Comprehensive investigation of ectoparasite community and abundance across life history stages of avian host

Fitness consequences of ectoparasitism are expressed over the lifetime of their hosts in relation to variation in composition and abundance of the entire ectoparasite community and across all host life history stages. However, most empirical studies have focused on parasite species-specific effects and only during some life history stages. We conducted a systematic, year-long survey of an ectoparasite community in a wild population of house finches Carpodacus mexicanus Müller in south-western Arizona, with a specific focus on ecological and behavioral correlates of ectoparasite prevalence and abundance. We investigated five ectoparasite species: two feather mite genera – both novel for house finches – Strelkoviacarus (Analgidae) and Dermoglyphus (Dermoglyphidae), the nest mite Pellonyssus reedi (Macronyssidae), and the lice Menacanthus alaudae (Menoponidae) and Ricinus microcephalus (Ricinidae). Mite P. reedi and louse Menacanthus alaudae abundance peaked during host breeding season, especially in older birds, whereas feather mite abundance peaked during molt. Overall, breeding birds had more P. reedi than non-breeders, molting males had greater abundance of feather mites than molting females and non-molting males, and young males had more feather mites than older males. We discuss these results in relation to natural history of ectoparasites under study and suggest that ectoparasites might synchronize their life cycles to those of their hosts. Pronounced differences in relative abundance of ectoparasite species among host's life history stages have important implications for evolution of parasite-specific host defenses.     

Comparative analysis of landscape effects on spatial genetic structure of the big brown bat and one of its cimicid ectoparasites

Identification of landscape features that correlate with genetic structure permits understanding of factors that may influence gene flow in a species. Comparing effects of the landscape on a parasite and host provides potential insights into parasite‐host ecology. We compared fine‐scale spatial genetic structure between big brown bats (Eptesicus fuscus) and their cimicid ectoparasite (Cimex adjunctus; class Insecta) in the lower Great Lakes region of the United States, in an area of about 160,000 km². We genotyped 142 big brown bat and 55 C. adjunctus samples at eight and seven microsatellite loci, respectively, and inferred effects of various types of land cover on the genetic structure of each species. We found significant associations between several land cover types and genetic distance in both species, although different land cover types were influential in each. Our results suggest that even in a parasite that is almost entirely reliant on its hosts for dispersal, land cover can affect gene flow differently than in the hosts, depending on key ecological aspects of both species.     

Alphacoronaviruses in New World bats: prevalence, persistence, phylogeny, and potential for interaction with humans

Bats are reservoirs for many different coronaviruses (CoVs) as well as many other important zoonotic viruses. We sampled feces and/or anal swabs of 1,044 insectivorous bats of 2 families and 17 species from 21 different locations within Colorado from 2007 to 2009. We detected alphacoronavirus RNA in bats of 4 species: big brown bats (Eptesicus fuscus), 10% prevalence; long-legged bats (Myotis volans), 8% prevalence; little brown bats (Myotis lucifugus), 3% prevalence; and western long-eared bats (Myotis evotis), 2% prevalence. Overall, juvenile bats were twice as likely to be positive for CoV RNA as adult bats. At two of the rural sampling sites, CoV RNAs were detected in big brown and long-legged bats during the three sequential summers of this study. CoV RNA was detected in big brown bats in all five of the urban maternity roosts sampled throughout each of the periods tested. Individually tagged big brown bats that were positive for CoV RNA and later sampled again all became CoV RNA negative. Nucleotide sequences in the RdRp gene fell into 3 main clusters, all distinct from those of Old World bats. Similar nucleotide sequences were found in amplicons from gene 1b and the spike gene in both a big-brown and a long-legged bat, indicating that a CoV may be capable of infecting bats of different genera. These data suggest that ongoing evolution of CoVs in bats creates the possibility of a continued threat for emergence into hosts of other species. Alphacoronavirus RNA was detected at a high prevalence in big brown bats in roosts in close proximity to human habitations (10%) and known to have direct contact with people (19%), suggesting that significant potential opportunities exist for cross-species transmission of these viruses. Further CoV surveillance studies in bats throughout the Americas are warranted.     

