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Bot fly (cuterebrid) prevalence and intensity in Southern Illinois peromyscus species and a comparison to the literature.

INTRODUCTION

Bot flies are a group of parasitic insects found in wild mammals. These parasitic flies are included in the Cuterebridae (Sabrosky 1986) or the Cuterebrinae subfamily of the Oestridae (Wood 1987; Pape 2001). There are over 30 Cuterebra species that have evolved to be host-specific obligate parasites (Sabrosky 1986; Wood 1987). Each of these species typically parasitizes only one or just a few species of two separate groups: (1) New World rodents, which include mice, rats, chipmunks, tree squirrels, and voles; and (2) lagomorphs which are comprised of rabbits and hares (Slansky 2007). Once infected, some studies have reported that the host individuals are well adapted and have no negative side effects, while other studies cite a need for further research on the impacts of these parasitic insects (Jaffe et al. 2005, Cramer and Cameron 2006)

Previous studies have indicated that prevalence (percentage of individuals infected) varies depending on the species of bot fly (Margolis et al. 1982). However, intensity (number of parasites per individual host) is not as commonly reported. The objective of this study was to document the prevalence and intensity of bot fly infection on Peromyscus spp. in southern Illinois upland hardwood forests.

METHODS

Six forested sites were established at Touch of Nature Environmental Center (UTM: 16S 308552, 4167338) in Jackson County in southern Illinois. Study site elevation ranged from 150-180 m and the soils were primarily well-drained, silty, alfisols. Average winter temperatures in the study area range from -6.7 to -1.1 [degrees]C and summer temperatures from 15 to 27 [degrees]C. Average annual precipitation is 122 cm per year. Each of the forested sites consisted of a 0.5 ha area within which a trapping web was established

The results of this study are part of a larger two-year project. Data is only presented for the trapping period from between July 23 and August 9, 2013. This is the only period when cuterebrid larvae where observed and during this time each of the six sites was trapped once. Each site had fifty Sherman live traps (H. B. Sherman Traps, Tallahassee, FL; 7.5 x 9.0 x 23.0 cm) that were arranged in a trapping-web design. Trapping webs consisted of 12 transects that were 40 m in length, all extending from a central point in 30[degrees] increments. Traps were set along each transect at 10, 20, 30, and 40 m. Two additional traps were placed in the center of the web, resulting in 50 traps per web. For bait, birdseed was placed inside each trap. All trapping efforts met the Southern Illinois University Institutional Animal Care and Use Committee protocol standards. Trapping was conducted daily each morning, from Tuesday until Friday.

All trapped individuals were examined for the presence of cuterebrid larvae and the intensity of infection within the host. Toe-clipping was used to identify individuals over the trapping period. Once all observations had been recorded and the specimen had been marked for recapture, the specimen was released in the same location that they were captured.

RESULTS

A total of 91 Peromyscus spp. individuals were caught throughout the three weeks of trapping. Among all six sites, average prevalence was 71.55% and average intensity was 1.49 bot flies per individual host. Bot flies can be identified to species by determining their preferred host, infection area on the host's body, and the seasonal occurrence of the myiasis. During this study, cuterebrid larvae were only found in hosts during the July 23-August 9 trapping period. Unfortunately, previous trapping in the area had concluded on June 14 and therefore we are unable to pinpoint the specific time when the bot fly infections began. A high percentage of individuals were still infected at the end of the trapping season but no more trapping was conducted making the range of seasonal infection hard to determine. The preferred hosts of the suspected species of Cuterebra are Peromyscus maniculatus and Peromyscus leucopus. All the infected individuals caught had one or more bot flies in the inguinal area, near the genitals. No other locations on the host's body were witnessed. With this information we determined that the species of Cuterebra being encountered was most likely Cuterebra fontinella. Peromyscus leucopus and P maniculatus are hosts of C. fontinella (Catts 1982; Cogley 1991). Typically the larval stage of this parasitic species develops near the inguinal area, as well as the rump (Catts 1982; Cogley 1991). It also has a seasonal occurrence of myiasis during the months of August through October which coincides with the dates that our infected individuals were caught (Hensley 1976; Catts 1982).

DISCUSSION

Multiple studies have examined at bot fly infection rates in P leucopus and P maniculatus throughout North America (Table 1). The reported prevalence from this study is considerably higher than almost all other bot fly field studies (Table 1). Wecker (1962), who conducted a small mammal trapping study in an oak-hickory forest in Michigan, had the closest prevalence values, ranging from 14.1-65.9%. Our values ranged from 50-82% which is considerably higher. Jaffe et al. (2005) reported prevalence over a 20 year trapping study in Pennsylvania. Overall, mean prevalence was 6.95% in P maniculatus, 9.09% in P leucopus. Prevalence peaked during the late summer and early fall season but was less than 50% for P maniculatus and 60% for P leucopus.

