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Four green roofs were selected from the urban center of Portland, Oregon (Figure 1). These locations were a component of a larger study on the biodiversity of beetles (Starry et al., 2018; Gonsalves et al., 2022) and other arthropod taxa present on these same roofs. Two of the green roofs selected for this study (EcoTrust, or ET, and Oregon College of Oriental Medicine, or OCOM) were dominated by succulent Sedum plants (Table 1). The OCOM roof also had two small areas of herbaceous ornamental plants but these comprised less than 10% of total vegetated area (Olyssa Starry, personal communication). The other two locations [Hamilton West (HW) and Central Wine Warehouse (CWW)] had been planted with a mix of herbaceous grasses and flowering plants (Table 1). Although these roofs were designed for storm-water management, they were also intended to promote urban biodiversity (Olyssa Starry, personal communication). The four green roofs were installed at different times and varied in soil depth and the amount of supplementary water they received (Table 1). All sites received partial to full sun exposure, with zones of shading created by rooftop structures (Gonsalves, 2016).

The city of Portland experiences a temperate climate, with temperatures that allow many invertebrates to live or reproduce year-round. During this study, the average monthly air temperature during April to June of 2015 for downtown Portland ranged from 10.3 to 21.7°C with the highest temperature recorded at 33.3°C (National Oceanic and Atmospheric Administration [NOAA], 2015). A seasonal drought occurred during the sampling period. The total precipitation during the study amounted to 9.4 cm, which is roughly 7 cm lower than the average rainfall for the urban center of Portland during April, May, and June (National Oceanic and Atmospheric Administration [NOAA], 2015). Three of the study sites received some level of supplemental irrigation (Table 1), which offset the dry conditions to varying extents.

Pitfall traps are among the most widely utilized sampling methods for cursorial invertebrates and were employed in this study. Traps were established according to Woodcock (2005), with 10 pitfall traps per green roof site distributed in a grid pattern at distances of 10 m wherever possible, and with no traps being closer than 5 m from each other. Ward et al. (2001) demonstrated that there was no statistical difference in total abundance of insects collected between pitfall traps placed 5 m apart as opposed to 10 m apart.

Each pitfall trap consisted of a 125-ml plastic cup nestled inside a 5-cm diameter PVC pipe connector (Gonsalves, 2016). Cups were firmly placed into the substrate and situated level with the soil layer. A cover was constructed to minimize overflow from excessive rain events. Each trap was filled to three-fourths capacity with a 10% acetic acid solution. Vinegar was chosen due to its relatively low volatility and chosen over ethylene glycol for its non-toxic effects on vertebrates. The cups were emptied and refilled with fresh vinegar solution approximately every 2 weeks covering a period from 9 April to 25 June 2015 (except for one collection date for OCOM). The contents of all pitfall traps for each roof were pooled into a single plastic container per collection date. To avoid degradation of the specimens collected, the contents from each site were rinsed in water and filtered before being transferred to and stored in 80% ethanol. Filtration and transfer of insects to ethanol occurred within a 2-week window post-collection.

Specimens were sorted according to taxonomic groups using a dissecting microscope. All parasitoid hymenopterans were handled using plastic pipettes to avoid damaging the specimens. Specimens were identified to morphospecies based upon wing venation patterns, total flagellomere number, shape of the antennae, and other key diagnostic characteristics (see Supplementary Table 1). When possible, specimens were identified to family level in collaboration with Dr. Heidi Liere (at Seattle University) and Diego Fernando Campos Moreno (at the National Pedagogical University) following the keys by Goulet and Huber (1993) and Broad (2011). Representative voucher specimens were preserved for each morphospecies and are stored in 80% ethanol at the Portland State University Museum of Natural History.

We constructed species accumulation curves to evaluate variation in wasp species diversity, and determine whether we had sampled sufficiently to capture the diversity present among the green roof sites. To compare the functional diversity and composition of Hymenoptera from the green roof sites, we sorted all specimens by taxonomic families and host preferences into bar charts, and then aggregated morphospecies types by roof site into pie charts. To account for the size of each location, we divided the raw number of specimens collected by the area (m²) of the site. Analyses were performed with Microsoft Excel and the R statistical environment (R Development Core Team, 2011).

