Urban ecosystems provide a suite of services for human health and well-being, including food production from urban gardens and commercial agriculture (1–3). However, such benefits should be weighed against potential disservices created as a result of these human-altered landscapes (4, 5). In particular, urban areas contain unique sets of social and ecological processes that may create focal points for the introduction, establishment and spread of non-native species (6–10).

Anthropogenic landscapes often exist along gradients of different land-use types, including urban and peri-urban cities, commercial agriculture, and a range of natural ecosystems (8, 11, 12). The particular spatial configurations of these landscapes in a given area are idiosyncratic, which suggests that a diverse interplay of social and ecological processes determine the initial risk of invasion, as well as if and when spillover into surrounding urban forest landscapes will occur (4, 10, 13, 14).

Cross-habitat spillover involving the movement of invasive species between agroecosystems and natural habitats have been documented (15, 16). Most studies have focused on asymmetric movement of insects between agricultural areas and surrounding natural habitats (13, 15, 17). Landscape features, such as the extent and characteristics of habitat edges and the relative proximity to source habitats, have been shown to affect spillover across habitats (13). Such spillover events can further influence community dynamics of the recipient habitat through processes such as parasitism, predation, and disease transmission (13, 14, 18, 19).

Southern California, a region characterized by extensive urban development, has recently experienced the introduction of numerous phytophagous insects (20). Of the ~10 exotic arthropod introduction events per year in the state, an estimated 20% become invasive pests (21). One invader of particular concern is the Asian citrus psyllid (Diaphorina citri) because of its ability to transmit the bacterium Candidatus Liberibacter asiaticus (CLas) associated with huanglongbing (HLB; citrus greening disease) [Grafton-Cardwell et al., (22)]. Symptoms of HLB, to which all commercial varieties of citrus are considered susceptible, include progressive yellowing of leaves, stunting of shoots, defoliation, reduced yield and fruit quality, and tree mortality (23). Citrus growing regions where both the pathogen and vector successfully invaded, such as Florida, have faced severe economic impacts (24).

Citrus has unique historical and cultural significance in California, following its likely introduction into the region by Spanish missionaries in the late 18th century (25). The first commercial production began in southern California in the mid-19th century, expanded to other areas of the state in subsequent decades, and eventually developed into what is currently estimated to be approximately 270,000 ac of citrus farmed at a yearly production value of more than $3B (25–27). The development of the citrus industry is credited with contributing to California's population expansion throughout the 19th century, the creation or evaluation of novel citrus varieties that are commonly grown today, and the widespread acceptance of biological control as an element of integrated pest management (25, 28). Enthusiasm for citrus carries over to urban and other residential areas of California where it is frequently grown as an ornamental and food plant. Surveys conducted in select neighborhoods in southern California estimated that more than 60% of properties had at least one citrus tree present (29). Thus, residential and commercial trees are both at risk to invasive pests and diseases, such as D. citri and huanglongbing, and indeed may exacerbate damage to each other in the event of cross-habitat spillover (Figure 1).

D. citri was first detected in California in a residential area of San Diego County in 2008 and in Los Angeles by 2009 (30). In response, a strategic plan was implemented to mitigate the impact of this invasive pathosystem in California (27). Over the next few years, the insect spread throughout urban and peri-urban areas, apparently driven by favorable climatic conditions and landscape characteristics in these environments (30, 31). D. citri was first detected in a handful of commercial citrus groves in 2011, and over the next few years became increasingly prevalent in these settings (30). Finally, the first case of HLB was detected in a residential area of Los Angeles County in 2012 (32). Disease surveys have subsequently identified upward of 2500 infected trees that have been removed to limit pathogen spread (27, 33). Thus far, all cases of the disease have occurred in residential areas, but there was one detection of a CLas positive psyllid from a commercial grove, and nearby groves are considered at risk.

