Botfly Parasitism Research Articles

Bot fly parasitism in mantled howler monkeys (Alouatta palliata): General patterns and climate influences.

Parasitism is a strong selective pressure, and its study is crucial for predicting the persistence of host species. Mantled howler monkeys are infected by the larvae of the bot fly Cuterebra baeri. This parasitosis produces myiasis and may have negative impacts on host health, although systematic information on the dynamics of this host-parasite relationship is very limited. Currently, all available information on infection patterns of C. baeri comes from a single mantled howler monkey population (Barro Colorado Island, Panama). Therefore, in this study we describe temporal variation in infection patterns for a newly mantled howler monkey population and analyze the relationship between climate and infection likelihood. We assessed the presence of C. baeri nodules in 17 adult individuals in Los Tuxtlas for 10 months through direct observation and compiled data on ambient temperature and rainfall. Most subjects had nodules during the study and there were no differences between sexes in the number of nodules. Nodules were usually located in the neck. Prevalence and abundance of nodules peaked thrice during the study (February, April, and September), a pattern that was very similar to that of parasitism intensity (February, April, and August). Incidence closely tracked these peaks, increasing before and decreasing after them. The likelihood of nodule appearance increased when both mean and minimum temperature decreased in the 24-21 prior days to nodule appearance. It also increased with decreased rainfall in the 5-2 prior days to nodule appearance. Although only three of the eight analyzed climate variables had a significant effect on parasitosis, these results suggest that climate may affect pupal development and the access of larvae to hosts. Besides contributing data on C. baeri parasitism for a new mantled howler monkey population, our study provides novel information on the influence of environmental factors on the dynamics of host-parasite systems.

SEASONAL AND HOST-ASSOCIATED VARIATION IN BOT FLY (OESTRIDAE: CUTEREBRINAE) PARASITISM OF LAGOMORPHS ACROSS AN ARID-LAND ECOSYSTEM IN SOUTHERN NEW MEXICO.

Bot flies (Oestridae: Cuterebrinae) are obligate mammalian parasites that complete the larval stage of their life cycle under the skin of their host. Most detailed studies of bot fly larval disease ecology have been conducted in temperate deciduous zone rodent systems. To understand the relative importance of seasonal and spatial factors, as well as factors intrinsic to the host, in underpinning the likelihood and extent of parasitism by bot flies in non-rodent hosts as well as in arid-land ecosystems, we examined the dynamic for black-tailed jackrabbit (Lepus californicus) and desert cottontail (Sylvilagus audubonii) parasitism by bot fly larvae (Cuterebra spp.) across 7 repeatedly sampled sites spread across approximately 500 km of the Chihuahuan Desert ecoregion of southern New Mexico. This environment is characterized by a climate that includes hot dry summers and cool to cold dry winters, as well as strongly seasonal summer monsoonal rains. Lagomorphs are a common mid-sized mammal in these landscapes. Bot fly parasitism was strongly seasonal, with peak prevalence and abundance in the spring, and there was spatial variation in the extent of parasitism between collection sites. Additionally, jackrabbits in better body condition were less likely to be parasitized (as indicated by kidney fat index). We did not find sex-based differences in bot fly parasitism between male and female jackrabbits. Thus, in arid-land ecoregions, abiotic factors are likely the primary driver of the bot fly-host interaction, whereas factors intrinsic to the host were of secondary importance for characterizing the interactions of bot flies and lagomorphs.

Demography of botfly (Cuterebra fontinella) parasitism in white-footed mice (Peromyscus leucopus) in Kansas

