Rasoolizadeh A, Goulet MC, Guay JF, Cloutier C, Michaud D. J Insect Physiol. 2018;106:125-133. doi: 10.1016/j.jinsphys.2017.03.001.
Herbivorous insects use complex protease complements to process plant proteins, useful to adjust their digestive functions to the plant diet and to elude the antidigestive effects of dietary protease inhibitors. We here assessed whether basic profiles and diet-related adjustments of the midgut protease complement may vary among populations of the insect herbivore Colorado potato beetle (Leptinotarsa decemlineata). Two laboratory colonies of this insect were used as models, derived from insect samples collected in potato fields ∼1200 km distant from each other in North America. Synchronized 4th-instar larvae reared on potato were kept on this plant, or switched to tomato or eggplant, to compare their midgut cathepsin activities and content of intestain Cys proteases under different diet regimes. Cathepsin D activity, cathepsin L activity, cathepsin B activity and total intestain content shortly after larval molting on potato leaves were about two times lower in one population compared to the other. By comparison, cathepsin D activity, cathepsin B activity, total intestain content and relative abundance of the most prominent intestain families were similar in the two populations after three days regardless of the plant diet, unlike cathepsin L activity and less prominent intestain families showing population-associated variability. Variation in Cys protease profiles translated into the differential efficiency of a Cys protease inhibitor, tomato cystatin SlCYS8, to inhibit cathepsin L activity in midgut extracts of the two insect groups. Despite quantitative differences, SlCYS8 single variants engineered to strongly inhibit Cys proteases showed improved potency against cathepsin L activity of either population. These data suggest the feasibility of designing cystatins to control L. decemlineata that are effective against different populations of this insect. They underline, on the other hand, the practical relevance of considering natural variability of the protease complement among L. decemlineata target populations, eventually determinant in the success or failure of cystatin-based control strategies on a large-scale basis.
Tigreros N, Wang EH, Thaler JS. Funct Ecol. 2018;32(4):982-989. doi: 10.1111/1365-2435.13046.
Prey species can respond to the risk of predation with a range of antipredator behaviours and physiological changes. While these responses increase chances of survival, they often involve feeding reductions and greater energy expenditure (e.g. increases in metabolic rate). As a consequence, a prey response is constrained by its own nutritional condition. While a number of studies indeed demonstrate that prey in better nutritional condition have stronger antipredator behaviours, we do not yet understand how condition impacts the physiological component of the prey's response. Previous research revealed that Leptinotarsa decemlineata beetles experiencing predation risk improve their offspring's nutritional condition by promoting intraclutch egg cannibalism. Importantly, egg cannibalism decreased offspring vulnerability by increasing larval behavioural responses to chronic predation risk. In this study we test if egg cannibalism similarly impacts larval physiological responses by comparing how risk of predation in cannibals and non-cannibals affects their behaviour (e.g. feeding reductions), metabolic rate and energy stores. We found that non-cannibals did not exhibit antipredator behaviours but responded physiologically, by increasing metabolic rates. In contrast, cannibals responded behaviourally, suppressing feeding, but without altering metabolism. While cannibals and non-cannibals coupled food intake and energy expenditure differently, both reached similar growth rates and had similar energy stores when facing chronic predation risk. These results indicate that increases in predator avoidance behaviours are not merely mirrored by a stronger physiological response. Instead, changes in metabolism appear to ameliorate, within our experimental conditions, the costs associated with the behavioural response. Prey in poorer nutritional state are not less responsive to predators but appear to rely more heavily on physiological responses, demonstrating that how prey integrates behaviour and physiology depends on their own nutritional state.
Hermann SL, Thaler JS. Oecologia. 2018;188(4):945-952. doi: 10.1007/s00442-018-4202-7.
Predator-prey interactions primarily focus on prey life-stages that are consumed. However, animals in less vulnerable life-stages might also be influenced by the presence of a predator, making our understanding of predation-related impacts across all life-stages of prey essential. It has been previously demonstrated that Podisus maculiventris is a voracious predator of eggs and larvae of Leptinotarsa decemlineata, and that larvae will alter their behavior to avoid predation. However, the adult beetles are not readily consumed by P. maculiventris, raising the question of whether they will respond to predators to protect themselves or their offspring. Here, we examine the effect of predation risk by P. maculiventris, on three adult behaviors of L. decemlineata; colonization, oviposition, and feeding, and the resulting impact on host plant damage. In an open-field test, there was no difference in natural beetle colonization between plots with predation risk and control treatments. However, subsequent host plant damage by adult beetles was 63.9% less in predation risk treatments. Over the lifetime of adult beetles in field mesocosms, per capita feeding was 23% less in the predation risk treatment. Beetle oviposition was 37% less in the presence of predators in a short-term, greenhouse assay, and marginally reduced in longer term field mesocosms. Our results indicate that predation risk can drive relatively invulnerable adult herbivores to adjust behaviors that affect themselves (feeding) and their offspring (oviposition). Thus, the full impact of predator presence must be considered across the prey life cycle.
