Abstract
Macrolophus pygmaeus (Rambur, 1839) (Hemiptera: Miridae) is a polyphagous predator used in programs of biological control and integrated pest management as a natural enemy against small arthropod pests including whiteflies, thrips, spider mites and aphid. This mirid is also successfully mass reared under factitious prey for commercial purposes. In the present study we assessed and compared the prey consumption, weight gain and conversion efficiency in females of two populations of M. pygmaeus, from mainland Portugal and the Azores, fed on single prey diets of Ephestia kuehniella Zeller (Lepidoptera: Pyralidae) eggs, or Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) eggs. We found that female’s prey consumption on eggs of T. absoluta was higher than that of E. kuehniella, presumably due to the comparative size/amount of biomass of the eggs. Translating prey consumption in biomass ingested, we only found a significant difference for consumption on E. kuehniella eggs by M. pygmaeus from the Azores. Despite the smaller size of females from the Azores, they were able to consume more prey and ultimately reaching a similar body weight and conversion efficiency compared with females from mainland, independently of the prey provided. Our results are in line with a previous study, showing differences in the life-history traits of M. pygmaeus from mainland Portugal and Azorean populations fed on alternative prey. From an applied perspective, our results are a contribution to the decision-making on the use of the most effective biocontrol agents for different prey and/or agroecosystem contexts.
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Introduction
The South American leaf miner, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) was firstly reported outside its native range in Eastern Spain in 2006 and, in 2007, dispersed to Africa via Algeria, Morocco and Tunisia (Desneux et al., 2011, 2022). Now, it is widely distributed in more than 100 countries (EPPO, 2023). It was firstly referred to the Azores, in 2012 (Vieira, 2016), but no information is available on the origin and date of colonization. Most likely, the Azorean populations have originated from mainland Portugal. The primary host of this pest seems to be Solanum lycopersicum L., although it can feed and develop on other plants within Solanaceae and Convolvulaceae, such as the bittersweet nightshade (Solanum dulcamara L.), black nightshade (Solanum nigrum L.), cape gooseberry (Physalis peruviana L.), common thorn (Datura stramonium L.), eggplant (Solanum melongena L.), pepper (Capsicum annuum L.), potato (Solanum tuberosum L.), sweet potato (Ipomea batatas (L.) Lam.), tobacco (Nicotiana tabacum L.) and wild tomato (Lycopersicon hirsutum Dunal) (Vieira, 2016). Tuta absoluta is a key pest of tomato crops, causing devastating economic impacts to growers (Biondi et al., 2018), sometimes reaching 100% of economic losses (Rostami et al., 2020). Foliage damage is the primary cause of economic losses, especially when populations are abundant. The larvae feed on leaf tissues producing mines that can destroy the leaves when infestations are high. The reduction of leaf tissues induces dispersion to the fruits. The larvae penetrate fruits, often below the calyx, facilitating fruit infection by pathogens (Chermiti et al., 2009; Balzan & Moonen, 2012; Guedes & Picanço, 2012). Just after its detection in the Azores, the management of T. absoluta populations was mainly based on chemical control (Oliveira et al., 2023). Over the last 5 years, additional biotechnical control strategies have been used into horticultural farms, namely water traps with pheromones and yellow sticky traps (Information provided by the Agricultural Services of the Azores). The legal regime for the conservation of nature and biodiversity at the Azores according to the Regional Legislative Decree (DLR no. 15/2012/A, of April 2) limits the introduction of exotic natural enemies and recommends the use of native biological agents.
The zoophytophagous mirid Macrolophus pygmaeus (Rambur) (Hemiptera: Miridae) is recognized as one of the most promising biological control agents against T. absoluta (Arnó et al., 2021). This mirid bug has been successfully mass reared for commercial purposes (van Lenteren, 2012) and used in the biological control of different arthropod pests, such as, aphids, thrips, whiteflies, and spider mites (Fauvel et al., 1987; Alvarado et al., 1997; Barnadas et al., 1998; Riudavets & Castañé, 1998; Margaritopoulos et al., 2003; Perdikis et al., 2008; Arnó et al., 2009; Calvo et al., 2009; Urbaneja et al., 2009; Castañé et al., 2011; Urbaneja et al., 2012). Although Dicyphini mirids are zoophytophagous, the level of damage they can cause to host plants is variable, depending on the species. Macrolophus pygmaeus has been seen as a candidate to replace Nesidiocoris tenuis (Reuter), in biological control in tomato crops, because the damage inflicted on plants is much less (Arnó et al., 2010; Castañé et al., 2011). In addition, plant feeding allows mirids being present in the field, when prey is scarce, which is advantageous for biological control (Abraços-Duarte et al., 2021; Pérez-Hedo et al., 2021; Coppel & Mertins, 1977).