Abstract Botflies (Diptera: Cuterebra sp.) are widely distributed and seasonally abundant parasites of small mammals in North America. To assess their effect on rodent survival, we studied the demography of botfly parasitism on small mammals in northeastern Kansas during 1995–1999. Additional comparisons on botflies parasitizing small mammals were made to a nearby old-field grid where mark–recapture studies continued from 1975 to 2003. White-footed mice, Peromyscus leucopus, were infected by botfly larvae (Cuterebra fontinella) each year during our study. The period of infection for P. leucopus was June–December, with the highest proportion of mice infected in July and August. A smaller, second peak of infection in October and November indicated that C. fontinella reproduced bimodally at this latitude with distinct summer and autumn population peaks. During the botfly seasons of the 5 years, 140 (23.3%) of 602 P. leucopus captured were infected. The percentages of individuals infected during 1995, 1996, 1997, and 1999 were not significantly different (22.4%, 17.3%, 17.1%, and 22.7%, respectively). However, in 1998, 32.4% individuals were infected with a higher incidence of multiple infections and a greater number of botfly larvae per host. Nearly half (47%) of the infected individuals caught in 1998 had infections in both summer and autumn, compared with 25% during the 1995–1997 seasons. In 1999, 63% of infected mice had at least a 2nd infection during the autumn. For all 5 years, 82%, 14%, and 4% of the infected mice had one, two, or three botflies, respectively. In 1998, 24% of the infected mice carried two or more botflies at one time, compared to 14% from 1995–1997 and 11% in 1999. Overall 94% of the infected mice were adults, with no differences between sexes. The variation seen in the prevalence of botfly parasitism of white-footed mice correlates to yearly weather fluctuations. Other demographic aspects of the infected mice, such as sex ratio, age, and longevity of those infected, did not change year to year. Our data suggest that infection with Cuterebra has little negative or positive impact upon populations of white-footed mice.

Individual and environmental determinants of Cuterebra bot fly parasitism in the eastern chipmunk (Tamias striatus).

Understanding the interactions between parasites, hosts, and their shared environment is central to ecology. Variation in infestation prevalence may be the result of varying environmental and population characteristics; however, variations in parasitism may also depend on individual characteristics that influence both the exposure and susceptibility to parasites. Using 12years of data from a population of wild eastern chipmunks relying on pulsed food resources, we investigated the determinants of bot fly parasitism at both the population and individual level. We assessed the relationship between infestation prevalence and weather conditions, population size and food abundance. Then, we assessed the relationship between infestation intensity and chipmunk behavior, sex, age, body mass and food abundance. Precipitation, temperature and population size were positively related to infestation prevalence, while beech masts were negatively related to infestation prevalence, highlighting the importance of local environmental conditions on hosts and parasites. We also found that the influence of activity and exploration on infestation intensity varied according to sex in adults. More active and faster exploring males had more parasites compared to females, suggesting that reproductive behaviors may influence parasite exposure. For juveniles, infestation intensity was greater when juveniles emerged in the spring as opposed to fall, possibly because spring emergence is synchronized with the peak of bot fly eggs in the environment, low food availability and longer activity period. Our results suggest that the environmental, population and host characteristics that are advantageous for reproduction and resource acquisition may come at the cost of increasing parasitism.

Brood parasitic nestlings benefit from unusual host defenses against botfly larvae (Philornis spp.)

Brood parasitic birds lay their eggs into the nests of other birds, abandoning parental care of their nestlings to the unsuspecting hosts. Parasite and host nestlings may themselves be parasitized by botfly larvae (Philornis: Muscidae), which burrow under the nestlings’ skin and can seriously affect growth and survival. Here, we provide the first direct evidence that adult baywings (Agelaioides badius), the primary host of the specialist brood parasitic screaming cowbird (Molothrus rufoaxillaris), regularly remove botfly larvae from their own and parasitic nestlings by pulling them out of the nestlings’ skin. This is the only bird species known to remove botfly larvae. By combining nestling cross-fostering with video recording of baywing nests, we show that due to prompt removal, infection with botfly larvae had negligible effects on nestling growth and survival despite high prevalence. Our results provide the first direct observations for larva removal behavior in botfly hosts. Screaming cowbirds may benefit from using baywings as its main host, as larva removal by adult baywings reduces the costs of botfly parasitism. Infection by botfly larvae of the genus Philornis (Muscidae) causes nestling mortality in many Neotropical birds. Despite the lethal effects, most Philornis hosts studied so far lack specific defenses against these larvae. The grayish baywing (Agelaioides badius), primary host of the brood parasitic screaming cowbird (Molothrus rufoaxillaris), is the only species that, based on indirect evidence, would be able to remove Philornis larvae from infected nestlings. We provide the first direct evidence that adult baywings do indeed remove botfly larvae from their own nestlings as well as from parasitic cowbird nestlings and that this unusual defense may increase the survival of own and screaming cowbird nestlings at infected nests.

