Untangling the aphid-parasitoid food web in citrus: Can hyperparasitoids disrupt biological control?

Molecular techniques are irreplaceable to untangle the trophic links in communities where immature entomophagous species (either in the third or fourth level) develop inside the phytophagous. This is the case of aphid-parasitoid communities. Here, we develop a DNA-based approach to untangle the structure of the aphid-parasitoid food web in citrus, where Aphis spiraecola Patch. (Hemiptera: Aphididae) is a key pest and Binodoxys angelicae Haliday (Hymenoptera: Braconidae), its dominant primary parasitoid, is attacked by a complex of hyperparasitoids. Aphid populations and parasitism were followed at weekly intervals in 2012 and 2013. Parasitism rates were low (∼0.04 in the four sampled orchards). Simultaneously, colonies harboring aphid mummies were collected. Approximately half of the mummies were reared to adulthood and at least six hymenopteran hyperparasitoid species were identified by classical means: Syrphophagus aphidivorus (Mayr) (Encyrtidae), Alloxysta sp. (Forster) (Figitidae), Asaphes sp. (Walker) (Pteromalidae), Pachyneuron aphidis (Bouché) (Pteromalidae), Dendrocerus sp. (Ratzeburg) (Megaspilidae) and Phaenoglyphis villosa (Hartig) (Figitidae). The other half was subjected to a Taqman-based multiplex PCR to investigate trophic relationships in this food web. We confirmed that all six species hyperparasitized B. angelicae. The most abundant hyperparasitoids were S. aphidivorus and Alloxysta sp. Both were abundant from the beginning of the season, and hyperparasitism rates remained high (∼0.4) throughout the season in the two study years. Although these species could share the same mummy, S. aphidivorus and Alloxysta sp. were the most abundant species and dominated this food web. Finally, hyperparasitoids also increased the secondary sex ratio of B. angelicae. Thus, hyperparasitism probably explains the low impact of B. angelicae on A. spiraecola populations.     

The impact of transgenic plants on natural enemies: a critical review of laboratory studies

We reviewed laboratory tests which studied the impact of genetically modified plants on arthropod natural enemies. A total of 18 species of predators and 14 species of parasitoids have been tested, most in only a few experiments. Certain groups (braconid wasps) or species (the green lacewing, Chrysoperla carnea) have attracted much effort, while representatives of others, including whole orders (e.g., Diptera), have never had a species tested. We conclude that laboratory tests are not the ‘worst case’ scenarios intended by the experimental designs, and are not often ecologically realistic: they typically provided ad libitum feeding, no prey choice, single prey type, no combination of stress factors and usually uniform temperatures. None of these are representative of field conditions, yet most could be easily mimicked in more complex laboratory tests. In most cases (94.6%), the studies were unable to indicate the level of power required to detect any impact. Small sample size and large variability are factors that mask all but very large differences in potential effects. For predators, 126 parameters were quantified, most commonly including survival/mortality (37 cases), development time (22), and body mass/size (20). For parasitoids, 128 parameters were quantified, the majority involving lectins or proteinase inhibitors. Most frequent measurements were: fecundity (23 experiments), adult longevity, extent of parasitism (17 each), body size, mortality, and larval development time. An aggregative scoring (summarising all quantified parameters) indicated that the laboratory tests quantified a remarkable number of cases (30% for predators, 39.8% for parasitoids), where the impacts of the genetically modified plant were significantly negative. These involve various parameters, organisms, test methods, and significance levels, but collectively they indicate that the use of genetically modified crops may result in negative effects on the natural enemies of crop pests.     

Feeding of pea leafminer larvae simultaneously activates jasmonic and salicylic acid pathways in plants to release a terpenoid for indirect defense

The pea leafminer, Liriomyza huidobrensis, is an important pest species affecting ornamental crops worldwide. Plant damage consists of oviposition and feeding punctures created by female adult flies as well as larva-bored mines in leaf mesophyll tissues. How plants indirectly defend themselves from these two types of leafminer damage has not been sufficiently investigated. In this study, we compared the indirect defense responses of bean plants infested by either female adults or larvae. Puncturing of leaves by adults released green leaf volatiles and terpenoids, while larval feeding caused plants to additionally emit methyl salicylate and (E,E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene (TMTT). Puncturing of plants by female adults induced increases in jasmonic acid (JA) and JA-related gene expressions but reduced the expressions of salicylic acid (SA)-related genes. In contrast, JA and SA and their-related gene expression levels were increased significantly by larval feeding. The exogenous application of JA+SA significantly triggered TMTT emission, thereby significantly inducing the orientation behavior of parasitoids. Our study has confirmed that larval feeding can trigger TMTT emission through the activation of both JA and SA pathways to attract parasitoids; however, TMTT alone is less attractive than the complete blend of volatiles released by infested plants.     

Assessing superparasitism with a model combining the functional response and the egg distribution of parasitoids

A model for superparasitism in insect parasitoids is developed. This model combines the study of superparasitism in terms of distribution of eggs among hosts (for a given number of hosts) and in terms of functional response (number of hosts attacked for a varying number of hosts available). Thus, it gives a synthetic treatment of problems that had been previously handled with separate models (e.g., Bakkeret al. (1972) on one hand and Arditi (1983) on the other hand). The combined model involves several parameters, among which important ones are the propensity to superparasitise, δ, and the average handling times spent on healthy and parasitised hosts, T_h and T_p. Special cases are those of an indiscriminate parasitoid (δ=1 and T_p=T_h) and of a “predator-like” parasitoid (δ=0 and T_p=0). In this paper, the emphasis is put on the problems related with model identification and parameter estimation from experimental data. According to the data available, three situations are considered: egg distribution alone, functional response alone, and both combined. The main conclusions are the following. (i) Egg distributions are described correctly when the parasitoid/host ratio is not too high. When the situation is very strained, i.e., when a small number of hosts are available per parasitoid, superparasitism occurs more frequently than predicted by the model. (ii) Functional response data are usually not precise enough to estimate all model parameters, particularly T_p. That is, it will usually not be possible to assess the discrimination capacity of a given species on the basis of a functional response curve only. (iii) If both a functional response and the corresponding egg distributions are available, it is better to fit the egg distribution model first and, depending on the estimated value of δ, to fit thereafter the appropriate functional response model.