Expansion to new habitats and a new commercial host (Malus domestica) by Anastrepha ludens (Tephritidae) likely influenced by global warming

Abstract

Anastrepha ludens (Mexican fruit-fly) is a highly polyphagous fruit fly species (Tephritidae) attacking wild and commercial fruit from Mexico to Panama. Here we report on a recent habitat and host range expansion as A. ludens lately started to attack apples (Malus domestica) in Mexico, a phenomenon likely influenced by global warming. We document natural infestations in apple-growing regions in the States of Nuevo León and Hidalgo, Mexico where A. ludens has started to attack the cultivars 'Golden Delicious', 'Rayada' and 'Criolla'. No infestations were found in the apple-growing region of Zacatlán, Puebla. To determine apple cultivar susceptibility to the attack of this emerging pest, we ran forced infestation assays in enclosed fruit-bearing branches in all three apple-growing regions and studied the metabolome of all fruit. A clear pattern emerged indicating that the cultivar 'Golden Delicious' was the most susceptible, with 'Criolla' exhibiting complete resistance in one location (Puebla). Although A. ludens can develop in this new host, development rates (egg-adult) and adult emergence were affected when compared with the performance in the natural host 'Marsh' grapefruit. Warmer temperatures and specific secondary metabolites of some apple cultivars are likely contributing to the territorial and host expansion of A. ludens.

Keywords: Apple metabolome; Habitat and host-range expansion; Mexican fruit-fly; Pest management; Warmer temperatures.

Fig. 1

Mean temperatures in the three study sites during the time when the forced infestation study was set up in the field. In the case of Zimapán, Hidalgo, the study was run in two parts: in the 1st experiment we worked with ‘Golden Delicious’ and ‘Rayada’ cultivars, and in the 2nd with ‘Criolla’, because fly emergences were not synchronized. Dates at the beginning of lines indicate when the experiment started at each site. Extreme temperatures are indicated when they occurred.

Fig. 2

Mean, maximum and minimum temperatures over a 40-year period in the three study sites, and the citrus growing region 83 km away (straight line) from the apple area in Zacatlán, Puebla. The dashed horizontal lines represent the trends, and the solid horizontal lines indicate overall mean temperatures; at the end of each line the difference in °C between the trend line and the mean temperatures over 40 years are shown. Source: NASA open access database https://power.larc.nasa.gov/data-access-viewer/.

Fig. 3

Mean ± SE of the coordinates of the color parameters (a) luminosity, (b) chromatic coordinates red/green and, (c) chromatic coordinates yellow/blue (L*a*b*) of the apple fruit skin of the apple cultivars growing in three sites of Mexico [Hidalgo (HG), Nuevo León (NL) and Puebla (PU)] where studies were conducted. Tukey’s contrasts are found in Table S3.

Fig. 4

Mean model estimates and their 95% CI resulting from the forced infestation bioassays of (a) the mean number of larvae per fruit of three apple cultivars at three different sites; (b) the pupation proportion obtained from three apple cultivars at different sites; (c) pupal weight from three apple cultivars at different sites; (d) the adult emergence proportion from three apple cultivars at different sites; (e) development time from egg to adult of flies from three apple cultivars at different sites; (f) adult lifespan of flies from three apple cultivars at different sites. Open symbols indicate data on individual trees. For illustrative comparative purposes only, the values in all parameters measured for grapefruit (natural host) were: (a) 39.63 ± 4.4 (SE), (b) 0.79 ± 0.03; (c) 19.69 ± 1.14; (d) 0.54 ± 0.02; (e) 65.57 ± 1.19; (f) 136.78 ± 16.44, respectively. Also, to illustrate the phenomenon better, we note that from 25 grapefruit we obtained 4558 larvae and from 25 ‘Golden Delicious’ – Hidalgo’ apples (the most infested cultivar/site), only 773 larvae. Tukey multiple comparisons in Tables S4–S7.

Fig. 5

ANOVA diagram (with p-value threshold 0.05) of phenolic compounds in general, representing the most influential ones in shaping the PCA by the size and color of the circle.

Fig. 6

PCA showing the two principal components. The explained variances are shown in brackets. Note that the cultivars ‘Criolla’-PU and ‘Rayada’-PU clearly form isolated groups.

Fig. 7

Heatmap of phenolic compounds and treatments. Data were arranged using the Euclidean distance as a similarity measure and the Ward clustering algorithm.

Fig. 8

Apple cultivars used in the A. ludens forced infestation bioassays in the states of Puebla, Hidalgo and Nuevo León, Mexico. We note that in Nuevo León the cultivar ‘Criolla’ is also referred to as ‘Perón Saltillense’ by some local growers. ‘Golden Delicious’ is also referred to as ‘Golden Agua Nueva’ by some local growers in the three study sites.