María G. Luna

The invasive South American tomato pinworm, Tuta absoluta, continues to spread in Afro-Eurasia and beyond: the new threat to tomato world production

The economic and ecological effects of invasive species, notably pests (Mack et al. 2000; Suckling and Brockerhoff 2010; Ragsdale et al. 2011), are now widely recognized (Thomas 1999; Pysek and Richardson 2010). The South American tomato pinworm Tuta absoluta Meyrick (Lepidoptera: Gelechiidae) is an invasive pest, native to South America which was detected in eastern Spain at the end of 2006. Since then, T. absoluta has spread to the European and the North African Mediterranean Basin countries where it has become a serious agricultural threat to tomato production in both greenhouse and outdoor tomato crops (see Desneux et al. 2010 for a thorough review). This pest spreads rapidly and its status in the world has completely changed within only a few years from a South American tomato pest to a major threat to tomato world production. In this letter, we update the available information on the current distribution of T. absoluta in the world. Moreover, we describe and discuss the threat represented by the rapid spread of T. absoluta and how this pest is going to change world tomato production.

Parasitism of Tuta absoluta (Lepidoptera, Gelechiidae) by Pseudapanteles dignus (Hymenoptera, Braconidae) Under Laboratory Conditions

Abstract Laboratory studies were conducted to measure selected life history traits and the functional response of the parasitoid Pseudapanteles dignus (Muesebeck), a major enemy of Tuta absoluta (Meyrick) in tomato crops in South America. Newly mated P. dignus females were individually exposed to 10 host larvae in mines for 24 h. We determined developmental time from egg to pupal formation and pupal stage duration, female adult life span, fecundity, reproductive period, daily parasitism rate, and sex ratio of offspring. For the functional response experiment, treatments consisted of six host densities: 3, 5, 7, 10, 15, 20, or 30 larvae. The number and proportion of parasitized hosts were calculated for each density. The shape of the functional response curve was analyzed by logistic regression. P. dignus females attacked hosts daily, exhibiting modest lifetime fecundity (≈32 parasitized hosts per female) and a female-biased offspring sex ratio. Female adult life span was 36 d. P. dignus showed a type I functional response within the range of host densities tested. We observed that females detect and parasitize the host within a wide range of densities, including low densities. The functional response curve reached an asymptote at a mean density of six hosts per day and seemed not to be egg-limited. Percent parasitism was ≈30%. The ecological implications of the results in relation to the potential of P. dignus for the biological control of T. absoluta in tomato are discussed.

Reproductive Biology and Functional Response of Dineulophus phtorimaeae, a Natural Enemy of the Tomato Moth, Tuta absoluta

Abstract The tomato moth, Tuta absoluta (Lepidoptera: Gelechiidae), is a major pest in South America and is at present an important invasive species in the Mediterranean Basin. The larval stadium mines leaves, stems, and fruits, and chemical control is the most used control method in both its original range and the invaded distribution regions. Since current T. absoluta control strategies seem limited, biological control is a prominent tool to be applied abroad. The naturally occurring larval ectoparasitoid in Argentina and Chile Dineulophus phtorimaeae (Hymenoptera: Eulophidae) has been reported to have potential biocontrol efficiency. In this study, the ovigeny strategy of D. phtorimaeae was analyzed throughout the adult female lifetime, and the functional response of females offered a range of 2–15 T. absoluta larvae was measured over a 48-hour period. Mean D. phtorimaeae egg load was 4.15 eggs, and egg production resulted in extremely synovigenic behavior. Meanwhile, a decreasing number of eggs, due to resorption, was found. Proportions of attacked (host-fed and/or parasitized) and only host-fed hosts by the ectoparasitoid were density independent for the tested host range, exhibiting a type I functional response to T. absoluta, with an attack rate of 0.20 host larvae. Meanings of this reproductive strategy in evolutionary time as well as the consequences for augmentative biological control programs are discussed.

