Potential of biological control agents against Tuta absoluta (Lepidoptera: Gelechiidae): current knowledge in Argentina.
In Argentina, pest management to protect tomato, including tactics against T. absoluta, involves weekly or bi-weekly pesticide treatments (Desneux et al. 2011). Currently, other complementary techniques, like pheromone trapping and applications of Bacillus thuringiensis, are starting to be used by producers as more sustainable forms of pest management (Luna et al. 2012a).
Limited attempts to employ other biological tactics against T. absoluta in Argentina have dealt with the use of imported egg parasitoids (Riquelme Virgala & Botto 2010). However, the results are still preliminary and we still cannot conclude that their commercial implementation in tomato crops is a possibility.
Several natural enemies of T. absoluta have been reported to occur naturally in tomato crops under various cultural practices in Argentina (Desneux et al. 2010; Luna et al. 2012b). Therefore, there is potential value in selecting those native species that are most effective and promising candidates for developing biological control programs.
In this article, we summarize past work and present recent original findings concerning several natural enemies of T. absoluta in tomato crops in Argentina.
PROSPECTS OF BIOLOGICAL CONTROL AGENTS AGAINST TUTA ABSOLUTA
Our initial research on natural enemies of T. absoluta took into account their abundance and seasonal synchronization with the pest as the main criterion for selecting species as biocontrol candidates. Subsequently, our studies included additional species of the T. absoluta enemy complex so as to have a thorough understanding of how they interact.
The parasitoid complex reported for the larval stage of T. absoluta consists of approximately 20 hymenopteran species (Colomo et al. 2002; Luna et al. 2007; Luna et al. 2012b). Yet, the koinobiont endoparasitoid Pseudapanteles dignus (Muesebeck, 1938) (Hymenoptera: Braconidae) and the idiobiont ectoparasitoid Dineulophus phthorimaeae (De Santis, 1983) (Hymenoptera: Eulophidae) accomplish over 50% of natural parasitism and exhibit promising attributes for either augmentative or conservation biological control in the native range of T. absoluta (Colomo et al. 2002; Luna et al. 2007; Sanchez et al. 2009; Savino et al. 2012, 2013). They may also be suitable for introduction in the new regions invaded by T. absoluta (Savino et al. 2012).
Pseudapanteles dignus is a solitary larval endoparasitoid of T. absoluta --and also reported for other gelechiids--commonly present in open field and greenhouse tomato crops, whether organic or sprayed with pesticides (Nieves et al. in press). Previous studies indicated that P. dignus exhibits some life history and ecological traits that could potentially limit T. absoluta populations in this crop (Table 1, Luna et al., 2007, 2010; Sanchez et al. 2009). Pseudapanteles dignus parasitizes all larval instars of its hosts. Population parameters estimated by a life table study under laboratory conditions (25 [+ or -] 2[degrees]C, 65 [+ or -] 5% RH, 14:10 h L: D), yielded a developmental time from egg to adult of 36 days (Nieves 2013; Nieves et al. in press). Female reproductive strategy was moderately synovigenic and time-limited, with a mean egg load of 52 eggs ready to be laid at the emergence of the adult, and a mean fecundity of 192 eggs throughout its adult life (Nieves et al. in press). On average, females laid eggs until the 20th day of adult life, and 50% of the total eggs were laid within the first 6 days (Luna et al. 2007; Nieves et al. in press). Mean parasitism per female (calculated as the total number of parasitized larvae during the female life span divided by the total number of offered larvae) was 47%. Although superparasitism was observed in the laboratory (30%), it rarely occurred in the field (10%) (Nieves 2013). Cohort studies in the laboratory revealed a pre-imago survival rate (egg to pupa) of 38%. Highest mortality occurred at the larval stage, and encapsulation by the host was identified as the main reason (Nieves 2013; Nieves et al. in press). When a single P dignus larva was present in the host, it could suffer up to 28% encapsulation, but superparasitism (~5 immatures per host) could lead up to 91% encapsulation (Nieves 2013).