While invasive species spillover between agricultural and natural ecosystems has been quantified, less is known about how common spillover is from urban to agricultural ecosystems, or the processes governing it across space and time. The general sequence of D. citri occurrence and patterns of CLas spread in Southern California are consistent with urban environments playing a potentially important role in facilitating the establishment of D. citri (30, 31, 33). Yet, formal analyses are lacking that identify the factors driving D. citri invasion of commercial citrus groves, which is critically important for refining disease detection and management strategies. Here, we quantify the magnitude of urban-to-agriculture D. citri spillover, and the underlying role of grove-level characteristics, urban landscape-context, and neighborhood proximity in governing the spatial and temporal distribution of D. citri activity in commercial groves.

Of the nearly 2,500 unique citrus groves for which D. citri trapping data was available, 539 had at least one detection by the end of 2014. The earliest commercial citrus detection occurred in April 2011, with six additional groves having detections in that year, an additional 208 groves in 2012, and the remainder in 2013 and 2014. Of those groves in which D. citri was detected, 6.5% (35/538) had a single trap detection, but with a maximum of 359 cumulative detections (mean ± SD: 18.76 ± 33.46).

Cross-habitat spillover of organisms is increasingly gaining recognition, particularly in agroecosystems and urban forests. Many studies have focused on the movement of organisms between agricultural habitats and natural habitats (13, 15, 17). Unlike these studies, our research addresses the less familiar spillover between urban and agricultural habitats within an anthropogenic-dominated landscape, and its importance for the spread and impact of an invasive insect pest of high economic significance. In our study area, citrus constitutes a substantial fraction of urban tree plantings (29). D. citri was first recorded in these urban micro-habitats (such as house backyards and gardens) of southern California in 2008. Within three years, D. citri had invaded commercial citrus groves (30). Overall, our results highlight the role of grove-level factors in combination with two spatially-explicit factors, namely urban landscape-level context and neighbor effects in modulating urban-agricultural spillover.

At the grove-level, grove area stood out as a common factor affecting both rate of invasion and magnitude of D. citri infestation such that large groves were invaded faster and also contained greater cumulative detections of D. citri. These results are not surprising given that, as noted earlier, trap number varied grove size. Yet, part of the observed effect may also be attributable to larger plantings of citrus trees acting as larger targets for D. citri invasion. A similar ‘magnetic effect’ has been reported among mass flowering crops wherein pollinators tend to spillover in large numbers during blooming periods (13, 44). After controlling for grove area, the proportion of citrus along grove edges and the extent of grove perforation only affected the rate of invasion. In both cases, a higher proportion of grove edge and grove perforation increased the rate of invasion. Studies have similarly shown that the amount and ecological nature of the edge, and consequent edge-effects, are often important drivers of spillover from groves to natural habitats (15). Citrus trees at the outer edge of groves have been shown to contain a higher abundance of D. citri compared to trees in the interior, particularly those groves on the exterior edge of large farms (34). Interestingly, grove edge and grove perforation had no significant effect on the cumulative number of D. citri detections in a citrus grove, perhaps indicating that once a grove is invaded local recruitment is an important element of D. citri population dynamics. Studies have shown that resource availability and abundance can affect population growth and eventual abundance of organisms that spillover into high quality recipient habitats such as mass flowering crops plants (45, 46).

Both urban landscape-level variables, distance to major roads and urbanization intensity, had significant effects on the rate of D. citri invasion. The distance to roads had an overall negative effect on the rate of spillover during early stages of invasion, but then shifted toward a positive effect in more recent years. Urbanization intensity increased the rate of invasion, implying that citrus groves surrounded by higher levels of urbanization are more quickly invaded by D. citri. Taken together, the positive effect of urbanization intensity on rate of invasion suggests heavily disturbed urban-grove edges, along with the distance to roads, can facilitate introduction pathways and hasten D. citri invasion. Distance to major roads tends to result in greater D. citri abundance within groves, which again suggests the role of roads in serving as introduction pathways and potentially affecting multiple introductions of D. citri individuals from the surrounding landscape. An earlier study on the initial D. citri detections within urban Los Angeles identified major roads entering the city as a likely introduction pathway (31). In the only other study known to us, proximity to anthropogenic edges such as roads was found to enhance parasitic attacks of a leaf miner in suburban woodland fragments (15, 47). Our findings highlight the importance of incorporating urban landscape-level factors in spillover studies.

