Field efficacy of deltamethrin for rodent flea control in San Bernardino County, California, U.S.A.

December, 2004 Journal of Vector Ecology 212 Field efficacy of deltamethrin for rodent flea control in San Bernardino County, California, U.S.A. Lal S. Mian 1, James C. Hitchcock 2, Minoo B. Madon 2, and Charles M. Myers 2 1 Department of Health Science and Human Ecology, California State University, San Bernardino, CA 92407-2397, U.S.A. 2 California Department of Health Services, Vector-Borne Disease Section, 2151 Convention Center Way, Suite 218B, Ontario, CA 91764-5429, U.S.A. Received 6 September 2003; Accepted 8 January 2004 ABSTRACT: A study was conducted to determine the initial and residual activity of deltamethrin (0.05% dust) applied to rodent burrows (at approximately 14 g/burrow) against fleas in the Silverwood Lake area of San Bernardino County. In initial toxicity (2-d post-treatment), deltamethrin provided 97% flea control and in residual toxicity it resulted in 68% control of the rodent fleas at 15-d post-treatment. The flea fauna consisted of Oropsylla montana (89.9%) and Hoplopsylls anomalus (10.1%). All rodents captured in this study were California ground squirrels, Spermophilus beecheyi. In mark-release-recapture trials, using the microchip identification implant method at the treatment site, the recapture rate of rodents was 29% from 2- to 58-d post-treatment, declining to 21% after 98 d. In the tail-clip method at the treatment site, the recapture rate of 40% at 15-d post-treatment rose to 87% and 73% at 56- and 58-d post-treatment, respectively. At the control site, the recapture rate of 100% at 15-d post-post-treatment dropped to 20% after 98 d. In another trial at Camp Cedar Crest in the Running Springs area, deltamethrin applied to rodent burrows resulted in 70% control of fleas infesting S. beecheyi. Based on the two trials, deltamethrin showed a good initial control of rodent fleas in enzootic or epizootic plague control. Journal of Vector Ecology 29 (2): 212-217. 2004. Keyword Index: Deltamethrin, flea control, plague, rodents (S. beecheyi). INTRODUCTION Plague is primarily a rodent-borne disease caused by the bacterium, Yersinia pestis. It is transmitted from host to host by the bite of infected fleas, through blood contamination in septicemic plague, or through inhalation in pneumonic plague (Meyer 1949, Poland and Barnes 1979). Humans are potentially exposed to the disease when they enter epizootic plague areas. In the southwestern United States in general and California in particular, plague enzootic foci are distributed over vast areas from sea level to foothills and mountainous ranges (Anonymous 1983). Sporadic epizootics occur from time to time. Plague surveillance in known enzootic areas is routinely carried out by local and/or state health agencies. In the event of plague activity as evidenced by plague positive antibody titers, infected fleas, a human or an animal case, flea control through the use of a registered chemical insecticide may be necessary to reduce the risk of human exposure to the plague organism. The number of choices for effective flea control is getting smaller due to environmental concerns. Insecticides with actual or potential use in rodent flea control include diazinon (Smith and Lusk 1990), permethrin (Beard et al. 1992, Gage et al. 1997), methoprene (Lane et al. 1998), lufenuron (Davis 1999), and aluminum phosphide (Fumitoxin) (Mian et al. 1997). In California, diazinon 2D, under a special use permit, is used as a burrow treatment or in bait stations to control rodent fleas at campgrounds and public parks. To augment the list of available insecticides in rodent flea control, deltamethrin, based on its label information, appears to be a good candidate to be evaluated for its efficacy against rodent fleas. The present study was carried out to determine the efficacy of deltamethrin in rodent flea control with data on rodent mark-release-recapture under actual field conditions. MATERIALS AND METHODS The study was conducted during the summer of 1997 at a group campsite west of Silverwood Lake, San Bernardino County, California. The site s coordinates (N34.17.31 latitude, W117.21.81 longitude, and 3,130

