Introduction
Leaf-footed bugs (Hemiptera: Coreidae), shield bugs (Hem: Acanthosomatidae), and stink bugs (Hem: Pentatomidae) are often phytophagous, polyphagous, and feed on cultivated, wild, and ornamental plants (Jones and Sullivan, Reference Jones and Sullivan1982; Kriticos et al., Reference Kriticos, Kean, Phillips, Senay, Acosta and Haye2017; Panizzi, Reference Panizzi2015). Some of them are pests that can cause significant crop damage and contribute to agricultural losses worldwide (Leskey and Nielsen, Reference Leskey and Nielsen2018; Panizzi, Reference Panizzi1997; Schaefer and Panizzi, Reference Schaefer and Panizzi2000). Understanding the factors influencing pest population dynamics is essential for targeting efficient and environmentally friendly pest management strategies. These strategies typically focus on the local field level; however, these bugs are generally highly mobile and use various habitat types throughout their life cycle (Tillman et al., Reference Tillman, Cottrell and Grabarczyk2022; Venugopal et al., Reference Venugopal, Coffey, Dively and Lamp2014).
South Tyrol, a mountain region located in northeastern Italy, is known for its diverse habitats and unique ecosystems (Kuttner et al., Reference Kuttner, Essl, Peterseil, Dullinger, Rabitsch, Schindler, Hübler, Gattringer and Moser2015). In this mountainous region, rich in woods, apple production (about 18,400 ha) covers the main valleys up to 1,100 m a.s.l. (Fischnaller et al., Reference Fischnaller, Rottensteiner, Graf, Ladurner, Schmidt, Unterthurner, Zelger and Wolf2022). In the context of apple production, most stink bugs can inflict damage to apple trees by piercing the fruit and sucking out plant fluids, leading to deformities and reduced fruit quality (Brown and Short, Reference Brown and Short2010). This results in significant economic losses for apple farmers and affect overall apple yields (Nielsen and Hamilton, Reference Nielsen and Hamilton2009). The situation worsened even more after the arrival of the brown marmorated stink bug Halyomorpha halys (Stål) (Hem.: Pentatomidae) in 2016 (Fischnaller et al., Reference Fischnaller, Rottensteiner, Graf, Ladurner, Schmidt, Unterthurner, Zelger and Wolf2022). Therefore, efforts have been made to monitor and study this pest, as well as other true bugs whose occurrence in this region appear to have increased in recent years not only in cultivated areas but also in urban areas (Zapponi et al., Reference Zapponi, Bon, Fouani, Anfora, Schmidt and Falagiarda2020).
The great diversity in environments, microclimates, and host plants in South Tyrol has an influence on the species composition of both true bugs and their egg parasitoids (Hymenoptera) (Falagiarda et al., Reference Falagiarda, Carnio, Chiesa, Pignalosa, Anfora, Angeli, Ioriatti, Mazzoni, Schmidt and Zapponi2023; Zapponi et al., Reference Zapponi, Bon, Fouani, Anfora, Schmidt and Falagiarda2020). In these environments, the presence of woodlands and inhabited areas bordering crops provides a wide variety of both wild and ornamental non-crop hosts for true bugs. It is known that these insects can move within and between crop and non-crop habitats throughout the season, depending on the suitability of host plants and food availability (Tillman et al., Reference Tillman, Cottrell, Mizell and Kramer2014). For instance, Venugopal et al. (Reference Venugopal, Coffey, Dively and Lamp2014) observed thatadjacent wooded, crop, and building habitats influenced the density of stink bugs in corn and soybean fields, with higher densities found at field edges. Moreover, specific wild plant species in woodlands could serve as a source of stink bugs dispersed into adjacent crops (Tillman, Reference Tillman2016).
In line with habitat type, elevation also represents a critical factor influencing various aspects of insect ecology, from species distribution and richness, to their abundance, biology, and behaviour, as well as interactions with plants and natural enemies, as evidenced by numerous studies (Corcos et al., Reference Corcos, Cerretti, Mei, Vigna Taglianti, Paniccia, Santoiemma, De Biase and Marini2018; Hodkinson, Reference Hodkinson2005; Kozlov et al., Reference Kozlov, Zverev and Zvereva2022). Moreover, climate change and rising temperatures in mountain regions will impact insect physiology and fitness, causing shifts in population distribution and composition of several insect species (Shah et al., Reference Shah, Dillon, Hotaling and Woods2020). Many mountain insects are already shifting to higher elevations (McCain and Garfinkel, Reference McCain and Garfinkel2021). Climate change scenarios predict altitudinal range expansion also for H. halys (Stoeckli et al., Reference Stoeckli, Felber and Haye2020). Other stink bug species, such as the coffee stink bug Antestiopsis thunbergii (Gmelin) (Hem.: Pentatomidae), already show higher population density at higher elevations due to immature stage susceptibility to extreme temperatures at lower altitudes (Azrag et al., Reference Azrag, Pirk, Yusuf, Pinard, Niassy, Mosomtai and Babin2018). Knowledge of variation in communities of true bug and their egg parasitoids as altitude changes could serve as a starting point for future investigations to track changes in species composition, distribution, and interactions in response to climate change.