Life history traits and population parameters of P dignus showed that it had the potential ability to suppress T. absoluta densities (Nieves et al. in press). The intrinsic rate of natural increase ([r.sub.m]) of P dignus was equal to that of T. absoluta ([r.sub.m] = 0.14), reared under the same experimental conditions (Pereyra & Sanchez 2006), and the instantaneous attack rate ([alpha]') of 0.22 (Luna et al. 2007) was larger than the [r.sub.m] of the pest.
In the field, P dignus showed a considerable ability to attack T. absoluta either at low or high densities (Sanchez et al. 2009). Parasitism by P dignus was density-independent, and thus the probability of being parasitized and the risk of parasitism increased with increasing population densities of T. absoluta (Sanchez et al. 2009). In greenhouse tomato, parasitism exhibited a high pest-parasitoid synchrony throughout the crop cycle. By calculating the impact of parasitism on the pest population by means of comparing the areas under the density curves of both populations throughout the season (as in Carey 1993), we showed that P dignus was able to reduce T. absoluta populations by 33-49% in early tomatoes (Sep to Dec) and up to 64% in late tomatoes (Jan to Jun) (Nieves et al. in press).
The mode of parasitism of D. phthorimaeae contrasted with that of P dignus (Table 1). Tuta absoluta and another gelechiid, Phthorimaea operculella (Zeller), were reported as hosts (De Santis 1983). With an ovigeny index equal to 0 (Savino et al. 2012), its female reproductive strategy was extremely synovigenic. Adult females were anautogenous, i.e., they needed to acquire additional nutrients to mature eggs by destructive host feeding. Host feeding by the wasp paralyzed T. absoluta larvae, causing arrest of further development (Luna et al. 2010; Savino et al. 2012). This requirement to host feed on larvae to develop eggs led to T. absoluta mortality by both host-feeding and larval parasitism. The mean lifetime fecundity of D. phthorimaeae was of 4.15 [+ or -] 0.4 eggs per female and showed a type I functional response; hence this species was found to be an egg-limited parasitoid (Luna et al. 2010; Savino et al. 2012) (Table 1). The potential of D. phthorimaeae as natural enemy of T. absoluta was based not only on the quantity of hosts it could parasitize but also on its host feeding behavior; the latter can caused 30% of extra mortality (Savino et al. 2012).
Pseudapanteles dignus and D. phthorimaeae commonly were observed to occur together in tomato crops in Argentina (Luna et al. 2010; Savino 2014). Therefore, we examined the interspecific relationships between both larval parasitoid species, to determine possible multiparasitism, i.e., the use of a single host individual by 2 or more different species of parasitoids. Pseudapanteles dignus and D. phthorimaeae were found to have an overlapping niche, sharing T. absoluta as their host mostly at the third larval instar (Luna et al. 2010; Savino 2014). Under these conditions, it was expected that the idiobiont ectoparasitoid, D. phthorimaeae, should outcompete the koinobiont endoparasitoid, P dignus, by at least 2 mechanisms (Hawkins 1994). Firstly, by killing heterospecific immatures due to host-feeding of already parasitized T. absoluta larvae. Secondly, by paralyzing T. absoluta larvae upon host feeding and by parasitization, thus removing hosts of P dignus, while the opposite it is not true, i.e., T. absoluta larvae parasitized by P. dignus may remain suitable for D. phtorimaeae (Savino 2014).
Host discrimination ability of D. phthorimaeae including its ability to distinguish P dignus parasitized hosts from unparasitized hosts was experimentally examined as follows: Tuta absoluta larvae were offered to individual endoparasitoid females (P dignus) in a cylindrical plastic box (600 mL) arena for 48 h. After that, these previously exposed host larvae were exposed to individual D. phthorimaeae females of 3 ages (1, 5, and 7 days old). Results indicated that young (3-day old) D. phthorimaeae females tended to attack healthy T. absoluta larvae; however, as each female's age progressed (5 days old and older) multiparasitism frequently occured (Savino 2014). The observed coexistence of both parasitoid species in the field could be promoted by the behavior of D. phthorimaeae to partially reject heterospecifically parasitized larvae. The combined effects of the age of the D. phthorimaeae females and the availability of hosts in a patch where both P dignus parasitized and non-parasitized T. absoluta larvae were already present could have played an important role in the dynamics of the interactions between the 2 parasitoid species.
