The international trade of mangosteen facilitates the spread of non‐native ants and their hemipteran mutualists

Dear Editor, Human-mediated trade activities serve as a critical vector for the successful “stowaway” of non-native species. With the intensification of global trade activities, the number of invasive taxa is projected to rise further, while reaching new regions (Seebens et al., 2015, 2018). Ants represent the most ecologically successful and diverse social insect group, using a wide range of habitats and engaging in a multitude of mutualistic interactions with various species of plants and animals (Parker & Kronauer, 2021). Among their key mutualistic partners are sap-feeding hemipterans, which have driven ants' evolutionary success and ecological dominance (Nelson & Mooney, 2022) while exerting broad impacts on the ecosystems they inhabit (Styrsky & Eubanks, 2007). Over 520 ant species have spread outside their native range (Wong et al., 2023), many developing mutualistic interactions with both native and introduced honeydew-producing Hemiptera within invaded ranges (Xu et al., 2022). These mutualistic interactions support ants’ ecological success and fuel large populations which can then impact invaded ecosystems (Helms & Vinson, 2002; O'Dowd et al., 2003; Wilder et al., 2011; Lee & Yang, 2022; Nelson & Mooney, 2022). Sap-feeding hemipterans, such as scale insects, are highly diverse and widely distributed worldwide, their characteristics as plant parasites have serious impacts on their host plants and even the broader ecosystem (Ryan et al., 2014; Neumann et al., 2016). In some of these invasions, an “invasional meltdown” has been demonstrated (Sun et al., 2024) where multiple species invading the same ecosystem mutually amplify the invasion processes, exacerbating negative impacts on native communities. More importantly, in invaded areas, scale insects and non-native ants may more commonly form mutualistic relationships to facilitate each other's invasion (Zhou et al., 2012). Consequently, mutualistic partners of invasive ant species warrant attention of equal importance as the invasive species themselves. In most cases, both ants and honeydew-producing Hemiptera are introduced accidentally through the transport of soil, plants or fruits and vegetables (Wong et al., 2023), although it is unclear if those are introduced independently or simultaneously. The “Queen of Fruits”—mangosteen (Garcinia mangostana L.)—is a tropical evergreen tree species native to countries such as Malaysia, Thailand, and Indonesia, and renowned for its significant economic value and bioactive compounds with medicinal properties. The fruits also host scale insects such as Aspidiotus destructor and Aonidiella orientalis (Mani, 2022). Given the tight mutualistic relationship between ants and scale insects, we hypothesize that ants may also exhibit close associations with mangosteens, particularly as their sepal structures provide natural shelters for nesting. In this note, we report that the increase in international trade of mangosteens may provide new opportunities for the spread of both ants and Hemiptera. Indeed, the concealed structure of mangosteens’ sepals (a natural nesting site) provide cryptic habitats for numerous non-native ant and Hemiptera species to evade quarantine measures and achieve successful stow away. Over the course of a survey in Hong Kong supermarkets, encompassing five batches (each batch included three randomly selected supermarkets, which remained fixed for subsequent surveys) of approximately one hundred mangosteens each (totaling over 500 fruits), a total of five ant species were identified. This included the invasive species: Dolichoderus thoracicus (Smith, F., 1860) (occurrence proportion on all mangosteens with ants, > 80%); two non-native ant Crematogaster species: Crematogaster fritzi Emery, 1901, known from Malaysia and Indonesia (< 2%), Physocrema sp., a Southeast Asian subgenus unknown from China except for Yunnan province (< 2%); two native ant species: Technomyrmex elatior Forel, 1902 (< 10%), and Technomyrmex albipes (Smith, F., 1861) (< 5%). Additionally, two invasive scale insect species Pseudococcus baliteus, Exallomochlus hispidus and another species belong to the Phenacoccus genus were identified (the ratio of the three scale insects is 12.5% : 37.5% : 50.0%). In all surveyed mangosteens, the incidence of ant existing was approximately 30% (exceeding 40% for those with complete sepals). In addition, both ant larvae (> 30%) and reproductives (< 5%) were observed, suggesting that the transported species have the possibility of establishing nests. The interaction rate between ants and scale insects was very low, with an average of five mangosteens out of every 100 containing ants found to have scale insects present. Among these, only two ant species were observed to interact with scale insects; D. thoracicus interacting with all three scale insect species, while T. albipes only interacted with Phenacoccus sp. These