In order to compare wasp biodiversity among the green roof sites, we calculated the observed species richness, as well as the effective number of species, or the number of equally abundant species that are required to create the same value of a diversity measure across sites (Hill numbers), using the iNext package (Chao et al., 2014; Hsieh et al., 2016, 2022). The importance of rare species change with the function of the parameter q, with q = 0 weighting all species equally, q = 1 weighting species by their relative abundance (exponential Shannon entropy), and q = 2 weighting rarer compounds as less important (Simpson’s inverse index). To test for the influence of roof age and height on observed species diversity, we normalized predictor values using the BBmisc package (Bischl et al., 2014) and then modeled the relationship using a Gaussian error structure.

To assess whether the surrounding landscape may have influenced the diversity of parasitoids on the green roofs, we gathered data on three measures of isolation from areas of nearby natural habitat. Using satellite imagery from GoogleEarth to provide an aerial view of landscape features around each of the four green roofs (see Figure 1), we measured: (1) distance to the nearest natural habitat (in linear meters), (2) total area (in hectares) of natural habitats within 0.5 km of each roof, and (3) total area (in hectares) of natural habitats within 1.0 km of each roof. For each of these measures, “natural habitat” was defined as a contiguous area of at least 0.50 ha that is predominantly vegetated (as opposed to paved or taken up by structures). The 0.50-ha threshold is equivalent to the size of one typical city block in downtown Portland. We then tested for correlations between these landscape measures and our measures of species diversity by running linear regressions between each landscape measure and each measure of species diversity.

Biological control agents include primarily predatory or parasitic insects that function as natural enemies of herbivorous pests, helping to keep populations of such pests in check. Host specialization, combined with the hyper-diverse nature of parasitoid wasps, makes them ideal agents for biological control (Strand and Obrycki, 1996). Wasps from three of the families we found on green roofs in Portland, Oregon, are commonly used in biological control: Aphelinidae, Encyrtidae, and Mymaridae (Kimberling, 2004). This suggests that Portland’s green roofs may be functioning as small-scale ecosystems with some internal capacity for pest control. Even though some of the parasitoids may exist in low numbers, the presence of such biocontrol agents could reduce the need for green roof managers to use chemical pesticides, which can have harmful unintended consequences and have been implicated in the decline of pollinators (Pimentel et al., 1992; Gill et al., 2012; Potts et al., 2016).

We documented that a diverse assemblage of parasitoid wasp taxa exists on green roofs within the urban core of downtown Portland. Although these isolated patches of habitat are located in a densely developed metropolitan center, we found them to contain a strikingly high abundance and diversity of these insects. Of the 119 specimens captured and identified over a 3-month period, there were 10 families present with 20 morphologically distinct species. In contrast, in a study of 15 green roofs in a semi-rural region of Argentina, only eight morphospecies of parasitoid wasps were found during the two peak months of arthropod activity (Dominguez et al., 2020). The Argentinian green roofs were all relatively new, with an average age of about 3 years since construction, which may have limited their biodiversity. However, in Portland, a seasonal drought occurred during our sampling period, and parasitoid wasp populations tend to decrease under drought conditions (Aslam et al., 2013; Portman et al., 2021). This is particularly relevant for CWW, which received no supplementary irrigation (Table 1). Our most biodiverse roof, HW, was only moderately irrigated, while the drought conditions were likely offset at the ET location, which had automated irrigation running regularly (Gonsalves, 2016). All told, the data available from this study and from Dominguez et al. (2020) suggest that green roofs in urban Portland support a more diverse assemblage of parasitoid wasps than green roofs in some semi-rural regions of the Americas.

Studies examining the role of biological control in urban greenspaces have shown mixed results as to how urbanization influences parasitoid assemblages. The degree of urban development did not impact the species richness of wasps collected across 15 remnant green spaces inside Sydney, Australia (Christie and Hochuli, 2009). However, in a study of 18 urban gardens across the central California coast, species richness decreased with increasing urbanization (Burks and Philpott, 2017). A recent meta-analysis on the effect of urbanization on biological control concluded that although the abundance of wasps was not greatly impacted, the effectiveness of parasitoid Hymenoptera tended to decline as urbanization increased (Korányi et al., 2022). These mixed results could be due to disparities in the degree of habitat fragmentation and complexity around the study locations, as well as differences in dispersal abilities of the biological control insects captured.