Botfly parasitism and tourism on the endangered black howler monkey of Belize

Tourism imposes costs and benefits on wild primates. Endangered black howler monkey (Alouatta pigra) troops with high exposure to tourism had higher levels of botfly (Alouattamyia baeri) parasitism. Edge habitat and juvenile numbers did not seem to confound the observed relationship. To improve the cost/benefit ratio of tourism, we recommend further investigation.

Host use by Philornis sp. in a passerine community in central Argentina

We studied host use by parasitic botflies (Philornis sp.) in a passerine community in central Argentina and analyzed characteristics of nests and hosts associated with botfly parasitism. We conducted a four-year field study as well as a bibliographical survey where we determined: presence of botfly parasitism, type of nest, presence of green material and small sticks in the nest, average height of the nest, date of last nesting attempt during the breeding season and egg volume (as a surrogate of species body mass). Our field study of 3 birds species showed that botflies parasitized Troglodytes aedon (25% of nests), but not Sicalis flaveola and Tachycineta leucorroha in spite of nesting in similar boxes, at the same place and during the same time of the year. However T. aedon built nests using dry material while S. flaveola and T. leucorroha used green material.The analysis of published data (35 species considered) showed a negative association between botfly parasitism and presence of green material in the nest, and a positive association between botfly parasitism and presence of small sticks in the nest and date of the last nesting attempt during the breeding season. Our results indicate that the materials used to build the nest and the extent of the breeding season are factors that influence host use by botflies in central Argentina.

Free-ranging eastern chipmunks (Tamias striatus) infected with bot fly (Cuterebra emasculator) larvae have higher resting but lower maximum metabolism

Given the ubiquity and evolutionary importance of parasites, their effect on the energy budget of mammals remains surprisingly unclear. The eastern chipmunk ( Tamias striatus (L., 1758)) is a burrowing rodent that is commonly infected by cuterebrid bot fly ( Cuterebra emasculator Fitch, 1856) larvae. We measured resting metabolic rate (RMR) and cold-induced Vo2-max (under heliox atmosphere) in 20 free-ranging individuals, of which 4 individuals were infected by one or two larva. We found that RMR was significantly higher in chipmunks infected by bot fly larvae (mean ± SE = 0.88 ± 0.05 W) than in uninfected individuals (0.74 ± 0.02 W). In contrast, Vo2-max was significantly lower in chipmunks infected by bot fly larvae (4.96 ± 0.70 W) than in uninfected individuals (6.37 ± 0.16 W). Consequently, the aerobic scope (ratio of Vo2-max to RMR) was negatively correlated with the number of bot fly larvae (infected individuals = 5.74 ± 1.03 W; noninfected individuals = 8.67 ± 0.26 W). Finally, after accounting for the effects of body mass and bot fly parasitism on RMR and Vo2-max, there was no correlation between the two variables among individuals within our population. In addition to providing the first estimate of Vo2-max in T. striatus, these results offer additional evidence that bot fly parasitism has significant impacts on the metabolic ecology of this host species.

Lethal and Sublethal Effects of Botfly (Philornis seguyi) Parasitism on House Wren Nestlings

We studied the effect of botfly (Philornis seguyi) parasitism on survival and growth of House Wren (Troglodytes aedon) nestlings. We investigated whether nestling survival was related to (1) the intensity of botfly infestation, (2) age of the nestling at the time it was parasitized, and (3) the order in which a chick hatched within a brood. The prevalence of botfly parasitism was 25%; the mean intensity and age at parasitism were 12.8 larvae per nestling and 3.9 days, respectively. Nestling survival was 42% lower in infested than in noninfested broods. Nestling survival was negatively associated with the mean intensity of parasitism of the brood and positively associated with the age of the nestling at the time it was parasitized. Within infested broods, nestling survival was higher in chicks hatched first than in chicks hatched last. Infested nestlings that survived until fledging grew at lower rates and remained in the nest longer than did nestlings in noninfested broods. Our results reveal that P. seguyi has lethal and sublethal effects on House Wren nestlings and that the intensity of parasitism, age of nestlings at the time they are infested, and sequence of hatching are important factors that influence the survival of parasitized nestlings.

