Ricardo Ramirez-Romero

Plant characteristics mediated by growing conditions can impact parasitoid’s ability to attack host aphids in winter canola

Winter canola (Brassica napus) is an important crop in various parts of the world. It is planted in fall, vernalized during winter and offers higher yields than spring canola. One of the key aphid pests of this crop is Myzus persicae Sulzer (Homoptera: Aphididae). Recent surveys in Europe showed that M. persicae in winter canola is parasitized by Aphidius matricariae and Diaeretiella rapae, but not by other aphidiine parasitoid species known to attack M. persicae in other crops. During vernalization, winter canola plants acclimatize to survive specific climatic conditions of winter, e.g. through the formation of epicuticular waxes on leaves. These waxes could affect efficiency on natural enemies. In this study, we characterized (1) the ability of aphidiine parasitoids to locate and attack M. persicae on winter canola, and (2) how plant vernalization influences parasitoid ability to attack suitable hosts. In the laboratory, the ability of A. ervi, A. matricariae and D. rapae to orient toward odors of the M. persicae-winter canola complex was studied in an olfactometer, as well as their ability to attack M. persicae on winter canola. In addition, the impact of plant species and plant vernalization on the ability of A. colemani to attack and locate M. persicae was evaluated. The results show that A. matricariae and D. rapae readily locate and attack M. persicae on winter canola as does A. ervi, albeit to lesser extent. Aphidius colemani shows low ability to parasitize M. persicae on this plant species. Vernalization of canola is an important factor mediating the ability of A. colemani to attack M. persicae and it likely results from the presence of Brassica’s waxes that reduce parasitoid mobility and impact foraging behavior. These results show that aphid parasitoids differ in their ability to locate and attack M. persicae on winter canola, the latter being a function of parasitoids’ capacity to cope with plant characteristics that are mediated by growing conditions.

Effect of continuous rearing on courtship acoustics of five braconid parasitoids, candidates for augmentative biological control of Anastrepha species

The courtship acoustics of five species of parasitoid wasps (Hymenoptera: Braconidae), potential candidates for augmentative biological control of Anastrepha (Schiner) species (Diptera: Tephritidae), were compared between recently colonized individuals and those continuously reared 70–148 generations. During courtship, males of these parasitoid species fan their wings and produce a series of low amplitude pulses. The first series of 15 or more continuous courtship pulses was used to measure the pulse duration, frequency, and interpulse interval (IPI) from the beginning, middle, and end of the pulse series. Each parameter was compared between young and old colonies, and among species. Several differences in courtship acoustics were detected in colonies that had been continuously reared. The pulse duration at the end of the pulse series was longer in old colonies for Doryctobracon crawfordi (Viereck) (Hymenoptera: Braconidae), but shorter for old colonies of Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae). The IPI of the middle pulse was shorter in old colonies of Opius hirtus (Fischer) (Hymenoptera: Braconidae), and was also shorter at the last pulse for old colonies of both Utetes anastrephae (Viereck) (Hymenoptera: Braconidae) and D. longicaudata. The duration of the middle pulse distinguished the three native species, and separated the two introduced species from each other. We discuss our findings in light of their biological and applied implications, particularly those dealing with quality control of mass-reared parasitoids.

Behavioral effects of insect-resistant genetically modified crops on phytophagous and beneficial arthropods: a review

Behavior is a main component of the survival and performance of arthropods. We have witnessed widespread adoption of insect-resistant genetically modified (IRGM) crops nowadays; however, no literature has reviewed the behavioral effects of IRGM crops on phytophagous and beneficial arthropods. In this review, we assessed the current information related to the effects of IRGM crops on arthropod behavior, mainly including locomotion (mobility, escape behavior and dispersal behavior), foraging (orientation, host plant selection/preference and feeding), mating, oviposition and other behaviors (associative learning). Almost all the studies have been conducted on Bt crops. The behavioral effects have been found in 54.2 %, 22 % and 33 % of the case studies on phytophagous arthropods, arthropod natural enemies and pollinators, respectively. Few behavioral studies have been documented on arthropod pollinators. The majority of cases reporting behavioral effects have derived from target phytophagous arthropods. Among them, locomotion and feeding behavior were the most frequently affected. For arthropod natural enemies, the cases using target prey/host in tri-trophic studies only accounted for a small proportion of behavioral effects observed on foraging behavior (host/prey selection). Overall, the effects through tri-trophic pathways on behaviors of natural enemies are limited. To conclude, while attention needs to be paid to several behavioral effects that may undermine the efficacy of IRGM crops in sustainable pest management, the behavioral effects generally do not disrupt the role of IRGM crops in achieving the goal of integrated pest management and crop production.

Attraction of the parasitoid Cotesia marginiventris to host (Spodoptera frugiperda) frass is affected by transgenic maize.