Habitat fragmentation and the prevalence of parasites (Diptera,Streblidae) on three Phyllostomid bat species

Ectoparasitism in bats seems to be influenced strongly by the type of roost preferred by the hosts, and group size; however, the effect of habitat loss and fragmentation on the prevalence of ectoparasites in bats has scarcely been studied. In northeastern Yucatan, Mexico, we estimated the prevalence of infestation by Streblidae flies in three phyllostomid bat species with different roost preferences (caves, trees, or both) in two types of landscape matrices (tropical semi‐deciduous forest and man‐made pastures) that differed in area of forest cover and the number of forest fragments. Habitat fragmentation and the presence of a contrasting matrix may limit the availability of roosts (trees) and the movement of bats across the landscape. Accordingly, we hypothesized higher prevalence of Streblidae infestation in the pasture matrix and in the group of bats that roost in trees. Bat abundance was higher in the pasture matrix; however, the prevalence of infestation was significantly higher in the continuous forest matrix and in bats that roosted in caves. The prevalence of some species of Streblidae was affected by habitat fragmentation in species that roost in caves, such as Desmodus rotundus, as well as those using foliage and caves, such as Artibeus jamaicensis. Our results provide evidence that some species of Streblidae may respond differently to habitat fragmentation than their hosts, generating changes to bat‐ectoparasite interactions in fragmented areas. Environmental variations involving roosts, not evaluated in this study, may influence our results, since these factors affect ectoparasite abundance and reproduction.     

Host association influences variation at salivary protein genes in the bat ectoparasite Cimex adjunctus

Parasite–host relationships create strong selection pressures that can lead to adaptation and increasing specialization of parasites to their hosts. Even in relatively loose host–parasite relationships, such as between generalist ectoparasites and their hosts, we may observe some degree of specialization of parasite populations to one of the multiple potential hosts. Salivary proteins are used by blood‐feeding ectoparasites to prevent hemostasis in the host and maximize energy intake. We investigated the influence of association with specific host species on allele frequencies of salivary protein genes in Cimex adjunctus, a generalist blood‐feeding ectoparasite of bats in North America. We analysed two salivary protein genes: an apyrase, which hydrolyses ATP at the feeding site and thus inhibits platelet aggregation, and a nitrophorin, which brings nitrous oxide to the feeding site, inhibiting platelet aggregation and vasoconstriction. We observed more variation at both salivary protein genes among parasite populations associated with different host species than among populations from different spatial locations associated with the same host species. The variation in salivary protein genes among populations on different host species was also greater than expected under a neutral scenario of genetic drift and gene flow. Finally, host species was an important predictor of allelic divergence in genotypes of individual C. adjunctus at both salivary protein genes. Our results suggest differing selection pressures on these two salivary protein genes in C. adjunctus depending on the host species.     

Metagenomic analysis of the viromes of three North American bat species: viral diversity among different bat species that share a common habitat

Effective prediction of future viral zoonoses requires an in-depth understanding of the heterologous viral population in key animal species that will likely serve as reservoir hosts or intermediates during the next viral epidemic. The importance of bats as natural hosts for several important viral zoonoses, including Ebola, Marburg, Nipah, Hendra, and rabies viruses and severe acute respiratory syndrome-coronavirus (SARS-CoV), has been established; however, the large viral population diversity (virome) of bats has been partially determined for only a few of the ～1,200 bat species. To assess the virome of North American bats, we collected fecal, oral, urine, and tissue samples from individual bats captured at an abandoned railroad tunnel in Maryland that is cohabitated by 7 to 10 different bat species. Here, we present preliminary characterization of the virome of three common North American bat species, including big brown bats (Eptesicus fuscus), tricolored bats (Perimyotis subflavus), and little brown myotis (Myotis lucifugus). In samples derived from these bats, we identified viral sequences that were similar to at least three novel group 1 CoVs, large numbers of insect and plant virus sequences, and nearly full-length genomic sequences of two novel bacteriophages. These observations suggest that bats encounter and disseminate a large assortment of viruses capable of infecting many different animals, insects, and plants in nature.     