Field surveys carried out in extensive areas of Argentina during 2009 through 2012 (Figure 1 and Table 2) showed a general spatial host density-independent pattern of parasitism for both parasitoid species occurring together on the same plant, regardless the region. Evidence of low-level and host density-independent multiparasitized T. absoluta were also found, indicating a weakly negative interspecific interaction between both parasitoid species (Savino et al. 2013).
Knowledge of host species and host plants that can provide refugia and alternative food resources for the population growth and maintenance of natural enemies is important in the design of biological control strategies for a pest species. Because of the lack of information related to the host ranges of D. phthorimaeae and P dignus, we initiated a survey on horticultural farms in northeastern Buenos Aires province by means of a centrifugal phylogenetic approach (Wapshere 1974). Solanaceous plants commonly cultivated in the region [tobacco Nicotiana tabacum L., eggplant Solanum melongena L., and sweet pepper Capsicum annuum L.], and spontaneous non-cultivated [such as the fierce thorn-apple Datura ferox L., longflower tobacco Nicotiana longiflora Cav., tree tobacco Nicotiana glauca Graham, lily of the valley vine Salpichroa origanifolia (Lam.) Baill., American black nightshade Solanum americanum Mill., and the sticky nightshade Solanum syssimbrifolium Lam.] were examined during 2013-2014, to detect signs of T. absoluta or damage of other gelechiid species. Leafminer hosts and parasitoids collected were identified and numbers of each per plant species were registered. So far, we recorded P dignus parasitizing T. absoluta on eggplant around the year and sporadically on S. americanum, while D. phthorimaeae was detected on T. absoluta only occasionally on eggplant (Salas Gervassio et al. 2014). This information was indicative that host plant species that are alternatives to L. lycopersicum could be playing a role in the maintenance of natural parasitoids of T. absoluta when this crop is absent.
By means of the sentinel egg technique (Moya-Raygoza et al. 2012), we obtained 2 species of egg parasitoids naturally occurring in tomato crops in Argentina: Trichogrammapretiosum (Riley, 1879) (Trichogrammatidae) and Encarsia porteri (Mercet, 1928) (Aphelinidae) (Luft et al. ms submitted). Trichogramma pretiosum had a broader distribution than the aphelinid wasp, which was collected only in Tucuman (northwestern Argentina). Percentages of parasitism were low (< 5%). When these 2 egg parasitoids co-occurred, 50% of the parasitized T. absoluta eggs were attacked by either one of the 2 species, and superparasitism was not observed.
A survey of tomato crops in northwestern Argentina revealed the presence of a native true bug predating a variety of mobile insects. The species was identified as Zelus obscuridorsis (Stal) (Hemiptera: Heteroptera: Reduviidae) (Speranza et al. 2014). Assays were conducted to assess its capability to prey on various developmental stages of T. absoluta. We found that Z. obscuridorsis preyed on the mobile stages, i.e., free larvae and adults, but did not eat larvae in their mines, pupae or eggs.
Discussion and Future Prospects
Any biological control program should select the best strategy for the use of natural enemies, and this includes a thorough knowledge of suitable biocontrol agents that naturally occur in a given region. Among the natural enemy complex of T. absoluta under study, the biological and ecological characteristics of P. dignus presented here and elsewhere (Luna et al. 2012b) meet various criteria as a potentially good biocontrol agent likely to induce sufficient pest suppression when applied in seasonal augmentative releases in commercial crops. For this reason, we have chosen P dignus to conduct experimental releases in tomato greenhouses, a technique to be used alone or in combination in IPM programs. Like many other Braconidae species, P dignus is quite easy to rear and manipulate under laboratory conditions. Results achieved in our studies allow improved P dignus methods for mass rearing, by reducing the frequency of encapsulation and increasing the survival of the offspring. In addition to developing additional knowledge of P dignus rearing, it would be essential to develop quality control guidelines for mass production.
