BACKGROUND
ectoparasites have evolved with their hosts for millenia, resulting in highly intimate host-parasite relationships  <cit> .
due to the intimacy of such relationships, studies of host-parasite interactions have the potential to provide novel insights into the ecology of both organisms involved and data collected on one of the partners can have implications for the other.
previous studies have directly monitored host resource usage and contacts to provide improved predictions about parasite and pathogen transmission  <cit> .
however, direct observation of social interactions is not feasible in species that are nocturnal, arboreal, subterranean or otherwise elusive.
additionally, direct transfers of ectoparasites between individually identifiable hosts has been difficult to document.
in this study we employ a novel method of tracking lice to collect empirical data on host social interactions, as well as reveal parasite-host interactions.
the hosts studied were brown mouse lemurs  of southestern madagascar's tropical montane rainforests which, at  <dig> g, are one of the world's smallest primates.
they are arboreal, noctural and cryptic, which has impeded collection of data on their social interactions despite advances in relevant technology.
they are the sole known host of lemurpediculus verruculosus  <cit> , one of the ~ <dig> described species of obligate, permanent blood-feeding sucking lice  that parasitize  <dig> of the  <dig> mammalian orders  <cit> .
sucking lice have evolved a morphology that is highly specialized for life on their hosts, including features that permit secure attachment to host hair and feeding directly upon host peripheral vasculature.
this specialization confers considerable advantages to sucking lice while they are on the host; however, it also restricts the amount of time lice can spend off a host to just a few hours  <cit> .
this limitation necessitates that louse transfers between hosts occur when two or more host individuals are in direct contact.
though some chewing lice are known to transfer between hosts phoretically by attaching to winged hippoboscid flies  <cit>  and other parasites can transfer fomitically via inanimate objects  <cit> , the highly specialized features of sucking lice preclude the use of these transfer routes  <cit> .
understanding patterns of sucking louse transfer is particularly important because some species are known to transmit blood-borne pathogens during their bloodmeals.
sucking lice parasitizing domestic animals are known to transmit pathogens such as poxvirus , mycoplasma    <cit> anaplasma , and rickettsia   <cit> , while human sucking lice transmit the pathogens responsible for trench fever , epidemic typhus  and epidemic relapsing fever   <cit> .
despite the well-established relationship between sucking louse transfer and the spread of louse-borne disease agents in humans, very little is known about sucking louse transfer in wild mammals.
thus, documenting louse transfer permits assessment of host vulnerability to vector-borne pathogens.
live-trapping data on the population of m. rufus at ranomafana national park indicate that individually identifiable lemurs are highly localized to their mode trap locale and are infrequently found in trap locales that would imply wide ranging.
this implies that mouse lemurs would be most likely to come into contact primarily with their nearest individuals.
based on this, we hypothesized that the frequency of louse transfers, and thus interactions, would decrease with increasing distance between the trap locations of paired individuals.
because m. rufus are solitary foragers with a polygynandrous mating system  <cit>  their brief annual breeding period in early october  <cit>  necessitates an increase in social interactions; we therefore hypothesized there would be an increase in louse transfers during the onset of the breeding season.
given the limited apparent ranges of the lemurs and the variation in number of near neighbours an individual may have, we also predicted that individual hosts would vary in their contributions to the overall parasite ecology of the population.
sucking lice are one of the most host dependent groups of ectoparasites and from their perspective the parasite-host relationship is completely inextricable.
based on the unique, direct link between sucking louse transmission and host contact, we developed a method of marking lice  with an individualized dot code and monitoring their movement through the host population to test hypotheses regarding host ranging patterns, social interactions, and individually varying roles in overall population parasite ecology.
