Introduction

In Tamaulipas, Mexico, citrus production (Citrus spp.; Sapindales: Rutaceae) covers 46 056 ha, producing 986 505 t with an economic value of 5 251 million pesos (Comité Estatal de Sanidad Vegetal de Tamaulipas [CESAVETAM], 2024). However, this activity is constrained by the damage caused by fruit flies (Anastrepha spp.; Diptera: Tephritidae), as females lay their eggs inside the fruit, and the larval instars feed on the pulp (Papadopoulos et al., 2024). In the absence of control strategies, losses are estimated to reach 763 527 t (Salcedo-Baca et al., 2010), representing 77 % of the current production and an economic impact of 4 043 million pesos. In orchards, this scenario would lead to a reduction in labor availability, increased insecticide application, higher production costs and adverse environmental effects (Salcedo-Baca et al., 2010).

According to the literature, there are around 4 000 species of the genus Anastrepha (Saldaña-Reyes et al., 2019), of which 10 are found in Tamaulipas, and four of these are considered of agricultural importance: Anastrepha ludens (Loew, 1873), Anastrepha obliqua (Macquart, 1835), Anastrepha serpentina (Wiedemann, 1830) and Anastrepha striata (Schiner, 1868) (Vanoye-Eligio et al., 2014). These species are polyphagous, meaning their feeding is not restricted to a single host (Hernández-Ortiz, 2007). In the case of Valencia orange (Citrus sinensis L. Osbeck) crops, it has been reported that A. ludens and A. obliqua show similar behavior, while A. serpentina and A. striata are less frequently observed (Tucuch-Cauich et al., 2008).

In the citrus-growing region of Tamaulipas, the relationship between A. ludens, A. obliqua, A. serpentina and A. striata with the crop variety has not been clearly established. In 2015, population fluctuations of A. ludens were reported based on the production season and climatic conditions (Vanoye-Eligio et al., 2015), excluding A. obliqua, A. serpentina and A. striata. Understanding the population fluctuation patterns of each species is crucial for the design of phytosanitary strategies. This is particularly important as the National Campaign Against Fruit Flies aims to control, suppress and eradicate these four agriculturally significant species (Servicio Nacional de Sanidad, Inocuidad y Calidad Agroalimentaria [SENASICA], 2022). Therefore, the objective of the present study was to determine the population fluctuation of A. ludens, A. obliqua, A. serpentina and A. striata in three citrus varieties in Tamaulipas, Mexico.

Materials and methos

Study area

The study was conducted from January to December 2023 in Early orange (Citrus sinensis (L.) Osbeck var. Navelina), Valencia orange (Citrus sinensis (L.) Osbeck) and Red grapefruit (Citrus paradisi Macfad var. Red Blush) crops, located in the central part of the citrus-growing region of Tamaulipas, Mexico (Table 1).

Table 1. Characteristics of the municipalities of Tamaulipas, Mexico, where the study was conducted

Trapping and identification of adult flies

Adults of A. ludens, A. obliqua, A. serpentina and A. striata were captured using Multilure traps baited with three pellets of hydrolyzed protein and 250 mL of water to attract insects (SENASICA, 2017). A total of 120 traps were deployed in the study area, with 30 traps per municipality and 10 per crop (Table 1). The traps were inspected and rebaited weekly for one year. Captured adults were placed in containers with 70 % alcohol and taken to the CESAVETAM laboratory for identification. The flies were placed in a Petri dish with 70 % alcohol and manipulated with fine-tipped straight tweezers for observation under a binocular stereoscopic microscope (DZ.1805, Euromex®). Identified specimens were sorted by species into separate Petri dishes. The identification was conducted by CESAVETAM technical staff using taxonomic keys published in the Guía de Identificación de Moscas de la Fruta (NOM-023-FITO-1995) (SENASICA, 2018).

Statistical analysis

Captures of A. ludens, A. obliqua, A. serpentina and A. striata from the three citrus varieties were subjected to a normality analysis using the Kolmogorov-Smirnov test. Then, the data were grouped by ranks and analyzed using analysis of variance and Tukey's mean comparison test (Henson, 2015) to assess differences. Additionally, the non-parametric Kruskal-Wallis test and a multiple rank mean comparison analysis were performed (Conover, 1999; Kruskal & Wallis, 1952). All tests were conducted with a significance level of 0.05 using Minitab 19.

The number of adults captured weekly per trap for each species in three citrus varieties was converted into the FTD index (NOM-023-FITO-1995). This index reflects the weekly phytosanitary conditions at the orchard or regional level and is expressed to four decimal places, where a value of 0.000 indicates the absence of populations (SENASICA, 2017; Vanoye-Eligio et al., 2015). The FTD index was estimated using the following formula:

where F represents the total number of flies/species captured per week, T is the total number of traps (120), and D is the number of days the trap was exposed in the field (7).

Results and discussion

The results of the Kolmogorov-Smirnov test indicated that the abundance of A. ludens follows a normal distribution, whereas A. obliqua, A. serpentina and A. striata did not meet this assumption. The analysis of variance and mean comparison revealed that the abundance of A. ludens was similar in three citrus varieties (Table 2). In contrast, the non-parametric Kruskal-Wallis test and multiple rank mean comparison showed significant differences in the abundance of A. obliqua in the Valencia orange crop (Table 3).

Table 2. Mean comparison of A. ludens abundance in three citrus varieties.

Table 3. Mean comparison of A. obliqua, A. serpentina and A. striata abundance in three citrus varieties.