In relation to the other natural control agents of the tomato moth in Argentina, we have continued to study the impact of their trophic interactions (parasitism, predation, competition, intra-guild predation, etc.) in pest suppression. Although less studied to date, these natural enemies could be important in taking advantage of little exploited host niches, i.e., eggs, mobile larvae, etc., by other species antagonistic to T. absoluta.
A thorough research program towards developing an IPM program for a given species should take into account all relevant natural enemies, as well as consider other co-occurring complexes of pests and beneficial species, under an agro-ecosystem approach. Such an approach would not only allow for the development of the best IPM strategy, but also result in a better understanding of the pest's trophic relationships in a given region.
We are grateful for the comments and suggestions made by 2 anonymous reviewers and the Associate Editor that greatly improved the manuscript. We also thank the Ministerio de Ciencia, Tecnologia e Innovacion Productiva (PICT 2012-1624), the Consejo Nacional de Investigaciones Cienti'ficas y Tecnicas (PIP 00112-2012), and the Universidad Nacional de La Plata (PI N 706 2013).
Carey JR. 1993. Applied demography for biologists with special emphasis on insects. New York: Oxford University Press, 206 pp.
Colomo MV, Berta DC, Chocobar MJ. 2002. El complejo de himenopteros parasitoides que atacan a la "polilla del tomate" Tuta absoluta (Lepidoptera: Gelechiidae) en la Argentina. Acta Zoologica Lilloana 46: 81-92.
De Santis L. 1983. Un nuevo genero y dos nuevas especies de Eulofidos Neotropicales (Insecta: Hymenoptera). Revista Peruana de Entomologia 26 (1): 1-4.
Desneux N, Wajnberg E, Wyckhuys K, Burgio G, Arpaia S, Narvaez-Vasquez C, Gonzalez-Cabrera J, Catalan-Ruescas D, Tabone E, Frandon J, Pizzol J, Poncet C, Cabello T, Urbaneja A. 2010. Biological invasion of European tomato crops by Tuta absoluta: ecology, geographic expansion and prospects for biological control. Journal of Pest Science 83: 197-215.
Desneux N, Luna MG, Guillemaud T, Urbaneja A. 2011. The invasive South American tomato pinworm, Tuta absoluta, continues to spread in AfroEurasia and beyond: The new threat to tomato world production. Journal of Pest Science 84: 403-408.
EPPO (European Plant Protection Organization). 2005. EPPO datasheets on quarantine pests: Tuta absoluta. EPPO Bulletin 35: 434-435.
Hawkins BA. 1994. Patterns and Processes In Host-Parasitoid Interactions. Cambridge Cambridge: Cambridge University Press, 190 p.
Luft E, Luna M, Galise G, Speranza S, Virla E. Natural mortality of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) eggs in Argentina and Italy. Submitted to Revista de la Facultad de Ciencias Agrarias de la Universidad Nacional de Cuyo. Mendoza. Argentina. In revision January 2015.
Luna MG, Sanchez NE, Pereyra PC. 2007. Parasitism of Tuta absoluta (Lepidoptera: Gelechiidae) by Pseudapanteles dignus (Hymenoptera: Braconidae) under laboratory conditions. Environmental Entomology 36: 887893.
Luna MG, Pereyra PC, Sanchez NE. 2012a. Biological control of Tuta absoluta (Lepidoptera: Gelechiidae) in protected tomato crops in Argentina. IOBC-WPRS Bulletin 80: 177-182.
Luna MG, Sanchez NE, Pereyra PC, Nieves EL, Savino V, Luft E, Virla E, Speranza S. 2012b. Biological control of Tuta absoluta in Argentina and Italy. Evaluation of indigenous insects as natural enemies. Bulletin OEPP/EPPO 42: 260-267.
Luna MG, Wada VI, Sanchez NE. 2010. Biology of Dineulophus phtorimaeae (Hymenoptera: Eulophidae) and field interaction with Pseudapanteles dignus (Hymenoptera: Braconidae), larval parasitoids of Tuta absoluta (Lepidoptera: Gelechiidae) in tomato. Annals of the Entomological Society of America 103: 936-942.
Moya-Raygoza G, Virla E, Luft E. 2012. Diversity of egg parasitoids attacking Dalbulus maidis (Hemiptera: Cicadellidae) populations at low and high elevation sites in Mexico and Argentina. Florida Entomologist 95: 105-112.