Spatial Patterns of Parasitism of the Solitary Parasitoid Pseudapanteles dignus (Hymenoptera: Braconidae) on Tuta absoluta (Lepidoptera: Gelechiidae)

We examined the interaction between the tomato leafminer, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae), a key pest of tomato crops in South America, and its main solitary larval parasitoid, Pseudapanteles dignus (Muesebeck) (Hymenoptera: Braconidae). The pattern of parasitism of T. absoluta by the parasitoid was studied at three scales on tomato crops: plant, leaf, and leaflet. Host density, spatial distributions of both host and parasitoid, percentages of parasitism, variation in the probability and risk of parasitism in relation to host density, and the spatial density dependence were assessed in a horticultural region in Argentina. The spatial distribution of T. absoluta was clumped at all sites and scales, whereas that of P. dignus was much more variable, fitting to negative, positive binomial distributions and to Poisson series. Percentages of parasitism were as follows: site 1, 17.06%; site 2, 27.53%; site 3, 26.47%; site 4, 45.95%. Parasitoid aggregation in relation to host density was found at leaf and leaflet scales. However, the proportion of parasitized hosts was independent of host density. The variability of parasitism rates exhibited at the three spatial scales seems to result in partial refuges for the host, which might contribute to the persistence of the interaction between host and parasitoid. We discuss our field observations in relation to ecological theory and its potential application to the biological control of T. absoluta on tomato.

Effects of Inbreeding Versus Outbreeding in Nasonia vitripennis (Hymenoptera: Pteromalidae)

Abstract Many species of parasitic Hymenoptera inbreed regularly and do not suffer inbreeding depression. However, these inbreeding species could experience outbreeding depression due to the breakup of coadapted gene complexes. We measured the effects of outbreeding on three fitness components of the ectoparasitoid Nasonia vitripennis Walker, a chronic inbreeder. Experimental treatments varied the mating structure within and among populations: inbred (sib-matings within families), outbred within strains (nonsib-matings among families within strains), and outbred among strains, for 15 generations. Life span, fecundity, and sex ratio were measured in the parental generation and in four selected filial generations. We found no evidence of outbreeding depression for any of the fitness parameters tested. However, modest inbreeding depression was suggested as increased life span and fecundity when females were paired with nonsibling males from the same geographic strain, and by increased fecundity for interstrain crosses. Sex ratio did not respond to any of the levels of outbreeding. Consequently, we reject our hypothesis that N. vitripennis suffers outbreeding depression. However, heterosis within and among strains suggests that at least some local populations of N. vitripennis may suffer from modest inbreeding depression.

Biology of Dineulophus phtorimaeae (Hymenoptera: Eulophidae) and Field Interaction with Pseudapanteles dignus (Hymenoptera: Braconidae), Larval Parasitoids of Tuta absoluta (Lepidoptera: Gelechiidae) in Tomato

ABSTRACT Some biological characteristics of the ectoparasitoid Dineulophus phtorimaeae (de Santis) (Hymenoptera: Eulophidae) and field interaction with the endoparasitoid Pseudapanteles dignus (Muesebeck), both larval parasitoids of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae), were examined. In addition, we completed the original description of D. phtorimaeae. Preimaginal developmental time of the ectoparasitoid was 11.17 ± 0.60 d for both sexes, and adult life span was 11.73 ± 0.92 d for females and 8.78 ± 0.93 d for males. The proportion of males to females was equal. In the field, hosts were parasitized at the third larval instar. On average, a female attacked ca. four hosts throughout her lifetime and deposited eggs in ≈50% of cases. The most successful female attacked six hosts, yielding a potential fecundity of ≈10 eggs. Host paralysis without parasitism was observed, suggesting stinging for host feeding. The daily oviposition curve is compatible with a synovigenic-type parasitoid. Our prediction stating that D. phtorimaeae would succeed when competing for hosts with P. dignus was correct, because the former species had greater parasitism rates. In the field, both T. absoluta parasitoids were able to coexist at leaf scale. The negative aspects of differences in feeding behavior, narrower host range (third instar), and lower fecundity of D. phtorimaeae would be compensated by its better attributes as natural enemy, in comparison with P. dignus, enabling coexistence.

Parasitoid assemblages of soybean defoliator Lepidoptera in north‐western Buenos Aires province, Argentina

1 The objective of this study was to examine the structure of parasitoid assemblages attacking soybean defoliator Lepidoptera in north‐western Buenos Aires province, Argentina.