The relationship of sex and ectoparasite infestation in the water rat Scapteromys aquaticus (Rodentia: Cricetidae) in La Plata, Argentina

I studied the relationship between sex and infestation with ectoparasites in the water rat Scapteromys aquaticus from La Plata river marshland, Argentina. The Relative Density's Index (RDI) for males was 3.90% (females 3.60%). A total of 2653 ectoparasites were collected on 33 male hosts, and 1945 on 31 females. Ectoparasite specific richness (S) and diversity (H) were S = 14, H = 1.17 on males, and S = 10, H = 1.52 on females. The similarity between male and female rodents according to their ectoparasites was 75.00%. Although no ectoparasite species showed significant mean abundance (MA) differences between host sexes (p < 0.05), and only Laelaps manguinhosi prevalence was significantly higher on male hosts (N = 2.01, p < 0.05) in this study, there are reasons to think that the sex of the water rat affects ectoparasite burden and specific richness. This information has epidemiological potential because the closely related Scapteromys tumidus is involved in the transmission of Rickettsia coronii, which causes Marsella fever in humans.     

Contribution to the Ectoparasite Fauna of Bats (Chiroptera: Vespertilionidae,Rhinolophidae) of Crimea

New data are presented on the ectoparasite fauna of several species of vesper and horseshoe bats (Chiroptera: Vespertilionidae, Rhinolophidae) of the Crimean Peninsula. In the studied territory, 11 species of ectoparasites (mites and insects) have been collected from 6 bat species; 2 of the ectoparasite species were new to Crimea. Findings of gamasid mites Ichoronyssus scutatus on an unusual host are discussed. The gamasid mite Spinturnix emarginatus (Acari: Mesostigmata: Gamasina) is described for the territory of Russia for the first time.     

Antibodies to Pseudogymnoascus destructans are not sufficient for protection against white‐nose syndrome

White‐nose syndrome (WNS) is a fungal disease caused by Pseudogymnoascus destructans (Pd) that affects bats during hibernation. Although millions of bats have died from WNS in North America, mass mortality has not been observed among European bats infected by the fungus, leading to the suggestion that bats in Europe are immune. We tested the hypothesis that an antibody‐mediated immune response can provide protection against WNS by quantifying antibodies reactive to Pd in blood samples from seven species of free‐ranging bats in North America and two free‐ranging species in Europe. We also quantified antibodies in blood samples from little brown myotis (Myotis lucifugus) that were part of a captive colony that we injected with live Pd spores mixed with adjuvant, as well as individuals surviving a captive Pd infection trial. Seroprevalence of antibodies against Pd, as well as antibody titers, was greater among little brown myotis than among four other species of cave‐hibernating bats in North America, including species with markedly lower WNS mortality rates. Among little brown myotis, the greatest titers occurred in populations occupying regions with longer histories of WNS, where bats lacked secondary symptoms of WNS. We detected antibodies cross‐reactive with Pd among little brown myotis naïve to the fungus. We observed high titers among captive little brown myotis injected with Pd. We did not detect antibodies against Pd in Pd‐infected European bats during winter, and titers during the active season were lower than among little brown myotis. These results show that antibody‐mediated immunity cannot explain survival of European bats infected with Pd and that little brown myotis respond differently to Pd than species with higher WNS survival rates. Although it appears that some species of bats in North America may be developing resistance to WNS, an antibody‐mediated immune response does not provide an explanation for these remnant populations.     