December, 2004 Journal of Vector Ecology 213 ft. altitude), were determined with a commercial GPS unit. The campsite is surrounded by a paved road to the east and north, a dry stream to the south, and sparsely vegetated flat ground to the west. In an east-west transect, the site is divided into three sub-sites, namely Valle, Baranca, and Rio. Valle was selected for the treatment, with Rio serving as a control and Baranca as the buffer zone. Pre-treatment Prior to the pesticide treatment, a rodent-flea survey was carried out at both the Valle and Rio sites using Tomahawk live traps (Lang and Wills 1991). After capture, the animals were anesthetized with ethyl ether while still in the traps. Using a sturdy toothbrush, fleas from each animal were brushed into a white enamel pan (34.3 x 25.4 x 3.8 cm deep) and transferred into prelabeled glass vials containing 2% saline solution. At the Valle site, blood samples were also drawn from the animals to test for plague antibodies at the California Department of Health Services or the University of California, Davis Laboratory. Treatment At the Valle site, deltamethrin (DeltaDust R, 0.05%) was applied to 113 active rodent burrows at the rate of approximately 14 g/burrow, using a 0.5 liter plastic bottle (hand duster type) with a dispenser (90 cm x 1.25 cm dia.) attachment. The dose per burrow was based on 2 g/ yd 2 of dust applied for 7 d (range 5-10 d). Every attempt was made to put the dust right into the burrow to avoid any environmental contamination. At both the Valle and Rio sites, post-treatment evaluations were carried out at 2-, 14-, 56-, and 98-d intervals. Each captured animal was processed to determine the flea index. The data on fleas and rodents were statistically analyzed. Percent flea control at each post-treatment interval was calculated according to the formula: % Control= C 1 x T 1 / C 2 x T 2 where C 1 and C 2 were pre- and post-treatment infestations in the control and T 1 and T 2 pre- and posttreatment infestations in the treatment, respectively (Mulla et al. 1971). Rodent recapture In a preliminary mark-release-recapture study, 24 animals were marked with the Avid microchip (Avid Identification System, Inc., Norco, CA) technology during the pre-treatment survey at the Valle site only. A pre-programmed identification number on a microchip was subcutaneously implanted into each animal s shoulder before it was released back into the habitat. Animals captured in subsequent trappings were scanned for reading the numbered chip. At the 2-d post-treatment trapping, however, 15 animals each at the Rio and Valle sites were marked by square clipping their tails to elucidate the recapture rate. Follow-up treatment In a follow-up study, the effectiveness of deltamethrin against rodent fleas was also evaluated at a plague-active private group camp, Cedar Crest, near Running Springs, San Bernardino County. This site, at an altitude of 6,300 ft, N34.13.00 latitude and W117.04.30 longitude, is approximately 30 km east of the Silverwood Lake campgrounds. The campsite reporting a rodent die-off was surveyed according to the method described earlier. Both blood samples and fleas collected (24 combined into one pool) during the survey were sent to the California Department of Health Services (CDHS) to test for plague activity. Serological tests were negative for the plague antibodies. The flea pool tested positive for Y. pestis by bacteriological culture and mouse inoculation. According to CDHS protocol, the campsite was closed for public use and plague warning signs were posted all over the campsite advising people to take extra precautions (Mian 1995). Because it was a privately owned facility, a licensed pest control operator was contracted to dust all visible rodent burrows around buildings with 0.05% deltamethrin dust. Following posttreatment evaluations 2 d later, the authors determined the flea index of the local rodent population. The data were analyzed using PSI-Plot (1993). With pre- and posttreatment flea indices, percent control was calculated. The post-treatment flea index was used in risk assessment of human exposure and reopening of the camp for public use. RESULTS AND DISCUSSION In pre-treatment