The braconid Utetes anastrephae (Viereck, 1913) (Hymenoptera: Braconidae) is a larva-pupal parasitoid of fruit flies of the genus Anastrepha Schiner, commonly associated with Anastrepha obliqua (Macquart, 1835) (Diptera: Tephritidae), the most important pest of mango (Mangifera indica L., 1753) in Mexico. This parasitoid was established in a laboratory colony using larvae of Anastrepha ludens (Loew, 1873) as host. Here we describe a demographic study to compare the reproductive and population parameters of this parasitoid reared on A. obliqua and A. ludens under laboratory conditions. Two U. anastrephae cohorts of 30 individual pairs each were set up, one was reared on A. obliqua larvae and the other one on A. ludens. Every day, 30 third instar larvae of each host species were exposed to an adult pair through the lifespan of the female. Daily mortality and fecundity were recorded. Life tables were constructed and sex ratios, parasitism rates, survival, reproductive and population parameters were estimated. Higher survival of U. anastrephae females was observed in females from A. obliqua (mean live expectancy of 22.4 days), but higher fecundity and parasitism occurred in females from A. ludens (net fecundity of 62.61 daughters/ female and 16.72% parasitism rate). The intrinsic rate of increase (r = 0.128 and r = 0.134 for A. obliqua and A. ludens respectively), mean generation time (27.88 and 28.30 days) and population doubling time (5.42 and 5.16 days) were similar in both cohorts, as well as the sex ratio (73 and 69% of females). These results suggest that A. ludens as host increase the production rates; however, any one of these two species could be used as host for mass rearing purposes.

biocontrol, fecundity, intrinsic rate of increase, life table, mass rearing, parasitism, survival

The use of native parasitoids for the management of Anastrepha fruit flies has been a subject of discussion, since these species would be used in an environment where fruit flies generally have a higher rate of natural increase (Vargas et al. 2002; Aluja et al. 2009). However, given the good results obtained with augmentative releases of Diachasmimorpha longicaudata (Ashmead, 1905) in different environments (e.g., Montoya et al. 2000; Montoya et al. 2007; Montoya et al. 2016; Cancino et al. 2019a), the potential for native species for the control of Anastrepha fruit flies is worth to explore.

Utetes anastrephae (Viereck, 1913) (Hymenoptera: Braconidae) is a koinobiont, solitary endoparasitoid (Ovruski et al. 2000) native to the Neotropics that parasitizes larva-pupa of fruit flies. It is found parasitizing Anastrepha obliqua (Macquart, 1835) (Diptera: Tephritidae) feeding upon Spondias spp. (Anacardiaceae), and in minor frequency in other species such as Anastrepha alveata Stone, 1942 and Anastrepha fraterculus (Wiedemann, 1830) (Aluja et al. 1990; Hernández-Ortíz et al. 1994; López et al. 1999). This parasitoid competes successfully with other native braconid parasitoid species, such as Doryctobracon areolatus (Szépligeti, 1911), Doryctobracon crawfordi (Viereck, 1911), and Opius hirtus Fischer, 1963; it even competes with the introduced D. longicaudata, showing a remarkable capacity for conspecific discrimination and heterospecific intrinsic competition in previously parasitized larvae (Aluja et al. 2013; Ayala et al. 2018; Murillo et al. 2018).

The use of a parasitoid species for augmentative biological control applications requires the development of methods for mass production of good quality individuals. One essential element is the selection of an adequate host species (Eitam et al. 2003; Cancino et al. 2009). Although A. ludens is not considered a preferred host for U. anastrephae, it can be used as an alternative host because it is a species relatively easy to rear, being a high-quality host that is currently used to produce massively D. longicaudata (Orozco-Dávila et al. 2017; Cancino et al. 2020). Under laboratory conditions U. anastrephae successfully parasitizes 5–8 days old A. obliqua larvae (Poncio et al. 2018) and 7–8 days old A. ludens larvae (Aluja et al. 2009; Cancino et al. 2009).

Knowledge of the demography of parasitoids, in addition to allowing a better understanding of their biology, allows us to compare the effect of different hosts and make mass rearing more efficient (Bellows et al. 1992; Carey and Roach 2020; Ganjisaffar and Perring 2020). For example, the intrinsic rate of natural increase (r) is a population parameter described as the potential growth of a population (Jervis and Copland 1996) and can be used as an indicator of the capacity of a parasitoid species to suppress or regulate the target pest population (Vargas et al. 2002; Stark et al. 2004). This parameter combines both the survival and reproduction of a population and allows comparison among different species of parasitoids or when species are evaluated under different environmental conditions (Núñez-Campero et al. 2014; Gonçalves et al. 2018; Fernandes et al. 2021).