Bat rabies in Illinois: 1965 to 1986

From 1968 to 1986, Illinois (USA) citizens and agencies submitted 4,272 bats to the Illinois Department of Public Health for rabies testing. Of this number, 6% tested positive, a rate comparable to similar studies from other parts of North America. Due to sampling biases, the true infection rate among bats in Illinois is probably lower than 6%. Additional analysis relied on a subsample (n = 2,433) of the specimens collected from 1965 to 1986. Prevalences were significantly different among years, but no linear trends were found over the study period. Evidence for a local outbreak of bat rabies was found. Prevalences for the species with sample sizes adequate for statistical analysis were, from high to low: hoary bat (Lasiurus cinereus), 11%; red bat (L. borealis), 5%; silver-haired bat (Lasionycteris noctivagans), 4%; little brown bat (Myotis lucifugus), 4%; big brown bat (Eptesicus fuscus), 3%; Keen's bat (Myotis keenii), 2%; and evening bat (Nycticeius humeralis), 2%. The higher prevalences found among the non-colonial species (hoary, red and silver-haired bats) were consistent with similar studies. Considerable annual variation in prevalences was found within species, and the prevalence rankings of the species varied over the study period. Prevalences were significantly higher in females (6%) than in males (4%) when species were pooled, but no significant differences between sexes were found within species. In contrast to the other species analyzed, all of which had sex ratios favoring females, the big brown bat sample had a large majority of males. Prevalences were significantly higher in adults (6%) than in juveniles (3%) when species were pooled. Within individual species, significant differences between age groups were found only for hoary and red bats; in two species, juveniles had higher prevalences. Above average prevalences were observed in May and August to November. Southern Illinois had the highest prevalences; prevalences were intermediate in the north and lowest in the central region. Overall, the patterns of rabies prevalence among bats submitted by the public in Illinois from 1965 to 1986 were similar to those reported from other parts of North America.     

Structure of parasitic arthropod communities in forest small mammals

Species composition and structure of ectoparasite arthropod communities were examined all year round six years in the bank vole Clethrionomys glareolus, Ural wood mouse Apodemus uralensis and the common shrew Sorex araneus in forests of the Ilmen'-Volkhov depression. In total, 4500 host samples have been examined and all ectoparasites have been collected. The species composition of ectoparasite community in small mammal species are as follows: the bank vole--29 insect, tick and mite species, the common shrew--23 species, the Ural wood mouse--16 species. In forest biotopes, many temporary ectoparasitic species occur on several host species living in the same habitats under a forest canopy and contacting each other. A parasitic supracommunity in the ecosystem examined has a pool of temporary ectoparasites, which is available for all the community of small mammals. A role of different rodent and shrew species are hosts of insects and ticks changes depending on a density of potential host populations and numerous other environment factors.     

Ectoparasites of Chevrier's field mouse, Apodemus chevrieri, in a focus of plague in southwest China

Chevrier's field mouse, Apodemus chevrieri Milne-Edwards (Rodentia: Muridae), has been identified as the main wild reservoir of plague in the sylvatic plague focus of Yunnan Province, southwest China. Here, the ectoparasite communities of A. chevrieri and the potential medical and veterinary importance of these ectoparasites are described. A high proportion (66%) of 321 mice were found to be infested with ectoparasites. A total of 81 species of ectoparasite, including 48 species of chigger mite, 25 species of mesostigmatid (gamasid) mite, six species of flea and two species of sucking louse were collected. Most species of ectoparasite were relatively uncommon, but a few were abundant. Within this ectoparasite complex, 16 species have previously been reported to be vectors of human disease agents. Apodemus chevrieri would appear therefore to be a natural reservoir for plague bacilli and epidemic haemorrhagic fever (Korean haemorrhagic fever) viruses.     

Rabies in insectivorous bats of western Canada, 1979 to 1983

A total of 1,745, 362, and 536 bats collected in Alberta, British Columbia, and Saskatchewan, respectively, was tested for rabies virus between 1979 and 1983. Only one (0.1%) of 769 bats collected at random from buildings was infected with rabies virus in contrast to 95 (5%) of 1,874 symptomatic, rabies-suspect bats submitted for testing. The pattern of infection in the rabies-suspect bats was similar in Alberta and Saskatchewan, but differed in British Columbia. Rabies was diagnosed in four species of bats in each of Alberta and Saskatchewan, but in seven species in British Columbia. Annual prevalence in rabies-suspect bats was similar in colonial species within each province. Rabies was found rarely in suspect little brown bats (Myotis lucifugus) (less than 1%). In suspect big brown bats (Eptesicus fuscus), the prevalence was low in Saskatchewan (3%), moderate in Alberta (10%), and high in British Columbia (25%). Big brown bats accounted for over 55% of the rabid bats detected in each province. Annual prevalence reported in silver-haired bats (Lasionycteris noctivagans) and hoary bats (Lasiurus cinereus) was variable in all three provinces. Rabies is enzootic in northern insectivorous bats.     