surveys at the Rio and Valle sites, rodent flea composition by species was 89.9% Oropsylla montana (Baker) and 10.1% Hoplopsylla anomalus (Baker), infesting the California ground squirrels (CGS), Spermophilus beecheyi (Richardson). Earlier studies have reported O. montana and H. anamalus as the primary species infesting the CGS (Barnes 1982, Mian and Hitchcock 1998). Whereas percent species composition remained consistent at both sites, flea infestation was significantly higher (2X, P> 0.05) at Valle than at Rio (Table 1). Data on pre- and post-treatment rodent surveys and flea infestation in both control and treated sites and percent flea control in the treated area are presented in Table 2. All rodents trapped in this study

214 Journal of Vector Ecology December, 2004 Table 1. Rodent flea composition by species collected during pre-treatment evaluations at the Rio and Valle campsites, Silverwood Lake, San Bernardino County, CA. Rio Valle Total Species #(M/F) % #(M/F) % # % Oropsylla montana 78(29/49) 90.7 168(68/100) 89.4 246 89.9 Hoplopsyllus anomalus 8(3/5) 9.3 20(3/17) 10.6 28 10.1 Total 86(32/54) 100 188(71/117) 100 274 100 Chi-square value 37.97* *Significant (P=0.05) were S. beecheyi. The number of rodents trapped, percent rodents with fleas, number with > 5 fleas, and the flea index were all higher in the treatment area (Valle) than those of the control (Rio). In initial toxicity, deltamethrin provided 97% flea control at 2-d post-treatment. In residual activity, it gave 68% flea control for up to 15 d, beyond which residual activity dropped to zero and 46% after 56 and 98 d post-treatment, respectively. The drop in activity at the 56-d mark could be due to a number of factors, such as rodent migration from surrounding untreated areas, rodents from hidden untreated burrows within the treated area, or animals from treated burrows visiting untreated burrows before being trapped. In the microchip ID implant method, the recapture rate remained at 29% for up to 56 d, falling to 21% after 98 d post-implant (Table 3). Of the 24 animals with ID implant, nine were not recaptured; the remaining 15 were recaptured one or more times. Of those captured initially with flea infestation, eight showed no fleas in subsequent recaptures. There were five animals (#038, 617, 772, 817 and 866) that, after exhibiting zero infestation at 2- to 15-d post-treatment, showed elevated numbers (2X- 5X of initial infestation level) of fleas at 56-d posttreatment. This suggested that the animals either visited Table 2. Data on rodents and their fleas collected pre- and post-treatment with deltamethrin dust (0.05% ) at two camp sites, Silverwood Lake, San Bernardino County, CA. Pre-treatment Post-treatment (days) Parameter 0 2 15 56 98 Chisquare* Rodents caught-valle 1/ 27 23 17 21 19 2.75 ----Rio 2/ 15 21 15 30 16 8.5 # with flea-------valle 25 5 11 19 12 2.13 -------Rio 11 21 13 25 13 8.9 % infestation----valle 92.6 21.7 65 90.6 63.2 50.6* ----Rio 73.3 100 86.7 83.3 81.2 4.5 Flea range/host-valle 0-23 0-5 0-8 0-28 0-10 -- --Rio 0-17 1-34 0-13 0-18 0-8 -- # with >5 flea---valle 18 1 2 14 3 31.2* ----Rio 8 15 7 7 3 9.5 Total fleas-------valle 188 12 31 211 37 232.6* -------Rio 86 200 69 103 43 143.8* Flea index-------valle 7.23 0.57 1.82 10.04 1.94 15.7* --------Rio 5.86 9.52 4.60 3.43 2.68 5.5 % Control 97 68 0 46 *Significant (4 df, P=0.05); 1/ treatment site; 2/control site

December, 2004 Journal of Vector Ecology 215 Table 3. Mark-release-recapture of California ground squirrels at the Valle campsite, Silverwood Lake, San Bernardino County, CA, using the chip implant method. Rodents 1/ Recapture of implanted rodents (R) with fleas (#) at different interval (days) after treatment ID #(fleas) Sex Stage/State 2 15 56 98 Frequency 038 (7) F J R (0) R (19) 2 058 (2) F A R (0) R (0) 2 075 (6) F A/L 0 097 (5) F J R (2) 1 098 (17) F A/L 0 099 (2) M J R (8) 1 124 (3) F J R (0) 1 295 (23) F A/L R (1) 1 301 (0) F A/L 0 337 (8) M J 0 377 (7) F A/PL R (6) R (1) 2 526 (2) F J R (8) R (0) 2 597 (8) F A/P R (1) R (20) 2 612 (12) F J R (1) 1 617 (2) F A/PL R (0) R (11) R (6) 3 633 (5) M J 0 772 (17) F A/PL R (0) R (0) R (28) R (0) 4 776 (11) F J 0 790 (6) F A/P R (0) 1 798 (3) M A/S 0 811 (28) F A/L 0 817 (1) F A/L R (0) R (4) 2 866 (5) A J R (15) 1 869 (9) F A/PL 0 Total 7 7 7 5 26 Mean 0.29 0.29 0.29 0.21 0.27 A adult, F female, J juvenile, L lactating, M male, PL post-lactating, R-recaptured, S-scrotal Table 4. Mark-release-recapture rate of California ground squirrels at Silverwood Lake camp sites, San Bernardino County, CA, using the tail-clip method. Percent recapture at post-treatment interval (days) Method 2 15 56 96 Rio (N=15) 40 40 87 73 Valle (N=15) 100 100 47 20 Chi-square 25.71* 25.71* 11.94* 15.10* *Significant (P=0.05)