Laboratory Population Parameters and Field Impact of the Larval Endoparasitoid Pseudapanteles dignus (Hymenoptera: Braconidae) on its Host Tuta absoluta (Lepidoptera: Gelechiidae) in Tomato Crops in Argentina

ABSTRACT The tomato moth, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae), is a key pest of tomato, Lycopersicon esculentum L., crops in Central and South America. At present it is dispersing rapidly in Africa and Eurasian continents as an invasive pest, threatening worldwide tomato production. Pseudapanteles dignus (Muesebeck) (Hymenoptera: Braconidae) is an American endoparasitoid reported as the main natural enemy of T. absoluta in commercial tomato. To gain knowledge of the potential role of P. dignus in the biological control of this pest, we determined its population parameters in laboratory and the parasitoids impact on T. absoluta in the field. In laboratory, lifetime fecundity was 193 eggs per female, and longevity was 24 and 26 d for female and male, respectively. The finite rate of increase (&lgr;) was 1.15 per female per day and the intrinsic rate of natural increase (rm) was 0.14. The net reproductive rate (R0) was found to be 51.2, and generation time (T) 28.8 d. The time for doubling the population (DT) was 5 d. Furthermore, field parasitism of T. absoluta varied between 33 and 64% in the different years studied. Population parameters estimated in this study can be considered baseline information for a mass-rearing protocol of this parasitoid. Moreover, growth rates of P. dignus, particularly rm, and its impact on field populations of T. absoluta indicated that this parasitoid is a valuable candidate for biological control of this pest.

Interspecific interactions between two Tuta absoluta (Lepidoptera: Gelechiidae) larval parasitoids with contrasting life histories.

Interspecific interactions between two larval parasitoids of Tuta absoluta (Meyrick) with partially overlapping host niches were studied: the idiobiont ectoparasitoid Dineulophus phthorimaeae De Santis, and the koinobiont endoparasitoid Pseudapanteles dignus (Muesebeck). T. absoluta is an important pest of tomato crops worldwide, and its management could be improved by understanding the competitive interactions and potential coexistence between these two parasitoids. Firstly, a 15-min fixed time laboratory test evaluated the host-searching ability of adult D. phthorimaeae and P. dignus wasps on T. absoluta larvae. Secondly, D. phthorimaeae host discrimination against endoparasitized and non-endoparasitized hosts by P. dignus, at different adult female ages, was experimentally examined. D. phthorimaeae wasps spent significantly more time in general searching in the presence of its competitor than in its absence, but, parasitism was only effective by P. dignus. Older D. phthorimaeae wasps discriminated significantly less than young wasps between T. absoluta larvae parasitized and unparasitized by P. dignus, and an interaction took place by non-concurrent host-feeding. Intra-guild predation of P. dignus larvae by D. phthorimaeae female feeding behaviour might have a minor effect in this system. Results are discussed in the context of literature supporting diverse evidence of coexistence in other parasitoid-host systems, with implications for T. absoluta biological control.

Performance of Pseudapanteles dignus (Hymenoptera: Braconidae), a Natural Enemy of Tuta absoluta (Lepidoptera: Gelechiidae) in Eggplant

Abstract Pseudapanteles dignus (Muesebeck; Hymenoptera: Braconidae) is an American endoparasitoid that attacks the South American tomato leafminer Tuta absoluta (Meyrick; Lepidoptera: Gelechiidae). The interaction between P. dignus and T. absoluta in tomato (Solanum lycopersicum L.; Solanales: Solanaceae) crops has demonstrated that this enemy exhibits some desirable ecological traits as an effective biological control agent of this pest. With the aim of extending the use of P. dignus to other solanaceous crops, laboratory experiments were carried out to assess some life history traits and the parasitism efficiency when parasitizing T. absoluta larvae fed on eggplant (Solanum melongena L.; Solanales: Solanaceae). Rearings and experiments were conducted at 25 ± 2°C, ≈70% RH, and 14:10 (L:D) h photoperiod, and T. absoluta was fed with eggplant. P. dignus developmental times of immature stages were lower (∼ 5 d) on S. melongena than on S. lycopersicum.The female did not exhibit a pre-reproductive period, and its oviposition period lasted longer (∼ 4 d) than that determined in tomato plants. Adult longevity was ca. 24 d for both sexes. Females produced ca. 61 cocoons during their lives and the maximum daily percentage of parasitism was 50% at the first day of adult emergence. Functional response of P. dignus on eggplant was density-independent of the host density offered, as in tomato plant, and the instantaneous attack rate (a′) was 0.24 attacked larvae/ available larvae, in 24 h. Our results indicate that although there are differences, P. dignus would have a similar performance in eggplant and tomato in terms of its efficacy in the control of T. absoluta.