RESULTS
all lice recorded were found on the ears, testes and eyelids .
we observed all stages of the l. verruculosus life cycle on the testes .
we found no evidence that capture rate was related to mean louse intensity or the percentage of marked lice a host would eventually transfer, with only 19% of variation in the former and 21% in the latter being explained by these variables.
twenty-three male lemurs were captured;  <dig> individuals were infested with lice and had their lice marked,  <dig> never had lice, and an additional male never had unique lice but received a louse through transfer .
nine females were captured; one was infested with lice but never engaged in transfer .
a total of  <dig> lice were marked and  <dig> transfers were recorded involving a minimum of  <dig> separate transfer events within a group of  <dig> male lemurs dispersed throughout the entire trapping transect .
louse intensities were low  for the first four weeks of trapping, and began to increase the week before the breeding period.
this was also the week from which the first set of recorded transfers originated and the first week that lice were found on the testes.
the majority of the marked recovered lice  were found on the testes of new hosts.
transfer rates and mean intensities remained high through the breeding season.
transfers increased in a stepwise manner at the onset of the breeding season rather than gradually with the total number marked lice.
the percentage of marked lice that transferred remained zero until the beginning of the breeding season at which point 12% transferred despite a very slight previous increase  in the marked louse population, suggesting that louse transfers are not a simple function of louse prevalence.
one host individual  was infested with lice only once, just before the breeding season began, and had transferred all of his lice within a week; however, his lice continued to reappear in the population through the week after the breeding season .
similar evidence of lice from a single host engaging in multiple transfers was recorded for a second individual  beginning in the breeding season, one week before peak breeding.
the individual with the highest overall louse intensity   not only began the breeding season with a high number of his own lice, but was also the recipient of the greatest number of transferred lice.
for all  <dig> males involved in louse transfers, each individual's mode trap location was used to calculate pair-wise distances.
pair-wise distance calculations were also made based on the centroid of each individual's trap locales.
the absolute minimum distance a transferred louse was observed to travel on its hosts based on mode trap locale was  <dig> m and the maximum distance was  <dig> m. centroid-based calculations yielded a minimum louse transfer distance of  <dig>  m and a maximum of  <dig> m. we found no significant difference in pair-wise distances calculated from mode or centroid values between the pairs of animals that transferred lice and those that did not  , indicating that the probability of animals transferring lice across long distances and short distances is comparable.
therefore, rather than supporting our hypothesis that lice are most frequently exchanged between neighbouring lemurs, the data indicate that louse transfers occur across short and long distances.
plotting the number of times an animal was captured against that animal's total number of trap locales showed that most animals were trapped at up to  <dig> trap locales .
however, there were four individuals that were captured more than  <dig> times at  <dig> or more trap locales which also showed the longest maximum distance between trapping locales .
we reran the louse transfer analysis removing those four individuals and the results show that the centroid distances between lemur transferring lice were now shorter compared to lemurs that did not transfer lice, although this difference remained non-significant .
social network analysis exposed that only  <dig> of the  <dig> predicted social contacts based on trapping data also were involved in louse transfers; however,  <dig> unique social contacts based on louse transfers alone could not be accounted for based on trapping data.
therefore, there is evidence that the louse marking technique revealed a lemur social network that would not have been derived using trapping data alone .
we recorded at least three lice that were each involved in multiple recorded transfers, beginning on one lemur, then being recaptured on at least two more.
these multiple transfers were identified conservatively and only when that was the sole possible explanation for the distribution of lice from a given host.
the longest period a single louse remained attached to its host was  <dig> days.
the locations in which lemurs were trapped did not cluster based on lemur sex or involvement in louse transferal.
transfers occurred over a range of distances up to the full length of the transect and occurred evenly throughout the trapped area.
donor scores  ranged from + <dig> to - <dig> and the vector potential scores  varied considerably throughout the population.
this variation was not significantly related to the variation seen in donor scores , but the lemur with the highest donor score also had the greatest vector potential .
individuals with an asterisk * are those whose individual lice transferred multiple times to different hosts.
these multiple transfers also resulted in the discrepancy between the totals of 'received' and 'donated' lice.
of the  <dig> mouse lemurs involved in louse transfers, those individuals that donated 50% or more of their marked lice received on average  <dig> ±  <dig>  lice from other individuals.
lemurs that donated less than 50% of their marked lice received on average  <dig>  ±  <dig>  lice .
when examining the number of lice donated and received out of the total number of lice  we find similar results.
lemurs that donated 50% or more of their total lice received fewer lice  than those that donated less than 50% of their total lice and received on average  <dig>  ±  <dig>  lice.