216 Journal of Vector Ecology December, 2004 Table 5. Evaluation of deltamethrin (0.05%) in rodent flea control at Camp Cedar Crest, Running Springs, San Bernardino County, CA. Pretreatment Posttreatment* Chi-square value** Number of rodents trapped 19 14 0.75 Number of rodents w/ fleas 13 5 3.55 % infestation 68.4 36 9.85* Number of rodents with >5 fleas 3 0 3.0 Number of fleas collected 40 9 19.6* Number of fleas range/host 0-11 0-4 3.26 Flea index 2.1 0.64 0.78 % Control 69.5 *2-days post-treatment **Significant (P=0.05) untreated burrows or treated burrows that had sub-lethal residues of the insecticide. Overall, this method, unlike the tail clip method, provided a more accurate account of individual animals recaptured in subsequent posttreatment trappings. Further studies using a larger sample size are needed to elucidate the application of the ID implant method in plague surveillance and control programs. In the tail-clip method, data on recaptured rodents showed a recapture rate of 100% during the first two wk in the untreated area, declining to 47% and 20% after 56- and 98-d post-treatment, respectively (Table 3). In the treated area, however, the recapture rate of 40% at 15-d post-treatment climbed to 87% and 73% after 56 and 98 d of treatment, respectively. In a subsequent trial at Camp Cedar Crest, following a plague positive flea pool and treatment with deltamethrin (Deltadust R, 0.5%) by a commercial pest control operator, post-treatment flea control was evaluated (Table 5). The data showed 69.5% flea control, resulting in a flea index of 0.64, down from a pretreatment flea index of 2.1. The animals trapped and tested in this trial included 14 male and 19 female S. beecheyi. During epizootic plague activity where a high risk of human exposure to the plague bacterium is evident, flea control is recommended to reduce the potential of flea bite transmission. A level of one flea or less per animal (flea index) is used as the criterion for reducing the human risk potential. A recreational facility showing plague activity may be temporarily closed for flea treatment and following a successful post-treatment evaluation and lowered flea index may be reopened for public use. Based on the foregoing discussion, deltamethrin provided a quick initial knockdown of rodent fleas and a residual activity of 68% control up to 15 d posttreatment. This product may be considered as an additional option in plague management programs in California and elsewhere. Its availability for use in recreational use facilities will require permission by the proper regulatory authority, special local need registration, or some language change in the product label. The current label restricts the use of deltamethrin to rodent burrows around buildings without specifying a maximum distance. Acknowledgments Lawrence Cermak and David Sullivan, California Department of Parks and Recreation, Silverwood Lake, are acknowledged for their collaboration during the course of this study. Acknowledgement is also due to Margie Koehler, AgrEvo Environmental Health, Inc. (currently Bayer Chemicals), for supplying deltamethrin (DetlaDust R ) for testing in the field. Last, but not least, Chris Nwadike, San Bernardino County Vector Control Program, Division of Environmental Health Services, San Bernardino County Department of Public Health, is acknowledged for his assistance in this study. REFERENCES CITED Anonymous. 1983. Plague. In: Control of Communicable Diseases in California. pp. 320-326. CA Dept. Hlth. Serv., Sacramento, CA. 594 pp. Barnes, A. M. 1982. Surveillance and control of plague in the United States. Symp. Zool. Soc. Lond. 50: 237-270.