Botfly Parasitism Effects on Nestling Growth and Mortality of Red-Crested Cardinals

We collected observational data in three consecutive breeding seasons to study interactions between the botfly Philornis seguyi and Red-crested Cardinals (Paroaria coronata) in a temperate zone near the southern limit of Philornis distribution. We analyzed: (1) seasonal trends in prevalence of parasitism, (2) influence of botfly parasitism on nestling growth rate and survival, and (3) the association between nest site vegetation at different scales (i.e., nest tree, vegetation surrounding the nest tree, and landscape) and probability of botfly parasitism. Prevalence of parasitism was 28% and was higher later in the breeding season. Botfly parasitism produced sub-lethal (lower growth rate of nestlings that survive) and lethal (lower nestling survival) effects. The lethal effect was negatively associated with age at the time nestlings were parasitized. Botfly parasitism was not associated with vegetation characteristics at the level of nesting tree or vegetation surrounding the nesting tree, but was associated with landscape features. Parasite prevalence was higher in large continuous woodland patches than in small isolated patches. However, we did not observe increased use of isolated patches of forest by Red-crested Cardinals, suggesting that use of nest sites with high botfly parasite intensity could be the consequence of high host density.

North American Deer Mouse, <em>Peromyscus maniculatus</em>, Consuming a Parasitizing Botfly Larva, Diptera: Cuterebridae

During a laboratory study in Algonquin Provincial Park, Ontario, Canada, I videotaped a female North American Deer Mouse, Peromyscus maniculatus gracilis, consuming a botfly larva, Family Cuterebridae, that had just emerged from her chest. Although botfly parasitism has been widely studied in several species of small mammals, there are no prior reports of the host consuming the emerged botfly parasite.

Effects of Bot Fly Parasitism on Movements of Peromyscus leucopus

Factors that affect movement of small mammals include vegetation structure, resource distribution, interspecific interactions and parasitism. The objective of this study was to assess the effect of bot fly (Cuterebra fontinella) parasitism on movement distance [estimated by mean squared distance (MSD)] of white-footed deermice (Peromyscus leucopus), using a repeated measures approach. Although there was no significant effect of infestation on MSD, there was a nonsignificant trend towards increased movement during infestation for females. In addition, there was no difference in MSD between individuals with single infestations and those harboring several larvae. These results are unexpected given the large size of the parasite relative to the host. Studies of fine-scale temporal movements within a single night could shed further light on the effects of infestation on movement.

Energetic cost of bot fly parasitism in free-ranging eastern chipmunks

The energy and nutrient demands of parasites on their hosts are frequently invoked as an explanation for negative impacts of parasitism on host survival and reproductive success. Although cuterebrid bot flies are among the physically largest and most-studied insect parasites of mammals, the only study conducted on metabolic consequences of bot fly parasitism revealed a surprisingly small effect of bot flies on host metabolism. Here we test the prediction that bot fly parasitism increases the resting metabolic rate (RMR) of free-ranging eastern chipmunks (Tamias striatus), particularly in juveniles who have not previously encountered parasites and have to allocate energy to growth. We found no effect of bot fly parasitism on adults. In juveniles, however, we found that RMR strongly increased with the number of bot fly larvae hosted. For a subset of 12 juveniles during a year where parasite prevalence was particularly high, we also compared the RMR before versus during the peak of bot fly prevalence, allowing each individual to act as its own control. Each bot fly larva resulted in a approximately 7.6% increase in the RMR of its host while reducing juvenile growth rates. Finally, bot fly parasitism at the juvenile stage was positively correlated with adult stage RMR, suggesting persistent effects of bot flies on RMR. This study is the first to show an important effect of bot fly parasitism on the metabolism and growth of a wild mammal. Our work highlights the importance of studying cost of parasitism over multiple years in natural settings, as negative effects on hosts are more likely to emerge in periods of high energetic demand (e.g. growing juveniles) and/or in harsh environmental conditions (e.g. low food availability).