Interrelationship between ectoparasites and wild rodents from northeastern Buenos Aires Province,Argentina

Infestation parameters and indices of mites, ticks and fleas associated with wild rodents from northeastern Buenos Aires Province, Argentina, were studied. Host species similarity was also analyzed in relation to their ectoparasites. Fifty-five rodents were captured from January 2000 to March 2001. In total, 1,022 ectoparasites were collected and three ectoparasite-host associations were new records. However, this is the first study on Craneopsylla minerva wolffhuegeli infesting parameters. Ectoparasite total mean abundance and total prevalence were higher in Holochilus brasiliensis (MA = 47.7; P = 100%) and Scapteromys aquaticus (MA = 25.4; P = 95.4%), meanwhile specific richness and diversity were higher in Oligoryzomys flavescens (S = 6; H = 1.3) and Akodon azarae (S = 4; H = 1.0). On the other hand, the only individual of Calomys laucha was not parasited. S. aquaticus-H. brasiliensis, which preferred similar microhabitats, shared the same ectoparasite species (Css = 100). Whereas, A. azarae, which was mostly associated with grassland, showed the highest difference with the other hosts (Css < 0.4). Considering every ectoparasite species, H. brasiliensis showed the highest mean abundance, prevalence and preference. The results suggest that the particular characteristics of this rodent would give it better possibilities not only of being infested by ectoparasites, but also of transmitting them to its progeny.     

Bat rabies in South Carolina, 1970-90.

This retrospective study examines the geographic and temporal distribution of bat species submitted for rabies testing in South Carolina (USA) from 1970 to 1990. Histories of human or animal exposures to rabid and nonrabid bats submitted during this time period were compared. Two hundred and thirty-one bats were found to be rabid from the 2,657 bats submitted over this 20 yr period. The two species most frequently submitted for testing were Lasiurus borealis with 785 specimens (30% of the total) and Nycticeius humeralis with 607 specimens (22% of the total). Lasiurus borealis also had the highest prevalence of rabies (18%) while N. humeralis had the lowest prevalence (3%). Fifty-one percent (1,259) of the bats received for testing were submitted from June through August. The majority (54%) of rabid bats were received from August through October.     

Pupal deposition and ecology of bat flies (Diptera: Streblidae): Trichobius sp. (caecus group) in a Mexican cave habitat

We studied the deposition of pupae of the winged bat fly Trichobius sp. (caecus group; Diptera), an ectoparasite of Natalus stramineus (Chiroptera, Natalidae), in a natural cave in Tamaulipas, Mexico. For the first time, we show a strong spatial segregation of populations of a streblid bat fly at different stages of development. Using molecular techniques we were able to match developmental stages to adults. Only 5 pupae were present in the main bat roosts. The overwhelming majority occurred exclusively in the bat flyway passages at a considerable distance from roosting bats. Pupal density corresponded positively with the average flight height of bats in the cave passage. Taken together, observations suggest that these ectoparasites must actively seek out their hosts by moving onto passing or roosting bats. The scarceness of pupae in the main roost may be dictated by environmental constraints for their development. The estimated population of viable pupae far exceeds the population of imagoes on the bats, and predation on adults by spiders is common.     

Determinants of ectoparasite assemblage structure on rodent hosts from South American marshlands: the effect of host species,locality and season

The relative effects of host species identity, locality and season on ectoparasite assemblages (relative abundances and species richness) harboured by four cricetid rodent hosts (Akodon azarae, Oligoryzomys flavescens, Oxymycterus rufus and Scapteromys aquaticus) were assessed across six closely located sites in Buenos Aires province, Argentina. Relative abundances of ectoparasites (14 species including gamasid mites, an ixodid tick, a trombiculid mite, lice and fleas), as well as total ectoparasite abundance and species richness, were determined mainly by host species and to a lesser extent by locality (despite the small spatial scale of the study), whereas seasonal effect was weak, albeit significant. The abundances of some ectoparasites were determined solely by host, whereas those of other ectoparasites (sometimes belonging to the same higher taxon) were also affected by locality and/or season. In gamasids, there was a significant effect of locality for some species, but not for others. In fleas and lice, the effect of locality was similar in different species, suggesting that this effect is related to the characteristic life history strategy.     