this distribution suggests that while mouse lemurs may fall along a continuous range of values, there is evidence of two louse transfer categories: 'donors' that are less likely to receive and more likely to donate lice, and 'recipients' that are more likely to receive and less likely to donate lice.
discussion
we were able to successfully track patterns of louse movement in a population of wild m. rufus.
recorded transfers occurred exclusively between males which may have been due to male-male contact resulting from nest-hole sharing  <cit> , agonistic interactions occurring during the breeding season  <cit> , or from multiple males mating with the same female.
no females, however, were ever found to have lice on or near the genitals.
the transfers were quite evenly distributed throughout the study area and showed no consistent distance, direction or clustering patterns.
this pattern of transfer contrasts with mouse lemur trapping data in the study area.
most of the louse transfers occurred between lemurs over  <dig> m from each other, and one transfer  spanned over  <dig> m. the transfers therefore demonstrate a degree of lemur ranging far greater than anticipated using standard trapping methods .
they also provide evidence of a lemur social network that could not have been predicted based on trapping data alone .
moreover, relatively few individual lemurs with broad ranging patterns appear to be largely responsible for the long-distance transfer of lice.
these patterns of parasite-host dynamics suggest that a small number of individuals can quickly spread parasites throughout the population.
as hypothesized, transfers increased significantly at the beginning of the breeding season, indicating an increase in host interactions.
we found that transfers occurred most frequently and nearly exclusively during the breeding season.
this combined with the restriction of transfers to male hosts suggest that the transfers were due to agonistic same-sex interactions associated with the breeding season.
a previous study  <cit>  in chipmunks indicated that breeding periods correspond to an increase in rates of louse transfer, but there are also arguments that louse transfer in general is not a common occurrence  <cit> .
the  <dig> transfers we tracked between  <dig> animals over the course of four weeks are therefore remarkable both with respect to the high rate at which they occurred, and their correlation with the breeding season.
although no marked lice were recaptured on female lemurs, it is possible that they were involved as intermediaries in male-male transfers.
all transfers observed required at least one incidence of direct contact; however, it is possible that an intermediate host could have facilitated these transfers between what we record as the donating and receiving hosts.
thus it is possible that a female received a louse from one male during a copulation event and transferred it to second male during a later copulation.
this is unlikely to be a common occurrence, however, as we only observed a single louse on a single female host over the entire duration of the study.
additionally, testosterone is known to increase the transmission potential of certain parasites  <cit> , suggesting that the high testosterone levels seen in male mouse lemurs may increase the transmission potential of louse-borne pathogens.
testosterone has also been implicated as an immunosuppressant  <cit> , and during the reproductive season animals experiencing increases in testosterone are more likely to be vulnerable to parasitic infestation  <cit> .
an increase in testosterone levels as the males invest in spermatogenesis for the annual breeding season may be a mechanism underlying the all-male transfers.
lice previously marked on the ears of one host were most frequently recaptured on the testes of that same host or other hosts, rather than the ears.
the frequent migration of lice to the testes and the presence of all stages of the louse life cycle there indicate that this is a preferred attachment site, potentially because of the area's rich peripheral blood supply and relatively sparse fur leading up to and during the breeding period when they are dramatically distended .
the timing of this increase in louse populations about one week before host breeding indicates that lice may be triggered to reproduce by increasing levels of host sex hormones in their bloodmeals as occurs in at least two species of fleas that parasitize rabbits  <cit> .
this could explain the appearance of lice on the testes immediately before the beginning of the breeding season.
we found no correlation between louse intensity and testicular volume in the  <dig> males involved in transfers .
the variation in donor scores indicates that host individuals do play varying roles in the transfer of lice and transmission of their potential pathogens throughout the population.
age of the host may be a factor determining which hosts act more as donors.
durden   <cit>  observed that juvenile hosts did not act as donors in louse transfers despite having larger louse infestations than adults.
indeed, the youngest host in this study had the heaviest louse infestation but donated only one louse.
however, we found no overall correlation between the age of the host and louse transfers , and the divide between 'donors' and 'recipients' does not appear to be the result of testicular volume, age or body mass.