We assessed in the laboratory the attraction of the parasitoid Cotesia marginiventris (Cresson) toward odors emitted by conventional maize (Zea mays L. ssp. mays) and Bt (Bacillus thuringiensis) maize seedlings following actual or simulated injury by Spodoptera frugiperda (Smith), the parasitoid’s host, and emitted by the host’s frass, produced following consumption of conventional or Bt maize seedlings. Females of C. marginiventris exhibited similarly strong responses to conventional and Bt maize seedlings injured by the host or with simulated injury, and these were stronger than responses to clean air. In contrast, the responses of C. marginiventris females were consistently weaker toward host frass derived from Bt maize tissue compared to frass derived from conventional maize tissue. We hypothesized that the weakened response was due to a detrimental effect of Bt endotoxins, present in the Bt maize tissue, on the bacterial community present in the host’s gut and frass, including bacteria that produce odors attractive to C. marginiventris. As an initial test of our hypothesis, we compared between the responses of C. marginiventris females to host frass produced following consumption of Bt maize and frass produced from conventional maize which had been treated with an antibiotic (tetracycline) to eliminate host gut bacteria. Our results showed that C. marginiventris females responded similarly weakly to host frass derived from conventional maize tissue treated with antibiotic and to frass derived from Bt maize tissue, treated or untreated with antibiotic, while they responded strongly to frass derived from conventional maize untreated with antibiotic, so provided initial, partial support for our hypothesis. We discussed the weakened response of C. marginiventris females to host frass derived from Bt maize in the context of plausible impacts of transgenic crop cultivars on parasitoid foraging and populations, and the implications for biological control of non-target, polyphagous pests, such as S. frugiperda.

Intraguild Predation on the Whitefly Parasitoid Eretmocerus eremicus by the Generalist Predator Geocoris punctipes: A Behavioral Approach

Intraguild predation (IGP) takes place when natural enemies that use similar resources attack each other. The impact of IGP on biological control can be significant if the survival of natural enemy species is disrupted. In the present study, we assessed whether Geocoris punctipes (Hemiptera: Lygaeidae) engages in IGP on Eretmocerus eremicus (Hymenoptera: Aphelinidae) while developing on whitefly nymphs of Trialeurodes vaporariorum (Hemiptera: Aleyrodidae). In choice and non-choice tests, we exposed G. punctipes to parasitized and non-parasitized whitefly nymphs. We found that G. punctipes does practice IGP on E. eremicus. However, choice tests assessing G. punctipes consumption revealed a significant preference for non-parasitized T. vaporariorum nymphs. Subsequently, we investigated whether E. eremicus females modify their foraging behavior when exposed to conditions involving IGP risk. To assess this, we analyzed wasp foraging behavior under the following treatments: i) whitefly nymphs only (control = C), ii) whitefly nymphs previously exposed to a predator ( = PEP) and, iii) whitefly nymphs and presence of a predator ( = PP). In non-choice tests we found that E. eremicus did not significantly modify its number of attacks, attack duration, oviposition duration, or behavior sequences. However, E. eremicus oviposited significantly more eggs in the PEP treatment. In the PP treatment, G. punctipes also preyed upon adult E. eremicus wasps, significantly reducing their number of ovipositions and residence time. When the wasps were studied under choice tests, in which they were exposed simultaneously to all three treatments, the number of attacks and frequency of selection were similar under all treatments. These results indicate that under IGP risk, E. eremicus maintains several behavioral traits, but can also increase its number of ovipositions in the presence of IG-predator cues. We discuss these findings in the context of population dynamics and biological control.

Are individuals from thelytokous and arrhenotokous populations equally adept as biocontrol agents? Orientation and host searching behavior of a fruit fly parasitoid

Hymenopteran parasitoids generally reproduce by arrhenotoky, in which males develop from unfertilized eggs and females from fertilized eggs. A minority reproduce by thelytoky, in which all-female broods are derived from unfertilized eggs. Thelytokous populations are potentially of interest for augmentative biological control programs since the exclusive production of females could significantly lower the costs of mass rearing. Behavioral traits are a major component of parasitoid efficacy. Here, we examined orientation and host searching behavior in thelytokous and arrhenotokous populations of the fruit fly parasitoid Odontosema anastrephae Borgmeier (Hymenoptera: Figitidae). Orientation behavior to various odorant sources was studied in a two-choice olfactometer. No major differences were found between thelytokous and arrhenotokous wasps for this behavior. However, when host-searching behaviors were analyzed, some differences were found. Thelytokous females arrived sooner, foraged longer, and remained longer on non-infested guavas than arrhenotokous females. Individuals of both forms exhibited similar stereotyped behavioral sequences vis-à-vis guava treatments, with only slight deviations detected. Our results suggest that individuals from selected thelytokous and arrhenotokous O. anastrephae populations have similar abilities to search for tephritid larvae, supporting the use of thelytokous strains for augmentative releases.

Foraging behaviour of the parasitoid Eretmocerus eremicus under intraguild predation risk by Macrolophus pygmaeus.