Structure and seasonal dynamics of an ectoparasite community on the common shrew (Sorex araneus) in the Il'men'-Volkhov lowland

Species composition, seasonal dynamics, and a load of ectoparasites per individual and population of the common shrew Sorex araneus have been examined in coniferous and mixed forests of the Ilmen'-Volkhov lowland (a neighbourhood of Oskuy village, Chudovo district, Novgorod Province) during the period 1999-2003. Trapping of mammals was carried monthly, with exception of few accidental gaps. The Gero traps were used for catching micromammalian hosts. The lines of trap were checked 2 times a day, places of lines changed each 3-5 day. Total number of micromammalians collected during the period of study is 3215, including 1115 specimens of the common shrew S. araneus and 246 ones of the pigmy shrew S. minutus. Parasite fauna on the common shrew included 23 ectoparasite species: fleas--12, ixodid ticks--2, gamasid mites--7, and myobiid mites--2 species. Among recorded species, 9 fleas species and some gamasid species are accidental parasites. These accidental ectoparasite species are common to the bank vole Clethrionomys glareolus in the territory investigated. Species composition, occurrence and abundance indices of parasites changed during the year. In total, about 55% shrew specimens are infected with ectoparasites. The infracommunity of ectoparasites on the common shrew usually consists of 6 species or less. Mean number of all ectoparasite individuals per one host specimens varies from 4 to 83. The greatest number of parasites (50 and 83) was recorded on the shrews, which carried 5 and 4 parasites species, respectively. Biodiversity of parasite species in the ectoparasite community on the common shrew and the load of parasites per one host specimen are lower than those in the bank vole. In forest biotopes explored, the most part of temporary ectoparasite species found on the common shrew was also recorded on other small mammals, which could have contacts with this host. It is possible to conclude that among the parasite supracommunity in the explored ecosystem, the temporary ectoparasites represent a "fond" of temporary parasites, which are common for most small mammal species. A role of different shrew and rodent species as main of additional hosts changes depending on a population density of potential mammalian hosts and other environment factors.     

Predictive Occurrence Models for Bat Species in California

Abstract: The ability to accurately predict the potential occurrence of species of management concern is useful for wildlife managers, particularly for those whose management activities involve large areas where sampling is difficult due to logistical or financial constraints. During the summers of 2002 and 2003, we used mist nets to capture bats (Myotis yumanensis, M. californicus, M. evotis, M. thysanodes, Eptesicus fuscus, Lasionycteris noctivagans, Tadarida brasiliensis, Antrozous pallidus, Lasiurus borealis, and Lasiurus cinereus) in Whiskeytown National Recreation Area in north-central California, USA. We used landscape-scale variables, logistic regression, and Akaike's Information Criterion (AIC_c) to model species distributions and produce spatially discerning predictive occurrence maps. We developed a priori models that we used to determine which landscape-scale variables best discriminated between capture sites and non-capture sites. The odds of capturing a bat were 3.3 greater when total edge increased by 10,000 m, whereas for Yuma myotis (Myotis yumanensis), the odds of predicting presence were 0.2 greater when distance to lakes and ponds decreased by 2,000 m. Elevation was important in predicting the distribution of silver-haired bats (Lasionycteris noctivagans) and big brown bats (Eptesicus fuscus). Increasing elevation by 400 m decreased the odds of capturing a silver-haired bat by 0.1 and a big brown bat by 0.4. Classification accuracy for our models ranged from 80.9% for all bat species combined to 72.3% for Yuma myotis and silver-haired bats. Predictive occurrence models can be valuable to bat conservation efforts because they provide spatial data important for evaluating the effects of management activities on species distributions.