Augmentative biological control is a widely used strategy to obtain an immediate control of pests in crops with a short production cycle or for control of pests during several generations in crops with a long production cycle. This strategy involves large-scale regular releases of mass-produced natural enemies, being a sound alternative to control pest populations in a wide range of crop systems (van Lenteren et al., 2018). Despite being one of the most destructive cosmopolitan pests of stored grains, particularly flour, Ephestia kuehniella Zeller (Lepidoptera: Pyralidae) eggs are a suitable substitute prey for mass rearing of a wide range of predator and parasitoid species to be used in augmentative biological control (Mamay et al., 2022). However, due to different nutritional quality in relation to natural prey, their use can alter traits of natural enemies, thus limiting mass production under controlled conditions (Awmack & Leather, 2002). Biological and ecological traits of pests and their natural enemies should be studied in order to predict how successful a biocontrol agent will be during augmentative biological control (Coppel & Mertins, 1977). Pest population suppression is largely determined by the relationship between the ability of the biocontrol agent to consume prey and pest population growth (Coppel & Mertins, 1977). Females are, in general, the most voracious developmental stage and, depending on the availability of prey, biomass consumption may translate in a positive reproductive numerical response. That is, changes in the number of predators on prey colonies may result from two different mechanisms: attraction of predators to prey aggregations (aggregational response) and increased rate of predator reproduction when prey is abundant (reproductive numerical response). Predation or parasitism rate must be higher than the growth rate of prey/host (Coppel & Mertins, 1977). In insect pests with fast population growth, such as aphids, it is essential that biocontrol agents have a high prey consumption (Borges et al., 2011, 2013). However, prey may differ in their suitability driving alterations on predator’s survival and development rate. The consumption of different prey species can have consequences for the predator’s reproductive numerical responses changing, by this way, the success of biological control. Predator egg production also requires nutritional intake beyond a maintenance level, and thus high-quality food sources are mandatory for supporting predator reproduction (Seagraves, 2009; Sebastião et al., 2015; Hodek, 1962; Hodek & Honek, 1996; Hodek & Evans, 2012).
Recently, Borges et al. (2023) provided experimental evidence that T. absoluta eggs are an essential prey for M. pygmaeus. That is, when fed only with T. absoluta eggs, nymphs of M. pygmaeus can complete development and the originated adults are able to reproduce. From an applied point of view, the assessment of the number of eaten (killed) eggs of T. absoluta is an important predictor of a predator’s potential as a biological control agent. Prey consumed by insects can vary greatly in quality. Prey quality affects growth, development and reproduction. The percentage of consumed prey biomass converted into predator biomass (the so-called efficiency of conversion of ingested material or relative growth rate) is a useful proxy to test food quality (Waldbauer, 1968). Expressing prey consumption as the amount of biomass intake, allows i) to compare similar biological traits among different prey, given that species do not have the same body weight and ii) to estimate some physiological parameters, as the conversion efficiency. Following biomass consumption, weight increases and conversion efficiency are good predictors of energy intake and associated costs (Odum, 1956; Waldbauer, 1968). According to the universal model of energy flow (Odum, 1956), conversion efficiency corresponds to the proportion of biomass consumed allocated to growth.
In the present study, we assessed the prey consumption, the weight gain and conversion efficiency of M. pygmaeus females when fed on T. absoluta eggs. We compared two field collected populations of M. pygmaeus, i.e., one from mainland Portugal and one from the Azores archipelago. The aim of our study was to understand the predatory activity of M. pygmaeus, including that of the native population of the Azores, assessing to what extent it will be possible to mass-rear under laboratory conditions, using as factitious prey, T. absoluta eggs, as well as investigating if prey consumption may vary among populations of different geographical origin.