vector potential scores, like donor scores, ranged widely between individuals; however, the two are not significantly correlated.
vector potential scores therefore provide a second distinct way of assessing the impact an individual lemur host can have on patterns of louse transmission and population-wide pathogen transmission.
the evidence of multiple host transfers also suggests a heightened probability of potential pathogen transmission as the probability for lice contacting and carrying a blood-borne pathogen increases with exposure to blood from an increasing number of hosts.
of the four animals removed from the distance analysis  one individual  was responsible for transfers over both short and long centroid-based distances.
interestingly, this same male was revealed by the vector potential analysis  to be the starting point for the greatest number of transfers.
lice act as vectors of blood-borne pathogens in other host species and two blood-borne pathogens found in lemurs, babesia cheirogalei and babesia propitheci, are known to be transmitted by ectoparasites   <cit> .
it remains to be determined if l. verruculosus transmits blood-borne pathogens.
microcebus spp.
are found throughout the island of madagascar and often come into close contact with humans through a combination of anthropogenic habitat destruction and their generalist behavior; thus it is potentially beneficial to understand their parasite ecology and its implications not only for their population but for other species, including humans, as well.
beldomenico and begon  <cit>  proposed that animals with poor body conditions are more susceptible to parasitic/pathogenic infections, which in turn would perpetuate their poor body conditions.
they refer to this as a 'vicious circle' which results in heavily infested animals that become 'superspreaders', who disproportionately contribute to the dispersal of parasites in a population.
our technique of following the movement of lice through a wild population revealed the presence of lemurs that did disproportionately contribute lice to the rest of the population, making them 'donors' or 'superspreaders'.
however, the mouse lemurs most heavily parasitized in this study were the ones that collected the most lice from others and hence not superspreaders, but rather 'recipients' or 'supercollectors'.
heavy louse infestation may be due to poorer overall body condition; however, as is seen in table  <dig>  we found no significant trend with body mass, age or testicular volume that would suggest that the supercollectors have the poorest body conditions.
the superspreaders suggested by  <cit>  as the primary carriers and distributors of parasites may make parasite populations vulnerable, as the host's poor body condition would result in an increased likelihood of being preyed upon  <cit> .
we suggest that rather than superspreaders simultaneously occurring as heavily infested supercollectors, the presence of both types of individuals occur independently in wild populations.
perhaps with further research tracking parasites in natural habitats, alternate disease dispersal routes will be revealed.
CONCLUSIONS
in conclusion, this study capitalizes on the biological features of lice to gather otherwise inaccessible social interaction and population parasite ecology data on its host, m. rufus.
we found indications of far greater lemur ranging distances and a more widespread social network than were estimated using live-trapping data.
we also found that although there is no evidence of louse transfer before the breeding season, there is a substantial increase in transfer rate as the season begins, implying an underlying acceleration in rates of direct social contact.
this increase in transfer rate continues through the host breeding season, as the rate of social interactions presumably increases.
finally, we determined that while different lemur individuals play varying roles as louse donors and recipients, all individuals would be at far greater risk from an introduced louse-borne pathogen during the breeding season due to the high rate at which it could spread through the male population.
the approach developed here has potential for application in any species parasitized by sucking lice, including the many trappable species of cryptic, nocturnal, subterraneous or otherwise elusive mammals in which host social contact and parasite exchange data are difficult to obtain.