December, 2004 Journal of Vector Ecology 217 Beard, M.L., S.T. Roes, A.M. Barnes, and J.A. Montenieri. 1992. Control of Oropsylla hirsute, a plague vector, by treatment of Prairie dog burrows with 0.5% permethrin dust. J. Med. Entomol. 29: 25-29. Davis, R.M. 1999. Use of orally administered chitin inhibitor (lufenuron) to control flea vectors of plague on ground squirrels in California. J. Med. Entomol. 36: 562-567. Gage, K.L., G.O. Maupin, J. Montinieri, J. Piesman, M. Dolan, and N.A. Panella. 1997. Flea (Siphonaptera: Ceratophyllidae, Hystrichopsyllidae) and tick (Acarina: Ixodidae) control on wood rats using hosttargeted liquid permethrin I bait tubes. J. Med. Entomol. 34: 46-51. Lane, R.S., L.E. Casher, C.A. Peavy, and J. Piesman. 1998. Modified bait tube controls disease-carrying ticks and fleas. CA Agric. 52: 43-47. Lang, J.D. and W. Wills. 1991. Ecology of sylvatic plague in the San Jacinto mountains of southern California. Bull. Soc. Vector Ecol. 16: 183-199. Meyer, K.F. 1949. Plague, Pasteurella pestis. In: R.J. Dubos (ed.). Bacterial and Mycotic Infections of Man. pp. 415-432. J.B. Lippincott Co., Philadelphia, PA. 785 pp. Mian, L.S. 1995. Guidelines for surveillance and control of plague in California. In: W.K. Reisen, V.L. Kramer, and L.S. Mian (eds). Interagency Guidelines for the Surveillance and Control of Selected Vector-borne Pathogens in California. pp. 57-75. Disease Control Subcommittee, Mosquito and Vector Control Association of California. Sacramento, CA. 94 pp. Mian, L.S. and J.C. Hitchcock. 1998. Plague surveillance in San Bernardino County: A decade (1988-97) in review. Proc. Papers Mosq. Vector Contr. Assoc. Calif. 66: 89-94. Mian, L.S., C.N. Nwadike, J.C. Hitchcock, M.B. Madon, and C.M. Myers. 1997. Plague activity in San Bernardino County during 1996. Proc. Papers Mosq. Vector Contr. Assoc. Calif. 65:76-79. Mulla, M.S., R.L. Norland, D.M. Fanara, H.A. Darwazeh, and D.W. McKean. 1971. Control of chironomid midges in recreational lakes. J. Econ. Entomol. 64: 300-307. Poland, J.D. and A.M. Barnes. 1979. Plague. In: J.H. Steele (ed.) CRC Handbook Series in Zoonoses, Section A: Bacterial, Rickettsial, and Mycotic Diseases. Vol. 1. pp. 515-556. CRC Press, Boca Raton, FL. 643 pp. PSI-Plot. 1993. Poly Software International: Technical Plotting and Data Processing, Salt Lake City, UT. Smith, C.R. and E.E. Lusk. 1990. Field evaluation of bendiocarb, chlorpyrifos, diazinon and permethrin for control of plague vectors in the northern Sierra Nevada of California. Proc. Calif. Mosq. Vector Contr. Assoc. 58: 169-175.