Expansion of the area of occurrence of Zaprionus tuberculatus (Diptera: Drosophilidae) in the Americas and registration of new host plants

The Afrotropical species Zaprionus tuberculatus Malloch. 1932, known as vinegar or pomace fly, is a species of Afrotropical origin (Yassin, 2008) that colonized Europe (Yassin and David, 2010; Chireceanu et al., 2015; Raspi et al., 2014, Ebejer, 2015), Asia (Yassin and David, 2010; Patlar et al., 2012) and recently the Americas (Cavalcanti et al., 2021). The species has been recorded in three units of the federation in Brazil: the Federal District (Cavalcanti et al., 2021), São Paulo state (Mateus and Machado, 2022; Montes and Vilela, 2022), and Rio de Janeiro state (Faria and Bitner-Mathé, 2023) collected by traps baited with fermented banana. Its presence raises the concern that its behavior is similar to that of other invasive drosophilids such as Zaprionus indianus Gupta, 1970 (Vieira et al., 2019) and Drosophila suzukii (Matsumura, 1931) (Garcia et al., 2022).

It is believed that exotic drosophilids, with geographical origins from different continents, probably reach new territories through passive diffusion, that is, the transport of fruits that were visually healthy but infested with insect eggs (Newbold et al., 2018, Garcia 2020a). These exotic drosophilid species represent a potential risk for biodiversity conservation, as they may outcompete native species and cause long-term environmental imbalances (Simberloff et al., 2013). In addition, many of these exotic drosophilids are generalist species that explore efficiently a wide range of native and exotic host plants (Valadão et al., 2019). Therefore, their impacts can be environmental, economic, and social, given that some invasive drosophilids cause a reduction in production, increase in control costs, and make it difficult to export fruits, mainly to Europe and the United States (Garcia, 2020b; Garcia et al., 2022).

Zaprionustuberculatus has been already recorded breeding on 49 species of 11 families of host plants (EPPO, 2023). Knowledge of preferred and alternative host plants of invasive species with potential for pest status is essential for the development of integrated pest management programs in an Area Wide approach (Lee et al., 2015; Garcia, 2020b). This work aims to record the expansion of the area of occurrence of Z. tuberculatus and new records of host plants.

Fruits were randomly collected from Vitis labrusca Linnaeus cv Isabel (Vitaceae) (31º 35' 54"S and 52º 28' 28"W) located in the rural area, and fruits from the urban area (Butia capitata (Mart.) Becc., 1916 (Arecaceae); Eugenia uniflora Linnaeus, 1753 (Myrtaceae), both (31º 45' 40"S and 52º 19' 51"W), and fruits from Psidium cattleianum Sabine, 1821 (Myrtaceae) (31º 45' 42"S and 52º 19' 52"W), all sampling were conducted in Pelotas, Rio Grande do Sul, Brazil, during January 2022 to February, 2023.

Each fruit was weighed and placed in a plastic bottle containing two centimeters of extra fine vermiculite. The opening of the container was covered with a transparent fabric of the “voile” type. The containers were kept under controlled conditions (25 ± 3°C, 70 ± 10% RH, and 12 h photophase). After seven days, experimental observation was carried out, sucking (removing) the emerged insects and placing them in a 2 mL Eppendorf tube with 70% alcohol for later identification of the species. Fruits of E. uniflora were also evaluated, but in a smaller quantity than the others, so the methodology was modified, packing all the fruits collectively in the same container until the emergence of the insects. Zaprionus tuberculatus specimens were identified based on the diagnostic characteristics provided by Cavalcanti et al. (2021).

The infestation indexes were calculated in two ways: (1) by dividing the total number of flies obtained by the number of fruits in the sample (flies/fruit); or (2) by dividing the total number of flies by the total mass (kg) of fruits in the sample (flies/kg) (Garcia and Norrbom, 2011).

The first detection of Z. tuberculatus (Figure 1) occurred in January 2023. In the urban area of the city of Pelotas, it was recorded breeding in B. capitata, E. uniflora, and P. cattleianum; and in a preserved rural area, it was found infesting grape berries (V. labrusca cv Isabel). This information demonstrates that the invasion of this species is recent in the region.

Figure 1
Dorsal view of adult Zaprionus tuberculatus (A); Lateral view of adult Zaprionus tuberculatus (B) and characteristic tubercle of the species on the first pair of legs (C).

In percentage terms, the fruits most infested by Z. tuberculatus were B. capitata (69.7%), V. labrusca L. (25.5%), and P. cattleianum (7.5%). The highest infestation rates related to the number of emerged flies per biomass were found in B. capitata (383 adults per kg), V. labrusca (429 adults per kg), and P. cattleianum (429 adults per kg) (Table 1).

Table 1
Plants sampled with their respective number of fruits sampled (n), weight, abundance of Zaprionus tuberculatus average number of Z. tuberculatus specimens per fruit, and average number of flies Z. tuberculatus per kg.

Hosts plants	n	Weight	Abundance	Flies per fruit	Flies per kg
Butia capitata (Mart.) Becc., 1916 (Arecaceae)	99	572.06	219	3.17	383
Eugenia uniflora L., 1753 (Myrtaceae)	50	*	4*	*	*
Psidium cattleianum Sabine, 1821 (Myrtaceae)	94	23.31	10	1.42	429
Vitis labrusca L. cv Isabel (Vitaceae)	47	32.61	14	1.16	429
Total	290	627.98	247	5.75	416

• ^*
  Values not quantified.

The number of host plants for Z. tuberculatus must be greater than that reported in the literature (EPPO, 2023) because the insects have been detected using traps in most published works, which makes it impossible to accurately associate with the hosts. The four host plants recorded in this work are new world records. Therefore, we suggest that the methodology used in our work should be used in future research aiming at the proper association of Z. tuberculatus with its hosts.

This record represents the southernmost occurrence of Z. tuberculatus in the Americas, given that the closest point is 1421 km away, which is fundamental for the construction of future studies of population dispersion, and models of potential and niche distribution and to serve as a subsidy for future pest management programs.

Acknowledgements

To Brazilian National Council for Scientific and Technological Development (CNPq) (Grant 311896/2021-9) for the FRMG research productivity scholarship, the PLK scientific initiation scholarship, and research funding (Grant 408479/2021-3). To Federal District Research Support Foundation (FAPDF) (Grant 00193-00001737/2022-15) for funding the research. Coordination for the Improvement of Higher Education Personnel (CAPES) (Finance Code 001) for KJ's doctoral scholarship. To Dr. Edison Zefa for taking the insect photos.

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Publication Dates

• Publication in this collection
  28 Aug 2023
• Date of issue
  2023

History

• Received
  14 Apr 2023
• Accepted
  10 July 2023