Survival rate of bat bugs (Cimex pipistrelli, Heteroptera) under different microclimatic conditions

Survival of facultative ectoparasites, e.g. bed bugs (Cimex spp.), is more intensely affected by climatic factors, namely temperature, than that of permanent ectoparasites. The ontogenetic time of the bat bug (Cimex pipistrelli) in bat roosts is limited by different survival rates under different temperatures in particular nymphal stages. This limitation could affect bug densities and cause asynchrony between the ectoparasite and bat reproductive cycle. Therefore, bug survival under different temperatures was tested in the laboratory. Survival success was evaluated by three types of survival analyses: Kaplan–Meier estimation, the Cox proportional hazards model and Weibull parametric regression. The bugs survived for only a few hours at 45°C; however, such a high temperature was never found in natural roosts. Different survival probability among different ontogenetic stages was found at the temperatures of 5–35°C, and it was the highest in adult females and nymphs of fourth and fifth instar. Early instars first to third were found to be the most sensitive with the highest mortality of all stages studied and having their best survival at 5°C. The hazard rate ratio of Weibull regression shows the low daily failure rate of 2.23–4.34% within the span of 5–35°C. C. pipistrelli had the shorter life cycle and the better survival at higher temperature (35°C) than C. lectularius. The ability of the former to survive high temperatures could be the consequence of its long-term coexistence with bats preferring crevice-like roosts or attics which become overheated during the summer months.     

Recolonization of bat roost by bat bugs (Cimex pipistrelli): could parasite load be a cause of bat roost switching?

Roost ectoparasites are believed to have a negative impact on fitness of their hosts as birds or mammals. Previous studies were mostly focussed on the synchronization between reproduction cycles of ectoparasites and hosts living in infested roosts. However, to date, it has not been examined how fast ectoparasites colonize new, non-infested roosts and thus increasing the impact on the local populations of hosts. The parasite–host model was studied, including bat bugs Cimex pipistrelli and soprano pipistrelles Pipistrellus pygmaeus, where bat behaviour was observed which tended to reduce the parasite load in bat roosts. We investigated (1) whether bats change their roosting behaviour when we discontinued synchronization of their reproduction and the life cycle of the bat bugs and (2) how fast and which stages of bat bugs reoccupy cleaned roosts. In a 3-year field experiment, we removed all bat bugs from six bat boxes in each spring. Pipistrelles bred young in all non-infested boxes during these 3 years. In addition, 8 years of regular observations before this experiment indicate that bats avoided breeding in the same bat boxes at all. Bat bugs were found again in clean boxes in mid-May. However, their densities did not maximise before the beginning of June, before parturition. A re-appearance of bugs was observed after 21–56 days after the first bat visit. Adult bugs, mainly females, colonised cleaned boxes first though at the same time there were a lot of younger and smaller instars in non-manipulated roosts in the vicinity.     

<Emphasis Type="Italic">Cimex pipistrelli</Emphasis> (Heteroptera,Cimicidae) and the dispersal propensity of bats: an experimental study

Previous results have shown frequent movements of crevice-dwelling bats between different shelters. Low roost fidelity of some dwelling bat species reduces the reproductive success of ectoparasites. The question of whether high densities of bat bugs (Cimex pipistrelli) represent a cost for crevice-dwelling bats (Pipistrellus pygmaeus), resulting in roost switching, has been examined. Sessions in a volary equipped with two bat boxes were carried out. One of the boxes was loaded with ectoparasites (low and high densities), the other served as a control and new roost for bats, which left the loaded box. Differences in the level of bat self-grooming, movements inside experimental boxes, and leaving the boxes between experiments with bat bugs and controls were significant. Allogrooming was observed only in few cases; therefore, the hypothesis of cooperation among individual bats in defense against bat bugs was rejected. Experiments with artificial parasitation, when bugs were added to a bat roost, showed that leaving a confined roost infested by bat bugs, i.e., roost switching, is a natural reaction of crevice-dwelling bat species, which reduces parasite load.     

Bat bugs (Cimex pipistrelli) and their impact on non-dwelling bats

Bat bugs are often roost ectoparasites of bats. Previous studies have shown that bats shifting roosts within the growing season prevent the massive reproduction of these parasites. We postulated that there could be other antiparasitic strategies of philopatric bats roosting in non-dwelling spacious roosts. Unfortunately, there are no studies devoted to such a topic. For 3?years, two attics highly and less infested by bat bugs (Cimex pipistrelli) with breeding females of Myotis myotis were monitored. From April, after the arrival of the bats, to November, abundance of all instars and adult bugs was sampled in the attics by adhesive traps. We found different patterns in the bug abundances and dynamics in the two attics. In highly infested attic, bat bugs induced pregnant females to move from the infested site of the attic to the non-infested one. Internal temperature and relative humidity were similar in both infested and non-infested sites. Females roosted in the infested site till time before parturition and then moved to the non-infested site within attic. When bats were absent in their old site, the abundance of nymphal instars of bugs decreased by half. Although adult bats can survive under high parasite loads of bat bugs, reproducing females prevent parasite reproduction and simultaneously reduce parasite load in the young by shifting inside spacious roosts.     