Meng Q, Q Xu, T Zhu, L Jin, K Fu, W Guo, G Li. PLoS Genetics. 2019;15(1):e1007423. doi: 10.1371/journal.pgen.1007423.
Many animals exploit several niches sequentially during their life cycles, a fitness referred to as ontogenetic niche shift (ONS). To successfully accomplish ONS, transition between development stages is often coupled with changes in one or more primitive, instinctive behaviors. Yet, the underlining molecular mechanisms remain elusive. We show here that Leptinotarsa decemlineata larvae finish their ONS at the wandering stage by leaving the plant and pupating in soil. At middle wandering phase, larvae also switch their phototactic behavior, from photophilic at foraging period to photophobic. We find that enhancement of juvenile hormone (JH) signal delays the phototactic switch, and vise verse. Moreover, RNA interference (RNAi)-aided knockdown of LdPTTH (prothoracicotropic hormone gene) or LdTorso (PTTH receptor gene) impairs avoidance response to light, a phenotype nonrescuable by 20-hydroxyecdysone. Consequently, the RNAi beetles pupate at the soil surface or in shallow layer of soil, with most of them failing to construct pupation chambers. Furthermore, a combination of depletion of LdPTTH/LdTorso and disturbance of JH signal causes no additive effects on light avoidance response and pupation site selection. Finally, we establish that TrpA1 (transient receptor potential (TRP) cation channel) is necessary for light avoidance behavior, acting downstream of PTTH. We conclude that JH/PTTH cascade concomitantly regulates metamorphosis and the phototaxis switch, to drive ONS of the wandering beetles from plant into soil to start the immobile pupal stage.
Maliszewska J, Tęgowska E. Int J Pest Manage. 2017;63(4):331-340.
The effectiveness of insecticides differs with changes in temperature, but insecticide toxicities are determined at constant temperatures. Constant thermal conditions do not occur in the field, where insects can change their behaviors to achieve a preferred temperature. The aim of this study was to assess whether the choice of ambient temperature affects the mortality rate of intoxicated firebugs and Colorado potato beetles. The insects' mortality following insecticide exposure was monitored at constant temperatures (15, 25, and 35°C) as well as in a thermal gradient system, where the insects could freely select their preferred ambient temperature. Firebugs treated with oxadiazine showed 58% higher mortality when held at a constant temperature post-treatment compared to mortality levels seen when able to choose a preferred temperature in a thermal gradient. Similar results were seen in Colorado potato beetles treated with oxadiazine (15%-33% higher mortality in constant vs. preferred temperature) or organophosphate (36% higher mortality in constant vs. preferred temperature). The insects' ability to mitigate the impacts of pesticide exposure by selecting more beneficial thermal conditions is an important consideration for pest management. Therefore, the application rates of insecticides used under field conditions should be additionally analyzed to take this factor into account.
Wetzel WC, Thaler JS. Oecologia. 2018;186(2):483-493. doi: 10.1007/s00442-017-4034-x.
A consequence of plant diversity is that it can allow or force herbivores to consume multiple plant species, which studies indicate can have major effects on herbivore fitness. An underappreciated but potentially important factor modulating the consequences of multi-species diets is the extent to which herbivores can choose their diets versus being forced to consume specific host-plant sequences. We examined how host-selection behavior alters the effects of multi-species diets using the Colorado potato beetle (Leptinotarsa decemlineata) and diets of potato plants (Solanum tuberosum), tomato plants (S. lycopersicum), or both. When we gave beetles simultaneous access to both plants, allowing them to choose their diets, their final mass was within 0.1% of the average mass across both monocultures and 43.6% lower than mass on potato, the superior host in monoculture. This result indicates these beetles do not benefit from a mixed diet, and that the presence of tomato, an inferior but suitable host, makes it difficult to use potato. In contrast, when we forced beetles to switch between host species, their final mass was 37.8% less than the average of beetles fed constant diets of either host species and within 3.5% of the mass on tomato even though they also fed on potato. This indicates preventing host-selection behavior magnified the negative effects of this multi-species diet. Our results imply that ecological contexts that constrain host-selection or force host-switches, such as communities with competition or predation, will lead plant species diversity to reduce the performance of insect herbivores.
