Tropical horticulture is economically important in Mexico; in the last few years Mexico has become one of the main exporters of mango (Mangifera indica Lour. [Anacardiaceae]) and papaya Carica papaya L. (Caricaceae) (Villegas-Monter & Mora-Aguilera 2011). Of all the states in Mexico, Guerrero produces the most mangoes, particularly the cultivars Manila and Ataulfo (SIAP 2016).

A key threat to horticultural development in Guerrero, and in other states, is the complex of phytophagous pests, amongst which some species in the family Tephritidae (fruit flies) are the most important (Aluja 1993, 1994; Hernández-Ortiz et al. 2010). Worldwide there are nearly 4,000 species belonging to 500 genera in the Tephritidae (White & Elson-Harris 1992), and almost 200 species are considered important pests due to the direct losses that they cause to many fruit tree species (Norrbom et al. 2012). Globally, the most widespread genera of fruit flies are Bactrocera, Ceratitis, Rhagoletis, Toxotrypana, and Anastrepha (all Diptera: Tephritidae) (Hernández-Ortiz et al. 2010). Anastrepha is one of the most diverse genera and is endemic to the Americas (Aluja 1994; Norrbom et al. 1999; Norrbom & Korytkowski 2009, 2011).

In the Americas, species of Anastrepha are distributed from Texas to the north of Argentina, including most Caribbean islands (Hernández-Ortiz & Aluja 1993; Aluja 1994). The genus has 209 described species (Hernández-Ortiz et al. 2010), 7 of which are considered economically important: Anastrepha ludens (Loew) (Mexican fruit fly); Anastrepha obliqua (Macquart) (West Indian fruit fly); Anastrepha fraterculus (Wiedemann) (South American fruit fly); Anastrepha suspensa (Loew) (Caribbean fruit fly); Anastrepha serpentina (Wiedemann) (sapote fruit fly); Anastrepha striata Schiner (guava fruit fly); and Anastrepha grandis (Macquart) (cucurbit fruit fly) (all Diptera: Tephritidae) (Hernández-Ortiz et al. 2010). Mexico has 37 species of Anastrepha, and the highest species diversity is found in the states of Chiapas and Veracruz (25 and 24 species, respectively). In Guerrero, 12 species have been recorded: Anastrepha tripunctata Wulp, Anastrepha bicolor (Stone), Anastrepha pallens Coquillett, Anastrepha montei Lima, Anastrepha spatulata Stone, Anastrepha chiclayae Greene, A. serpentina (Wiedemann), A. striata Schiner, Anastrepha acris Stone, Anastrepha distincta Greene, A. ludens (Loew), and A. obliqua (Macquart) (all Diptera: Tephritidae) (Hernández-Ortiz 2007).

Currently, the National Campaign against Fruit Flies (NCFF) is active in 26 states of Mexico, where monitoring activity (adult trapping and fruit sampling) and control strategies are implemented under an Integrated Pest Management scheme, with the aim of establishing and keeping fruit fly-free areas and reducing fruit fly populations to low prevalence levels (= fruit flies per trap per d [FTD] of ≤⃒ 0.01) (SENASICA 2017). It is recognized that understanding the population dynamics of these pests in particular regions of the country can inform control measures (Aluja 1993). The objectives of this research were to: (a) update knowledge on the diversity of fruit fly species from the family Tephritidae and determine the diversity and seasonal distribution of tephritid fruit flies in the state of Guerrero; and (b) identify fruit fly hosts in the municipalities of Tetipac and Atoyac de Álvarez, Guerrero, Mexico.

Materials and Methods

Results

DIVERSITY OF FRUIT FLIES FROM FRUIT SAMPLES

The most important population peaks of fruit flies in both municipalities was related to the phenological stages of the fruit trees in each study area, such as fruit development stage, fruit maturity, and harvesting period (Fig. 3).

Table 1.

Species of fruit flies and total abundance in 2 municipalities of Guerrero, 2015–2016.

Table 2.

Total species richness and fruit fly diversity in 2 municipalities of Guerrero, 2015–2016. S: Species richness; H´: Shannon-Wiener index; 1-λ: Simpson index.