Materials and methods
Biological materials
Specimens of M. pygmaeus were obtained from two field populations of different geographical origin: 1) Mainland Portugal population, specimens originated from the Oeste region of Portugal (Azueira, Mafra: 39°00′43.8″ N 9°16′49.1″ W; Silveira, Torres Vedras: 39°07′02.5″ N 9°21′54.1″ W; Tapada da Ajuda, Lisbon: 38°42′45.8″ N 9°11′02.8″ W), collected both in greenhouse and open field crops, and maintained in laboratory conditions during several generations; 2) Azorean population, based on specimens collected in S. Miguel Island, on S. lycopersicum plants, in five different locations (Pico da Pedra: 37°47′48.1″ N 25°35′51.7″ W; Lagoa: 37°45′4.3″ N 25°34′27.2″ W; Ribeira Grande: 37°48′49.59″ N 25°31′41.10″ W; two locations on Arrifes: 37°45′1.54″ N 25°41′28.70″ W; 37°45′1.54″ N 25°41′28.70″ W). Laboratory populations were maintained, separately, in rearing net cages (40 × 40 × 40 cm). The experiments with M. pygmaeus collected in the Azores were performed shortly after its collection in the field, not remaining for more than 2 to 3 generations under laboratory conditions. For mainland populations maintained in laboratory conditions during several generations, monthly refreshments were made.
One potted tomato plant, as well as E. kuehniella eggs, provided as a source of protein, were offered twice a week to the mirids within the cages. The eggs of, E. kuehniella was used as a reference diet. Ephestia kuehniella is an important pest of stored products (Cox & Bell, 1991; Hill, 2006) and its eggs have been commonly used to mass-rear different biocontrol agents (Hamasaki & Matsui, 2006; Vandekerkhove & De Clercq, 2010; Moghaddassi et al., 2019; Gallego et al., 2022). Additionally, the mirids were fed on honey droplets (50% in water) placed over the leaflets. Tomato plant was substituted by a fresh one, every two days. The mirids were reared at 25 ± 1 °C, 75 ± 5% relative humidity and 16 L:8D light regime.
Ephestia kuehniella eggs were provided by CBA (Centre of Biotechnology of the Azores), where the lepidopteran is mass reared. Tuta absoluta was collected in a greenhouse in S. Miguel Island and used to start a small-scale mass rearing program in the laboratory, as described in Borges et al. (2023).
Prey consumption
Several rearing cages were made to obtain enough nymphs of the mirid populations for the experiments. Approximately, 50 M. pygmaeus adults from the stock population were placed in a rearing cage, and E. kuehniella eggs and honey diluted in water were provided over a tomato leaf placed in a water container. These procedures were the same for both mirid populations. After 10-days exposure, all adult mirids were removed and each cage was kept for nymphal development. Twice a week, fresh E. kuehniella eggs were provided, as well as honey diluted in water. Recently emerged adults were picked up every two days and transferred to a separate rearing cage, until reaching 9 to 12 days old. At that time, females were collected to be used in the prey consumption tests. The sex of adult specimens was identified based upon the abdomen shape: rounded, thick, and symmetric, ventrally with a central groove for females; and thin, asymmetric, without groove and tapered near the end for males.
Twenty-four hours prior to testing, females were fed only with a tomato plant and a droplet of honey diluted in water. For the prey consumption test, 50 eggs of E. kuehniella or 80 eggs of T. absoluta were offered over a tomato leaflet to a single predator female in an acrylic box (3 cm diameter × 2 cm height), for 24 hours. The weight of the eggs of E. kuehniella, T. absoluta and females of M. pygmaeus were recorded before and after the 24 hour-test, using Sartorius ultra-microbalance. Female prey consumption was expressed in terms of the number of prey eggs and the amount of biomass ingested. Weight gain by females of M. pygmaeus expresses the difference of the body weight assessed before and after the 24 hour-test and the percentage of biomass ingested was calculated by balancing the difference in the weight loss of the eggs, relative to the initial weight. Biomass ingested (BI), relative growth rate (RGR), and conversion efficiency (CE) by females were calculated according to the formulas (Soares et al., 2004):
where, EWi and EWf are the initial and final weight of the eggs, and PWi and PWf are the initial and final weights of the predator. The experiment was conducted with 10 replicates.