Tucuch-Cauich et al. (2008) found that the abundance of A. obliqua in citrus orchards is higher than expected, which could explain why its mean was different from that of A. serpentina and A. striata. Nolasco and Iannacone (2008) note that the latter two species are less predominant due to their specificity for certain crops. Furthermore, Hernández-Ortiz and Aluja (1993) and Hernández-Ortiz (2007) mention that although A. obliqua, A. serpentina and A. striata are considered polyphagous, their host range is relatively limited. It has been reported that A. obliqua prefers mango fruits, A. serpentina favors chicozapote and A. striata is more closely associated with guava fruits, which could explain their lower abundance in citrus crops compared to A. ludens.

Based on the information above, the presence of A. obliqua, A. serpentina and A. striata in citrus orchards may be influenced by the proximity of their primary hosts or the use of food attractants such as hydrolyzed protein. This idea is further supported by the fact that 922.26 ha of mangoes are planted near the sampled orchards (Servicio de Información Agroalimentaria y Pesquera [SIAP], 2023), along with chicozapote and guava trees in nearby backyards and along orchard fences. Therefore, it is advisable to plan citrus production in areas where mangoes are grown, because these crops fruit at different times of the year (Vanoye-Eligio et al., 2023). Moreover, it is important to develop an integrated management plan that includes monitoring nearby host plants, because the abundance and distribution of Anastrepha may be influenced by the variety of hosts in the study area (Jenkins & Goenaga, 2008).

The results of the FTD index indicated that the increase in A. ludens captures occurred before that of A. obliqua, A. serpentina and A. striata. Additionally, this index showed that the population fluctuation of the four fly species varied in the three citrus varieties (Figure 1). The maximum FTD for A. ludens (0.0190) was lower than the value reported the previous year (1.3285) by Vargas-Tovar et al. (2024), possibly because during this study, the fruit's market price favored its commercialization, which reduced the availability of fruits on trees. However, in the Early orange crop, the population of A. ludens was recorded from January to June and from October to December, with maximum FTD values (0.0007) in May and October. Meanwhile, A. obliqua (FTD = 0.0001) and A. serpentina (FTD = 0.0001) appeared occasionally in March, and A. striata (FTD = 0.0000) was not recorded in this crop (Figure 1a).

In the case of the Valencia orange crop, A. ludens, A. obliqua and A. serpentina reached their maximum FTD values in March (0.0179, 0.0024 and 0.0048, respectively), while A. striata peaked in February (0.0012); however, the population dynamics of these species were different. A. ludens was present from December to October, A. obliqua was observed from February to April and from June to August, A. serpentina appeared from February to April and A. striata was only recorded in February (Figure 1b). In contrast, in Red grapefruit crops, A. ludens was present year-round, with the highest FTD value (0.0190) in May, while A. obliqua (FTD = 0.0012) and A. serpentina (FTD = 0.0012) were only occasionally recorded in April and March, respectively, and A. striata was absent (FTD = 0.000) (Figure 1c).

These results are consistent with those reported by Baker et al. (1944), Birke et al. (2006), Robacker and Fraser (2002), and Vanoye-Eligio et al. (2015), who state that both orange and grapefruit crops experience high infestation levels of A. ludens, because they are considered to be their preferred hosts. In the citrus-growing region of Tamaulipas, this species shows high population levels from December to March (the harvest season for orange and grapefruit fruits) (Vargas-Tovar et al., 2024). In contrast, in Campeche, Mexico, the highest infestations of A. ludens occur from June to July, while A. obliqua populations increase from October to November, A. serpentina is more abundant from April to July and A. striata peaks in December (Tucuch-Cauich et al., 2008). However, similar to this study, these variations depend on the fruiting season of their host plants.

A crucial factor in the population dynamics of Anastrepha in citrus orchards is the presence of interspersed varieties, which provide sustenance for the flies (Aluja, 1994; Vanoye-Eligio et al., 2015). According to Thomas (2003), in northwestern Mexico, the oviposition of females in grapefruit fruits from October to November leads to the emergence of adults between January and February, a period that coincides with the first detections of Anastrepha in Texas, USA. In this context, considering that in the citrus-growing region of Tamaulipas, the maturation period for Early orange occurs from August to February, for Valencia orange from October to May, and for Red grapefruit from September to March (Vargas-Tovar et al., 2024), it is reasonable to assume that Anastrepha populations are supported year-round. Additionally, Nolasco and Iannacone (2008) state that even when fruits are not in the maturation stage, the presence of fallen fruits allows Anastrepha to persist (Sivinski et al., 2004). This could explain the year-round presence of A. ludens in the grapefruit crop.

Based on the above, planning citrus production becomes a key management strategy. Martínez-Jiménez et al. (2020) propose standardizing and redistributing production, meaning reducing output in March (the month with the highest production) and increasing it in January, February and April (months with lower production). This strategy could be applied to both citrus and mango crops through pruning and the use of gibberellic acid and 2-chloroethylphosphonic acid to delay and advance production, respectively (Padrón-Chávez & Rocha-Peña, 2007; Soto-Ortíz et al., 1994). For citrus, implementing this strategy is estimated to increase profits for producers by 32 million pesos (Martínez-Jiménez et al., 2020). This means that if adopted, there would be annual production increases and a reduction in pesticide use. This sets the stage for developing new integrated management strategies against fruit flies.

Conclusions

Variations in fruit fly population fluctuations make it difficult to establish recommendations for integrated management. However, adequate control from January to August is essential in all three citrus varieties. Integrated management in Red grapefruit crops may be more relevant than in Early orange and Valencia orange crops, as it has a higher efficiency potential and lower cost compared to the latter two crops.