Understanding the natural biological control of true bugs in different habitats is necessary for the development of effective management strategies. Egg parasitoids are among the main natural enemies of true bugs, which, in some cases, can reach high levels of parasitism, contributing to the regulation of bug populations (Koppel et al., Reference Koppel, Herbert, Kuhar and Kamminga2009; Maltese et al., Reference Maltese, Caleca, Guerrieri and Strong2012; Paz‐Neto et al., Reference Paz‐Neto, Querino and Margaría2015). Research on parasitism has predominantly focused on agricultural systems, while investigations across other habitat types remain limited. Because stink bugs, such as H. halys, use urban structures for overwintering (Hancock et al., Reference Hancock, Lee, Bergh, Morrison and Leskey2018; Lee and Leskey, Reference Lee and Leskey2015), urban habitats were included in a large-scale monitoring programme of this pest’s parasitoids in 2019 (Zapponi et al., Reference Zapponi, Tortorici, Anfora, Bardella, Bariselli, Benvenuto, Bernardinelli, Butturini, Caruso, Colla, Costi, Culatti, Di Bella, Falagiarda, Giovannini, Haye, Maistrello, Malossini, Marazzi, Marianelli, Mele, Michelon, Moraglio, Pozzebon, Preti, Salvetti, Scaccini, Schmidt, Szalatnay, Roversi, Tavella, Tommasini, Vaccari, Zandigiacomo and Sabbatini-Peverieri2021). Interestingly, these environments hosted high numbers of parasitised egg masses on ornamental trees in gardens, parks, parking lots, and streets. Another study showed a higher presence of H. halys egg masses in urban areas than in apple orchards, and different patterns in parasitoid species distribution in these two habitats (Zapponi et al., Reference Zapponi, Bon, Fouani, Anfora, Schmidt and Falagiarda2020). In fact, parasitoids can also disperse from woodlands to crops, and the extent of their dispersal is influenced by factors such as the presence of alternative flowering hosts (Tillman, Reference Tillman2016, Reference Tillman2017). For instance, Anastatus sp. (Hym.: Eupelmidae) parasitises the egg masses of Euschistos servus (Say) (Hem.: Pentatomidae) in corn crops, because of its proximity to a woodland habitat, where the parasitoid was mainly found on woody trees parasitising Chinavia hilaris (Say) eggs (Tillman, Reference Tillman2016).
In South Tyrol, monitoring of parasitoid species attacking H. halys and indigenous bugs resulted in the discovery of two exotic parasitoids: Trissolcus japonicus (Ashmead) and Trissolcus mitsukurii (Ashmead) (Hym.: Scelionidae) (Scaccini et al., Reference Scaccini, Falagiarda, Tortorici, Martinez-Sañudo, Tirello, Reyes-Domínguez, Gallmetzer, Tavella, Zandigiacomo, Duso and Pozzebon2020; Zapponi et al., Reference Zapponi, Bon, Fouani, Anfora, Schmidt and Falagiarda2020). Moreover, starting from 2020, releases of T. japonicus were performed according to a national programme of classical biological control of H. halys (MATTM, 2020). Since then, this parasitoid has spread and established in several areas of northern Italy, showing a promising impact as biocontrol agent against the target host (Falagiarda et al., Reference Falagiarda, Carnio, Chiesa, Pignalosa, Anfora, Angeli, Ioriatti, Mazzoni, Schmidt and Zapponi2023). However, it is still too early to estimate its long-term regulating efficacy and non-target effects.
Despite existing knowledge, comprehensive studies on the distribution of true bugs and their egg parasitoids in a mountain agro-ecosystem are still lacking. As mentioned above, habitats located at different altitudes can offer various resources for insects (Hodkinson, Reference Hodkinson2005). Perennial crops can support stink bug populations by providing host plants during late spring and summer, while forests and urban areas are expected to primarily serve as overwintering sites, and provide alternative host plants and suitable environments for reproduction and development (Panizzi, Reference Panizzi1997). Therefore, this study aimed to understand the influence of habitat type and altitude on true bug and parasitoid species composition. Two-year field surveys were carried out to assess species abundance and diversity across three distinct habitats within the study region – perennial crops (i.e., apple orchards), urban areas, and forests – covering an elevation gradient from 200 to 1000 m a.s.l.
Materials and methods
Study sites
Surveys were conducted over the 2-year period 2022–2023 in 27 sites in South Tyrol, selected across three different habitat types, including apple orchards, forest margins, and urban areas. These sites were located within distinct altitude ranges, spanning from 200 to 500 m, 501 to 800 m, and above 801 m a.s.l. (fig. 1, Supplementary Table 1). In total, three sites were monitored for each habitat in a specific altitude range. The surveyed apple orchards were managed according to integrated pest management guidelines (Beratungsring, Reference Beratungsring2022), except for the site 19, which was an organically managed apple orchard. The study sites were not involved in the T. japonicus release programme implemented in Italy starting in 2020.
Figure 1. Study area location showing the distribution of the survey points, according to habitat type and altitude.