Statistical analysis
For statistical analysis, the following independent variables were considered: i) prey species (T. absoluta or E. kuehniella eggs); and ii) origin of population (Azores or Portugal mainland). Generalized Linear Models (GZLM) were used to test statistical significance of the biological parameters for prey, regions and interactions between independent factors. Data were firstly examined for normal distribution, using the Kolmogorov-Smirnov test. When the previous condition of normality was not verified, the data were log-transformed. If normal distribution was confirmed, GZLM analyses considered the normal error distribution and the identity link function. If not, Poisson error distribution and the Log link function were applied. Pairwise multi-comparisons were carried out and P values corrected using Bonferroni test.
Mean values were considered significantly different when P < 0.05. SPSS v. 27 was used to perform the statistical analyses (IBM Corp 2020).
Results
Initial weight of the eggs
No significant interaction was found between prey species (T. absoluta or E. kuehniella eggs) and the population origin of M. pygmaeus (Azores or Portugal mainland) in relation to the initial weight of the eggs provided to M. pygmaeus females (Chi-Square = 2.926, df = 1, P = 0.087; Table 1). The eggs of E. kuehniella (1.32 ± 0.01 mg) were significantly heavier than those of T. absoluta (0.83 ± 0.01 mg) (Chi-Square = 1516.76, df = 1, P ≤ 0.0001) and the eggs provided to M. pygmaeus females of mainland population was significantly heavier (1.10 ± 0.01 mg) than those provided to Azorean females (1.05 ± 0.01 mg) (Chi-Square = 14.89, df = 1, P = 0.001).
Final weight of the eggs
A significant interaction was found between prey species (T. absoluta or E. kuehniella eggs) and the population origin of M. pygmaeus (Azores or Portugal mainland) in relation to the final weight of the eggs (mg) provided to M. pygmaeus females (Chi-Square = 11.84, df = 1, P = 0.001; Table 1). We only found a significant difference for the final weight of E. kuehniella after being consumed by M. pygmaeus females from mainland Portugal, that is, the final weight of the eggs was significant higher (Table 1).
Prey consumption
No significant interaction was found between prey species (T. absoluta or E. kuehniella eggs) and population origin of M. pygmaeus (Azores or Portugal mainland) with respect to the prey consumption of M. pygmaeus females (Chi-Square = 3.456, df = 1, P = 0.063). The females of M. pygmaeus consumed a significantly higher number of eggs of T. absoluta (40.70 ± 4.56) in comparison to E. kuehniella (26.00 ± 3.56) (Chi-Square = 9.018, df = 1, P = 0.003). Females of M. pygmaeus from the Azores population were significantly more voracious (42.70 ± 3.53 eggs consumed) compared to M. pygmaeus from mainland Portugal (24.00 ± 4.48 eggs consumed) (Chi-Square = 14.593, df = 1, P < 0.001) (Table 1).
Amount of biomass ingested
We found a significant interaction between prey species (T. absoluta or E. kuehniella eggs) and population origin of M. pygmaeus (Azores or mainland Portugal) (Chi-Square = 13.74, df = 1, P = 0.001). A significant difference between populations of M. pygmaeus on the amount of ingested mass was observed in the case of E. kuehniella eggs only, with a higher performance shown by M. pygmaeus females from the Azores (Table 1).
Percentage of biomass ingested
A significant interaction was found between the prey species (T. absoluta or E. kuehniella eggs) and the population origin of M. pygmaeus (Azores or Portugal mainland) (Chi-Square = 5.374, df = 1, P = 0.02; Table 1). The M. pygmaeus females from the Azores ingested a higher rate of biomass from eggs of E. kuehniella in comparison to those from mainland.
