The preference-performance relationship as a means of classifying parasitoids according to their specialization degree.

Host range in parasitoids could be described by the preference-performance hypothesis (PPH) where preference is defined as host acceptance and performance is defined as the sum of all species on which parasitoid offspring can complete their life cycle. The PPH predicts that highly suitable hosts will be preferred by ovipositing females. However, generalist parasitoids may not conform to this hypothesis if they attack a large range of hosts of varying suitability. Under laboratory conditions, we tested the PPH relationship of three aphid parasitoids currently considered as generalist species (Aphelinus abdominalis, Aphidius ervi, Diaeretiella rapae). As expected, the three parasitoids species showed low selectivity, i.e., females stung all aphid species encountered (at least in some extent). However, depending on the parasitoid species, only 42%-58% of aphid species enabled producing parasitoid offspring. We did not find a correlation between the extent of preference and the performance of three generalist aphid parasitoids. For A. ervi, host phylogeny is also important as females showed higher attack and developmental rates on hosts closely related to the most suitable one. In addition, traits such as (a) the presence of protective secondary endosymbionts, for example, Hamiltonella defensa detected in Aphis fabae and Metopolophium dirhodum and (b) the sequestration of plant toxins as defense mechanism against parasitism, for example, in Aphis nerii and Brevicoryne brassicae, were likely at play to some extent in narrowing parasitoid host range. The lack of PPH relationship involved a low selectivity leading to a high adaptability, as well as selection pressure; the combination of which enabled the production of offspring in a new host species or a new environment. Testing for PPH relationships in parasitoids may provide useful cues to classify parasitoids in terms of specialization degree.

Nitrogen and water inputs to tomato plant do not trigger bottom-up effects on a leafminer parasitoid through host and non-host exposures.

BACKGROUND: Bottom-up and top-down forces are major components of biological control against pests in an agro-ecosystem. Understanding the multi-trophic interactions between plants and secondary consumers would help optimize pest control strategies. We manipulated nitrogen and/or water inputs to tomato plants (Solanum lycopersicum) to test whether these manipulations could trigger bottom-up effects on the parasitoid Necremnus tutae via host (Tuta absoluta) and/or non-host (Bemisia tabaci) exposures, and compared the control efficacy of N. tutae on T. absoluta in the presence and absence of B. tabaci. RESULTS: The results showed no cascading effects of plant nitrogen and/or water inputs on N. tutae via either host or non-host exposure. The bottom-up force was mitigated by chewing or sap-feeding insect consumers at the second energy level. By contrast, the top-down force on T. absoluta from parasitoids was enhanced by an additionally provided non-host, which could produce alternative food sources extending N. tutae longevity and enhancing the fitness of its offspring. CONCLUSION: Our results provided evidence for the combination of bottom-up and top-down approaches in tomato integrated pest management programs. © 2017 Society of Chemical Industry.

Does Plant Cultivar Difference Modify the Bottom-Up Effects of Resource Limitation on Plant-Insect Herbivore Interactions?

Variation in resource input to plants triggers bottom-up effects on plant-insect herbivore interactions. However, variation in plant intrinsic traits in response to resource availability may modify the bottom-up effects. Furthermore, the consequences also may depend on the feeding strategy of insect herbivores belonging to different feeding guilds. We evaluated the performance of two insect herbivores from distinct feeding guilds, the leaf miner Tuta absoluta and the phloem feeder Bemisia tabaci. We offered the insects two tomato cultivars growing under optimal nitrogen input vs. nitrogen limitation, or under optimal water input vs. water limitation. We found that: (i) the two cultivars differed in their responses to nitrogen and water limitation by regulating primary (leaf-gas exchange related parameters, leaf nitrogen content, and leaf C/N ratio) and secondary metabolism (main defensive compounds: glycoalkaloids); (ii) for both plant cultivars, nitrogen or water limitation significantly affected T. absoluta survival and development, while B. tabaci survival was affected only by nitrogen limitation; and surprisingly (iii) plant cultivar differences did not modify the negative bottom-up effects of resource limitation on the two insect herbivores. In conclusion, the negative effects of resource limitation cascaded up to insect herbivores even though plant cultivars exhibited various adaptive traits to resource limitation.

New parasitoid-predator associations: female parasitoids do not avoid competition with generalist predators when sharing invasive prey.

Optimal habitat selection is essential for species survival in ecosystems, and interspecific competition is a key ecological mechanism for many observed species association patterns. Specialized animal species are commonly affected by resource and interference competition with generalist and/or omnivorous competitors, so avoidance behavior could be expected. We hypothesize that specialist species may exploit broad range cues from such potential resource competitors (i.e., cues possibly common to various generalist and/or omnivorous predators) to avoid costly competition regarding food or reproduction, even in new species associations. We tested this hypothesis by studying short-term interactions between a native larval parasitoid and a native generalist omnivorous predator recently sharing the same invasive host/prey, the leaf miner Tuta absoluta. We observed a strong negative effect of kleptoparasitism (food resource stealing) instead of classical intraguild predation on immature parasitoids. There was no evidence that parasitoid females avoided the omnivorous predator when searching for oviposition sites, although we studied both long- and short-range known detection mechanisms. Therefore, we conclude that broad range cue avoidance may not exist in our biological system, probably because it would lead to too much oviposition site avoidance which would not be an efficient and, thus, beneficial strategy. If confirmed in other parasitoids or specialist predators, our findings may have implications for population dynamics, especially in the current context of increasing invasive species and the resulting creation of many new species associations.

Nitrogen and water availability to tomato plants triggers bottom-up effects on the leafminer Tuta absoluta.

