cold hardiness. These results are important in determining species range limits, population phenology, modelling pest risk status and allows temporal life-stage specific targeting of management strategies.

Water Balance and Desiccation Tolerance of the Invasive South American Tomato Pinworm.

Temperature and dehydration stress are two major co-occurring environmental stressors threatening the physiology, biochemistry, and ecology of insects. As such, understanding adaptive responses to desiccation stress is critical for predicting climate change impacts, particularly its influence on insect invasions. Here, we assessed water balance and desiccation resistance of the invasive Tuta absoluta (Meyrick, 1917) (Lepidoptera: Gelechiidae), and infer how eco-physiology shapes its niche. We measured basal body water and lipid content, water loss rates (WLRs), and desiccation resistance in larvae (second to fourth instars) and adults. Body -water, -lipid, and WLRs significantly varied across life stages. Second instars recorded the lowest while fourth instars exhibited the highest body water and lipid content. Adult body water and lipid content were higher than second and third instars and lower than fourth instars while proportion of body water and lipid contents were highest in adults and second larval instars respectively. Water loss rates were significantly highest in fourth-instar larvae compared to other life stages, but differences among stages were less apparent at longer exposure durations (48 h). Desiccation resistance assays showed that second instars had greatest mortality while fourth-instar larvae and adults were the most desiccation tolerant. Our results show that T. absoluta fourth-instar larvae and adults are the most resilient developmental stages and potentially contribute most to the invasion success of the pest in arid environments. Incorporation of these species-specific eco-physiological traits in predictive models can help refine invasive species potential spread under changing climates.

Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) on the "Offensive" in Africa: Prospects for Integrated Management Initiatives.

The South American tomato pinworm Tuta absoluta (Meyrick) has aggressively invaded the African continent. Since its first detection in North Africa in Morocco and Tunisia in 2008, it has successfully invaded the entire southern, eastern and western Africa, where it has been on the offensive, causing significant damage to Solanaceous food crops. While control of this prolific invader is primarily based on conventional synthetic pesticides, this form of control is consistently losing societal approval owing to (1) pesticide resistance development and consequential loss of field efficacy; (2) growing public health concerns; (3) environmental contamination and loss of biological diversity and its associated ecological services; and (4) unsustainable costs, particularly for resource-poor African farmers. As such, more ecologically sound pest management strategies, e.g., the use of natural substances (NSs), may offer a more sustainable approach to tackling this offensive. A systematic literature search through digital libraries and online databases (JSTOR, PubMed, Web of Science, SCOPUS and Google Scholar) was conducted using predetermined keywords on T. absoluta, e.g., South American tomato pinworm. We use this to explain the invasion of T. absoluta in Africa, citing mechanisms facilitating African invasion and exploring the potential of its control using diverse biological control agents, natural and low-risk substances. Specifically, we explore how botanicals, entomopathogens, semiochemicals, predators, parasitoids, host plant resistance, sterile insect technique and others have been spatially employed to control T. absoluta and discuss the potential of these control agents in African landscapes using more integrated approaches. We discuss the use of NSs as assets to general insect pest control, some potential associated liabilities and explain the potential use and barriers to adoption in African systems from a legislative, economic, ecological and social standpoint.

Comparative assessment of the thermal tolerance of spotted stemborer, Chilo partellus (Lepidoptera: Crambidae) and its larval parasitoid, Cotesia sesamiae (Hymenoptera: Braconidae).

Under stressful thermal environments, insects adjust their behavior and physiology to maintain key life-history activities and improve survival. For interacting species, mutual or antagonistic, thermal stress may affect the participants in differing ways, which may then affect the outcome of the ecological relationship. In agroecosystems, this may be the fate of relationships between insect pests and their antagonistic parasitoids under acute and chronic thermal variability. Against this background, we investigated the thermal tolerance of different developmental stages of Chilo partellus Swinhoe (Lepidoptera: Crambidae) and its larval parasitoid, Cotesia sesamiae Cameron (Hymenoptera: Braconidae) using both dynamic and static protocols. When exposed for 2 h to a static temperature, lower lethal temperatures ranged from -9 to 6 °C, -14 to -2 °C, and -1 to 4 °C while upper lethal temperatures ranged from 37 to 48 °C, 41 to 49 °C, and 36 to 39 °C for C. partellus eggs, larvae, and C. sesamiae adults, respectively. Faster heating rates improved critical thermal maxima (CTmax ) in C. partellus larvae and adult C. partellus and C. sesamiae. Lower cooling rates improved critical thermal minima (CTmin ) in C. partellus and C. sesamiae adults while compromising CTmin in C. partellus larvae. The mean supercooling points (SCPs) for C. partellus larvae, pupae, and adults were -11.82 ± 1.78, -10.43 ± 1.73 and -15.75 ± 2.47, respectively. Heat knock-down time (HKDT) and chill-coma recovery time (CCRT) varied significantly between C. partellus larvae and adults. Larvae had higher HKDT than adults, while the latter recovered significantly faster following chill-coma. Current results suggest developmental stage differences in C. partellus thermal tolerance (with respect to lethal temperatures and critical thermal limits) and a compromised temperature tolerance of parasitoid C. sesamiae relative to its host, suggesting potential asynchrony between host-parasitoid population phenology and consequently biocontrol efficacy under global change. These results have broad implications to biological pest management insect-natural enemy interactions under rapidly changing thermal environments.