 ectoparasites have evolved with their hosts for millenia, resulting in highly intimate host-parasite relationships. due to the intimacy of such relationships, studies of host-parasite interactions have the potential to provide novel insights into the ecology of both organisms involved and data collected on one of the partners can have implications for the other. previous studies have directly monitored host resource usage and contacts to provide improved predictions about parasite and pathogen transmission. however, direct observation of social interactions is not feasible in species that are nocturnal, arboreal, subterranean or otherwise elusive. additionally, direct transfers of ectoparasites between individually identifiable hosts has been difficult to document. in this study we employ a novel method of tracking lice to collect empirical data on host social interactions, as well as reveal parasite-host interactions. the hosts studied were brown mouse lemurs of southestern madagascar's tropical montane rainforests which, at g, are one of the world's smallest primates. they are arboreal, noctural and cryptic, which has impeded collection of data on their social interactions despite advances in relevant technology. they are the sole known host of lemurpediculus verruculosus, one of the ~ described species of obligate, permanent blood-feeding sucking lice that parasitize of the mammalian orders. sucking lice have evolved a morphology that is highly specialized for life on their hosts, including features that permit secure attachment to host hair and feeding directly upon host peripheral vasculature. this specialization confers considerable advantages to sucking lice while they are on the host; however, it also restricts the amount of time lice can spend off a host to just a few hours. this limitation necessitates that louse transfers between hosts occur when two or more host individuals are in direct contact. though some chewing lice are known to transfer between hosts phoretically by attaching to winged hippoboscid flies and other parasites can transfer fomitically via inanimate objects, the highly specialized features of sucking lice preclude the use of these transfer routes. understanding patterns of sucking louse transfer is particularly important because some species are known to transmit blood-borne pathogens during their bloodmeals. sucking lice parasitizing domestic animals are known to transmit pathogens such as poxvirus, mycoplasma anaplasma, and rickettsia, while human sucking lice transmit the pathogens responsible for trench fever, epidemic typhus and epidemic relapsing fever. despite the well-established relationship between sucking louse transfer and the spread of louse-borne disease agents in humans, very little is known about sucking louse transfer in wild mammals. thus, documenting louse transfer permits assessment of host vulnerability to vector-borne pathogens. live-trapping data on the population of m. rufus at ranomafana national park indicate that individually identifiable lemurs are highly localized to their mode trap locale and are infrequently found in trap locales that would imply wide ranging. this implies that mouse lemurs would be most likely to come into contact primarily with their nearest individuals. based on this, we hypothesized that the frequency of louse transfers, and thus interactions, would decrease with increasing distance between the trap locations of paired individuals. because m. rufus are solitary foragers with a polygynandrous mating system their brief annual breeding period in early october necessitates an increase in social interactions; we therefore hypothesized there would be an increase in louse transfers during the onset of the breeding season. given the limited apparent ranges of the lemurs and the variation in number of near neighbours an individual may have, we also predicted that individual hosts would vary in their contributions to the overall parasite ecology of the population. sucking lice are one of the most host dependent groups of ectoparasites and from their perspective the parasite-host relationship is completely inextricable. based on the unique, direct link between sucking louse transmission and host contact, we developed a method of marking lice with an individualized dot code and monitoring their movement through the host population to test hypotheses regarding host ranging patterns, social interactions, and individually varying roles in overall population parasite ecology.  all lice recorded were found on the ears, testes and eyelids. we observed all stages of the l. verruculosus life cycle on the testes. we found no evidence that capture rate was related to mean louse intensity or the percentage of marked lice a host would eventually transfer, with only 19% of variation in the former and 21% in the latter being explained by these variables. twenty-three male lemurs were captured; individuals were infested with lice and had their lice marked, never had lice, and an additional male never had unique lice but received a louse through transfer. nine females were captured; one was infested with lice but never engaged in transfer. a total of lice were marked and transfers were recorded involving a minimum of separate transfer events within a group of male lemurs dispersed throughout the entire trapping transect. louse intensities were low for the first four weeks of trapping, and began to increase the week before the breeding period. this was also the week from which the first set of recorded transfers originated and the first week that lice were found on the testes. the majority of the marked recovered lice were found on the testes of new hosts. transfer rates and mean intensities remained high through the breeding season. transfers increased in a stepwise manner at the onset of the breeding season rather than gradually with the total number marked lice. the percentage of marked lice that transferred remained zero until the