Urban Ecology and the Effectiveness of Aedes Control Urban Ecology and the Effectiveness of AedesControl

Past initiatives to control Aedes mosquitoes were successful, in part because they implemented draconian top-down control programs. To achieve similar results now, explicit recognition of the complexity in urban ecologies in terms of land ownership, law enforcement and accessibility for control interventions are required. By combining these attributes, four classes of spaces, along with corresponding control strategies, are suggested to better target Aedes species population control efforts. On one end of the spectrum there are accessible and accountable spaces (e.g. backyards and closely managed public facilities), where interventions can rely predominantly on bottom-up strategies with the local population playing the principle role in the implementation of actions, but with government coordination. On the other end of the spectrum are inaccessible and unaccountable spaces, which require top-down and extensive approaches. By identifying these and the intermediate classes of space, government and private resources can be allocated in a more efficient customized manner. Based on this new framework, a set of actions is proposed that might be implemented in dengue and other Aedes -borne crises. The framework considers existing limitations and opportunities associated with modern societies – which are fundamentally different from those associated with the successful control of Aedes species in the past.


Introduction
Urban pest species are highly effective and opportunistic in their use of the physical, legal and administrative interstices of the landscape we inhabit, and Aedes mosquitoes are a case in point. Any inaccessible nook or cranny, any vacant land or neglected facility permits adult mosquitoes to hide and, in as little water as might accumulate in the lid of a bottle, find ideal breeding places. Aedes mosquitoes take advantage of the heterogeneous urban ecologies through "skip oviposition," laying a few eggs, spread across the largest possible number of sites. It is an especially well suited strategy for urban environments with abundant, but sparse and even temporary breeding sites [1].
The control of Aedes mosquitoes is failing in most tropical regions [1][2][3], and human diseases transmitted by this vector, like dengue, chikungunya, yellow fever and Zika, are among the top public health priorities [4,5]. The strategies for suppressing mosquito populations below a threshold at which they no longer support viral amplification [6][7][8][9][10] has focused on two strategies [7,11,12]: (a) negating larval development opportunities by eliminating breeding places and the sites of immature stages; and (b) killing adults by fumigation with insecticides. More recently biomolecular and biogenetic approaches have also been suggested, although their effectiveness under field conditions are uncertain [13,14]. Therefore new approaches are urgently needed, especially in urban landscapes [15].
Here we propose that an important strategic aspect that is currently overlooked in Aedes control programs: recognition of the complexity of urban ecologies in terms of land ownership, enforcement and accessibility for control interventions. We suggest that a systematic strategy that accounts for this physical complexity is essential to best implement Aedes control.