Studies have shown that cross-habitat spillover can influence community dynamics of the recipient habitat through processes such as predation, parasitism, and disease transmission (13, 14, 18, 19). While grove-level characteristics set the risk threshold for invasion, neighbor effects suggest that proximity to D. citri invaded neighborhoods are the eventual deterministic factor driving the spillover. In this respect, it is important to note that the early-phase distance to nearest urban occurrence (urban early-phase) and late-phase distance to nearest grove occurrence (grove late-phase) are negatively related to the rate of invasion. In other words, there appear to be strong spatial linkages between urban occurrences of D. citri and its arrival in nearby groves, and among groves once one of them is invaded. The relatively sporadic presence of citrus host plants in urban micro-habitats can initiate the urban-grove spillover, which suggests the need for more spatially comprehensive management plans that take into consideration the potential role of surrounding landscape.

The strong effects of early-phase urban and late-phase grove invasion implies that the spillover pressure from D. citri invasion is most pronounced after spreading substantially in the surrounding landscape. In a recent spillover study, the magnitude of bee spillover from mass flowering citrus groves to nearby woodland patches was similarly found to vary in both space and time, such that spillover was not only higher in woodland patches in landscapes with high cover of mass flowering citrus groves but was particularly higher after the citrus blooming period (44). The study further demonstrated that the observed spillover dynamics are largely driven by variation in flower cover across the landscape, and hence is considered to be resource-mediated. Our findings point to a similar resource-mediated mechanism behind the spillover but with the striking difference that the movement of D. citri individuals were initially from relatively resource-poor urban conditions to resource-rich groves. Overall, the neighbor effects suggest that spillover of D. citri is not merely a function of spatial proximity to nearest invaded grove and/or urban location but is also shaped by the temporal trajectory of D. citri invasion.

To mitigate the impact of the D. citri invasion in Southern California, a strategic plan was implemented that included monitoring for D. citri and CLas, removal of infected trees, the release of biological control agents, a residential insecticide treatment program, restrictions on the movement of plant material, and community outreach (27, 48). Despite this, urban-to-agriculture spillover occurred within the first few years of the southern California invasion. This observed early-phase effect of urban invasion suggests D. citri spillover into citrus groves was initially driven by D. citri from citrus plantings in urban and peri-urban locations in close proximity to groves. Later citrus grove invasions were driven largely by spillover from nearby invaded groves, which suggests that the source of D. citri spillover into citrus groves shifts over time. This apparent shift in spillover dynamics has implications for management of D. citri and similar insect pests that are not restricted to a single habitat type. Specifically, for areas where the invasion is at an advanced stage, such as in Southern California, attempts to mitigate further D. citri spread into commercial citrus will likely benefit more from management of invaded groves than from measures focused in residential areas (27, 48). Conversely, in areas where D. citri is not as well-established, such as the Central Valley of California (49), given competing demands on resources, our results indicate mitigating future D. citri invasion of groves is likely to benefit most from management in urban areas. Meanwhile, attempts to mitigate further spread of CLas and huanglongbing may require different strategies. Given that to date all of the ~1,500 documented cases of huanglongbing in California have occurred in residential citrus (33), and within cumulative counts of D. citri in groves indicating a continuing influx from urban areas, concentrating vector control and inoculum reduction programs (27) in urban areas is likely to be more impactful than in commercial citrus. In other words, development of appropriate management strategies requires a recognition of the fluid nature of invasion dynamics and careful consideration of the specific management objectives.

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

BB and MD: conceptualization and study design. BB, MD, and ST: statistical analysis and writing. MD: funding acquisition and supervision. GS: data acquisition. All authors contributed to the article and approved the submitted version.

This project was supported by funding from USDA-APHIS-PPQ to MD.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.