beginning of the breeding season at which point 12% transferred despite a very slight previous increase in the marked louse population, suggesting that louse transfers are not a simple function of louse prevalence. one host individual was infested with lice only once, just before the breeding season began, and had transferred all of his lice within a week; however, his lice continued to reappear in the population through the week after the breeding season. similar evidence of lice from a single host engaging in multiple transfers was recorded for a second individual beginning in the breeding season, one week before peak breeding. the individual with the highest overall louse intensity not only began the breeding season with a high number of his own lice, but was also the recipient of the greatest number of transferred lice. for all males involved in louse transfers, each individual's mode trap location was used to calculate pair-wise distances. pair-wise distance calculations were also made based on the centroid of each individual's trap locales. the absolute minimum distance a transferred louse was observed to travel on its hosts based on mode trap locale was m and the maximum distance was m. centroid-based calculations yielded a minimum louse transfer distance of m and a maximum of m. we found no significant difference in pair-wise distances calculated from mode or centroid values between the pairs of animals that transferred lice and those that did not, indicating that the probability of animals transferring lice across long distances and short distances is comparable. therefore, rather than supporting our hypothesis that lice are most frequently exchanged between neighbouring lemurs, the data indicate that louse transfers occur across short and long distances. plotting the number of times an animal was captured against that animal's total number of trap locales showed that most animals were trapped at up to trap locales. however, there were four individuals that were captured more than times at or more trap locales which also showed the longest maximum distance between trapping locales. we reran the louse transfer analysis removing those four individuals and the results show that the centroid distances between lemur transferring lice were now shorter compared to lemurs that did not transfer lice, although this difference remained non-significant. social network analysis exposed that only of the predicted social contacts based on trapping data also were involved in louse transfers; however, unique social contacts based on louse transfers alone could not be accounted for based on trapping data. therefore, there is evidence that the louse marking technique revealed a lemur social network that would not have been derived using trapping data alone. we recorded at least three lice that were each involved in multiple recorded transfers, beginning on one lemur, then being recaptured on at least two more. these multiple transfers were identified conservatively and only when that was the sole possible explanation for the distribution of lice from a given host. the longest period a single louse remained attached to its host was days. the locations in which lemurs were trapped did not cluster based on lemur sex or involvement in louse transferal. transfers occurred over a range of distances up to the full length of the transect and occurred evenly throughout the trapped area. donor scores ranged from + to - and the vector potential scores varied considerably throughout the population. this variation was not significantly related to the variation seen in donor scores, but the lemur with the highest donor score also had the greatest vector potential. individuals with an asterisk * are those whose individual lice transferred multiple times to different hosts. these multiple transfers also resulted in the discrepancy between the totals of'received' and'donated' lice. of the mouse lemurs involved in louse transfers, those individuals that donated 50% or more of their marked lice received on average ± lice from other individuals. lemurs that donated less than 50% of their marked lice received on average ± lice. when examining the number of lice donated and received out of the total number of lice we find similar results. lemurs that donated 50% or more of their total lice received fewer lice than those that donated less than 50% of their total lice and received on average ± lice. this distribution suggests that while mouse lemurs may fall along a continuous range of values, there is evidence of two louse transfer categories:'donors' that are less likely to receive and more likely to donate lice, and'recipients' that are more likely to receive and less likely to donate lice. discussion we were able to successfully track patterns of louse movement in a population of wild m. rufus. recorded transfers occurred exclusively between males which may have been due to male-male contact resulting from nest-hole sharing, agonistic interactions occurring during the breeding season, or from multiple males mating with the same female. no females, however, were ever found to have lice on or near the genitals. the transfers were quite evenly distributed throughout the study area and showed no consistent distance, direction or clustering patterns. this pattern of transfer contrasts with mouse lemur trapping data in the study area. most of the louse transfers occurred between lemurs over m from each other, and one transfer spanned over m. the transfers therefore demonstrate a degree of lemur ranging far greater than anticipated using standard trapping methods. they also provide evidence of a lemur social network that could not have been predicted based on trapping data alone. moreover, relatively few individual lemurs with broad ranging patterns appear to be largely responsible for the long-distance transfer of lice. these patterns of parasite-host dynamics suggest that a small number of individuals can quickly spread parasites