Bug sampling and identification
In each site, monthly surveys were performed starting from early April, and extending through September in both 2022 and 2023, so as to capture seasonal variations in true bug populations. As in similar studies (e.g., Kawatsu et al., Reference Kawatsu, Ushio, van Veen and Kondoh2021; Majeed et al., Reference Majeed, Khawaja, Rana, de Azevedo Koch, Naseem and Nargis2022), sampling was conducted on a monthly basis as it could identify major seasonal trends and allow consistent comparisons between sites during the growing season. In the surveyed sites, true bug populations were monitored in an area with a radius of approximately 50 m using two methods: beat sheet and direct observation through visual inspection of host plants. Surveys were performed in the morning between 8 and 11 in all sites, to avoid high temperatures that usually make the insects more active and therefore more difficult to detect during sampling.
Plant species on which true bugs were monitored included shrubs and trees and changed from site to site, and even within the same site during the season. In both urban and woodland settings, beat sheet samples were taken on six different plant species with 15 beats per species, for a total of 90 beats per survey and site. In apple orchards, a total of 45 beats were carried out on three apple plants (15 per plant), changing rows in the successive samples. The beat sheet had an opening in the middle to which a plastic bag was attached to directly collect the insects. Plastic bags with samples were labelled and transported to the laboratory, where they were kept in a freezer at −30°C.
Visual inspection of vegetation was conducted for 1 person-hour per survey and site, at a standardised height of approximately 1.5 m. Bug species and their developmental stages were recorded on site in case of the most common species. Only the least common species, or those of uncertain identification, were collected and brought to the laboratory.
In the laboratory, the field collected bugs were examined using a stereomicroscope and morphologically identified following the keys in Derjanschi and Péricart (Reference Derjanschi and Péricart2005), Péricart (Reference Péricart2010), Ribes and Pagola-Carte (Reference Ribes and Pagola-Carte2013), and Tamanini (Reference Tamanini1989).
Egg collection and parasitoid identification
Egg sampling was performed by collecting all egg masses or single eggs observed by visual inspection during the surveys. Field collected egg masses and single eggs were placed in plastic Petri dishes (Ø 90 mm), labelled, brought to the laboratory, and held in a climatic chamber at 25 ± 1°C and 60 ± 5% relative humidity for emergence of bug nymphs or adult parasitoids. All egg masses and eggs were examined using a stereomicroscope and identified to the species or family level according to Derjanschi and Péricart (Reference Derjanschi and Péricart2005), Péricart (Reference Péricart2010), and Ribes and Pagola-Carte (Reference Ribes and Pagola-Carte2013). Three to four weeks after collection, all eggs were categorised as hatched, unhatched, predated, or parasitised. Parasitoids emerged from true bug egg masses were stored in 1.5-mL Eppendorf® (Eppendorf SE, Germany) tubes with 70% ethanol. Hymenoptera specimens were morphologically identified under a stereomicroscope by using taxonomic keys provided by Moraglio et al. (Reference Moraglio, Tortorici, Visentin, Pansa and Tavella2021a), Talamas et al. (Reference Talamas, Johnson and Buffington2015, Reference Talamas, Buffington and Hoelmer2017), and Tortorici et al. (Reference Tortorici, Talamas, Moraglio, Pansa, Asadi-Farfar, Tavella and Caleca2019) for genus Trissolcus Ashmead, Tortorici et al. (Reference Tortorici, Orrù, Timokhov, Bout, Bon, Tavella and Talamas2024) for genus Telenomus Haliday, and Kononova and Kozlov (Reference Kononova and Kozlov2008) for genus Hadronotus Förster for Scelionidae, Askew and Nieves-Aldrey (Reference Askew and Nieves-Aldrey2004) and Peng et al. (Reference Peng, Gibson, Tang and Xiang2020) for Eupelmidae, Sabbatini-Peverieri et al. (Reference Sabbatini-Peverieri, Mitroiu, Bon, Balusu, Benvenuto, Bernardinelli, Fadamiro, Falagiarda, Fusu, Grove, Haye, Hoelmer, Lemke, Malossini, Marianelli, Moore, Pozzebon, Roversi, Scaccini, Shrewsbury, Tillman, Tirello, Waterworth and Talamas2019) for genus Acroclisoides Girault and Dodd, and Graham (Reference Graham1991) for Eulophidae.
All specimens used for morphological analysis were deposited in the Laimburg Research Centre, Institute for Plant Health, Laimburg, Italy, and Dipartimento di Scienze Agrarie, Forestali e Alimentari (DISAFA), University of Torino, Italy.
Data analysis
All analyses were performed using R software version 4.3.1 (R Core Team, 2023). The two sampling methods, beat sheet and visual inspection, were compared by Mann–Whitney–Wilcoxon test to assess if the number of individuals recorded during surveys was influenced by the monitoring method. For the comparison, raw data points from all dates and sites were aggregated into a unified dataset, with each observation representing an individual count from either beat sheet or visual inspection method. This approach allowed a direct comparison of the relative efficiency of each method across the entire study period and area, rather than comparing method performance at specific spatiotemporal points. As the two methods did not show any significant difference in the number of individuals counted (W = 19,217, p = 0.091), data were processed jointly for further analyses. To compare the composition of true bug assemblies according to habitat and altitude, permutation multivariate analysis of variance (PERMANOVA) was performed, using the adonis2 function from the vegan package (Anderson, Reference Anderson2014). Principal Coordinate Analysis (PCoA) based on Bray-Curtis dissimilarity was applied to visualise the relationship between the variables. To identify the predominant species in each habitat and altitude range, rank-abundance curves were used. This involved ranking species based on their relative abundance, calculated as the total number of individuals collected divided by the overall number of individuals. The analysis used the rankabundance function from the Biodiversity R package (Kindt and Coe, Reference Kindt and Coe2005). Linear regression was conducted to characterise the associations between altitude and the occurrence of stink bugs, focusing on the three prevalent species. Egg fate was calculated for each bug species as the percentage of hatched, unhatched, predated, and parasitised eggs.