Initial body weight of M. pygmaeus females
No significant interaction was found between prey species (T. absoluta or E. kuehniella eggs) and the population origin of M. pygmaeus (Azores or mainland Portugal) on the initial body weight of M. pygmaeus females (Chi-Square = 3.219, df = 1, P = 0.073; Table 2). Initial body weight of M. pygmaeus females fed with T. absoluta eggs (1.16 ± 0.04 mg) did not significantly differ from that of females fed with E. kuehniella eggs (1.16 ± 0.03 mg) (Chi-Square = 0.008, df = 1, P = 0.928). Initial body weight of M. pygmaeus females from the mainland (1.24 ± 0.03 mg) was significantly higher that of the females from Azores (1.09 ± 0.03) (Chi-Square = 18.153, df = 1, P < 0.001).
Final body weight of M. pygmaeus females
No significant interaction was found between prey species (T. absoluta or E. kuehniella eggs) and population origin of M. pygmaeus (Azores or Portugal mainland) on the final body weight of M. pygmaeus females (Chi-Square = 3.721, df = 1, P = 0.0543; Table 2). Final body weight of M. pygmaeus females fed with T. absoluta eggs (1.26 ± 0.04 mg) did not significantly differ from that of females provided with E. kuehniella eggs (1.33 ± 0.04 mg) (Chi-Square = 2.173, df = 1, P = 0.140). Final body weight of females of M. pygmaeus from the mainland (1.32 ± 0.03 mg) did not differ from that of the females of the Azores (1.27 ± 0.04 mg) (Chi-Square = 0.998, df = 1, P = 0.318) (Table 2).
Weight gain
No significant interaction was found between prey species (T. absoluta or E. kuehniella eggs) and the population origin of M. pygmaeus (Azores or Portugal mainland) on the weight gain of M. pygmaeus females (Chi-Square = 0.567, df = 1, P = 0.451; Table 2). Weight gain M. pygmaeus females fed with E. kuehniella eggs (0.17 ± 0.03 mg) was significantly higher than that of females fed with T. absoluta eggs (0.09 ± 0.04 mg) (Chi-Square = 3.894, df = 1, P = 0.048). Weight gain of Azorean M. pygmaeus females (0.18 ± 0.03 mg) was significantly higher than that of females from mainland (0.08 ± 0.03 mg) (Chi-Square = 78.293, df = 1, P = 0.007).
Relative growth rate
No significant interaction was found between prey species (T. absoluta or E. kuehniella eggs) and the population origin of M. pygmaeus (Azores or Portugal mainland) on the relative growth rate of M. pygmaeus females (Chi-Square = 0.497, df = 1, P = 0.481; Table 2). Relative growth of M. pygmaeus females fed with E. kuehniella eggs (14.90 ± 2.98%) was significantly higher than that of females fed with T. absoluta eggs (0.09 ± 0.04%) (Chi-Square = 8.593, df = 1, P = 0.003). Relative growth rate of Azorean M. pygmaeus females (16.80 ± 3.00 mg) did not significantly differ of females from mainland (6.64 ± 2.04%) (Chi-Square = 3.374, df = 1, P = 0.066).
Conversion efficiency
No significant interaction was found between prey species (T. absoluta or E. kuehniella eggs) and population origin of M. pygmaeus (Azores or Portugal mainland) on the conversion efficiency of M. pygmaeus females (Chi-Square = 2.513, df = 1, P = 0.113; Table 2). Conversion efficiency of M. pygmaeus females fed with E. kuehniella eggs (0.25 ± 0.06) did not significantly differ from that of females fed with T. absoluta eggs (0.17 ± 0.07) (Chi-Square = 0.990, df = 1, P = 0.320). No significant differences were observed between M. pygmaeus females from the Azores (0.28 ± 0.04) and those from mainland (0.14 ± 0.08) (Chi-Square = 2. 923, df = 1, P = 0.087) for the same variable.
Discussion
We assessed and compared the number of eggs of E. kuehniella or T. absoluta consumed by females of M. pygmaeus from populations of two different geographical origins. We found that the number of eggs of T. absoluta consumed by M. pygmaeus females was higher than that of E. kuehniella. This maybe related with the relative amount of biomass of the two prey-species eggs. The eggs of T. absoluta are very small, even compared with other Lepidopteran species (0.36 mm long and 0.22 mm in diameter (EPPO, 2005)). In our study, the weight of E. kuehniella eggs was 1.59 times higher than that of T. absoluta eggs (1.32 vs 0.83, respectively). Using the same comparative relationship, the prey consumption of M. pygmaeus females on T. absoluta eggs was 1.56 higher than on E. kuehniella eggs.