The reproductive success of the parasitic bat fly Basilia nana (Diptera: Nycteribiidae) is affected by the low roost fidelity of its host, the Bechstein’s bat (Myotis bechsteinii)

We studied the reproductive ecology of the bat fly Basilia nana on free-ranging colonial female and solitary male Bechstein’s bats (Myotis bechsteinii) during one reproductive season. The reproduction of B. nana took place from April to September, and the production of puparia in bat roosts was high. The metamorphosis of the flies took a minimum of 30 days, and at least 86% of the puparia metamorphosed successfully. However, only about 30% of flies from puparia deposited in female roosts and 57% of flies from puparia deposited in male roosts emerged in the presence of Bechstein’s bats and were thus able to survive. The significantly higher emergence success of bat flies in male roosts was caused by the higher roost fidelity of the solitary males compared with the social females. Our results indicate that bats can control the reproductive success of bat flies by switching and selecting roosts.     

Observations on the transmission and development ofToxocara pteropodis (Ascaridoidea: Nematoda) in the Australian Grey-Headed Flying-Fox,Pteropus poliocephalus (Pteropodidae: Megachiroptera)

Findings in the Australian Grey-Headed Flying-Fox,Pteropus poliocephalus, have elucidated the life-cycle ofToxocara pteropodis. In adult bats, other than parturient females, larvae were found only in the livers. Following parturition, larvae were recovered only from mammary glands up to 2 weeks post-partum. Developing larvae were found only in the intestine of young bats from the age of two days onwards; there was no evidence of pulmonary migration. The evidence indicates that juvenile bats commence passingToxocara eggs in their faeces at about 2 months of age and expel the worms spontaneously following weaning at about 5 months. The eggs passed in the faeces of the young bat and its mother are disseminated through-out their environment and embryonate rapidly, being infective to mice after 10 days. Under natural conditions the eggs remain viable for 6 weeks or less and are infective to bats by the oral route.     

Detection of human blood in the bat tick Carios (Ornithodoros) kelleyi (Acari: Argasidae) in Iowa

The argasid tick Carios (Ornithodoros) kelleyi Cooley & Kohls is a common ectoparasite of bats and has been found in massive numbers in homes with associated bat colonies in eastern Iowa. This tick feeds nearly exclusively on bats in nature. Several inhabitants of infested homes complained of "bug bites" at night while asleep that may have resulted in erythematous, edematous, urticaric skin lesions and constitutional signs and symptoms. We provide laboratory evidence that a single, engorged C. kelleyi nymph contained host blood from a human female. The clinical implications of our findings are intriguing but unclear.     

The life history of Pleurogenoides orientatis (Srivastava, 1934) (Trematoda: Lecithodendriidae)

The life history of Pleurogenoides orientalis (Srivastava 1934), a lecithodendriid trematode of frogs in India is reported and stages in the life history are described. Natural infections with cercariae, which are virgulate xiphidiocercous type, were found in the prosobranch snail Alocinma travancorica. Metacercarial cysts were found in dragon-fly naiads (Tholymis tillarga and Tramea limbata) and aquatic bugs (Laccotrephes griseus and Ranatra elongata) collected from a stream. Adults occurred in the intestine of the pong frog, Rana cyanophlyctis. Laboratory reared A. travancorica fed with eggs of P. orientalis started shedding cercariae from 30 days post feeding. Development of cercariae into infective metacercariae in dragon-fly naiads took 18 days. Mature flukes were recovered from the intestine of experimentally infected R. cyanophlyctis. The entire life cycle from egg to egg producing adult takes 2 1/2 to 3 months.     

Natural infection of vertebrate hosts by different lineages of Buggy Creek virus (family Togaviridae, genus Alphavirus)

Buggy Creek virus (BCRV; family Togaviridae, genus Alphavirus) is an arbovirus transmitted by the ectoparasitic swallow bug (Hemiptera: Cimicidae: Oeciacus vicarius) to cliff swallows (Petrochelidon pyrrhonota) and house sparrows (Passer domesticus). BCRV occurs in two lineages (A and B) that are sympatric in bird nesting colonies in the central Great Plains, USA. Previous work on lineages isolated exclusively from swallow bugs suggested that lineage A relies on amplification by avian hosts, in contrast to lineage B, which is maintained mostly among bugs. We report the first data on the BCRV lineages isolated from vertebrate hosts under natural conditions. Lineage A was overrepresented among isolates from nestling house sparrows, relative to the proportions of the two lineages found in unfed bug vectors at the same site at the start of the summer transmission season. Haplotype diversity of each lineage was higher in bugs than in sparrows, indicating reduced genetic diversity of virus amplified in the vertebrate host. BCRV appears to have diverged into two lineages based on different modes of transmission.     