This study examined the effects of various levels of nitrogen inputs (optimal, insufficient and excessive) and water inputs (optimal, low drought and high drought) to tomato plants (Solanum lycopersicum) on survival and development of an invasive tomato leafminer, Tuta absoluta (Meytick) (Lepidoptera: Gelechiidae). Plant growth i.e. plant height and the number of nodes declined under insufficient or excessive nitrogen treatment. Compared to optimal N, insufficient N treatment decreased leaf N content and increased the carbon/nitrogen ratio (C/N) whereas an excess of N had no effect on both leaf N content and leaf C/N ratio. Sub-optimal nitrogen supplies, water treatments and their interactions, significantly reduced the leafminer survival rate and slowed down its development. Together with the findings from three recent companion studies, we assumed that a combination of changes in nutritional value and chemical defense could explain these observed effects. Furthermore, our findings supported both the "Plant vigor hypothesis" and the "Nitrogen limitation hypothesis".

Preference and prey switching in a generalist predator attacking local and invasive alien pests.

Invasive pest species may strongly affect biotic interactions in agro-ecosystems. The ability of generalist predators to prey on new invasive pests may result in drastic changes in the population dynamics of local pest species owing to predator-mediated indirect interactions among prey. On a short time scale, the nature and strength of such indirect interactions depend largely on preferences between prey and on predator behavior patterns. Under laboratory conditions we evaluated the prey preference of the generalist predator Macrolophus pygmaeus Rambur (Heteroptera: Miridae) when it encounters simultaneously the local tomato pest Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) and the invasive alien pest Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). We tested various ratios of local vs. alien prey numbers, measuring switching by the predator from one prey to the other, and assessing what conditions (e.g. prey species abundance and prey development stage) may favor such prey switching. The total predation activity of M. pygmaeus was affected by the presence of T. absoluta in the prey complex with an opposite effect when comparing adult and juvenile predators. The predator showed similar preference toward T. absoluta eggs and B. tabaci nymphs, but T. absoluta larvae were clearly less attacked. However, prey preference strongly depended on prey relative abundance with a disproportionately high predation on the most abundant prey and disproportionately low predation on the rarest prey. Together with the findings of a recent companion study (Bompard et al. 2013, Population Ecology), the insight obtained on M. pygmaeus prey switching may be useful for Integrated Pest Management in tomato crops, notably for optimal simultaneous management of B. tabaci and T. absoluta, which very frequently co-occur on tomato.

Biology and developmental strategies of the Palaearctic parasitoid Bracon nigricans (Hymenoptera: Braconidae) on the neotropical moth Tuta absoluta (Lepidoptera: Gelechiidae).

During the years after the invasion of Western Palaearctic tomato crops by the South American tomato leafminer, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae), several indigenous generalist parasitoids have been recorded on this new host. Among these, Bracon nigricans Szépligeti (Hymenoptera: Braconidae) is widely distributed in the Palaearctic region, and has been frequently recovered from South American tomato leafminer. However, most of the available data on this species deal with taxonomic aspects and its recovery in faunistic surveys. The current study documents the biology of B. nigricans on South American tomato leafminer, and provides a scientific basis for its inclusion in South American tomato leafminer management programs in Afro-Eurasia. We studied several B. nigricans life-history traits relevant to juvenile development and reproduction by females. B. nigricans proved to be an idiobiont and a synovigenic ectoparasitoid of mature South American tomato leafminer larvae. Several B. nigricans reproductive traits were influenced by the age of the mothers; on average, the progeny had a slightly male-biased sex ratio (60% males) and a low rate of successful development (37%). Adult females lived 42.8 d and produced an average of 29.8 offspring. These biological parameters yielded an intrinsic rate of increase of 0.052. Females showed behavioral plasticity in host use, as initial host paralysis was followed by host-feeding, oviposition, or host rejection, with a consequent high mortality rate among hosts exposed to parasitism. Although further field studies are needed, these data, obtained in laboratory conditions, suggest that B. nigricans should be considered as a potential biological control agent of in newly invaded areas of the Palaearctic region.

Spatiotemporal patterns of induced resistance and susceptibility linking diverse plant parasites.

Induced defenses mediate interactions between parasites sharing the same host plant, but the outcomes of these interactions are challenging to predict because of spatiotemporal variation in plant responses and differences in defense pathways elicited by herbivores or pathogens. Dissecting these mediating factors necessitates an approach that encompasses a diversity of parasitic feeding styles and tracks interactions over space and time. We tested indirect plant-mediated relationships across three tomato (Solanum lycopersicum) consumers: (1) the fungal pathogen-powdery mildew, Oidium neolycopersici; (2) a sap-feeding insect-silverleaf whitefly, Bemisia tabaci; and (3) a chewing insect-the leaf miner, Tuta absoluta. Further, we evaluated insect/pathogen responses on local vs. systemic leaves and over short (1 day) vs. long (4 days) time scales. Overall, we documented: (1) a bi-directional negative effect between O. neolycopersici and B. tabaci; (2) an asymmetrical negative effect of B. tabaci on T. absoluta; and (3) an asymmetrical positive effect of T. absoluta on O. neolycopersici. Spatiotemporal patterns varied depending on the species pair (e.g., whitefly effects on leaf miner performance were highly localized to the induced leaf, whereas effects on pathogen growth were both local and systemic). These results highlight the context-dependent effects of induced defenses on a diverse community of tomato parasites. Notably, the outcomes correspond to those predicted by phytohormonal theory based on feeding guild differences with key implications for the recent European invasion by T. absoluta.