We also found that the eggs provided to M. pygmaeus females of mainland population was significantly heavier (1.10 ± 0.01 mg) than those provided to Azorean females (1.05 ± 0.01 mg). Despite that statistical difference, this represents a residual difference of 4% in egg.
The number of T. absoluta eggs consumed in 24 h by M. pygmaeus females (40.70 ± 4.56) is within the range of values reported by previous studies. Urbaneja et al. (2009), reported that when females were provided with 60 eggs of T. absoluta, they were able to consume in 24 h all the eggs. Chailleux et al. (2013), for an experimental period of 12 h, recorded a mean value of about 10 eggs of T. absoluta. In a more recent study, the daily prey consumption of M. pygmaeus females was 60.7 ± 5.3 eggs of T. absoluta (author’s personal observations).
Our results suggest a higher performance of the females from the Azorean population of M. pygmaeus in comparison to those of mainland population. In fact, we found that M. pygmaeus females from the Azores consumed about 78% more eggs of both preys than those from mainland (42.7 vs 24.0 eggs). In respect to the biomass ingested, the Azorean females also showed a higher performance, with about 54% to 68% of the prey egg biomass ingested, in comparison with 25% to 41%, in the case of mainland females. Nevertheless, no differences were observed between the two populations in relation to the relative growth rate and conversion efficiency.
These results are in line with Borges et al. (2023), which was aimed at contrasting life-history variables of two field populations of M. pygmaeus (Azores vs Portugal mainland) under two alternative prey (T. absoluta vs E. kuehniella eggs). Data revealed that variables with direct impact on fitness, such as lifetime fertility, give a better performance to the Azorean population of the predator. Azorean M. pygmaeus females were bigger in size, matured earlier and had a higher reproduction rate for longer periods than those of the mainland population. Genetic structure differs between field populations of M. pygmaeus, as well as between naturally occurring or mass-reared ones (Sanchez et al., 2012; Streito et al., 2017). Evolutionary context may have caused variation in the genetic structure in several populations of Mediterranean region. For example, during glaciations, populations geographically isolated by ice fields or permafrost that covered northern and center of Europe (Hewitt, 2000) might have evolved independently and become genetically differentiated (Sanchez et al., 2012). In the previous study (Borges et al., 2023) we found that the origin can affect the initial body weight of mirid. However, in the present study, we found no differences in the initial body weight between the two studied populations of M. pygmaeus, reared with the same diet, i.e., E. kuehniella.
In the present study, we also assessed the effect of population origin (Azores vs mainland Portugal) and prey diets (T. absoluta vs E. kuehniella eggs) on the weight gain and conversion efficiency of M. pygmaeus females. We found that the weight gain of M. pygmaeus females was similar in both tested diets, i.e., T. absoluta eggs and E. kuehniella eggs, but differed between the two studied populations of M. pygmaeus, with the Azorean females showing higher values than mainland females. Analyzing some results obtained in this study, it comes evident that, in general, females from the Azores were able to consume more prey (Azores: 42.70 ± 3.53 eggs consumed vs mainland: 24.00 ± 4.48 eggs consumed) and ultimately reaching a similar body weight comparing with females from mainland (mainland: 1.32 ± 0.03 mg vs Azores: 1.27 ± 0.04 mg), independently of the prey provided. Considering the general model of biomass/energy flow (Odum, 1956), we estimated that about 3.9% to 20.5% of egg-prey biomass ingested is converted to body biomass by M. pygmaeus females, corresponding to a relative growth rate between 3 to 31%, depending on prey species and population origin of the predator. Our results provide new information on how M. pygmaeus may perform under different prey resources and what are the physiological consequences in terms of each of the resource used for growth and basal metabolism maintenance. As far as we know, our study is the first aiming to access conversion efficiency of M. pygmaeus females. A previous study on Lygus hesperus Knight (Miridae) reported that females ingested in 24 hours an amount of prey corresponding to 169% of their body weight, while males ingested only 98% (Strong & Landes, 1965). A study on consumption requirements of the mirid predator Blepharidopterus angulus (Fallen) (Miridae) of Eucallipterus tiliae L., aphids under low temperatures (14 °C), reported that the efficiency in the transformation of the weight of aphids absorbed into the weight of the body of the predator decreases from the 3rd larval stage (from 46% for the 1st stage to 19% in adult females) (Glen, 1973). Body weight of Azorean females were similar to females of M. pygmaeus reared for 30 generations either on tobacco leaves and fed on eggs of E. kuehniella and without plants (1.36 ± 0.03) (Vandekerkhove et al., 2011).