Data is lacking on how most parasitoids arrive and become established atop green roofs. At our Portland sites, we found multiple wasps that specialize in parasitizing the eggs of their hosts, despite the small size and presumed limited dispersal ability of these Hymenopterans. For example, four morphospecies of wasps in the family Mymaridae were found on three of the four green roofs in our survey. All species of Mymaridae are parasitoids of the eggs of other insects, and could be important general biological control agents. They are small, rarely more than 1.5 mm (Goulet and Huber, 1993), and it has been suggested that such parasitoids would be unlikely to colonize urban green roofs due to their small size (Quispe and Fenoglio, 2015). However, Corbett and Rosenheim (1996) demonstrated that one species of Mymarid wasp managed to disperse up to 24.5 m/day, including traveling upwind. Vergnes et al. (2017) suggested that passive aerial dispersal of arthropods could be a driving force for biodiversity of urban green roofs, as they found diverse families of insects caught in aerial traps on buildings in the urban core of Paris, France. While data suggest that parasitoid wasps can colonize roofs, further research is needed to determine when Mymarid wasps can be expected to occur on green roofs and what conditions might facilitate their arrival.

Although it is possible that the parasitoid taxa we collected were initially brought in along with green roof plantings or with soil amendments, we think that is unlikely, as we would have expected to see more similar results across the four study sites had that been the case. Instead, we found that wasp diversity across sites was highly variable and was greatest on a roof that harbored a complex plant community, the HW roof (Table 2). The HW roof was planted much longer ago than the other three roofs sampled (16 years ago, versus seven or fewer years), and the diversity of parasitoids present may mirror the diversity of their host taxa on these roofs. Indeed, in a study of the beetle diversity on green roofs in Portland, this same roof was found to be more similar to the (highly diverse) ground sites that were sampled than to other comparably planted green roofs (Gonsalves et al., 2022). We suggest that this particular roof may be comparable to a later successional stage of an ecosystem, having accumulated through time an increasingly diverse assemblage of fauna.

If wasps establish on green roofs naturally by airborne dispersal from surrounding regions, then we might expect to find that roofs closer to areas of natural habitat, or those with greater amounts of natural habitat nearby, would show greater species diversity. In classic island biogeography theory, islands closer to source populations are expected to accumulate larger numbers of species. Our analyses of measures of natural habitat in the landscape surrounding the roof sites showed only the slightest suggestion of such a “distance effect” expected from theory. Of nine regression tests, only one showed a significant relationship: species richness was positively correlated with the total area of natural habitat within 1.0 km of each roof. The HW roof, which had the greatest species richness (as well as the greatest number of wasps), also had by far the most natural habitat nearby, as its location toward the edge of the downtown urban core placed it in closer proximity to residential neighborhoods with large amounts of tree cover.

Proximity to natural areas of vegetated habitat could well play an important role in shaping the diversity on green roofs. However, given our small sample size of four roofs, the highly complex nature of the urban environment, and the difficulty of knowledgably identifying productive source habitat for dispersing wasps, one should perhaps not be surprised that a stronger distance effect was not detected. Indeed, few green-roof studies have shown an island biogeographic effect, and controlling for the many variables present among different roofs and the small number of roofs sampled in each study creates challenges for drawing strong conclusions about whether green roofs follow the standard predictions of island biogeography theory (Blank et al., 2017).

We found the species richness of parasitoid wasps to be higher on the herbaceous roofs than on the Sedum-dominated roofs. Each herbaceous roof (CWW and HW) ranked substantially higher than the Sedum-dominated roofs (ET and OCOM) in terms of diversity as shown by both the effective species number and Simpson’s reciprocal index (Table 3). The species accumulation curves suggest that even with continued sampling effort, the two Sedum-dominated roofs would continue to produce fewer species than the two herbaceous roofs (Figure 6). A major difference between these two types of roofs is that the herbaceous roofs feature a more complex vegetative structure. Although it is difficult to draw strong conclusions given the limited number of roofs used in this study, our results suggest that a structurally diverse plant community can better support a diverse parasitoid wasp community. Each green roof provides site-specific habitat, which can directly affect the abundance and diversity of the invertebrates found there (Brenneisen, 2006). And indeed, Madre et al. (2013) and Gonsalves et al. (2022) showed with green roofs that a higher species richness for several arthropod taxa was correlated with greater structural complexity.