BACKGROUND Intraguild predation (IGP), predation between species that use a common resource, can affect the populations of a pest, of the pests natural enemy (IG prey) and of the predator of the pests natural enemy (IG predator). In this study, we determined whether the parasitoid Eretmocerus eremicus (Hymenoptera: Aphelinidae) (IG prey), modifies its foraging behaviour under the risk of IGP by Macrolophus pygmaeus (Hemiptera: Miridae) (IG predator). Parasitoid behaviour was analysed using two bioassays (choice and no-choice) with the following treatments: (i) control, tomato leaf infested with whitefly nymphs; and (ii) PEP, tomato leaf infested with whitefly nymphs and previously exposed to the IG predator; and (iii) PP, tomato leaf infested with whitefly nymphs, with both, the IG predator and the IG prey present. RESULTS In both bioassays, we found that E. eremicus did not significantly modify the number of ovipositions, time of residence, duration of oviposition or behavioural sequence. However, in the no-choice bioassay, the number of attacks was higher and their duration shorter in the PEP treatment than in the control. CONCLUSION Our results indicate that the parasitoid may detect IGP risk to a certain extent, but it did not significantly modify its foraging behaviour, suggesting that simultaneous release of the two natural enemies can be successfully employed.

Genetic Characteristics of Bisexual and Female-Only Populations of Odontosema anastrephae (Hymenoptera: Figitidae)

ABSTRACT Odontosema anastrephae Borgmeier is a figitid parasitoid of Anastrepha fruit fly larvae infesting fallen fruit. It is of potential use in biological control as a complement to parasitoids that attack larvae infesting fruit still on the tree and to parasitoids that can only oviposit into larvae near the surface of the fruit, because Odontosema pursues larvae deep within the pulp. A newly discovered Mexican all-female (presumably thelytokous) population, provisionally referred to here as O. near anastrephae, appears to be morphologically indistinguishable from arrhenotokous individuals. Thelytokous reproduction can potentially lower costs in mass rearing facilities and increase parasitoid efficacy in the field. PCR amplification and sequencing of mitochondrial (COI) and nuclear (ITS2) genetic sequences suggested that these populations are genetically distinct, but no more so than often occurs among distinct populations within recognized species. In addition to the description of an all-female population of Odontosema, this study presents the first genetic sequence data for members of the genus Odontosema, enabling phylogenetic comparison between Odontosema and other figitid genera and the development of methods for the identification of Odontosema species by PCR. The implications of thelytoky for a cladistic definition of speciation, especially for newly diverging populations such as these, as well as the potential practical implications of our findings for fruit fly biological control, are discussed.

Behavioral asymmetries in the mealybug parasitoid Anagyrus sp. near pseudococci : does lateralized antennal tapping predict male mating success?

Lateralization is a fundamental principle of the brain organization widespread among vertebrates but rather unknown in invertebrates. Evidences of lateralized courtship and mating behavioral traits in parasitic wasps are extremely rare. Here, courtship and mating sequences and the presence of mating lateralization in Anagyrus sp. near pseudococci, one of the most effective biological control agents of mealybugs, were investigated. Courtship and mating behavior in A. sp. near pseudococci consisted in the male chasing of the female, pre-copula, copula, and post-copula phases. Males mating success was not related to the duration of chasing and pre-copula. High-speed videos showed population-level lateralization in A. sp. near pseudococci during courtship. Most the wasps used the right antenna to start antennal tapping and this led to a higher mating success, although lateralization had no impact on the frequency of the antennal tapping. Both females and males displayed this behavior. Higher mating success was detected when females displayed antennal tapping during sexual interaction, though male tapping was performed with a slightly higher frequency. To the best of our knowledge, this report on behavioral asymmetries of mating traits in A. sp. near pseudococci represents a quite rare evidence of lateralized behavior in parasitic wasps of economic importance. Our findings add basic knowledge on the behavioral ecology of this biocontrol agent with potential implications on the optimization of mass-rearing procedures aimed at using this parasitoid in Integrated Pest Management.

Intraguild predation of Geocoris punctipes on Eretmocerus eremicus and its influence on the control of the whitefly Trialeurodes vaporariorum.

BACKGROUND Geocoris punctipes (Hemiptera: Lygaeidae) and Eretmocerus eremicus (Hymenoptera: Aphelinidae) are whitefly natural enemies. Previously, under laboratory conditions, we showed that G. punctipes engages in intraguild predation (IGP), the attack of one natural enemy by another, on E. eremicus. However, it is unknown whether this IGP interaction takes place under more complex scenarios, such as semi-field conditions. Even more importantly, the effect of this interaction on the density of the prey population requires investigation. Therefore, the present study aimed to establish whether this IGP takes place under semi-field conditions and to determine whether the predation rate of G. punctipes on the whitefly decreases when IGP takes place. RESULTS Molecular analysis showed that, under semi-field conditions, G. punctipes performed IGP on E. eremicus. However, although IGP did take place, the predation rate by G. punctipes on the whitefly was nevertheless higher when both natural enemies were present together than when the predator was present alone. CONCLUSION While IGP of G. punctipes on E. eremicus does occur under semi-field conditions, it does not adversely affect whitefly control. The concomitant use of these two natural enemies seems a valid option for inundative biological control programmes of T. vaporariorum in tomato.