Our previous trials, trying to establish a colony of U. anastrephae using A. obliqua larvae as host, were unsuccessful, despite being considered its natural host. Here, we used a strain of U. anastrephae reared on A. ludens larvae as host, applying the concept of factitious host used for Trichogramma spp. mass rearing (Iranipour et al. 2010; Gowda et al. 2021). Our hypothesis was that the demographic parameters of U. anastrephae would be affected by the host species used for the development of their offspring. Therefore, our aim was to determine the effect of two different hosts, A. obliqua (the preferred host in nature) and A. ludens (the host used in laboratory rearing), on the survival, reproductive and population parameters of U. anastrephae. Our results improved our understanding of the performance of U. anastrephae reared on both host species and indicate that both can be used for mass rearing it as a biocontrol agent of Anastrepha fruit flies.

It was interesting to find that U. anastrephae could develop equally successfully in both hosts, one of them being its most frequent natural host (A. obliqua), and the other its host in the laboratory rearing colony (A. ludens). Anastrepha ludens has been reported as the natural host of U. anastrephae very rarely (Montoya et al. 2016). However, since most studies on natural parasitism of fruit fly parasitoids have generally been directed to the same fruits of specific interest (Aluja et al. 1990; López et al. 1999; García et al. 2020); it is possible that other fruits that have not been inspected are hosting A. ludens parasitized by U. anastrephae. Likewise, there may be confusion regarding the emergence of U. anastrephae from A. obliqua when it could also emerge from A. ludens, since parasitoids have been detected in mango, where both species of flies are present (Aluja et al. 1990). However, this assumption needs to be investigated.

The higher reproductive rates found when A. ludens larvae were the host, compared to A. obliqua, can be attributed to three factors: 1) the effect of host switch, 2) the quality of the host, and/or 3) the immunological response. It is known that host switching may adversely affect the fitness of parasitoid species during the very first generations in a new host, although in subsequent generations their performance can improve (Zenil et al. 2004; Jones et al. 2015; Poncio et al. 2016). When the parasitoid D. longicaudata was previously maintained on A. fraterculus larvae, the adults parasitized more on this host than when Ceratitis capitata larvae (Wiedemann, 1824) were offered as an alternative host (Ovruski et al. 2011; Rohr et al. 2019). Something similar was observed with Fopius arisanus (Sonan, 1932) reared on C. capitata larvae for 28 generations. When adults were exposed to Anastrepha species larvae, the percentage of adult emergence was lower than in those exposed to C. capitata larvae (Zenil et al. 2004).

The use of alternative (factitious) hosts for parasitoid rearing has been an important technique (Pluke and Leibee 2006). When parasitoid colonization with the native host is a difficult, or expensive process, the use of this factitious host becomes an option (Boycheva et al. 2019). As mentioned above, U. anastrephae colonization with A. obliqua as host was an ineffective process. The use of A. ludens larvae as factitious host represented a good option.

Regarding the immune response of A. obliqua to parasitoids, it has been reported that its larva possesses 5–6 types of haemocytes that generate a strong immune response (phagocytosis and production of reactive oxygen species) (Silva et al. 2002; Gómez-Alonso et al. 2022). The presence of these haemocytes resulted in the melanization and encapsulation of the first immature stages of parasitoids (Silva et al. 2002; Cancino et al. 2022), which has not been observed in A. ludens (Poncio et al. 2016; Cancino et al. 2020). This high immunity response of A. obliqua larva represents an important factor in increasing parasitoid mortality during development.

Host quality could be another factor. Anastrepha ludens larvae are larger in size than the A. obliqua ones. Under mass-rearing conditions, the mean pupal weight is 20 mg for A. obliqua and 24 mg for A. ludens (Orozco-Dávila et al. 2017). Usually, larger size hosts are preferred by parasitoids, showing an increase in their fecundity (Brodeur and Boivin 2004; Cohen et al. 2005; Gao et al. 2016). Another reason may be the better adaptation and more stability of A. ludens to mass rearing conditions. Compared with A. obliqua, it has been, easier to colonize and maintain under laboratory conditions (Orozco-Dávila et al. 2017; Aceituno-Medina et al. 2020).