Results
True bug species richness and diversity
A total of 1,239 true bug adults and nymphs belonging to three families were recorded during the survey period, among which 25 species were identified (table 1). In the superfamily Pentatomoidea, 3 species were found in the family Acanthosomatidae and 18 species in the family Pentatomidae, while in the superfamily Coreoidea 4 species belonging to the family Coreidae were collected. Notably, more phytophagous species (24 in total) were identified, in stark contrast to the only predatory species, Arma custos (F.) (Hem.: Pentatomidae).
Table 1. Species richness, abundance, and individuals of Acanthosomatidae, Coreidae, and Pentatomidae collected according to habitat types and altitude ranges
Unless otherwise specified, abundance values refer to the total number of individuals collected in both sampling years and at all sites within the same habitat type or altitudinal range. Maximum relative abundance was found in urban areas (753 individuals), followed by forests (426) and orchards (60). Based on altitude range, the highest abundance was found between 501 and 800 m a.s.l. (527 individuals), while 371 and 341 individuals were recorded at higher and lower elevations, respectively. In urban areas and forests, 21 species were recorded, whereas only nine species were found in orchards. Six species were singletons. PERMANOVA results showed a significant influence of both habitat and altitude on species composition, and also the interaction of the two variables had an impact on species diversity and abundance (table 2). The PCoA plots obtained with the presence/absence data showed a clear distinction in the sorting space of the different habitats and the altitude ranges (fig. 2A, B).
Figure 2. Ordination diagrams (PCoA) of the 27 sites based on site-to-site dissimilarity measures used in this study. The measures represent site-to-site dissimilarities in species composition according to habitat type (A) and altitude (B), respectively.
Table 2. PERMANOVA results for habitat type and altitude range influencing true bug species composition
Rank abundance curves for habitat type and altitude range showed that the most abundant species above 801 m and in woodland habitats was Pentatoma rufipes (L.) (Hem.: Pentatomidae), followed in both cases by Palomena prasina (L.) (Hem.: Pentatomidae). At lower altitudes and in urban areas and orchards, the predominant species was the invasive H. halys (fig. 3). In fact, altitude was found to be negatively correlated with H. halys abundance (r = −0.44; R 2 = 0.19; p = 0.024), while it was positively correlated with P. rufipes abundance (r = 0.49; R 2 = 0.24; p = 0.010). Moreover, altitude was not significantly correlated with P. prasina abundance (r = 0.26; R 2 = 0.07; p = 0.183) (fig. 4).
Figure 3. Rank abundance curves of true bug species collected in the surveyed sites in 2022 and 2023, according to habitat type (A) and altitude (B). Species names are shown for the first five species.
Figure 4. Correlation between altitude and number of individuals of the three main stink bug species found in South Tyrol, Halyomorpha halys (A), Pentatoma rufipes (B), and Palomena prasina (C).
True bug egg fate and associated parasitoid species
Across years and sites, a total of 270 egg masses plus 43 single eggs were collected for a total of 6,626 eggs of 10 true bug species (table 3, Supplementary Table 2). Almost 80% of the collected egg masses belonged to the three most representative species for South Tyrol, H. halys, P. rufipes, and P. prasina. Egg fate varied greatly by species. For instance, the hatching rate for H. halys eggs exceeded 56%, while for the native P. rufipes and P. prasina it reached 41% and 31%, respectively. Furthermore, eggs of these two species recorded parasitism rates of almost 50%, while H. halys parasitism only reached 28.5%. For all species, predation rates were negligible.
Table 3. Fate of true bug egg masses and eggs in the surveyed sites in 2022 and 2023
Twelve species of parasitoids, including nine scelionids, one eupelmid, one pteromalid, and one eulophid, parasitised naturally occurring egg masses of true bugs (table 4). Trissolcus japonicus was the prevalent species in urban areas and mainly emerged from H. halys eggs. It was only sporadically found emerging from eggs of native bug species, mainly from Rhaphigaster nebulosa (Poda) and P. prasina, and rarely from Acrosternum heegeri (Fieber), Nezara viridula (L.), and P. rufipes. Trissolcus cultratus (Mayr) was mainly associated with P. rufipes in forests and urban areas, while Telenomus truncatus (Nees von Esenbeck) and Telenomus turesis Walker (Hym.: Scelionidae) emerged from P. prasina eggs in each of the three habitats, including apple orchards. Other scelionids, such as Trissolcus kozlovi (Rjachovskij), Trissolcus semistriatus (Nees von Esenbeck), and Trissolcus belenus (Walker), rarely emerged from P. rufipes and P. prasina eggs. Hadronotus muscaeformis (Nees von Esenbeck) and Trissolcus elasmuchae (Watanabe) specifically emerged from Coreidae spp. and Elasmucha grisea (L.) eggs, respectively. In forests, the generalist Anastatus bifasciatus (Geoffroy) (Hym.: Eupelmidae) was the most frequent parasitoid species and parasitised eggs of several bug species. The hyperparasitoid Acroclisoides sinicus (Huang and Liao) (Hym.: Pteromalidae) was found in both forests and urban areas, and emerged from egg masses of four stink bug species. Four individuals of Baryscapus oophagus (Otten) (Hym.: Eulophidae) emerged from a H. halys egg mass in one urban habitat.