The two roof types in our study also differed greatly in abundance of the different types of parasitoids, with some being substantially more prevalent than others (Table 2). Interestingly, the two roofs planted primarily with Sedum plants were dominated by wasps in the family Aphelinidae (91% of ET and 76% of OCOM). The majority of aphelinids are parasitoids of the suborder Sternorrhyncha (Hemiptera), particularly the Aphidoidea (aphids), Aleyrodoidea (whiteflies), and Coccoidea (scale insects) (Goulet and Huber, 1993). Rand and Tscharntke (2007) demonstrated that parasitoids that are aphid specialists are limited by local host availability, in contrast to generalist natural enemy groups, which are less reliant on local host densities. Sedum-dominated roofs are generally a monoculture and are therefore more vulnerable to herbivore pest outbreaks than are the biodiverse plantings of an herbaceous roof. While both roof types had wasps from the generalist families of Pteromalidae and Ceraphronidae, the herbaceous roof types contained wasps from four additional generalist families (Table 2).

We found that the oldest roof (HW) supported the highest number of species overall and the highest number of species unique to a location, despite the fact that it was the second-smallest roof in area vegetated (Table 1 and Figure 3). This is somewhat surprising in terms of expectations from island biogeography theory, as larger land masses (or in this case, larger green roofs) would be predicted to harbor more biodiversity. On the other hand, older roofs have had more time to accumulate biodiversity, leading to the expectation that diversity should rise with roof age, which is consistent with our findings. If we compare our two roofs planted with herbaceous plants and grasses, similar patterns are revealed. The CWW roof is more than three times larger than the HW roof, but less than half its age (7 years for CWW as opposed to 16 years for HW). In terms of parasitoid abundance, CWW held only about one-sixth as many individuals, and its species richness was less than half that of HW. Thus, our results appear to suggest that in this system, age may play a more influential role than area in contributing to species diversity.

Our finding of increased diversity with increased age of the green roof is mirrored by some previous studies of taxa on green roofs, but differs from other studies. Some predatory arthropod taxa, including parasitoid Hymenoptera, have been shown to increase in diversity with roof age for young roofs less than 4 years of age (Kyrö et al., 2022). Also in support of the idea that biodiversity can correlate with age, a study on green roofs in Argentina found that roof age was correlated with abundance of insect predators, which included parasitoid wasps (Fabian et al., 2021).

In contrast, a study of beetles on green roofs in Switzerland found that the age of the roof was negatively correlated with beetle diversity (Kyrö et al., 2018). The beetles that were collected were primarily herbivorous habitat generalists adapted to dry conditions and the authors suggested that these are species adapted to early successional habitats (Kyrö et al., 2018). However, in a study designed to assess whether green roofs undergo successional changes, it was found that there was not a general pattern of plant community succession, but instead, that other biotic and abiotic factors influenced species richness and diversity (Ksiazek-Mikenas et al., 2018). Still, that study did find that arthropod diversity generally increased with age of the roof, although those results were not statistically significant (Ksiazek-Mikenas et al., 2018).

While our results suggest that plant community structure and the age of urban green roofs may each affect parasitoid diversity, firm conclusions await further study. Future research with more roofs and longer monitoring periods could potentially speak to which type of roof vegetation best supports more varied wasp communities. Our species accumulation data suggest that longer monitoring at our sites would have resulted in additional taxa continuing to be found, particularly for the CWW site (Figure 6). Indeed, Gonsalves (2016) was still recovering beetles from pitfall traps at all of these green roof sites into the month of September, illustrating that other insects survive on green roofs for much of the year. Testing explicitly for the influence of roof age on biodiversity patterns in future studies would be useful, but could be difficult due to the fact that the number of green roofs more than a decade old is limited.

The use of different sampling methods could potentially influence results obtained. A reliance on sampling by pitfall traps has the potential to bias the collection of parasitoid wasp specimens toward those taxa with limited flight ability or those that attach to cursorial invertebrates. As this study did not include a secondary trapping method, it is likely that we under-sampled the overall presence of parasitoids at our study sites. This makes the diversity that we did find especially notable, as adult parasitoid wasps can fly and a majority of their hosts would have been on the plants instead of in the soil. Indeed, for these reasons it seems likely that a substantially greater number and diversity of parasitoid wasps was in fact present on the green roofs we sampled. Future research could expand the sampling reach by using Malaise traps, which have been suggested as an optimal technique to understand the relationship between parasitoid abundance or diversity and habitat characteristics (Fraser et al., 2008).

An additional and important caveat to this study is that we analyzed data for only one field season. It is known that Hymenopteran communities typically experience species turnover from year to year in habitats in which they normally reside (e.g., Christie and Hochuli, 2009). As a result, we might expect that data from subsequent years from these sites could yield somewhat differing results.