throughout the population. as hypothesized, transfers increased significantly at the beginning of the breeding season, indicating an increase in host interactions. we found that transfers occurred most frequently and nearly exclusively during the breeding season. this combined with the restriction of transfers to male hosts suggest that the transfers were due to agonistic same-sex interactions associated with the breeding season. a previous study in chipmunks indicated that breeding periods correspond to an increase in rates of louse transfer, but there are also arguments that louse transfer in general is not a common occurrence. the transfers we tracked between animals over the course of four weeks are therefore remarkable both with respect to the high rate at which they occurred, and their correlation with the breeding season. although no marked lice were recaptured on female lemurs, it is possible that they were involved as intermediaries in male-male transfers. all transfers observed required at least one incidence of direct contact; however, it is possible that an intermediate host could have facilitated these transfers between what we record as the donating and receiving hosts. thus it is possible that a female received a louse from one male during a copulation event and transferred it to second male during a later copulation. this is unlikely to be a common occurrence, however, as we only observed a single louse on a single female host over the entire duration of the study. additionally, testosterone is known to increase the transmission potential of certain parasites, suggesting that the high testosterone levels seen in male mouse lemurs may increase the transmission potential of louse-borne pathogens. testosterone has also been implicated as an immunosuppressant, and during the reproductive season animals experiencing increases in testosterone are more likely to be vulnerable to parasitic infestation. an increase in testosterone levels as the males invest in spermatogenesis for the annual breeding season may be a mechanism underlying the all-male transfers. lice previously marked on the ears of one host were most frequently recaptured on the testes of that same host or other hosts, rather than the ears. the frequent migration of lice to the testes and the presence of all stages of the louse life cycle there indicate that this is a preferred attachment site, potentially because of the area's rich peripheral blood supply and relatively sparse fur leading up to and during the breeding period when they are dramatically distended. the timing of this increase in louse populations about one week before host breeding indicates that lice may be triggered to reproduce by increasing levels of host sex hormones in their bloodmeals as occurs in at least two species of fleas that parasitize rabbits. this could explain the appearance of lice on the testes immediately before the beginning of the breeding season. we found no correlation between louse intensity and testicular volume in the males involved in transfers. the variation in donor scores indicates that host individuals do play varying roles in the transfer of lice and transmission of their potential pathogens throughout the population. age of the host may be a factor determining which hosts act more as donors. durden observed that juvenile hosts did not act as donors in louse transfers despite having larger louse infestations than adults. indeed, the youngest host in this study had the heaviest louse infestation but donated only one louse. however, we found no overall correlation between the age of the host and louse transfers, and the divide between'donors' and'recipients' does not appear to be the result of testicular volume, age or body mass. vector potential scores, like donor scores, ranged widely between individuals; however, the two are not significantly correlated. vector potential scores therefore provide a second distinct way of assessing the impact an individual lemur host can have on patterns of louse transmission and population-wide pathogen transmission. the evidence of multiple host transfers also suggests a heightened probability of potential pathogen transmission as the probability for lice contacting and carrying a blood-borne pathogen increases with exposure to blood from an increasing number of hosts. of the four animals removed from the distance analysis one individual was responsible for transfers over both short and long centroid-based distances. interestingly, this same male was revealed by the vector potential analysis to be the starting point for the greatest number of transfers. lice act as vectors of blood-borne pathogens in other host species and two blood-borne pathogens found in lemurs, babesia cheirogalei and babesia propitheci, are known to be transmitted by ectoparasites. it remains to be determined if l. verruculosus transmits blood-borne pathogens. microcebus spp. are found throughout the island of madagascar and often come into close contact with humans through a combination of anthropogenic habitat destruction and their generalist behavior; thus it is potentially beneficial to understand their parasite ecology and its implications not only for their population but for other species, including humans, as well. beldomenico and begon proposed that animals with poor body conditions are more susceptible to parasitic/pathogenic infections, which in turn would perpetuate their poor body conditions. they refer to this as a'vicious circle' which results in heavily infested animals that become'superspreaders', who disproportionately contribute to the dispersal of parasites in a population. our technique of following the movement of lice through a wild population revealed the presence of lemurs that did disproportionately contribute lice to the rest of the population, making them'donors' or'superspreaders'. however, the mouse lemurs most heavily parasitized in this study were the ones that collected the most lice from others and hence not superspreaders, but rather'recipients' or'supercollectors'. heavy louse infestation may be due to poorer overall body condition; however, as is seen in table we found no significant trend with body mass, age or testicular volume that would suggest that the supercollectors have the poorest body conditions. the superspreaders suggested by as the primary carriers and distributors of parasites may make parasite populations vulnerable, as the host's poor body condition would result in an increased likelihood of being preyed upon. we suggest that rather than superspreaders simultaneously occurring as heavily infested supercollectors, the presence of both types of individuals occur independently in wild populations. perhaps with further research tracking parasites in natural habitats, alternate disease dispersal routes will be revealed.  