It is difficult to explain the higher prevalence rates observed in our study. Very little is known about the habitat preferences and associations of cuterebrid species, although seasonal and annual variations in prevalence have been reported (Jaffe et al 2005). It has been suggested that increased soil temperature during the months of April and May might have a positive effect on later populations (Sillman 1956). This is the time in which the cuterebrid eggs are within the soil and this may contribute to egg survivability (Dunaway et al. 1967). Another possible factor is the soil moisture during the months of high infestation, June through August (Layne 1963). We conducted a companion study in the previous year (2012) and small mammals were trapped within the same general area during the same time periods. During this time, no captures were witnessed to have a cuterebrid larvae present. Temperatures for May and April of 2012 were 2-3[degrees] higher than historical averages and precipitation for June-August was 5-9 cm lower compared to historical levels. In comparison, 2013 saw spring temperatures very close to historical ranges and higher precipitation levels. In June 2013 alone, southern Illinois received 17 cm of rainfall compared to the 11 cm historical averages. It is possible that moisture levels during the summer months may have increased C. fontinella populations later in the summer.

In the literature, intensity (number of bots per host) is often overlooked and rarely reported. However, some studies have made remarks on levels of intensity and our findings support these previous studies (Table 2). In our study intensity was 1.49 bots per host which is comparable to other studies, 1.40 bots per host (Wecker 1962) to 1.46 bots per host (Timm and Cook 1979). Wolf and Batzil (2000) reported slightly lower levels ranging from 1.00 and 1.24 bots per host in a hardwood forest in Illinois. All three studies used for comparison had similar sample sizes.

This study has provided evidence to support the possibility that increased summer precipitation may increase populations of C. fontinella and the prevalence individuals on Peromyscus hosts. Further research is needed throughout the species range and among the different cuterebrid species to expand upon the effects of weather and host populations on cuterebrid population dynamics.

ACKNOWLEDGEMENTS

We would like to thank Dr. John Groninger for a previous review of this manuscript. Thank you also to Jorista van der Merwe for help with trapping methods and to all the undergraduate help without whom trapping would not have been possible.

LITERATURE CITED

Abbott HG, Parsons MA. 1961. Cuterebra infestation in Peromyscus. J. Mammol. 42: 383-385. Brown LN. 1965. Botfly parasitism in the brush mouse and white-footed mouse in the Ozarks. J. Parasitol. 51: 302-304.

Catts EP. 1982. Biology of New World bot flies: Cuterebridae. Annu. Rev. Entomol. 27: 313338.

Cogley T.P. 1991.Warble development by the rodent bot Cuterebra fontinella (Diptera: Cuterebridae) in the deer mouse." Vet. Parasitol..38: 275-288.

Cramer MJ, Cameron GN. 2006 Effects of Bot Fly Parasitism on Movements of Peromyscus leucopus. Am. Midi. Nat. 163: 455-462

Dalmat HT. 1943. A contribution to the knowledge of the rodent warble flies (Cuterebridae). J. Parasitol. 29: 311-318

Dunaway PB, Payne JA, Lewis LL, Story JD. 1967. Incidence and effects of Cuterebra in Peromyscus. J. Mammal. 48: 38-51.

Hensley MS. 1976. Prevalence of cuterebrid parasitism among woodmice in Virginia. J. Wildlife Dis. 12:172-179.

Jaffe G, Zegers DA, Steele MA, Merritt JF. 2005. Long-term patterns of botfly parasitism in Peromyscus maniculatus, P leucopus, and Tamias striatus. J. Mammal. 86: 39-45.

Layne, JN. 1963. A study of the paraforest types of the Florida mouse, Peromyscus floridanus, in relation to host and environmental factors. Tulane Studies Zool. 11: 1-27.

Margolis L, Esch GW, Holmes JC, Kuris AM, Schad GA. 1982. The use of ecological terms in parasitology (report of an ad hoc committee of the American Society of Parasitologists). J. Parisitol. 68: 131-133.

Pape T 2001. Phylogeny of Oestridae (Insecta: Diptera). Syst. Entomol. 26: 133-171.