Booth E, Alyokhin A, Pinatti S. Insect Science. 2017;24(2):295-302. doi: 10.1111/1744-7917.12286.
Cannibalism, or intraspecific predation, can play a major role in changing individual fitness and population processes. In insects, cannibalism frequently occurs across life stages, with cannibals consuming a smaller or more vulnerable stage. Predation of adult insects on one another is considered to be uncommon. We investigated adult cannibalism in the Colorado potato beetle, Leptinotarsa decemlineata (Say), which is an oligophagous herbivore specializing on plants in family Solanaceae, and an important agricultural pest. Under laboratory conditions, starvation and crowding encouraged teneral adults to feed upon each other, which reduced their weight loss during the period of starvation. However, pupae were attacked and consumed before adults. Injured beetles had a higher probability of being cannibalized than intact beetles. Males were more frequently attacked than females, but that appeared to be a function of their smaller size rather than other gender-specific traits. Cannibalizing eggs at a larval stage did not affect beetle propensity to cannibalize adults at an adult stage. When given a choice between conspecific adults and mealworms, the beetles preferred to eat conspecifics. Cannibalistic behavior, including adult cannibalism, could be important for population persistence in this species.
Tryjanowski P, Sparks TH, Blecharczyk A, Małecka-Jankowiak I, Switek S, Sawinska Z. American Journal of Potato Research. 2018;95(1):26-32. doi: 10.1007/s12230-017-9611-3.
Potato Solanum tuberosum is one of the world's four most important crops. Its cultivation is steadily increasing in response to the need to feed a growing world population. The yield of potato is influenced inter alia by both climate and pests. The main defoliator pest of potato is Colorado potato beetle Leptinotarsa decemlineata. Using data from a long-term experiment (1958-2013) in western Poland, we show that increasing temperature has affected the trophic relationship between potato and Colorado potato beetle. The planting, leafing, flowering and harvest dates for potato were advanced, after controlling for different cultivars, by 2.00 days, 3.04 days, 3.80 days and 3.42 days respectively for every 1°C increase in temperature. In contrast, first treatment against Colorado potato beetle advanced by 4.66 days for every 1°C increase in temperature, and, furthermore, the number of treatments against the beetle increased by 0.204 per 1°C increase in temperature. This suggests that the beetle responds faster to increasing temperature than the plant does, but both parts of the system are probably greatly modified by farming practices.
Crossley MS, Pélissié B, Cohen Z, Schoville SD. Great Lakes Entomol. 2017;50(3):93-97.
Egg, larval, and adult life stages of Colorado potato beetle, Leptinotarsa decemlineata (Say), were observed feeding on or attached to a previously undocumented host plant belonging to the genus Chamaesaracha in eastern Colorado on July 2017. At one site, L. decemlineata were more abundant on Chamaesaracha sp. than the accepted ancestral host plant, Solanum rostratum (Dunal). While future studies should confirm the ancestral status of the observed L. decemlineata and suitability of Chamaesaracha sp. for completion of development, our observations suggest a need for further characterization of the ancestral host range of L. decemlineata.
Tigreros, N., Norris, R. H., Wang, E. H. and Thaler, J. S. (2017) Ecol Lett. doi:10.1111/ele.12752
Theory on condition-dependent risk-taking indicates that when prey are in poor condition, their anti-predator responses should be weak. However, variation in responses resulting from differences in condition is generally considered an incidental by-product of organisms living in a heterogeneous environment. Using Leptinotarsa decemlineata beetles and stinkbug (Podisus maculiventris) predators, we hypothesised that in response to predation risk, parents improve larval nutritional condition and expression of anti-predator responses by promoting intraclutch cannibalism. We showed that mothers experiencing predation risk increase production of unviable trophic eggs, which assures provisioning of an egg meal to the newly hatched offspring. Next, we experimentally demonstrated that egg cannibalism reduces L. decemlineata vulnerability to predation by improving larval nutritional condition and expression of anti-predator responses. Intraclutch cannibalism in herbivorous insects might be a ubiquitous strategy, aimed to overcome the dual challenge of feeding on protein-limited diets while living under constant predation threat.