Table 4. Egg parasitoid species emerged from true bug eggs collected in the surveyed sites in 2022 and 2023
a Hh, Halyomorpha halys; Pp, Palomena prasina; Pr, Pentatoma rufipes; Rn, Rhaphigaster nebulosa; Ah, Acrosternum heegeri; Nv, Nezara viridula; Eg, Elasmucha grisea; Ac, Arma custos; C. sp., Coreidae sp.
* These species are recorded for the first time in South Tyrol.
Parasitism of H. halys eggs in urban areas reached almost 40%, while the percentage was highly reduced in orchards and woodlands (fig. 5). Eggs of the native P. rufipes and P. prasina showed high parasitism rates in both urban areas and forests, and the number of parasitised eggs of P. prasina also exceeded 30% in apple orchards. Predation was negligible in urban environments, while it reached 15% of H. halys eggs in forests and 20% of P. prasina eggs in orchards. In relation to altitudinal range, parasitoid activity appeared to be more strongly associated with host egg availability than with altitude. Higher parasitism rates generally corresponded to areas of higher egg abundance, consequently below 800 m for H. halys, and above 800 m for P. prasina and P. rufipes.
Discussion
In the 2-year field survey, 25 true bug species belonging to three families, almost all of them phytophagous, were collected. The species composition, with distinct patterns observed in PCoA plots, was significantly influenced by habitat type and altitude. The invasive H. halys, and the native P. rufipes and P. prasina were the three most common species. Among them, P. rufipes is commonly found in many parts of the Palaearctic region, and it is particularly associated with deciduous trees. Also known as forest bug, it can be found in woodlands all year-round, feeding on various species, including oak, beech, and hazel (Powell, Reference Powell2020). Palomena prasina has a broad distribution across the Eurosiberian region and is considered a harmful hazelnut pest in many regions (Driss et al., Reference Driss, Hamidi, Andalo and Magro2024; Hamidi et al., Reference Hamidi, Calvy, Valentie, Driss, Guignet, Thomas and Tavella2022). These two species were the most common in forests, and P. rufipes was also the prevalent species found in urban settlements above 800 m. The presence of this species at high elevations, up to 1500 m, has already been observed in the Italian and Austrian Alps (Alma et al., Reference Alma, Bocca, Čermak, Chen, D’Urso, Exnerová, Goula, Guglielmino, Kunz, Lauterer, Malenovsky, Mazzoglio, Nicoli Aldini, Ouvrard, Remane, Rintala, Seljak, Söderman, Soulier-Perkins, Štis, Tavella, Tedeschi and Wilson2009; König, Reference König2015). Previous studies recorded populations of P. rufipes in apple and pear orchards in northern Europe, where it is considered as emerging pest of fruit trees (Alkarrat et al., Reference Alkarrat, Kienzle and Zebitz2020; Powell, Reference Powell2020). Nevertheless, no P. rufipes individuals were found in apple orchards in South Tyrol during the surveys.
Similarly, several true bug species found in forest and urban areas were not observed in apple orchards. Certainly, management practices, such as pesticide applications in apple orchards, may negatively affect true bug populations compared to undisturbed woodland sites. Most pentatomid species spend only a third of their lifespan feeding on spring/summer crops, while the rest is devoted to feeding and reproducing on wild hosts or using these plants as overwintering sites (Panizzi, Reference Panizzi1997). This may explain the highest relative abundance of bugs observed in urban areas, followed by forests and orchards. This trend reflects the availability of various plant species, which serve as hosts for several species of Pentatomidae (Holthouse et al., Reference Holthouse, Spears and Alston2021; Palumbo et al., Reference Palumbo, Perring, Millar and Reed2016).
Likewise, the positive correlation between the abundance of the invasive H. halys and urbanised areas is consistent with earlier findings reported in the mid-Atlantic region in the United States (Venugopal et al., Reference Venugopal, Dively, Herbert, Malone, Whalen and Lamp2016; Wallner et al., Reference Wallner, Hamilton, Nielsen, Hahn, Green and Rodriguez-Saona2014). Landscape characteristics are known to influence the distribution and dynamics of H. halys and its natural enemies. Although different studies reported high-density populations of H. halys in agricultural areas adjacent to forests (Acebes-Doria et al., Reference Acebes-Doria, Leskey and Bergh2016; Quinn et al., Reference Quinn, Talamas, Acebes-Doria, Leskey and Bergh2019; Venugopal et al., Reference Venugopal, Coffey, Dively and Lamp2014), this pest shows high abundance in urban areas (Wallner et al., Reference Wallner, Hamilton, Nielsen, Hahn, Green and Rodriguez-Saona2014), probably because its host plants, such as Ailanthus altissima (Mill.) Swingle, Paulownia tomentosa (Thunb.) Steud., Acer spp., and Prunus spp. (Bergmann et al., Reference Bergmann, Venugopal, Martinson, Raupp and Shrewsbury2016; Holthouse et al., Reference Holthouse, Spears and Alston2021), are more prevalent in urban environments, such as parks and hedges, than in forest habitats. Furthermore, urban areas may support higher pest densities not only because of the availability of host plants, but also because of the presence of suitable overwintering structures and stable microclimatic conditions (Bergh et al., Reference Bergh, Morrison, Joseph and Leskey2017; Rice et al., Reference Rice, Troyer, Watrous, Tooker and Fleischer2017). Conversely, agricultural landscapes bordering semi-natural habitats can enhance the activity of natural enemies, particularly egg parasitoids, through spillover effects and the presence of alternative hosts and floral resources (Abram et al., Reference Abram, Mills and Beers2020; Dieckhoff et al., Reference Dieckhoff, Tatman and Hoelmer2017). In our study, however, the high parasitism rate observed in urban areas is likely due to a higher concentration of host eggs in these environments, and a density-dependent response of parasitoids to increased host availability.
