Adult female cockroach feeding on gel bait. (Photo: John Obermeyer)
Despite the emergence of new active ingredients (AIs) and control technologies in the last decade, insecticide resistance remains one of the biggest challenges to effective cockroach control. This article revisits the now 60-year-old topic of cockroach resistance. It provides information on effective use of cockroach baits and advice on achieving long-term success in cockroach management programs while, at the same time, maintaining long-term product efficacy.
German Cockroaches as Pests.
Perhaps the main reason German cockroaches have become such important urban pests is their high reproductive potential. For example, German cockroaches have (on average) a three-month life cycle, females produce multiple egg cases in their lifetime from a single mating and there are 35 to 45 offspring produced per egg case.
German cockroaches are both aesthetic and health pests. Their mere presence and odors are enough to make us want to eradicate them, but on top of this, German cockroaches carry food-borne bacteria, and they produce at least six significant human allergens. With regard to allergies, we now know that German cockroaches are the leading cause of asthma among inner-city children in the United States (Gruchalla et al. 2005).
When considering these biological and human factors together (i.e., reproductive potential and pest status), it is no surprise that insecticides have been heavily used for cockroach management/control. As a result, cockroaches have developed resistance to nearly every insecticide and product targeted to them since the 1950s.
The Switch to Baits.
The federal Food Quality Protection Act (FQPA) was signed into law in 1996 and slowly took effect over the next several years. Some of the main provisions of FQPA included cancellation of most cholinesterase inhibitor pesticides, elimination of indoor broadcast applications, redefinition of “harm” as caused by pesticides to even molecular-level effects, and generally, increased emphasis on protecting children from pesticide exposure. Aside from the benefits of the FQPA, some of its long-term consequences have included the industry’s move to gel baits as a primary means for controlling cockroaches, and (allegedly) the resurgence of bed bugs because of the elimination of indoor broadcast applications (another story entirely!).
Gel baits have proven to be effective for the professional pest management industry since their large-scale use began in the late 1990s. Some positive aspects of gel baits include highly controlled and cost-effective deployment, new “low impact” AIs, highly palatable formulations, compatibility with IPM programs and horizontal transfer to other cockroaches leading to effects known as secondary and tertiary kill (Buczkowski et al. 2008).
Regarding IPM, gel baits can be effective when used in combination with a holistic IPM program (see box above), but what about when gel bait applications fail? When should we expect resistance to be the cause? Because cockroaches typically consume large amounts of gel baits (and thereby insecticide), baits have been thought to have a reduced resistance risk; however, decades of research have taught us that no pesticides are immune from resistance.
What Is Resistance?
What is resistance? Our working definition of resistance is: control failures that result from physiological and behavioral adaptations in cockroaches after exposure to insecticides in earlier generations.
In general, pesticide resistance develops following Darwinian evolutionary principles, meaning that it is “pre-adaptive” (resulting from natural mutations that are not caused by pesticides) and “selectable” (builds over time in response to removing non-resistant individuals from the population). In cockroaches, since there is widespread resistance to all but two or three AIs ever used, we can safely conclude resistance is probably an inevitable consequence of all insecticidal pest management. In fact, some data suggests that once low-level resistance is detectable in a cockroach population, it can progress to problem levels in as little as one generation (Scharf et al. 1998).
In terms of contact insecticides, some older materials and their year of first documented resistance in German cockroaches are as follows: chlordane (1953), pyrethrins (1956), DDT (1959), chlorpyrifos (1980), bendiocarb (1987) and cypermethrin (1998).
Regarding bait actives, isolated cases of low-level resistance have been reported to fipronil (2003) and abamectin (2004). A recent case study of fipronil susceptibility in the “GNV-R” field strain from Gainesville, Fla., identified 35x resistance to fipronil by enzymatic and nerve-insensitivity mechanisms, which is the highest level of fipronil resistance yet reported in the refereed scientific literature (Gondhalekar & Scharf 2012). Interestingly, this strain also had resistance levels more than 100x to DDT and cyclodienes, more than 70x to pyrethroids, 25x to organophosphates and 13x to carbamates, but only 5x resistance to another bait active, indoxacarb. It is important to note, however, that the GNV-R strain remained susceptible to a fipronil bait product containing a higher concentration of AI.
Resistance Monitoring Studies.
Presently, a major bait product in use in the global pest control market is Syngenta Professional Products’ Advion gel bait containing the AI indoxacarb, which was introduced commercially in 2006. Our research program on indoxacarb began with the development of susceptibility monitoring bioassays that used lower concentrations of AI than appeared in commercial products (Gondhalekar et al. 2011). This strategy allowed us to see resistance development in its earliest stages — something never before accomplished in the history of chemical cockroach control.
As a next step, we collected 13 cockroach populations from across the United States and tested them in the monitoring program using both feeding and surface-contact bioassays (Gondhalekar et al. 2013). We found that most populations remained susceptible to Advion bait, but we did find one potential problem strain from North Carolina, and another from Cocoa Beach, Fla., that increased its tolerance levels by 2x with one year of exposure to indoxacarb and fipronil baits.