Physical and legal accessibility for control purposes
In the current absence of safe and economically sustainable methods to sterilize or kill whole populations of adult mosquitoes, and especially ones that might be deployed on a scale and speed required to impact an epidemic, control over potential breeding and resting sites (PBRP) continues to play a pivotal role in the strategies against Aedes.
We suggest tackling this challenge by framing it based on these two variables that are especially relevant to the control of PBRPs: accessibility and accountability. The first relates to how easily breeding sites can be accessed for cleaning and intervention purposes. Although most PBRPs can be readily managed by private citizens (e.g., plant pots, fountains, household refuse and sidewalks), some are physically difficulty to locate or access for control purposes (e.g., roof gutters, cracks in houses or water-containing holes in trees). The second factor relates to how the stewardship of land is distributed between individuals, companies or the state. Even though all PBRPs are, in theory, under some legal responsibility (private residence, public buildings and tended public spaces), neglected public spaces (particularly in developing nations) and areas with uncertain ownership are under de facto diffuse or a non-accountable authority and frequently result in a state of abandonment (e.g. vacant lands, neglected public parks, open sewage).
The interaction between these physical and legal factors yields an actionable categorization of areas for vector control (Figure 1) that goes beyond the traditional system of "domestic, peridomestic and public spaces" [16], which is limited to types of habitat. The framework proposed in Figure 1 distinguishes societal actors (individuals, communities, government) who can be engaged in and held responsible for Aedes management. This classification, detailed below, enables both the identification of optimal allocation of private and public responsibilities in each case, but also defines the most suitable set of strategies: (A) Easily accessible & accountable PBRPs. In areas that are both easily accessed and under accountable stewardship, for example, occupied private dwellings, or public facilities under effective management, we propose that the private individuals within the premises are engaged and mobilized. Plates under potted plants, water tanks, garden fountains, birdbaths, water bowls for pets, laundry tubs, toys, swimming pools, cisterns, ponds, etc. can be directly managed by individuals either by draining out the water or filling with sand to prevent adults laying eggs. Current WHO recommendations [17,18] already charge private individuals with management of PBRPs within 100 m of their homes, which is likely to capture the majority of Aedes aegypti PBRPs [19,20], and places of public congregation. However we would suggest this be expanded to all owners of accessible spaces with the active encouragement and support of government agencies (an interesting example is the "domestic trap strategy"; Box 1). Such activities are likely to be regular, for example putting out garbage, or infrequent, for example putting lids on water containers, but are seldom labor intensive, assuming changes in routine behavior. Ironically, some urban areas may be more accountable to individuals than municipal authorities as facilities (such as piped water or sewerage) fail to keep pace with urban spread [21,22]. BOX 1. Domestic traps: Crowdsourcing Aedes elimination. Controlling domestic pests like cockroaches, fleas, flies or ants depends on denying them basic resources (e.g., exposed food and breeding places). However, more radical measures are often needed, and traps are a popular choice, not only due to their effectiveness, but also because they (as opposed to chemical sprays) present less danger to humans and pets. The use of mosquito traps domestically is, however, not simple. For example, blood-feeding traps are not practical, as they can hardly compete with mosquitoes' attraction towards human bodies. Similarly, nectar-feeding based traps have no specificity, and would kill many insects (including bees and butterflies). Breeding traps, although potentially effective, are perceived as dangerous if not well implemented or supervised could promote the multiplication of mosquitoes.
Domestic breeding traps that eliminate the aquatic stages of mosquitoes hold great potential if their hazardous implementation can be eliminated. One way to attempt to bias oviposition to more manageable sites is the use of domestic traps that can be readily managed through regular reminders, once a week, for volunteer households and public facility managers who are charged with cleaning out the water in containers functioning as PBRPs [23][24][25].
The domestic trap strategy (which would be greatly beneficial to the Mosquito Drain; Box 2) is gaining impetus with the invention of an ingenious house-made trap made with widely available and affordable components ( Figure 2, an empty PET bottle, adhesive tape and few square centimeters of mesh fabric source). When the eggs hatch in the cone, the larvae migrate to the bottom of the trap through the mesh, but this same mesh prevents adult mosquitoes from leaving the trap. The "mosquitérica," as it is known, presents several advantages over other domestic trap methods. First, it eliminates the concern about occasional negligence in the periodic need to cleaning up and/or adding larvicide to breeding traps. Second, it is unlikely that mosquitoes would develop resistance to this sort of trap -as opposed to chemical spray or even traps that use larvicide (as in the latter case mosquitoes could avoid surfaces or breeding places based on the odors of those substances). And third, it has been shown that egg-laying females are most attracted to sites containing other immature Ae. aegypti [9] something this trap offers, since only the hatching adults are killed (by entrapment). Instructions for building such traps went viral in social networks, and it is having wide acceptance among the population.
This crowdsourcing method of mosquito elimination could be promoted by governments through, for instance, calls for co-ordinated action on a fixed date (e.g. mosquito eradication day [26]). Setting a weekly reminder during the epidemic season would be epidemiologically sound, as it is more frequent than the time of larval development (approximately 8-10 days), hence ideal for cleaning plant pots, water fountains, etc. Concerted action propelled by an official reminder (mainly in TV and social media) could create a collective drive and a positive sense of societal engagement-a study of community-based Aedes control showed, the most prominent benefit was the satisfaction created by 'working together' [27].
(B) Difficult to access, but accountable PBRP sites. Despite the best efforts of conscientious individuals, it can be difficult to eliminate all breeding places that can be hidden in corners of the urban landscape such as building cracks, roof gutters, crevices in the high trees canopy and slabs [1]. Both private and public agents who find such situations should be encouraged to request professional assistance. Legislation can also be used to improve building practices to   [29]. However, the inevitable existence of those PBRPs almost ubiquitously demand interventions that are applied in a "diffuse way", such as "peri-focal" interventions with residual insecticides [1], release of sterile adult mosquitoes or strategies involving multiple traps ("Mosquito Drain"; Box 2).