Concerning altitude range, the highest abundance of true bugs was observed between 500 and 800 m, where summer mean temperatures range approximately between 15°C and 25°C. Since plant community composition was relatively consistent at the studied sites, all located below 1000 m where substantial vegetation transitions do not typically occur, the observed altitudinal patterns in bug populations can be primarily attributed to climatic factors rather than vegetation changes (Zhao et al., Reference Zhao, Gao, Liu, Liu, Li, Men and Zhang2023). Variations in elevation lead to differences in temperature, which have an impact on the geographic distribution and prevalence of bug species. This phenomenon is attributable to the temperature ranges and tolerances exhibited by different true bug species, especially by egg masses and early juvenile stages (Daane et al., Reference Daane, da Silva, Stahl, Scaccini and Wang2022; Venugopal et al., Reference Venugopal, Dively, Herbert, Malone, Whalen and Lamp2016). For instance, laboratory studies indicate 25°C as H. halys optimal survival and developmental temperature (Haye et al., Reference Haye, Abdallah, Gariepy and Wyniger2014; Nielsen et al., Reference Nielsen, Hamilton and Matadha2008), as well as for N. viridula (Ali and Ewiess, Reference Ali and Ewiess1977; Chanthy et al., Reference Chanthy, Martin, Gunning and Andrew2015). Unfortunately, data on the developmental temperature thresholds for P. rufipes are currently lacking (Powell, Reference Powell2020). Nonetheless, our findings indicate that this species is likely to have lower optimal temperatures compared to the invasive H. halys, as it was mostly found at higher altitudes. Halyomorpha halys was mainly recorded up to 800 m, which is consistent with the current known distribution patterns of this species recorded in Switzerland (Stoeckli et al., Reference Stoeckli, Felber and Haye2020).
Twelve parasitoid species were identified in this study, of which the two Telenomus species, and H. muscaeformis, are recorded for the first time in South Tyrol. Generally, higher levels of parasitism were found in native bug species compared to the invasive H. halys. Notable parasitism rates of P. prasina and P. rufipes eggs in urban and forest habitats indicate effective host-parasitoid interactions for these autochthonous species in the studied environments. The main parasitoids of these two native species belonged to the family Scelionidae: five Trissolcus species, including T. japonicus, and two Telenomus species. Among them, T. kozlovi emerged only from P. rufipes eggs in urban areas above 500 m. Previous studies found this species sporadically parasitising H. halys in the field (Falagiarda et al., Reference Falagiarda, Carnio, Chiesa, Pignalosa, Anfora, Angeli, Ioriatti, Mazzoni, Schmidt and Zapponi2023; Moraglio et al., Reference Moraglio, Tortorici, Giromini, Pansa, Visentin and Tavella2021b; Scaccini et al., Reference Scaccini, Falagiarda, Tortorici, Martinez-Sañudo, Tirello, Reyes-Domínguez, Gallmetzer, Tavella, Zandigiacomo, Duso and Pozzebon2020), and investigated its potential as a biocontrol agent of the pest (Moraglio et al., Reference Moraglio, Tortorici, Visentin, Pansa and Tavella2021a, Reference Moraglio, Tortorici, Giromini, Pansa, Visentin and Tavella2021b). Nevertheless, its limited success as a biocontrol agent could be explained by the different habitat suitability compared to that of H. halys, as suggested by our study.
Trissolcus belenus and T. semistriatus emerged only from P. prasina eggs in our survey, but were recorded parasitising other hosts in previous studies (Falagiarda et al., Reference Falagiarda, Carnio, Chiesa, Pignalosa, Anfora, Angeli, Ioriatti, Mazzoni, Schmidt and Zapponi2023; Moraglio et al., Reference Moraglio, Tortorici, Giromini, Pansa, Visentin and Tavella2021b). Both Telenomus species emerged from P. prasina eggs, consistent with observations from another study (Tortorici et al., Reference Tortorici, Orrù, Timokhov, Bout, Bon, Tavella and Talamas2024). While T. turesis was present in all habitats, T. truncatus was observed only in urban areas, where it also emerged from eggs of Dolycoris baccarum (L.) (Hem.: Pentatomidae), R. nebulosa, and also of the predatory stink bug A. custos. Therefore, while high parasitism rates can be advantageous for the control of potential pests, they are undesirable in the case of predatory arthropods, as they may interfere with the control of other insects (Fei et al., Reference Fei, Gols and Harvey2023). This is precisely the case of A. custos, on which high parasitism was recorded not only in this study, but also by Moraglio et al. (Reference Moraglio, Tortorici, Giromini, Pansa, Visentin and Tavella2021b).