Prevalence of larvae of the bot fly Cuterebra simulans (Diptera, Oestridae) on Gracilinanus microtarsus (Didelphimorphia, Didelphidae) in southeastern Cerrado from Brazil

The prevalence of Cuterebra simulans bot fly parasitism on marsupial Gracilinanus microtarsus was compared between sexes and seasons of the year. No significant difference was observed between females and males but prevalence was higher in warm-wet season than cool-dry season. This pattern agree with observations of others studies with oestrids flies in southern Neotropical areas, suggesting the occurrence of latitudinal change in the peak of bot flies reproductive activity related to seasons of the year along these systems. This is the first record of C. simulans larvae parasitism on G. microtarsus and its occurrence in southern areas of the Neotropical region.

Bot fly parasitism of the red-backed vole: host survival, infection risk, and population growth

Parasites can play an important role in the dynamics of host populations, but empirical evidence remains sparse. We investigated the role of bot fly (Cuterebra spp.) parasitism in red-backed voles (Myodes gapperi) by first assessing the impacts of the parasite on the probability of vole survival under stressful conditions as well as on the reproductive activity of females. We then identified the main factors driving both the individual risk of infection and the abundance of bot flies inside red-backed voles. Finally, we evaluated the impacts of bot fly prevalence on the growth rate of vole populations between mid-July and mid-August. Thirty-six populations of red-backed voles were sampled in the boreal forest of Québec, Canada. The presence and the abundance of parasites in voles, two host life history traits (sex and body condition), three indices of habitat complexity (tree basal area, sapling basal area, coarse woody debris volume), and vole abundance were considered in models evaluating the effects of bot flies on host populations. We found that the probability of survival of red-backed voles in live traps decreased with bot fly infection. Both the individual risk of infection and the abundance of bot flies in red-backed voles were driven mainly by vole abundance rather than by the two host life history traits or the three variables of habitat complexity. Parasitism had population consequences: bot fly prevalence was linked to a decrease in short-term growth rate of vole populations over the summer. We found that bot flies have the potential to reduce survival of red-backed voles, an effect that may apply to large portions of populations.

Early Infestation by Bot Flies (Philornis Seguyi) Decreases Chick Survival and Nesting Success in Chalk-Browed Mockingbirds (Mimus Saturninus)

AbstractBot flies (Diptera: Muscidae: Philornis spp.) are a group of flies comprising mostly species with a Neotropical distribution. Their larvae parasitize several species of birds, living subcutaneously on altricial chicks. We investigated the effect of parasitism by bot flies (P. seguyi) on the reproductive success of Chalk-browed Mockingbirds (Mimus saturninus) in temperate grasslands near the southern limit of bot fly distributions. We analyzed seasonal variation of bot fly prevalence during three consecutive years and how the timing and intensity of bot fly infestation affected growth and survival of Chalk-browed Mockingbird nestlings. Bot fly prevalence was 58.3%, 30.7%, and 45.5% each year, and in all years, it increased with time of breeding. Most of the infested nests fledged no chicks. In these nests, chicks had a lower tarsus growth rate than in noninfested nests and died 3–4 days after parasitism. The average time from hatching of the first chick until infestation was 4.4 days. The age of the chicks at the time of infestation was associated positively with nesting success and negatively with intensity of parasitism. Bot fly parasitism also reduced the survival of Shiny Cowbird (Molothrus bonariensis) chicks present in Chalk-browed Mockingbird nests, but the presence of Shiny Cowbird chicks did not affect timing of infestation or fledging success of Chalk-browed Mockingbird chicks. Our results show that an intermediate prevalence of bot fly parasitism produces an important decrease in the reproductive success of Chalk-browed Mockingbirds and suggest that bot flies may play an important role as selective agents in the evolution of host life-history strategies.La Infestación Temprana con Larvas de Philornis seguyi Disminuye la Supervivencia de los Pichones y el Éxito de Nidificación de Mimus saturninus