The lower survival of the parasitoids exposed to A. ludens larvae can be explained by the cost of reproduction, the higher the fecundity, the lower the longevity. Since the net reproductive rate and the intrinsic rate of increase were higher for parasitoids reared on A. ludens than those reared on A. obliqua (Table 2), this trade-off can be considered convenient in terms of fitness.

The demographic parameters we found here were like those reported by Vargas et al (2002) with other larval-pupal braconid endoparasitoid reared on different hosts. For example, the intrinsic rate of increase for D. longicaudata and Psyttalia incisi (Silvestri, 1916) was r = 0.12 and 0.10, respectively, both reared on Bactrocera dorsalis larvae (Hendell, 1912). This suggests that U. anastrephae has the potential to be used as a biocontrol agent, as it has growth rates like other parasitoid species that have been used for the control of fruit flies.

The intrinsic growth rate we found here with A. ludens as a host (r = 0.134) was 2-fold greater than that reported by Aluja et al. (2009) using the same host when they were colonizing this species for laboratory rearing (r = 0.079). This means that the U. anastrephae strain tested here has adapted to this alternative host species, and it can be used for mass production. The sex ratio is a fundamental aspect for biological control, since the females are the ones that attack the host and contribute to population growth. A female-biased sex ratio would be most desirable (Montoya et al. 2013; Nurkomar et al. 2021). Here we found that the sex ratio was female-biased, about 70% female (≈ 3:1) for both hosts used. This proportion coincides with that obtained by Poncio et al. (2018), with a percentage of 65% using A. obliqua larvae as hosts. This proportion is adequate for the purposes of augmentative biological control.

The reason why under natural conditions U. anastrephae is commonly associated to A. obliqua could be the size of the fruit species used by the fruit fly species (Hernández-Ortíz et al. 1994; López et al. 1999). Utetes anastrephae has a short ovipositor that might be strongly adapted to small fruits. In general, A. obliqua infest fruits that are smaller in size (Spondias spp., Psidium guajava L.) than those commonly infested by A. ludens (Citrus spp., Casimiroa edulis La Llave & Lex). Then, in large fruits the host larvae might be out of reach for U. anastrephae. Also, semiochemicals emitted by fruits infested by A. obliqua (usually small) can determine this preference (Aluja et al. 2013). Another possibility, derived from our results, will be to use A. obliqua as a host for several generations, expecting that reproductive and population parameters could increase. However, the greater difficulty and cost of producing A. obliqua should be considered.

This demographic analysis of U. anastrephae comparing two hosts indicates that A. ludens can be used as a suitable host for mass production, although releases of parasitoids be strategically targeted to control A. obliqua. Biological control of A. obliqua in non-commercial hosts could be a strategy to prevent the movement of populations from these hosts to fruit orchards (i.e., mango orchards), where fruits are grown for commercial purpose (Cancino et al. 2019b; Montoya et al. 2000). Anastrepha obliqua is a major pest of mango in the Americas and is highly desirable to have a biocontrol alternative to minimize its damage (Cancino et al. 2019b; Ruiz-Arce et al. 2019).

The information generated here can be useful for decision making on the use of native parasitoids in augmentative biological control and new proposals to complement or improve current strategies for managing Anastrepha fruit flies. It would be interesting to know the behaviour of U. anastrephae reared in A. ludens larvae, on host preference in the presence of these two host species studied here, both in the laboratory and under field conditions.

This study provides information about the potential use of the native parasitoid U. anastrephae in augmentative biocontrol programs against A. obliqua fruit flies. Our results show that both, A. obliqua and A. ludens larvae can be used as hosts for mass rearing purposes. Although A. ludens is not a common natural host, it can be used as a factitious host, considering the higher fecundity rate observed and considering that A. ludens is easier to mass produce than A. obliqua (Orozco-Dávila et al. 2017).

We thank to Amanda Ayala, Patricia Rosario, and Bigail Bravo (Laboratory of Biological Control, of the Programa Moscafrut) for technical support, to the Moscafrut Facility (SENASICA-SADER) for providing the biological material. This paper is a partial requirement for MDEM doctoral program. MDEM thanks the Consejo Nacional de Ciencia y Tecnología (CONACYT) for her graduate scholarship (CVU 658503).