The predatory bug A. custos was parasitised also by the generalist A. bifasciatus. Confirming its wide host range (Stahl et al., Reference Stahl, Babendreier and Haye2018); this parasitoid emerged from the highest number of hosts among true bugs, and was found in all altitude ranges in both urban and forest habitats, and it was even the predominant species in the latter. Previous studies reported a predominance of A. bifasciatus as a parasitoid of bug species in urban and suburban areas (Rot et al., Reference Rot, Maistrello, Costi, Bernardinelli, Malossini, Benvenuto and Trdan2021; Zapponi et al., Reference Zapponi, Bon, Fouani, Anfora, Schmidt and Falagiarda2020). This might be due to higher biodiversity in forests, which represents a source of different hosts (e.g., lepidopterans, other hemipterans) for this parasitoid.
Figure 5. Fate of H. halys (Hh), P. prasina (Pp), and P. rufipes (Pr) eggs: percentage of hatched, unhatched, predated, and parasitised eggs in the three habitats.
In our study, the exotic T. japonicus was prevalent in urban areas where its main host, H. halys, was the predominant species. In this environment, parasitism rates were higher than in the other habitats. This observation is in line with surveys conducted in Slovenia, where the urban areas showed the highest number of H. halys eggs and the highest parasitism rate (Rot et al., Reference Rot, Maistrello, Costi, Bernardinelli, Malossini, Benvenuto and Trdan2021). The high abundance of H. halys in the apple orchard was not related to an equally high abundance of T. japonicus. Indeed, the percentage of hatched eggs was higher in apple orchards than in forest and urban areas. This suggests that pest management practices could have a significant impact on parasitoid development and establishment.
Analysis of parasitism rates at different elevations revealed that parasitoid activity was more strongly associated with host egg availability than with altitude per se. The correspondence of higher parasitism rates with areas of higher egg mass abundance suggests density-dependent parasitism dynamics. Following the distribution patterns of its main host H. halys, T. japonicus was mainly found up to 800 m. According to the geographic distribution model developed by Tortorici et al. (Reference Tortorici, Bombi, Loru, Mele, Moraglio, Scaccini, Pozzebon, Pantaleoni and Tavella2023), the patterns of suitable habitats for T. japonicus across Europe resemble the core areas for H. halys. Several studies reported parasitism of T. japonicus on different pentatomid species (Falagiarda et al., Reference Falagiarda, Carnio, Chiesa, Pignalosa, Anfora, Angeli, Ioriatti, Mazzoni, Schmidt and Zapponi2023; Haye et al., Reference Haye, Moraglio, Tortorici, Marazzi, Gariepy and Tavella2024; Zapponi et al., Reference Zapponi, Tortorici, Anfora, Bardella, Bariselli, Benvenuto, Bernardinelli, Butturini, Caruso, Colla, Costi, Culatti, Di Bella, Falagiarda, Giovannini, Haye, Maistrello, Malossini, Marazzi, Marianelli, Mele, Michelon, Moraglio, Pozzebon, Preti, Salvetti, Scaccini, Schmidt, Szalatnay, Roversi, Tavella, Tommasini, Vaccari, Zandigiacomo and Sabbatini-Peverieri2021), which can be considered both non-target hosts and at the same time support the increase of the parasitoid populations. However, in our study, the exotic parasitoid had minimal impact on native species, due to their different habitat preferences and phenology compared to its primary host, H. halys. Trissolcus japonicus occasionally emerged from the eggs of A. heegeri, N. viridula, P. prasina, P. rufipes, and R. nebulosa, and mainly in sites located up to 500 m. These species were successfully parasitised by T. japonicus under laboratory conditions, with the exception of N. viridula, which was attacked but not found to be suitable for parasitoid development (Haye et al., Reference Haye, Moraglio, Stahl, Visentin, Gregorio and Tavella2020; Moraglio et al., Reference Moraglio, Tortorici, Giromini, Pansa, Visentin and Tavella2021b; Sabbatini-Peverieri et al., Reference Sabbatini-Peverieri, Boncompagni, Mazza, Paoli, Dapporto, Giovannini, Marianelli, Hoelmer and Roversi2021). Oviposition in this host resulted in significant non-reproductive mortality. Haye et al. (Reference Haye, Moraglio, Tortorici, Marazzi, Gariepy and Tavella2024) found a high proportion of unemerged eggs from field-collected N. viridula egg masses containing T. japonicus DNA, confirming the parasitoid-induced non-reproductive mortality. This could explain the high percentage (45%) of unhatched N. viridula eggs recorded in our study. Further investigations on the seasonal dynamics of T. japonicus parasitism could help clarify the exploitation of other hosts rather than H. halys.