Thermal plasticity potentially mediates the interaction between host Chilo partellus Swinhoe (Lepidoptera: Crambidae) and endoparasitoid Cotesia flavipes Cameron (Hymenoptera: Braconidae) in rapidly changing environments.

BACKGROUND: Increasing climatic average temperatures and variability elicit various insect physiological responses that affect fitness and survival and may influence subsequent trophic interactions in agroecosystems. In this background, we investigated short- and long-term plastic responses to temperature of the laboratory-reared stemborer Chilo partellus and its larval endoparasitoid Cotesia flavipes. RESULTS: Rapid cold- and heat-hardening effects in C. partellus larvae, pupae and adults and C. flavipes adults were highly significant (P < 0.001). High-temperature acclimation improved critical thermal limits and heat knockdown time in C. partellus larvae and C. flavipes adults, respectively. Low-temperature acclimation enhanced the supercooling point in C. flavipes and the chill coma recovery time in both C. partellus larvae and C. flavipes adults. CONCLUSION: The results of this study suggest that thermal plasticity may enhance the survival of these two species when they are subjected to lethal low and high temperatures. However, C. partellus appeared to be more plastic than C. flavipes. These results have three major implications: (1) C. partellus may inhabit slightly warmer environments than C. flavipes, suggesting a potential mismatch in biogeography; (2) host-parasitoid relationships are complex and are probably trait dependent, and (3) host-parasitoid differential thermal plastic responses may offset biocontrol efficacy. These results may help inform biocontrol decision making under conditions of global change. © 2017 Society of Chemical Industry.

Thermal resilience may shape population abundance of two sympatric congeneric Cotesia species (Hymenoptera: Braconidae).

Basal and plasticity of thermal tolerance determine abundance, biogeographical patterns and activity of insects over spatial and temporal scales. For coexisting stemborer parasitoids, offering synergistic impact for biological control, mismatches in thermal tolerance may influence their ultimate impact in biocontrol programs under climate variability. Using laboratory-reared congeneric parasitoid species Cotesia sesamiae Cameron and Cotesia flavipes Cameron (Hymenoptera: Braconidae), we examined basal thermal tolerance to understand potential impact of climate variability on their survival and limits to activity. We measured upper- and lower -lethal temperatures (ULTs and LLTs), critical thermal limits [CTLs] (CTmin and CTmax), supercooling points (SCPs), chill-coma recovery time (CCRT) and heat knock-down time (HKDT) of adults. Results showed LLTs ranging -5 to 5°C and -15 to -1°C whilst ULTs ranged 35 to 42°C and 37 to 44°C for C. sesamiae and C. flavipes respectively. Cotesia flavipes had significantly higher heat tolerance (measured as CTmax), as well as cold tolerance (measured as CTmin) relative to C. sesamiae (P<0.0001). While SCPs did not vary significantly (P>0.05), C. flavipes recovered significantly faster following chill-coma and had higher HKDT compared to C. sesamiae. The results suggest marked differential basal thermal tolerance responses between the two congeners, with C. flavipes having an advantage at both temperature extremes. Thus, under predicted climate change, the two species may differ in phenologies and biogeography with consequences on their efficacy as biological control agents. These results may assist in predicting spatio-temporal activity patterns which can be used in integrated pest management programs under climate variability.

Climate variability differentially impacts thermal fitness traits in three coprophagic beetle species.

While the impacts of extreme and rising mean temperatures are well documented, increased thermal variability associated with climate change may also threaten ectotherm fitness and survival, but remains poorly explored. Using three wild collected coprophagic species Copris elphenor, Metacatharsius opacus and Scarabaeus zambezianus, we explored the effects of thermal amplitude around the mean on thermal tolerance. Using standardized protocols, we measured traits of high- (critical thermal maxima [CTmax] and heat knockdown time [HKDT]) and -low temperature tolerance (critical thermal minima [CTmin], chill coma recovery time [CCRT] and supercooling points [SCPs]) following variable temperature pulses (δ0, δ3, δ6 and δ9°C) around the mean (27°C). Our results show that increased temperature variability may offset basal and plastic responses to temperature and differs across species and metrics tested. Furthermore, we also show differential effects of body mass, body water content (BWC) and body lipid content (BLC) on traits of thermal tolerance. For example, body mass significantly influenced C. elphenor and S. zambezianus CTmax and S. zambezianus HKDT but not CTmin and CCRT. BWC significantly affected M. opacus and C. elphenor CTmax and in only M. opacus HKDT, CTmin and CCRT. Similarly, BLC only had a significant effect for M opacus CTmin. These results suggest differential and species dependent effects of climate variability of thermal fitness traits. It is therefore likely that the ecological services provided by these species may be constrained in the face of climate change. This implies that, to develop more realistic predictions for the effects of climate change on insect biodiversity and ecosystem function, thermal variability is a significant determinant.