Sabrosky CW 1986. North American species of Cuterebra, the Rabbit and Rodent Bot Flies (Diptera: Cuterebridae). College Park, MD. Entomological Society of America. 240 p.

Sealander, JA. 1961. Hematological values in deer mice in relation to botfly infection. J. Mammal. 42: 57-60.

Sillman EI. 1956. Further laboratory and field observations on the ecology of some Ontario Cuterebridae (Diptera), in particular, Cuterebra angustifrons Dalmat Ann. Rept. Entomol. Soc. Ontario, 87th report: 28-49.

Slansky F. 2007. Insect/mammal associations: effects of cuterebrid bot fly paraforest types on their hosts. Annu. Rev. Entomol. 52: 17-36.

Timm RM, Cook EF. 1979. The effect of bot fly larvae on reproduction in white-footed mice, Peromyscus leucopus. Am. Midl. Nat. 101: 211217.

Wecker SC. 1962. The effects of botfly parasitism on a local population of white-footed mouse. Ecology. 43: 561-565.

Wolf M., Batzli GO. 2000. Increased prevalence of bot flies (Cuterbebra fontinella) on white-footed mice (Peromyscus leucopus) near forest edges. Can. J. Zool. 79: 106-109.

Wood DM. 1987. Oestridae. In Manual of Neartic Diptera. Vol. 2, ed JF McAlpine. Ottawa: Agriculture Canada. 1147-1158.

Stephanie J Hayes, Eric J Holzmueller (1), and Clayton K Nielsen

Department of Forestry, Southern Illinois University, 1205 Lincoln Drive, Carbondale, IL 62901

(1) Corresponding author (email: eholzmue@siu.edu)

received 7/30/14

accepted 1/26/15
Table 1. Comparisons of studies reporting prevalence (percent of
infected individuals) for botfly infections in Peromyscus leucopus
and Peromyscus maniculatus. Results of this study are shown in
italics.

Location              Dates of Study           Sample Size

Southern Illinois     July 2013 J              91
Powdermill Biologi-   1979-1998$               1511 *; 858 *
cal Station, PA
Ozarks, MO            Feb. 1961-July 1962      661
                        [double dagger]
Oak Ridge, TN         1958-1964                511 [dagger]
Ontario               Aug.-July 1958           66 [dagger]
                        [double dagger]
Ames, Iowa            1940                     68 [dagger]
Massachusetts         1959 [double dagger]     214 [dagger]
Michigan              May-Oct. 1958            72 [dagger]
                        [double dagger]
Minnesota             Sept. 1956- Sept. 1958   1050 [dagger]
                        [double dagger]
Central Illinois      July-Nov. 1997           551 [dagger]
                       [double dagger]

Location              Prevalence (%)   Author

Southern Illinois     71.55            Hayes et al.
Powdermill Biologi-   6.95 *; 9.09 *   Jaffe et al., 2005
cal Station, PA
Ozarks, MO            0.3              Brown, 1965

Oak Ridge, TN         24.7 [dagger]    Dunaway et al., 1967
Ontario               31.8 [dagger]    Sealander, 1961

Ames, Iowa            38.0 [dagger]    Dalmat, 1943
Massachusetts         27.6 [dagger]    Abbott and Parsons, 1961
Michigan              14.1-65.9        Wecker, 1962
                        [dagger]
Minnesota             9.2 [dagger]     Timm and Cook, 1979

Central Illinois      8.9-24.3         Wolf and Batzli, 2000
                        [dagger]

* P maniculatus and P leucopus numbers listed separately; [dagger]
Only P leucopus data included; [double dagger] Includes data only
when bot flies present.

Table 2. Comparisons of studies reporting intensity (number of bots
per host) for botfly infections in Peromyscus leucopus and Peromyscus
maniculatus. Results of this study are shown in italics.

Location    Dates of Study     Sample   Intensity       Author
                               Size

Southern    July 2013          91       1.49            Hayes et al.
Illinois
Michigan    May-Oct. 1958      72       1.46 ([dagger]) Wecker, 1962
Minnesota   Sept. 1956-Sept.   97       1.4 ([dagger])  Timm and Cook,
              1958                                      1979
Central     July-Nov. 1997     75       1.0-1.24        Wolf and
Illinois                                  ([dagger])    Batzil, 2000

([dagger]) Only P. leucopus data included.
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Author:Hayes, Stephanie J.; Holzmueller, Eric J.; Nielsen, Clayton K.
Publication:Transactions of the Illinois State Academy of Science
Article Type:Report
Geographic Code:1USA
Date:Jan 1, 2015
Words:2071
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