Box 2. Mosquito drain.
The Mosquito Drain is based on the idea of attracting females to ubiquitous oviposition places where larvae can be eliminated (e.g. domestic breeding traps, see Box 1) rather than natural, but inaccessible sites thereby eliminating the next generation of mosquitoes.
In an urban environment, some breeding and resting sites are likely to be inaccessible for cleaning and control (e.g., roofs, crevices, tree holes, etc.; Figure 1). However, not all potential breeding places are equally attractive to laying mosquitoes and "compete" for females' preference. Removal of accessible breeding sites would have the following effects on female mosquitoes in search for oviposition sites: 1. impel females to search for alternative potential breeding places; 2. impel females to over-disperse [30,31] (so infected mosquitoes will cover an area quicker) 3. reduce the quality of potential breeding places sought by females (potential reduction -but not elimination-of viable broods).
Because "egg-laying females were most attracted to sites containing other immature Aedes, rather than to sites containing the most food" [9], home traps could become especially attractive to gravid females, and therefore be disproportionally important in reducing the mosquito population. Alternatively, attractants can be added to encourage mosquitoes to preferentially use lethal ovitraps that can be managed or left to biodegrade rather than inaccessible natural PBRPs [32][33][34]. The Mosquito Drain posits that it is not necessary to eliminate all breeding sites to cause the population to crash, which would not be practicable anyway, but that by (i) removing manageable breeding sites (e.g. putting lids on water containers), (ii) providing alternative attractive breeding sites that are easily managed (e.g. 'lure' breeding adults with a suitable trap) and that (iii) kill future generations of mosquitoes (e.g. adding larvicide to ovitraps) would eliminate sufficient reproductive capability of the mosquito population as to drive the population to extinction or at least pushing the biting population below levels at which virus circulation is sustained.
This is a societal effort that depends on collaboration between (many) individuals and government agencies: individuals would be in charge of eliminating any larvae, pupae and/or eggs that could have been accumulated in domestic breeding places (like plant pots and fountains) whilst governments should broadcast a reminder and coordinate that effort. Government agencies would then be freed to tackle hard to access and public spaces.
(C) Accessible, but non-accountable PBRP sites. Neglected public spaces with rubble, trash (tires, cups, cans, plastic bags and discarded containers) and facilities in neglected public spaces and vacant lands or empty lots are accessible to individuals without special knowledge or expertise. Volunteers from the neighborhood (e.g. coordinated by the community), could engaged, and perhaps incentivized, by government or emerging from social media networks in clean-up campaigns where, periodically, debris is removed, trash cleaned, ditches on the ground sealed, and other sensible interventions that destroy and negate breeding sites for Aedes performed. A survey in Singapore found that vacant properties and construction sites (the latter more appropriately belonging to accountable sites) had a four to seven times higher premises index than landed premises (which were three and a half times higher than apartments) [19,35].
(D) Difficult to access and non-accountable sites. A comprehensive strategy that accounts for the whole gamut of access for mosquito control measures cannot ignore that there are patches where the capability of the government to influence behavior, enforce the law, or simply access places can provide major challenges -for example due to violent conflict. In those circumstances, top-down interventions (fogging, aerial fumigation, biological control and release of biologically modified Aedes males [7,11,36]) may be the only strategies that can promote vector control. We need to be caution about these approaches though, as these specialized and expensive activities offer diffuse control efforts that target adult mosquitoes rather than destroy PBRPs have a long history of use, but little recent evidence for effectiveness in reducing disease burden [37]. Restricting their use to epidemics is recommended because of cost and environmental impact [17].