EFFECTS OF BOT FLY (CUTEREBRA FONTINELLA) PARASITISM ON A POPULATION OF WHITE-FOOTED MICE (PEROMYSCUS LEUCOPUS)

Bot flies are common parasites of Peromyscus leucopus, although determination of a cost to the host has been elusive. The goal of this study was to further explore the potential costs of bot fly parasites for a population of P. leucopus. We investigated the effects of parasitism on host condition (mass after controlling for parasite mass and host body length) and survivorship (the number of days animals persisted on trapping grids). Parasitism was quantified by prevalence (proportion of the population infected), intensity (the number of parasites per infected host), and dispersion of parasites within hosts (clumped, regular, or random). In addition, we searched for spatial and temporal patterns in infection. Finally, we analyzed the relationship between population demography and parasitism. Contrary to expectations, we found that infected mice persisted longer on trapping grids and were in better condition than uninfected mice. Also, we discovered that when considering overall infection levels, parasites were clumped within hosts, but when considering the number of simultaneous infections, parasites were randomly distributed among hosts. Although most animals had single infections, there was a high incidence of reinfections, leading to bimodal patterns of parasitism. Prevalence was not correlated with host density, sex ratio, or proportion reproductive, but there were significant relationships between intensity and density and sex ratio in 1 year. In addition, prevalence and proportion of reproductively active animals were asynchronous. These results suggest that bot flies do not impose an obvious cost to their hosts, and hosts may express some degree of tolerance for bot fly parasitism.

The incidence of Botfly parasitism in small mammals near White River, Ontario, Canada

The incidence of Botfly parasitism in small mammals near White River, Ontario, Canada

A PRESCRIPTION FOR LONGER LIFE? BOT FLY PARASITISM OF THE WHITE-FOOTED MOUSE

Investigation of host–parasite interactions typically reveals a negative impact of parasitism on the host species. In contrast, mounting evidence indicates that bot fly (Cuterebra sp.) infestation enhances the survival of white-footed mice (Peromyscus leucopus). We propose that life history trade-offs, namely, between reproduction and survival, can explain this counterintuitive observation. By using an extensive data set spanning a decade, 12 sites in two states, and over 30 000 mouse captures, we offer a new perspective on the effects of bot fly parasitism on white-footed mice. Analysis of persistence time corroborated earlier studies that showed significantly higher survival rates of infested mice. Although a higher proportion of infested than uninfested females were in breeding condition, secondary reproductive success appeared to be negatively impacted by parasitism via declines in the number of litters and the total number of offspring produced by infested females. Population growth rates were negatively correlated with infestation prevalence, further indicating a negative effect of parasitism. Based on the negative impact of parasitism on reproduction, we propose that enhanced survival of infested mice can be explained by the diversion of resources from reproduction to body maintenance. Parasite-induced life history shifts in which mice decrease current reproduction to promote future reproduction, such as increasing the age at maturity, may also contribute to the decline in population growth rate observed in years of high infestation prevalence.

The effect of botfly parasitism of Metacuterebra apicalis (Diptera)on reproduction, survival and general health of Oryzomys russatus (Rodentia), in Southeastern Brazil

Les myiases dues a des Dipteres Cuterebrides peuvent compromettre la reproduction et la survie des hotes infestes. Nous examinons l'effet du parasitisme par ces mouches (Metacuterebra apicalis) sur la bonne sante generale d'Oryzomys russatus. Cette etude a ete entreprise dans les forets atlantiques du sud-est du Bresil, de fevrier 1993 a janvier 1995. La prevalence de cette myiase chez O. russatus a ete nettement saisonniere, augmentant au cours des mois chauds et humides, et diminuant au cours des mois froids et secs. Les hotes mâles ont ete infectes, de maniere significative, plus souvent que les femelles, mais nos resultats suggerent que la survie, la bonne sante generale et la reproduction de O. russatus n'ont pas ete alterees par ce parasitisme.