Among the hymenopteran parasitoids obtained from the field-collected bug eggs, B. oophagus is recorded for the first time emerging from eggs of H. halys. Previously, this species has been reported attacking the common pine sawfly, Diprion pini (L.) (Hym.: Diprionidae) (Graham, Reference Graham1991) and the lackey moth, Malacosoma neustria (L.) (Lepidoptera: Lasiocampidae) (Özbek and Coruh, Reference Özbek and Coruh2010; Žikić et al., Reference Žikić, Stanković, Kavallieratos, Athanassiou, Georgiou, Tschorsnig and van Achterberg2017), while other species of Baryscapus Förster are hyperparasitoids that attack the primary parasitoids of caterpillars and other insect larvae (Marshall, Reference Marshall2023). It will therefore need to be verified whether this is an isolated case or not. On the contrary, the finding of the hyperparasitoid A. sinicus is definitely not an isolated case, as it was found in all habitats and altitude ranges, and emerged from the eggs of four stink bug species, in greater numbers from the native species in comparison with H. halys. This hyperparasitoid, whose taxonomic position has recently been clarified (Sabbatini-Peverieri et al., Reference Sabbatini-Peverieri, Mitroiu, Bon, Balusu, Benvenuto, Bernardinelli, Fadamiro, Falagiarda, Fusu, Grove, Haye, Hoelmer, Lemke, Malossini, Marianelli, Moore, Pozzebon, Roversi, Scaccini, Shrewsbury, Tillman, Tirello, Waterworth and Talamas2019), was first reported in Europe during investigations of the indigenous parasitoid complex capable of adapting to the exotic H. halys (Moraglio et al., Reference Moraglio, Tortorici, Pansa, Castelli, Pontini, Scovero, Visentin and Tavella2020). Studies to date aimed to ascertain which conditions are most favourable and which species of exotic Trissolcus is most suitable for the development of the hyperparasitoid (Giovannini et al., Reference Giovannini, Sabbatini‐Peverieri, Tillman, Hoelmer and Roversi2021; Mele et al., Reference Mele, Scaccini and Pozzebon2021), while there are no studies on the relationships of this hyperparasitoid, with indigenous Trissolcus species. The fact that it emerged from the eggs of P. prasina and P. rufipes, even at altitudes that did not appear suitable for T. japonicus, prompts further research into the origin and distribution as well as the indigenous hosts of A. sinicus.
This study extends previous research by investigating a wider range of habitats and altitudes, providing a more comprehensive understanding of the ecology of true bugs and associated egg parasitoids in the region. Urban environments are particularly important for the biodiversity protection, because they provide habitat, support ecosystem services, and offer conservation opportunities through the management of urban green spaces (Dearborn and Kark, Reference Dearborn and Kark2010; Goddard et al., Reference Goddard, Dougill and Benton2010). In our study, these areas were widely used for reproduction by true bugs, offering a wide variety of ornamental plants. Moreover, urban areas in South Tyrol are not as extensive as in other regions and are often located in proximity of forests, especially at higher elevations. Different studies underlined the importance of forest habitats for the overwintering of several true bug species (Laterza et al., Reference Laterza, Dioli and Tamburini2023; Musolin, Reference Musolin2012; Schaefer and Panizzi, Reference Schaefer and Panizzi2000). Identifying areas in the agro-ecosystem, where pests consistently thrive, is crucial for effective pest management (Grabarczyk et al., Reference Grabarczyk, Cottrell and Tillman2021; Panizzi and Lucini, Reference Panizzi and Lucini2024), enables the assessment of outbreak risks, and facilitates the implementation of precise control measures. For example, the infestation risk could be reduced by using wild hosts as trap plants to concentrate populations in limited areas, where they can be easily controlled eradicated, and by decreasing the presence of wild hosts in production zones (Hokkanen, Reference Hokkanen1991; Mizell et al., Reference Mizell, Riddle and Blount2008; Panizzi, Reference Panizzi1997; Rea et al., Reference Rea, Wratten, Sedcole, Cameron, Davis and Chapman2002). Designing habitats to encourage parasitoids is promising but has had limited success in reducing pest damage so far (Tillman, Reference Tillman2017). Parasitoids and predators of true bugs can exploit certain plant and flower resources. Therefore, incorporating these natural resources into the agricultural ecosystem could promote biological regulation and enhance biodiversity conservation (Landis et al., Reference Landis, Wratten and Gurr2000; Rusch et al., Reference Rusch, Bommarco, Jonsson, Smith and Ekbom2013). However, further research is needed to understand how these are best compatible with local regulation strategies. Future efforts should focus on developing strategies to mitigate the economic damage caused by true bugs, maintaining populations of natural enemies in and around orchards, and promoting biodiversity in agricultural landscapes. Understanding these ecological dynamics is crucial for the preservation of different habitats that enhance both true bug and egg parasitoid abundance and diversity.
Supplementary material
The supplementary material for this article can be found at https://doi.org/10.1017/S0007485325100412.
Acknowledgements
We thank Paolo Navone for identification of Eulophidae. Antonio Pignalosa and Alessia Conci assisted with field work. Funding was provided by the Laimburg Research Centre. Francesco Tortorici was supported by Agritech National Research Center of Italy and received funding from the European Union Next-Generation EU (Piano Nazionale di Ripresa e Resilienza ‘PNRR’ – Missione 4, Componente 2, Investimento 1.4 – D.D. 1032 17/06/2022, CN00000022). This manuscript reflects only the authors’ views and opinions, neither the European Union nor the European Commission can be considered responsible for them.
Competing interests
None.
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