de Mendonça, P.G. (2005). Gregariousness versus solitude: Impact of nesting habits on tick infestation in yellow-necked mice. Presentation to the 5th International Conference on Ticks and Tick-borne Pathogens, University of Neuchâtel, Switzerland, 29.8-2.9.2005.
Philippe Gil de Mendonça
Gregariousness versus solitude: Impact of nesting habits on tick infestation in yellow-necked mice
INTRODUCTION Small rodents are host to many ectoparasitic arthropods amongst which ticks. In Welsh yellow-necked mice (Apodemus flavicollis wintoni) tick prevalence and load fluctuate widely. Usually mice harbour only a few ticks, however, unfortunate mice foraging by a tick nest may become infested with numerous larvae. Tick larvae are the most frequent stage on yellow-necked mice (53%), followed by nymphs (33%) and adults (14%). Larvae and nymphs are usually attached to the earflap, whereas most adult ticks are to be found on the back, usually between the shoulder blades (1).
 Cases of cofeeding nymphs and larvae are infrequent (3.5%). Heterospecific cofeeding also occurs: numerous Trombiculid larvae were sometimes (3.7%) observed cofeeding with adult ticks (1). Cofeeding is known to be an amplifying factor in Borrelia transmission (2).Apodemus mice (A. flavicollis and A. sylvaticus) are known to be reservoirs for Borrelia spp, the causative agents of Lyme disease (3,4,5). Furthermore, Apodemus mice present a higher potential infectivity for questing ticks than voles do (3). In addition, there is evidence of concurrent infection with Borrelia burgdorferi andBabesia microti in both ticks and various rodent reservoir hosts (6,7,8,9,10). In Europe, the reported prevalence for Babesia microti in A. flavicollis is 11.8% (11).
 It is usually considered (12) and sometimes proven (13) that animals with high contact rates, e.g. gregarious species, are exposed to an increased risk of contracting diseases. Yellow-necked mice are particularly suitable for the investigation of the impact of communal nesting and group size on tick infestation and subsequent microbial transmission. Indeed, within the same population, up to 47% of the individuals are found to nest alone while the remainder of the population lives in groups of two to eight individuals, group size being density-dependent (1). Solitary mice and gregarious mice can thus be compared during the same time interval and in the same environment.Radio-tracking is unsuitable to distinguish solitary and gregarious mice. Indeed, misallocation cases are bound to occur (1). Furthermore, radio-collars prevent mice from grooming thoroughly, thus causing enhanced tick infestation levels in radio-tagged individuals (14). Alternative techniques had thus to be designed, namely the combined use of artificial burrows and nest-boxes (1,15). MATERIAL & METHODS Seventeen underground artificial burrows (1,15) and 150 arboreal nest-boxes (1) were installed in 12 suitable woods (16) in Gwent (South Wales). Artificial nests were inspected on a fortnightly basis from December 2000 to October 2002 where feasible (several field sites were not accessible during the British epidemic of foot-and-mouth disease). All mice were sexed, weighed, individually marked, and inspected for ectoparasites under light anaesthesia before release in their nest.Blood was collected from a subsample of these mice of known nesting status. Heparinised blood (9µl) samples were centrifuged for 8 minutes at 11,500 rpm in a battery operated portable centrifuge (Ames M1101, Bayer diagnostics, Munich, Germany) and haematocrit subsequently read with an accuracy of ±1% (17,18,19). Blood smears were prepared with non-heparinised blood, air-dried (19), fixed in absolute methanol for 30 minutes, and then stained with Giemsa. A differential leukocyte count was then performed, based on 200+ cells (18,19). For comparative purposes, foraging mice were live-trapped on a monthly basis and inspected for ectoparasites before release at the point of capture. RESULTS Tick infestation levels were quantified for 455 observations of solitary (n=75) versus gregarious (n=380) mice found in artificial nests. Numbers of ticks per hostare not distributed evenly, nor randomly. Instead, most mice harboured no or few ticks whereas a few mice harboured many. This pattern is consistent with a negative binomial distribution (solitary mice: variance/mean ratio: 1.216, K=0.850, p=0.8365 ; gregarious mice: variance/mean ratio: 1.169, K=0.480, p=0.9422).In contrast to this overdispersed distribution, the various ectoparasite species infest a host independently of each other (variance ~ mean).
 There were statistically significant differences in frequency distribution for ticks between solitary and gregarious mice (Gadj = 6.244914, d.f.=1, p=0.0124, n=455).Solitary mice were host to more ticks than gregarious mice (prevalence: 17.3% versus 7.4% respectively). Group size had no influence on tick load (p=0.9924).There was no sex bias in tick load in nesting mice (p=0.9122). Prevalence varied with season, being nil in winter, rising in spring, and reaching a peak in autumn.
 Mice captured in live-traps (n=1611) were host to more ticks than mice found in artificial nests, and males harboured significantly more ticks than females did(p=0.0009). Winter prevalence for mice caught in traps reached 20.5%. There was no relation between body mass and tick load (mice from nests: p=0.2697 ;mice from traps: p=0.4341).Haematocrit is sensitive to and decreases with increasing tick load, however, this relation is not statistically significant (p=0.1951, n=137) and very littlehaematocrit variation is explained by tick load (1.2%). When all ectoparasitic species are considered, this relation becomes highly statistically significant (p<0.01).The intracellular protozoa Babesia microti was absent from all blood smears. Only one case of intracellular protozoan parasite was observed in lymphocytes froma solitary mouse.Neither nesting habits nor tick load had any influence on leukocytic pattern (p>0.05). DISCUSSION The results presented here are inconsistent with the "high contact rate = increased risk of contracting diseases" theory. Instead, solitary mice are more heavily infested than gregarious mice. Ticks found on mice in this sample are essentially larval and nymphal stages, i.e. they are (a) very small, (b) very tightly and strongly attached to the host's skin, and (c) always located on the earflap. This makes biting by a nest-mate much more efficient at removing these immature ticks than self-scratching does. Indeed, social grooming is widespread in yellow-necked mice (1).Mice spend a large proportion of their time grooming inside their nests. Not surprisingly mice found inside artificial nests were host to less ticks than mice captured in live-traps. The latter category was exposed to questing ticks while foraging until mice were caught in single-catch traps where social grooming is impossible. Males range more widely than females (20) and are thus more exposed to questing ticks.Ticks are blood sucking parasites. However mice harbour mostly larvae and nymphs. Their blood meal is therefore relatively small. In addition, other parasites(e.g. fleas) also cause blood losses. Haematocrit is an integrative measure of anaemia, as such it reflects the overall parasite burden, not just tick load.In this sample, the cost of tick infestation appears to be small, however it may have hidden effects.Are solitary mice, particularly males, better reservoirs for Borrelia spp than gregarious mice? Further research is required in order to answer this question. ACKNOWLEDGEMENTS This research was supported by a grant (TMR20) from the Swiss National Science Foundation. Additional support was provided by the Cambridge Philosophical Society and Churchill College (University of Cambridge). For permission to access their land for field work, thanks are due to : Sir Richard Hanbury Tenison, the Morgan family, and Forestry Commission. REFERENCES
de Mendonça, P.G. (2005). Gregariousness versus solitude: Impact of nesting habits on tick infestation in yellow-necked mice. Presentation to the 5th International Conference on Ticks and Tick-borne Pathogens, University of Neuchâtel, Switzerland, 29.8-2.9.2005. |