A comprehensive approach for engaging society
Mosquito control depends on human actions, yet those actions are often at the mercy of legal and physical constraints. Dissecting the legal and physical complexity of contemporary urban ecosystems results in a categorization that can assist the effective implementation of interventions. These categoriesbased on the diversity of putative oviposition and resting sitescan be easily integrated into existing habitat management behaviors, and can be readily integrated into GIS mapping technologies to generate actionable information to tackle endemic infestations and unfolding outbreaks [29,38].
One principle reason for successful control in the past century was the implementation of aggressive top-down measures [8,12,39]. The erosion of governmental capabilities to interfere with individual liberties does not necessarily impede mosquito control, as that "loss" may be compensated by an increasingly technologically-savvy, knowledge-avid and social media linked population can be mobilized to combat mosquito populations [40][41][42]. The proposed framework assumes that it is possible to effectively engage the local population [7], not only by suppressing areas of infection where they can easily act (e.g. their properties), but also by collaborating in a forcing a "Mosquito Drain" (Box 2) to reach beyond their immediate domain of direct impact.
Prioritizing citizens' actions has several potential benefits: (a) reduced strain on limited public resources that are stretched during public health crises (e.g. epidemics); (b) individuals can act on more targeted and sustained activities [43]; (c) reduction of harmful interventions (e.g. use of fogging in urban spaces that can be practically managed by community initiatives). The local population is also most likely to recognize hotspots of mosquitoes [41,44,45] and appreciate local conditions of epidemiological importance [18]. Although evidence for effectiveness of individual community-based interventions is sparse [37], it appears that integrating community participation into schemes reduces costs and increases effectiveness [46][47][48].
Engaging populations need not be costly (in time or money) given new communication technologies [40] (Figure 3) and, by stimulating and coordinating positive bottom-up initiatives, health agencies can co-opt allies in collective health emergencies [49]. In contrast, topdown approaches to combat Aedes risk treating citizens like irresponsible actors (for example threatening fines [35,39]) fail to realize the emergent benefits of community participation.
Emphasizing the power of bottom-up initiatives is not meant to marginalize the role of topdown activities [7,8,12]: as shown in our categorization (Figure 1), even the most engaged community will not be able to manage all putative mosquitoes breeding sites. Public authorities have an immense role to play, but are perhaps more efficient exercising their mandate in the expensive activities of avoiding a state of neglect in public spaces that risks them becoming the foci of urban pests and then efficiently using a smaller budget to encourage and support societal initiatives (e.g. nudging behavioral change [52]) to address readily accessible environments that would otherwise rapidly drain central resources.
The challenge is also to effectively manage activities, whether top-down or bottom-up that risk being popular, but ill conceived. The WHO emphasizes detailed planning to achieve successful behavioral change and recommend a series of steps to capitalize on public engagement to avoid what they consider the two greatest barriers of doing nothing or, perhaps worse, doing the wrong thing (hence putting people off further interventions if their efforts fail) [50]. In addition to combating lack of knowledge or misinformation, governmental activities need to manage social engagement campaigns beyond planning and into co-ordination since such campaigns to change behaviors have been most successful when combined with feedback Figure 3. Interface from a citizen-science mosquito identification and reporting application used in Spain to assist in the surveillance efforts. Provided by mosquito alert CC-BY [41]. and regular reminders [39,51]-for example to clean out water containers, mosquito traps or remove refuse each week [17]. Over reliance on past success risks mosquito populations rebounding, for example because surveillance priorities shift and vigilance suffers [35].
The key challenge in community participation is sustaining interest. As an example of citizen engagement in action, in two Cuban cities house blocks were randomly enrolled in a trial to control PBRPs (2000)(2001)(2002), resulting in 75% reduction in Aedes populations through adding lids to water containers (i.e. monitoring accessible and accountable), repairing drains and transforming areas of garbage into (maintained) flowerbeds (i.e. accessible but not necessarily accountable) [53]. Importantly, these neighborhood task forces were still in operation 5 years later when there was an outbreak of dengue and proved cost and health effective [43,47,48]. However this sustainability may be unusual with evidence from other studies suggest that success may lead to changes in focus that risk lapses in effort [35], volunteers lose enthusiasm [22] and that adherence to control measures diminishes over time (though still out-perform no activity) [54,55], more so if initiatives (and official cajoling) end [21]. Evidence of citizen science mosquito surveillance suggests good initial participation that rapidly decreased [41], and the few studies that evaluate the effectiveness of community interventions, whilst generally positive for vector control, lasted a year of less [55,56]. Encouraging appropriate community participation in control measures is likely to be easier in the midst of epidemics when the benefits are visible, but it remains unclear whether this is sustainable in the longer-term in between episodes of, for example, dengue. That is why it is so important that control measures are "cross-cutting" within the context of a community, as we will see below.

Transforming cities in a large mosquito trap while improving their livability
Aedes-transmitted diseases are, largely, diseases emanating from neglected private and social spaces [57]. In backyards, buildings, vacant lands and empty lots, trash and untended structures provide perfect breeding places not only for Aedes mosquitoes, but also for many other urban and domestic pests. These neglected places have a negative impact on the environment and quality of life of the community, as well as on their economic development and safety [58]. Therefore, a campaign to remove mosquito breeding places is also a campaign to reinvigorate depressed or unplanned urban areas, thereby improving living conditions [59][60][61].
It is important to highlight that mosquito control has to be integrated into "cross-cutting" solutions for public health, turning societal vulnerabilities into resilience [61,62] i.e. what is good for elimination of Aedes, should also be beneficial on other societal fronts. For instance, environmental management of Aedes might discourage traditional ad hoc water storage practices such as private water-storage systems [16,28]. But resilience to crises and catastrophes are enhanced through decentralized and resource-autonomous societies [63], for example potable water that is locally collected, treated [64] and appropriately stored (so that it is inaccessible to mosquitoes) would still be available even if the water supply from a centralized provider is unavailable, disrupted or fails.

Conclusion
The impact of Aedes mosquitoes on human health and the prospect of losing the battle against this species requires urgent and scientifically sound strategies [6,7]. Here, we propose an adaptation to existing recommendations to rationalize, catalyze and coordinate the capabilities of modern society. More responsible societal co-ordination and allocation of limited resources based on existing accountability and physical accessibility can more effectively eliminate these deadly foes, but as a fortuitous by-product presents an opportunity to additionally improve the quality of life by improving the livability, cleanliness and beauty of shared social spaces.