The species of fruit flies detected by direct fruit sampling from the main host species in Tetipac were: A. ludens in mango; A. striata in guava; A. obliqua in jobo and mango; and T. curvicauda in bonete. In Atoyac de Álvarez only A. obliqua was recorded in mango. In addition to the emergence of adult fruit flies sampled from fruits on trees and fallen fruits, the emergence of adults of the parasitoid D. longicaudata was recorded from mango, guava, and jobo in Tetipac; no parasitoids were recorded emerging from fruit collected in Atoyac de Álvarez (Table 3).

Discussion

In Mexico, research on the population fluctuations of Tephritidae have focused mainly on species of economic importance (González-Hernández & Tejada 1979; Thomas 2003; Tucuch-Cauich et al. 2008; Aluja et al. 2012; Vanoye-Eligio et al. 2015; Hernández-Adame et al. 2015). However, some studies have provided full lists of the species of fruit fly present in a given area, their primary hosts, and at least some data on their population dynamics (Celedonio-Hurtado et al. 1995; Miranda-Salcedo & Leyva 1996; Martínez & Serna 2005; Martínez-Alava 2007; Nolasco & Lannacone 2008; Gonzáles et al. 2011; Miranda-Salcedo 2012; René-Arias et al. 2014; Montoya-Alvarez et al. 2014; Vanoye-Eligio et al. 2014).

Of the 11 species of fruit flies previously recorded in the state of Guerrero, 5 also were found in this study and in both municipalities, and they are all considered of economic importance. These are A. ludens, A. striata, A. obliqua, A. serpentina, and T. curvicauda (Aluja 1993; Hernández-Ortiz & Aluja 1993; Hernández-Ortiz et al. 2010). In the municipality of Tetipac, in addition to these species, A. bicolor, A. spatulata, and A. dentata also were found, which have already been documented in Mexico (Hernández-Ortiz 2007), as well as R. ramosae, which was described for the first time from material from Guerrero and Michoacán (Hernández-Ortiz 1985), and Z. cocoyoc, a species that had been recorded already in the states of Guerrero, Chiapas, and Morelos (Norrbom 2002).

The fact that higher species richness and diversity of fruit fly species were recorded in Tetipac (S = 10 and H′ = 1.30, λ = 0.68) than in Atoyac de Álvarez (S = 5 and H′ = 0.39, λ = 0.17) is probably due to the presence in every backyard in Tetipac of a greater diversity of backyard fruit trees, such as jobo, orange (Citrus sinensis L. [Rutaceae], mango, papaya, mamey (or sapote) (Puteria sapota Jacq. [Sapotaceae]), and peach (Prunus persica L. [Rosaceae]) in addition to guava, which is the main crop of the region. According to Aluja (1993) and Hernández-Ortiz (2007), backyard fruit trees are hosts of a range of fruit fly species. In contrast, Atoyac de Álvarez is an area where commercial mango production predominates due to its great economic importance; mango also is grown in every backyard, and is found amongst wild vegetation. The sites where NCFF traps were established did not allow the detection of a higher diversity of species owing to the reduced number of alternative hosts near commercial orchards.

Fig. 1.

Fruit flies per trap per day of fruit flies in Tetipac, Guerrero 2015–2016. Other = A. serpentina, A. spatulata, A. bicolor, A. dentata, T. curvicauda, Z. cocoyoc, and R. ramosae.

During the period from Oct 2015 to Oct 2016, the total abundance of fruit flies was higher in Tetipac (70.18%) than in Atoyac de Álvarez, and the most common species was A. ludens, which is characterized by a higher capacity for adaptation to more elevated areas (> 900 masl) (Hernández-Ortiz 1992), followed by A. striata and A. obliqua. These 3 species were present throughout the entire monitoring period, because the season for fruit production of each tree species occurs in different months; thus, the insects have host fruits available throughout the year. This confirms other studies where fruit production has been documented as the main factor affecting fruit fly populations in tropical environments (Celedonio-Hurtado et al. 1995; Nolasco & Lannacone 2008; Tucuch-Cauich et al. 2008; Gonzáles et al. 2011; Aluja et al. 2012; Hernández-Adame et al. 2015; Vanoye-Eligio et al. 2015). Populations of the other fruit fly species detected in this study and others occurred sporadically from Mar to Sep 2016 with only a few individuals captured.