From an applied point of view, our study provides information on prey consumption of T. absoluta by adult females of M. pygmaeus and new insights on how its predation performance may vary among populations. With regard to these traits, some differences were significant, including differences between females of the two populations. Tuta absoluta and E. kuehniella were readily consumed by M. pygmaeus. In terms of the number of eggs consumed, females of the Azores were more voracious against T. absoluta but, when prey consumption was expressed in the amount of biomass ingested, females from mainland were more voracious against E. kuehniella. The consumption of E. kuehniella translates in a higher weight gain and relative growth rate and Azorean female gain more weigh independently of the prey, but conversion was marginally not significant. Despite the observed differences in some biological traits, the results of this study provide evidence of the suitability of using E. kueniella eggs as factitious prey to mass-rear M. pygmaeus, under laboratory conditions. Further studies on the nymphal performance of the predator (Perdikis et al., 1999; Lykouressis et al., 2009) are needed for a more complete idea about the potential of M. pygmaeus as a biological control agent of T. absoluta. Finally, gathering data on the biology and ecology of biocontrol agents feeding on different prey species are vital to implemented sustainable pest management programs of T. absoluta in Portugal. In this context, a recent study shows the economic and financial commercial viability of a continuous mass production of M. pygmaeus to implement an augmentative biological control approach (Dutra et al., 2023).
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Open access funding provided by FCT|FCCN (b-on). This study was financed by FEDER in 85% and by Azorean Public funds by 15% through Operational Program Azores 2020, under the following project: ECO2 – TUTA (ACORES-01-0145-FEDER-000081). Elisabete Figueiredo was funded by Portuguese national funds FCT Umbert-ECO PTDC/ASPPLA/29110/2017. José Carlos Franco and Elisabete Figueiredo received backing from Forest Research Centre (CEF) and Linking Landscape, Environment, Agriculture and Food (LEAF) research center, respectively, research units funded by Fundação para a Ciência e a Tecnologia (FCT), Portugal (UIDB/00239/2020 and UIDB/AGR/04129/2020, respectively), and both researchers from the Laboratory for Sustainable Land Use and Ecosystem Services–TERRA (LA/P/0092/2020) and FCT Aster PRIMA (PRIMA/0001/2021).
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Conceptualization, Isabel Borges, Luísa Oliveira, Elisabete Figueiredo, José Carlos Franco and António Onofre Soares; methodology, Isabel Borges, Luísa Oliveira, Elisabete Figueiredo, José Carlos Franco and António Onofre Soares; formal analysis, Isabel Borges and António Onofre Soares; investigation, Isabel Borges, Ana Catarina Durão and Francisco Barbosa; writing—Original draft preparation, Isabel Borges and António Onofre Soares; writing—Review and editing, Isabel Borges, Luísa Oliveira, Ana Catarina Durão, Francisco Barbosa, Elisabete Figueiredo, José Carlos Franco and António Onofre Soares; supervision, Isabel Borges; project administration, António Onofre Soares; funding acquisition, António Onofre Soares. All authors have read and agreed to the published version of the manuscript.
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Borges, I., Oliveira, L., Barbosa, F. et al. Prey consumption and conversion efficiency in females of two feral populations of Macrolophus pygmaeus, a biocontrol agent of Tuta absoluta. Phytoparasitica 52, 31 (2024). https://doi.org/10.1007/s12600-024-01130-0
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DOI: https://doi.org/10.1007/s12600-024-01130-0