Nieves EL. 2013. Evaluacion del parasitoide, Pseudapanteles dignus (Hymenoptera: Braconidae) como agente de control biologico de la "polilla del tomate", Tuta absoluta (Lepidoptera, Gelechiidae). PhD thesis, Universidad Nacional de La Plata (UNLP), Argentina. 129 pp.
Nieves EL, Pereyra PC, Luna MG, Medone P, Sanchez NE. 2015. 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. Journal of Economic Entomology (in press).
Pereyra PC, Sanchez NE 2006. Effect of two solanaceous plants on developmental and population parameters of the tomato leaf miner, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Neotropical Entomology 35: 671-676.
Riquelme Virgala, MB, Botto EN. 2010. Biological studies on Trichogrammatoidea bactrae Nagaraja (Hymenoptera: Trichogrammatidae), egg parasitoid of Tuta absoluta Meyrick (Lepidoptera: Gelechiidae). Neotropical Entomology 39: 612-617.
Salas Gervassio, NG, Luna MG, Lee S, Salvo A, Sanchez NE. 2014. Parasitoid complex associated to Tuta absoluta (Lepidoptera: Gelechiidae) and other leafminers in cultivated and non-cultivated Solanaceae, in Argentina. 62nd Annual Meeting of ESA, Portland, OR, USA. Abstract.
Sanchez NE, Pereyra PC, Luna MG. 2009. Spatial patterns of parasitism of the solitary parasitoid Pseudapanteles dignus (Hymenoptera: Braconidae) on Tuta absoluta (Lepidoptera: Gelechiidae). Environmental Entomology 38: 365-374.
Savino V. 2014. Biologia reproductiva del ectoparasitoide Dineulophus phthorimaeae de Santis y su interaccion con el endoparasitoide Pseudapanteles dignus (Muesebeck). Implicancias para el control biologico de la polilla del tomate Tuta absoluta (Meyrick). PhD thesis, Universidad Nacional de La Plata (UNLP), Argentina. 146 pp.
Savino V, Luna MG, Coviella CE. 2013. Interspecific competence between the ectoparasitoid Dineulophus phtorimaeae de Santis (Hymenoptera: Eulophidae) and the endoparasitoid Pseudapanteles dignus (Muesebeck) (Hymenoptera: Braconidae), attacking Tuta absoluta larvae in the laboratory. 61st Annual Meeting of the Entomological Society of America, Austin, TX, USA. Abstract.
Savino V, Coviella CE, Luna MG. 2012. Reproductive biology and functional response of Dineulophus phtorimaeae a natural enemy of the tomato moth, Tuta absoluta. Journal of Insect Science 12: 1-14.
Speranza S, Melo M, Luna M, Virla E. 2014. First record of Zelus obscuridorsis (Hemiptera: Reduviidae) as a predator of the South American tomato leafminer, Tuta absoluta (Lepidoptera: Gelechiidae). Florida Entomologist 97: 295-297.
USDA-APHIS, 2011. New Pest Response Guidelines: Tomato Leafminer (Tuta absoluta). USDA-APHIS-PPQ-EDP-Emergency Management, Riverdale, Maryland, USA (http://www.aphis.usda.gov/import_export/plants/manuals/emergency/downloads/Tuta-absoluta.pdf. Accesed 5-I-2015).
Wapshere AJ. 1974. A strategy for evaluating the safety of organisms for biological weed control. Annals of Applied Biology 77: 201-211.
Zlof V, Suffert M. 2012. Report of the EPPO/FAO/IOBC/NEPPO Joint International Symposium on Management of Tuta absoluta (tomato borer). Bulletin OEPP/EPPO 42: 203-204.