Despite showing the potential for resistance development, all strains tested remained susceptible to formulated product. Also, although a recent study reported on the sensory mechanism involved in glucose aversion-based bait resistance (Wada-Katsumata et al. 2013), our studies have yet to reveal any evidence of behavioral resistance to indoxacarb or fipronil baits. Glucose aversion has been known to exist for more than 20 years and manufacturers have acknowledged its presence and adjusted bait formulations accordingly for nearly as long (Silverman & Bieman 1993; Wang et al. 2004). More importantly, these research findings underscore the need for routine use of resistance management practices in all cockroach management programs, as well as emphasize the need for effective, science-based resistance management programs.
Adult male cockroach feeding on gel bait. (Photo: John Obermeyer)
Three general strategies are applicable for resistance management in cockroaches and other urban pests: (1) insecticide rotations, (2) insecticide mixtures and (3) non-chemical IPM. For rotation-based resistance management (see graph on page 44), insecticide products and formulations are used in sequence, on a generational basis. For German cockroaches the average generation time is three months, thus, we recommend (1) rotating AIs every three months and (2) rotating through at least three AIs before returning to the original. In this case, the term “AI” is used rather than “product” because in some cases the same AIs exist in different products or formulations, such as baits and sprays. Ongoing research may result in eventual modification to this recommendation, but the “three-month/three-AI” strategy is the most well-developed strategy available at the present time (Scharf et al. 1998; Gondhalekar et al. 2013).
Although more research is needed to better define rotation parameters especially for bait products, rotations are recognized as the most viable resistance management option by the Insecticide Resistance Action Committee (IRAC). IRAC is a consortium of insecticide manufacturers with a vested interest in product preservation and stewardship. The IRAC web site (www.irac-online.org) provides mode of action classification information that is updated annually to assist pest managers in choosing AIs for use in rotations. Other useful information on insecticide classifications and mode of action can be found in an earlier PCT article (Scharf & Suiter 2011).
Mixture-based resistance management involves the use of two insecticide AIs concurrently. For mixtures to be effective and not cause greater resistance problems, both AIs have to be equally persistent and no cross-resistance can exist between them. It is for these two reasons primarily that the mixture strategy is not considered compatible with baiting.
The only viable mixture options for cockroach control are (1) newer spray products that combine two AIs (e.g., nicotinoids + pyrethroids; Syngenta’s Tandem, FMC Corp.’s Transport, Bayer Environmental Science’s Temprid) or (2) mixtures of conventional insecticides (pyrethroids) and synergist products that contain PBO or MGK-264, etc. Synergists are essentially non-toxic on their own, but when combined with insecticides, will block insect detoxification and increase the contact insecticide’s potency. Conversely, mixing two different products or formulations with the same AI would be considered disadvantageous (e.g., Advion and Syngenta’s Arilon, or BASF’s Alpine spray and bait), since this would only increase resistance to the AI if it already existed.
Finally, IPM and other non-chemical pest management approaches can be excellent strategies for resistance management. These non-chemical approaches may not work well as stand-alone techniques, but there is no question they make conventional insecticides and baits more effective. First and foremost is sanitation, which limits food and moisture that compete with baits and reduces clutter and harborage, making baits more accessible to cockroaches.
Exclusion is effective for preventing new cockroaches from entering an account and keeping them from accessing resources in adjoining locations. Trapping and vacuuming carry additional costs (particularly vacuuming in terms of time), but these two techniques can be very effective for physically removing cockroaches from an account. Likewise, heat can be a costly approach, but with the growing availability of heating equipment for bed bug control, this is certainly another cockroach IPM tool for PMPs to consider. Finally, client communication or “Integrated People Management” underlies all successful, long-term cockroach control programs. Teaching clients and occupants how to identify and prevent conducive conditions for cockroaches will pay big dividends when it comes to maximizing the efficacy of chemical control.
In summary, insecticide resistance is a heritable, evolutionary phenomenon that can progress towards problem levels in as little as a single generation. Resistance can be caused by physiological factors, where pests develop biochemical mechanisms that allow them to tolerate insecticides (most common), or behavioral changes, where pests can better detect components of insecticide baits or sprays and thus avoid AIs (less common and does not involve “learning”).
Insecticide resistance in German cockroaches was first noted more than 50 years ago and, despite having new AIs and delivery methods, it persists through the present day. Unfortunately, resistance does not evolve the same way in every situation for every insecticide, and thus it is extremely difficult to predict the effective market life for any product. For this reason, resistance monitoring programs are of key importance. In this case, resistance monitoring can involve sending field-collected strains to consultants or university researchers for testing, or it can be done by PMPs themselves by holding collected cockroaches directly with gel baits — any survival past 72 hours is a strong indicator that resistance is present.
Also, importantly, we recommend that PMPs make some kind of resistance management practice mandatory in their regular business operations (especially rotation and non-chemical IPM). The integrated use of product/AI rotations and non-chemical pest management is the best option available for resistance prevention and management. Many resources are available for developing your own custom resistance management programs, including the refereed scientific literature, industry consultants, academic scientists and IRAC Internet resources available at www.irac-online.org.
Authors’ note: We thank Gary Bennett and Grzesiek Buczkowski for helpful feedback, and acknowledge DuPont, Syngenta and the O.W. Rollins/Orkin Endowment at Purdue University for research support.
Ameya D. Gondhalekar is a research assistant professor and Michael E. Scharf is O.W. Rollins/Orkin Chair at the Center for Urban and Industrial Pest Management, Department of Entomology, Purdue University.
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