During the period from Oct 2015 to Oct 2016, the total abundance of fruit flies was lower in Atoyac de Álvarez (29.8%) than in Tetipac (70.2%), and the most common species was A. obliqua, which is more adapted to areas at a low elevation (< 500 masl) (Hernández-Ortiz 1992); the species was recorded in 46 of the 53 wk monitored, and from Feb to Sep 2016. In contrast, in this municipality, populations of A. striata, A. ludens, A. chiclayae, and T. curvicauda were small; only 1 individual of T. curvicauda was recorded in the entire year.

Fig. 2.

Fruit flies per trap per day of fruit flies in Atoyac de Álvarez, Guerrero 2015–2016. Other = A. chiclayae and T. curvicauda.

Fig. 3.

Phenology of the principal fruit trees in the municipalities of Atoyac de Álvarez and Tetipac, Guerrero. (1) Vegetative period; (2) Flowering; (3) Fruit production; (4) Maturity and harvest.

In both areas of study, the populations of fruit flies collected were predominantly female, as seen in other studies (Nolasco & Lannacone 2008; Espolador-São João et al. 2014; René-Arias et al. 2014; MontoyaÁlvarez et al. 2014; Hernández-Adame et al. 2015) (Table 2). This is because the food bait used in traps to catch adults (torula yeast and borax) is based on proteins that are important for oocyte formation in females.

The presence of the most common species of fruit flies throughout the study, such as A. ludens, A. striata, and A. obliqua, coincided with the phenological stages of fruit production, fruit maturity, and harvest period for the tree species present in each region (Fig. 3). Collecting infested fruits helped to confirm the host range and host preference of the fruit fly species associated with the municipalities of Tetipac and Atoyac de Álvarez. In Tetipac, A. ludens was recorded in mango, A. striata in guava, A. obliqua in jobo and mango, and T. curvicauda in bonete, as has been recorded previously (Aluja 1993, 1994; Hernández-Ortiz & Aluja 1993; Hernández-Ortiz 2007; Martínez-Barrera et al. 2015). In Atoyac de Álvarez, A. obliqua was recorded only in mango (Table 3).

Analysis of the fruit flies per trap per d data for 2015–2016 for the economically important fruit fly species showed that in Tetipac, A. ludens, A. striata, and A. obliqua were the species most frequently captured in the area. Population peaks in most cases had fruit flies per trap per d values higher than 0.01 (zones under plant protection actions). This means that the NCFF must apply several control strategies, such as chemical, cultural, and biological control (IPM), if fruit fly populations are to be controlled. These 3 fruit fly species may be present at the range of altitudes of the sites where the study was conducted (50–1,660 masl), but this depends on the host tree diversity. In contrast, in Atoyac de Álvarez, A. obliqua was the species most frequently captured, while populations of A. striata, and A. ludens were small, and the population peaks always had fruit flies per trap per d values below 0.01 (low prevalence zone). For this category it is sufficient for the NCFF to release sterile flies to suppress fruit fly populations. In this area, altitude may not influence host tree diversity for fruit flies, because mango trees are present more frequently.

Table 3.

Species of fruit flies and parasitoids detected in host fruits in 2 municipalities of Guerrero, 2015–2016.

Finally, of the 4 fruit fly species of economic importance detected in the 2 study sites, A. serpentina had the smallest populations in Tetipac, with fruit flies per trap per d values always being below 0.01, and in Atoyac de Álvarez no individuals of this species were caught in traps. According to the Mexican Plant Protection Standard NOM-023-FITO-1995 (SAGAR 1999), the incidence levels of these 4 fruit fly species are used to define the plant protection zones or categories that have been established for the NCFF, namely Free Zone with FTD = 0.00; Zone of Low Prevalence (with FTD ≤⃒ 0.01; and Zones under Plant Protection Actions (FTD > 0.01, with an upper limit of > 0.08); management strategies proposed by the NCFF are carried out taking these categories into account.

In general, it can be observed that fruit fly populations in Tetipac maintain fruit flies per trap per d values of > 0.01, whereas in Atoyac, populations maintain fruit flies per trap per d values of < 0.01. The results of the present study show that the municipality of Tetipac is in the Zones under Plant Protection Actions category, which means it has high levels of fruit fly incidence. In contrast, Atoyac de Álvarez is in the Zones of Low Prevalence category, and it may attain the Free Zone category in the future, which would reduce management costs, and producers could freely trade fruits such as mango in domestic and international markets without quarantine restrictions.