The highly significant inverse correlation between the numbers of D. citri nymphs versus rainfall indicated that this abiotic factor regulates the population densities of the pest in the rainy periods. Kiritani (2013) reported that, although density-dependent processes regulate the population density of any organism, density-independent processes also influence it, and its magnitude may vary. Studies have shown that rainfall can limit the population development of D. citri (Chavez-Medina et al. 2016). Furthermore, Aubert (1987) reported that monthly rainfall exceeding 150 mm is generally associated with low populations of D. citri due to the washing of eggs and nymphs from the plant surface.
At the end of the rainy season, the population densities of D. citri increased and within the interaction of the plant–psyllid system, another density-dependent process came into play, i.e., the parasitoid, T. radiata. The importance of T. radiata as a biocontrol agent of D. citri on M. paniculata was supported by the high inverse correlation (r: − 0.9119, P < 0.05) between the number of parasitized and non-parasitized D. citri nymphs that resulted in high parasitism rates (Fig. 3a).
The importance of parasitism by T. radiata on D. citri has been previously established for M. paniculata and citrus species. Pluke et al. (2008) observed levels of parasitism, ranged between 70–100 and 48–70% for Citrus spp. and M. paniculata, respectively. Releases of T. radiata decreased the number of D. citri nymphs per flush from 42 to 3.8, which represented (91.2%) of the population reduction (Flores and Ciomperlik 2017). Four years of study in different regions of Southern California indicated a significant mortality of D. citri due to high rates of parasitism by T. radiata in citrus plants (Milosavljević et al. 2021).
Parasitism rates of T. radiata on D. citri on M. paniculata and C. x aurantiifolia in Manabí province showed a colonization process of an exotic insect pest and the phenological desynchronization in the colonization of its parasitoid. Thus, the fieldwork showed that M. paniculata was colonized by D. citri in Manabí province approximately in August 2016 (Navarrete et al. 2016) and approximately 2 years later, in May 2018, T. radiata parasitized D. citri nymphs were observed (Cuadros et al. 2020).
Subsequently, C. x aurantiifolia, colonized by D. citri at the end of 2018 and this process, together with the absence of parasitism, may explain the high densities detected in that year and especially in the following year (2019). With an asynchrony of 2 years, in July 2020, in this agro-ecosystem, the parasitoid T. radiata became part of the interaction with very low rates of parasitism at the beginning, which increased over time.
A similar case of phenological desynchronization (insect host—parasitoid) was reported in Venezuela with the guava cottony scale, Capulinia linarosae Kondo and Gullan, 2016 (Hemiptera: Eriococcidae), a pest of the guava tree, Psidium guajava L. (Myrtaceae). In 1993, this invasive insect species of unknown origin appeared colonizing the guava crop in different guava producing regions of Venezuela (Cermeli and Geraud-Pouey 1997). With a difference of approximately 2 years (January 1996), the wasp parasitoid Metaphycus marensis Chirinos and Kondo, 2019 (Hymenoptera: Encyrtidae) was observed parasitizing C. linarosae on guava (Cermeli and Geraud-Pouey 1997). By 1999, the parasitoid, M. marensis, was fully established and interacting with its host, C. linarosae in the different regions of Venezuela where guava is grown (Geraud-Pouey et al. 2001).
Jeffs and Lewis (2013) reported that time is fundamental for many interspecific interactions that evolve to optimize temporal overlap and additionally mentioned that asynchrony can be part of the adaptive process. The same researchers indicated that few studies have observed the potential for phenological asynchrony between parasitoids and their insect hosts.
The colonization and establishment of D. citri and T. radiata in Manabí province likely occurred first on M. paniculata. D. citri was found for the first time on citrus trees and M. paniculata (= M. exotica) plants in Guayaquil, in the province of Guayas, where the highest population densities (approx. 20 nymphs per flush) were observed on the latter host (Cornejo and Chica 2014). Likewise, the parasitoid T. radiata was also found for the first-time parasitizing D. citri nymphs infesting M. paniculata in Guayas province (Portalanza et al. 2017). Thus, it is likely that D. citri and T. radiata were introduced to the city of Portoviejo, in Manabí province, from the province of Guayas through the retail trade of orange jasmine and other rutaceous plants. A similar situation occurred in Florida, U.S.A., where D. citri dispersed throughout the state through migration of the adult psyllids and the commercial trade of infested M. paniculata plants that were sold as ornamentals (Halbert et al. 2008).
On the other hand, the citrus growing region of Mejía is located 8 km from the city of Portoviejo and thus it is likely that the psyllid and its parasitoid were introduced on D. citri infested orange jasmine plants brought from Mejía city, and posteriorly colonized citrus orchards. Thus, the probable pathway, followed by D. citri and T. radiata in Manabí province, is as follows: orange jasmine (Guayas)—orange jasmine (Portoviejo city)—orange jasmine (Mejía)—key lime (Mejía).
Despite the short distance between Mejía and Portoviejo cities, the colonization of C. x aurantiifolia by the Asian citrus psyllid occurred 2 years later. Parasitization of T. radiata on D. citri nymphs in orange jasmine in Portoviejo city, probably delayed the colonization of the citrus growing region. The process of colonization and establishment of the plant–psyllid–parasitoid interaction observed in M. paniculata may be repeated in C. x aurantiifolia. The same pattern in the population dynamics of D. citri nymphs occurred on both host plants in terms of the effect of rainfall, the phenological desynchronization between colonization and the establishment of the plant–psyllid–parasitoid interaction. Based on the data gathered on the pattern of colonization of D. citri and T. radiata in M. paniculata, a model for estimating the number of T. radiata parasitized D. citri nymphs on M. paniculata and C. x aurantiifolia can be calculated.
Frequency of colonization and establishment events of the Asian citrus psyllid on M. paniculata and C. x aurantiifolia and subsequent appearance of the parasitoid and its establishment on M. paniculata, may be estimated by the end of 2022, populations of D. citri might fluctuate at low levels associated with high percentages of parasitism by T. radiata on C. x aurantiifolia. However, in Ecuador, a high percentage of citrus farmers use chemical insecticides to control insect pests (Sornoza-Robles et al. 2020), which would affect the levels of parasitism by T. radiata in commercial citrus orchards. Field and laboratory studies have demonstrated the lethal and sublethal effects of pesticides belonging to various chemical groups on T. radiata (Beloti et al. 2015). Therefore, it is important to establish biological control and/or integrated pest management programs for the conservation of T. radiata and other natural enemies.