Maria G. Luna (1) *, Patricia C. Pereyra (1), Carlos E. Coviella (2), Eliana Nieves (1), Vivina Savino (2), Nadia G. Salas Gervassio (1), Erica Luft (3,4), Eduardo Virla (3,4), and Norma E. Sanchez (1)
(1) Centro de Estudios Parasitologicos y de Vectores (CEPAVE), La Plata, Argentina
(2) Departamento de Ciencias Basicas e INEDES. Programa de Investigaciones en Ecologia Terrestre (UNLu). Lujan, Argentina
(3) PROIMI (CONICET), San Miguel de Tucuman, Argentina
(4) Instituto de Entomologia (FML), Tucuman, Argentina
* Corresponding author; E-mail: email@example.com
Caption: Fig. 1. Relationships among the proportions of Tuta absoluta per tomato plant parasitized by Pseudapanteles dingus, or by Dineulophus phtorimaeae phthorimaeae or by both species (multiparasitism) at various densities of T. absoluta in 2 regions of Argentina, i.e., (a) La Plata, northern Buenos Aires province and (b) Tucuman. Relevant logistic regression parameters are shown in Table 2.
Table 1. Life history traits comparison between Pseudapanteles dignus and Dineulophus phthorimaeae, parasitoids of Tuta absoluta (summarized from Luna et al. 2007, 2010, 2012a; Sanchez et al. 2009, Nieves 2013, Nieves et al. in press, Savino et al. 2012, Savino 2014). Life history strategy Pseudapanteles dignus Dineulophus phtorimaeae Endoparasitoid, Ectoparasitoid, koinobiont idiobiont Mean life-time 192.36 ([+ or -] 4.15 ([+ or -] 0.4 fecundity 17.17) eggs per female eggs) per female Sex ratio (females 1: 1.25 1:1 per offspring) Mean ([+ or -] SE) 22.69 [+ or -] 0.22 11.17 [+ or -] 0.60 developmental time (from egg to adult emergence) (days) Life cycle (days) [approximately [approximately equal to] 36 equal to] 23 Host larval instar From 1st to 4th Only 3rd attacked Host-feeding No Yes Aggregative response Yes Yes to host density Foraging behavior Time limited Egg limited Mass rearing Straight forward Not available yet Table 2. Parameters of the logistic regression between the proportion of Tuta absoluta larvae per plant parasitized by Dineulophus phthorimaeae, Pseudapanteles dignus or multiparasitized by both parasitoids against T. absoluta density in Argentina. Years Tucuman (26[degrees]54' 34" S, 65[degrees]20' 37" W) * Dineulophus phthorimaeae 2009, 2011, B0 [beta] P [chi N 2012 square] -1.35 0.0006 NS 0.0035 58 La Plata (34[degrees] 56' 08" S, 58[degrees]06' 03" W) ([dagger]) D. phthorimaeae 2010, 2011, B0 [beta] P [chi N 2012 square] -1.33 0.02 NS 0.54 50 Years Tucuman (26[degrees] 54' 34" S, 65[degrees] 20' 37" W) * Pseudapanteles dignus 2009, 2011, B0 [beta] P [chi N 2012 square] -0.9 -0.009 NS 0.08 58 La Plata (34[degrees] 56' 08" S, 58[degrees]06' 03" W) ([dagger]) P. dignus 2010, 2011, B0 [beta] P [chi N 2012 square] -0.99 0.02 NS 0.27 50 Years Tucuman (26[degrees] 54' 34" S, 65[degrees] 20' 37" W) * Multiparasitized 2009, 2011, B0 [beta] P [chi N 2012 square] -3.55 0.03 NS 0.33 58 La Plata (34[degrees] 56' 08" S, 58[degrees]06' 03" W) ([dagger]) Multiparasitized 2010, 2011, B0 [beta] P [chi N 2012 square] -3.8 0.04 NS 0.31 50 B0: coefficient for the intercept, regression parameter. Linear coefficients ([beta]) not significantly different from zero indicate that the proportions of parasitized hosts were independent of host densities. * sampling size: 7 sites, 20 plants per site. ([dagger]) sampling size: 5 sites, 20 plants per site. N = number of valid cases for logistic regression (logit) model NS: not significant at P [less than or equal to] 0.05
Please note: Some tables or figures were omitted from this article.
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|Author:||Luna, Maria G.; Pereyra, Patricia C.; Coviella, Carlos E.; Nieves, Eliana; Savino, Vivina; Gervassio|
|Date:||Jun 1, 2015|
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