in conclusion, this study capitalizes on the biological features of lice to gather otherwise inaccessible social interaction and population parasite ecology data on its host, m. rufus. we found indications of far greater lemur ranging distances and a more widespread social network than were estimated using live-trapping data. we also found that although there is no evidence of louse transfer before the breeding season, there is a substantial increase in transfer rate as the season begins, implying an underlying acceleration in rates of direct social contact. this increase in transfer rate continues through the host breeding season, as the rate of social interactions presumably increases. finally, we determined that while different lemur individuals play varying roles as louse donors and recipients, all individuals would be at far greater risk from an introduced louse-borne pathogen during the breeding season due to the high rate at which it could spread through the male population. the approach developed here has potential for application in any species parasitized by sucking lice, including the many trappable species of cryptic, nocturnal, subterraneous or otherwise elusive mammals in which host social contact and parasite exchange data are difficult to obtain. 
we monitored the movement of sucking lice, parasites that require direct host-host contact to be transferred, in their host population of wild mouse lemurs. we then tested the hypotheses that 1) the frequency of louse transfers, and thus interactions, would decrease with increasing distance between paired individual lemurs; 2) due to host polygynandry, social interactions and hence louse transfers would increase during the onset of the breeding season; and 3) individual mouse lemurs would vary in their contributions to the spread of lice. studies of host-parasite interactions have the potential to provide insights into the ecology of both organisms involved. we show that louse transfers involved % of the studied lemur population, exclusively males. louse transfers peaked during the breeding season, perhaps due to increased social interactions between lemurs. our approach demonstrates the potential to uncover otherwise inaccessible parasite-host, and host social interaction data in any trappable species parasitized by sucking lice. this method not only provided insight into the previously unseen parasite movement between lemurs, but also allowed us to infer social interactions between them. we developed a simple, cost effective method exploiting the intimate relationship between louse and lemur, whereby individual lice were marked, without removal from their host, with an individualized code, and tracked throughout the lemur population.
 studies of host-parasite interactions have the potential to provide insights into the ecology of both organisms involved. we monitored the movement of sucking lice, parasites that require direct host-host contact to be transferred, in their host population of wild mouse lemurs. these lemurs live in the rainforests of madagascar, are small, arboreal, nocturnal, solitary foraging primates for which data on population-wide interactions are difficult to obtain. we developed a simple, cost effective method exploiting the intimate relationship between louse and lemur, whereby individual lice were marked, without removal from their host, with an individualized code, and tracked throughout the lemur population. we then tested the hypotheses that 1) the frequency of louse transfers, and thus interactions, would decrease with increasing distance between paired individual lemurs; 2) due to host polygynandry, social interactions and hence louse transfers would increase during the onset of the breeding season; and 3) individual mouse lemurs would vary in their contributions to the spread of lice.  we show that louse transfers involved % of the studied lemur population, exclusively males. louse transfers peaked during the breeding season, perhaps due to increased social interactions between lemurs. although trap-based individual lemur ranging patterns are restricted, louse transfer rate does not correlate with the distance between lemur trapping locales, indicating wider host ranging behavior and a greater risk of rapid population-wide pathogen transmission than predicted by standard trapping data alone. furthermore, relatively few lemur individuals contributed disproportionately to the rapid spread of lice throughout the population.  using a simple method, we were able to visualize exchanges of lice in a population of cryptic wild primates. this method not only provided insight into the previously unseen parasite movement between lemurs, but also allowed us to infer social interactions between them. as lice are known pathogen vectors, our method also allowed us to identify the lemurs most likely to facilitate louse-mediated epidemics. our approach demonstrates the potential to uncover otherwise inaccessible parasite-host, and host social interaction data in any trappable species parasitized by sucking lice. primateparasitelicesocial contactmouse lemurvector potential 