findings highlight the tangible reality of co-dispersal of mutualistic species through transnational or cross-regional transportation of mangosteens. Whether this easily overlooked dispersal mechanism facilitates their colonization in new regions and impacts native species remains unknown. Due to the harm it causes to the ecosystems in Taiwan, China, D. thoracicus has been confirmed as an invasive pest (Chen et al., 2025). Within Southeast Asia, Rahardjo et al. (2023) reported a close mutualistic association between members of the genus Phenacoccus and D. thoracicus, and Saleh & Ahmad (2020) observed the symbiotic relationship between D. thoracicus and E. hispidus on the mangosteen, which aligns with our findings. In our results, D. thoracicus emerged as the dominant ant species on mangosteen, exhibiting the highest frequency and interaction with scale insects (Fig. 1). It is worth noting that, although there are currently no reports on the interaction between P. baliteus and ants, it is listed as a quarantine pest for the import of durian from Thailand and mangosteen from Indonesia and has been designated as a quarantine pest not only in China and Southeast Asia, but also in countries including Japan and the United States (Zhao et al., 2023). Therefore, D. thoracicus nesting within the sepals of mangosteen may serve as a primary protective vector for the introduction and establishment of more invasive scale insects. Various countries and regions have stringent quarantine systems for invasive species. Whether dealing with independent ant invasions or independent scale insect invasions, they generally face stricter quarantine measures. On one hand, when these invasive species disperse independently, their populations may be larger and remain in transit for longer periods, making detection more likely. On the other hand, fruit trade typically undergoes shorter inspection times, and aside from obvious pests or diseases on the fruit surface, those concealed in less visible areas of the fruit, such as the calyx or within the pulp are harder to detect. This synergistic dispersal undoubtedly poses greater challenges for biological control, necessitating further strengthening of quarantine efforts and improving relevant policies. Our findings provide evidence that ants may serve as critical vectors for scale insect dispersal. Additionally, while our sampling effort remains modest, the survey documents for the first time the dispersal of C. fritzi and of a species of the Crematogaster subgenus Physocrema, both introduced outside of their native range. To the best of our knowledge, no introduced record of a species of the subgenus Physocrema, which includes twelve species had been recorded previously outside of South-East Asia (Hosoishi & Ogata, 2009; Hosoishi et al., 2023). However, no mutualistic interactions between invasive scale insects and Physocrema sp., C. fritzi, T. albipes, or T. elatior have been reported to date, nor did we observe close associations between these ants and scale insects in mangosteens. Notably, our randomized survey results likely underestimate the true extent of invasive species introductions, as additional alien species and their symbiotic partners hitchhiking on mangosteens may remain undetected. This underscores the need for intensified efforts to prevent the introduction of invasive species, particularly in economically significant crops that are often overlooked, or in regions with insufficient biosecurity measures. Indeed, our results confirm the role of Hong Kong as a major stepping-stone in the introduction of exotic species to mainland China (Lu et al., 2018). Other instances of invasive ant species introduced with mangosteen exist, such as in the case of Solenopsis geminata imported from Thailand to South Korea in 2006 (Lee et al., 2008). In addition, observations of introduced ants and other insects on fruit stall have been made in other regions as well. For instance, in the mid-2000s, one of the authors (BG) observed ants (e.g., species of Dolichoderus, Technomyrmex, Monomorium), Hemiptera and other insects (beetles) on fruits within Asian markets in Montréal (Canada), including during wintertime. Similarly, in the European Union region with a substantial volume of fruit imports, invasive insects have been found on fruits causing significant damage (Asplen et al., 2015). These indicate that specific biosecurity measures and inspections are needed at both the origin and the destination points to prevent such introductions from occurring to limit the potential establishment of insects through plant material either used for consumption (e.g., fruits and vegetables), construction (e.g., bamboo) or ornamental (e.g., horticulture) purposes. Thanks for the funding provided by the National Natural Science Foundation of China (32261160374), and thanks Dr. Xinyi Zheng for identifying the scale insect specimens. The authors declare that they have no conflict of interests.

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