Prairie Dogs, Persistent Plague, Flocking Fleas, and Pernicious Positive Feedback

Abstract

Plague (caused by the bacterium Yersinia pestis ) is a deadly flea-borne disease that remains a threat to public health nearly worldwide and is particularly disruptive ecologically where it has been introduced. We review hypotheses regarding maintenance and transmission of Y. pestis , emphasizing recent data from North America supporting maintenance by persistent transmission that results in sustained non-epizootic (but variable) rates of mortality in hosts. This maintenance mechanism may facilitate periodic epizootic eruptions “in place” because the need for repeated reinvasion from disjunct sources is eliminated. Resulting explosive outbreaks that spread rapidly in time and space are likely enhanced by synergistic positive feedback (PFB) cycles involving flea vectors, hosts, and the plague bacterium itself. Although PFB has been implied in plague literature for at least 50 years, we propose this mechanism, particularly with regard to flea responses, as central to epizootic plague rather than a phenomenon worthy of just peripheral mention. We also present new data on increases in flea:host ratios resulting from recreational shooting and poisoning as possible triggers for the transition from enzootic maintenance to PFB cycles and epizootic explosions. Although plague outbreaks have received much historic attention, PFB cycles that result in decimation of host populations lead to speculation that epizootic eruptions might not be part of the adaptive evolutionary strategy of Y. pestis but might instead be a tolerated intermittent cost of its modus operandi . We also speculate that there may be mammal communities where epizootics, as we define them, are rare or absent. Absence of plague epizootics might translate into reduced public health risk but does not necessarily equate to inconsequential ecologic impact.

Managing plague on prairie dog colonies: insecticides as ectoparasiticides

“…Deltamethrin and fipronil suppressed fleas for at least 12 months (for other examples of similar effects, see Biggins et al 2010, Tripp et al 2017, Poché et al 2017, Eads et al 2019, Eads and Biggins 2019). Deltamethrin and fipronil might be used in rotation for integrated plague management on BTPD colonies (Eads et al 2019).…”

“…We infused ∼8 g of deltamethrin dust per burrow, considerably more than the common rate of 4–6 g. Delivering a higher dose may provide more consistent delivery of a minimum effective dose. Moreover, in some cases, using more than 4–6 g of deltamethrin dust may overcome flea resistance, allowing for effective flea control (Eads and Biggins 2019).…”

“…Previous deltamethrin treatments at Prairie Wind in 2016 and a potential lingering effect of deltamethrin (Eads and Biggins 2019) may have affected our experiments in 2018–19. Any lingering effect of deltamethrin on the baseline sites should have suppressed ectoparasite densities on those sites, thereby reducing our ability to detect significant trends in 2018–19.…”

“…The most widely used insecticide is deltamethrin, which is infused into PD burrows, usually with specialized machinery. When infused at 4–6 g/PD burrow (Biggins et al 2010), deltamethrin dust is capable of suppressing fleas for 12 months, and sometimes up to at least two years (Eads and Biggins 2019). With repeated use of deltamethrin on PD colonies, however, fleas can develop resistance (Eads et al 2018), motivating research on additional insecticides.…”

Enzootic maintenance of sylvatic plague in Canada's threatened black‐tailed prairie dog ecosystem

“…Drier conditions are likely to increase the intensity of flea infestation indirectly through an effect on food availability, which can lower host body conditions and consequently affect both immune system and behaviorally mediated ectoparasite defenses negatively (Eads et al 2016). Higher intensity of flea infestation can further diminish BTPD body condition (Beldomenico and Begon 2010), as well as potentially elevate the risk of plague‐related mortality—thus creating positive feedback cycles (Biggins and Eads 2019)—even if this does not reach the magnitude of an outbreak. Given indications that burrow dusting positively affects BTPD abundance, our data support the value of reducing flea prevalence through insecticide application, particularly during drier periods.…”