Bat flies (Diptera: Streblidae, Nycteribiidae) and mites (Acari) associated with bats (Mammalia: Chiroptera) in a high-altitude region in southern Minas Gerais, Brazil

A total of 71 bat flies belonging to families Nycteribiidae and Streblidae, and 37 mites were collected on 12 species of bats (Phyllostomidae and Vespertilionidae) from the Chapada do Abanador (Minas Gerais, Brazil), between July 2009 and April 2010. Two new occurrences of ectoparasites were recorded on Histiotus velatus (bat fly Basilia producta) and on Carollia perspicillata (mite Parichoronyssus bakeri). Five new occurrences were recorded for the state of Minas Gerais, increasing the range for bat flies Anatrichobius passosi, Paraeuctenodes similis, Basilia juquiensis, Basilia producta and for mite Periglischrus vargasi. Moreover, two new species of mites were recorded for Brazil (P. bakeri and Macronyssus aff. leislerianus). With regard to infracommunities, the most frequent association was between Anastrebla modestini and Exastinion clovisi on bat Anoura geoffroyi. This study contributed to characterize the fauna of bat ectoparasites in representative but poorly-sampled environments of the Atlantic Forest, the campos de altitude (high altitude grasslands) and cloud forests of southern Minas Gerais.     

Ectoparasitic mites (Acari) of sympatric Brazilian free-tailed bats and big brown bats in Alabama.

Seven species of mites were recovered from 133 Brazilian free-tailed bats, Tadarida brasiliensis, and 94 big brown bats, Eptesicus fuscus, from February through November 1990 in colonies that shared roosting space in east-central Alabama. The macronyssid Chiroptonyssus robustipes (Ewing) was the most common mite on T. brasiliensis (964 mites, 87% of bats infested) and on E. fuscus (109 mites, 29% of bats infested). However, C. rubustipes normally is a specific parasite of T. brasiliensis. The macronyssids Steatonyssus ceratognathus (Ewing) and S. occidentalis (Ewing) were recovered from both species of bats in low numbers. S. ceratognathus is not a typical parasite of either species of bat, but S. occidentalis normally is specific to E. fuscus. Predictably, S. occidentalis was most frequently collected from E. fuscus (16 mites, 9% of bats infested), but two specimens were recovered from T. brasiliensis. Five specimens of the laelapid Androlaelaps casalis (Berlese) (a mite that is frequently associated with rodents) and one specimen of the myobiid mite Ewingana (Doreyana) longa (Ewing) (a specific ectoparasite of T. brasiliensis) were also recovered from T. brasiliensis. Singletons of the rosensteiniids Mydopholeus sp. and Nycteriglyphites pennsylvanicus Fain, Lukoschus & Whitaker were the only additional mites collected from E. fuscus; both of these mites have previously been collected from bats or their guano but are recorded here from Alabama for the first time. With respect to ectoparasite cross-infestations, E. fuscus appears to be at greater risk from sharing roots with T. brasiliensis. This is highlighted by the comparatively large numbers of C. robustipes that occurred on E. fuscus and the low numbers of S. occidentalis on T. brasiliensis. Although mites were the only arthropods recovered from bats in this study, a separate survey in 1991 revealed that the bat bug Cimex adjunctus Barber infested some other colonies of T. brasiliensis and E. fuscus in Alabama.     

Host ecology moderates the specialization of Neotropical bat-fly interaction networks

The transmission of diseases through parasites is a key mechanism in the regulation of plant and animal populations in ecosystems. Therefore, it is necessary to investigate the relative effect of the variables that can shape the specificity of host-parasite interactions. Previous studies have found that specialization of antagonistic interactions between fly ectoparasites and bats changes according to forest type, host richness, and roosting ecology of bats. In this study, we tested these hypotheses using data from 48 bat communities. In general, our results support previous findings that bat-fly interactions are specialized, resulting in lower niche overlap among bat flies species. In addition, we found that the specificity of bat-fly interactions is lower in tropical mountain forests and is positively related with the richness of bat host species of each study site. Finally, there was a higher bat flies niche overlap in smaller bat-fly interaction networks recorded in bat roosts in caves. We conclude that the roosting ecology of bats could be a key factor to understand the mechanisms related to the horizontal transmission of ectoparasitic flies among bats.

     

Parasitism by bat flies (Diptera: Streblidae) on neotropical bats: effects of host body size,distribution, and abundance

We examined the correlations between prevalence (proportion of infested individuals), mean intensity (number of parasites per infested individual), and the number of bat fly species parasitizing bats in Venezuela with host body mass, distribution, and abundance. Of 133 bat species sampled, 53 species in six families were captured frequently enough to allow estimation of their parasite loads. Over all species and six families, prevalence and mean intensity were uncorrelated with these variables, but the number of fly species was correlated with host body mass. Correlations of parasitism with body mass were strengthened among the 44 species of Phyllostomidae. Earlier studies showed that bat roosting habits influence their parasitism by bat flies with more permanent, enclosed roosts being with heavier parasitism. Multiple regressions of all measures of parasitism showed that roosting habits and host body mass, respectively, were the first variables to enter stepwise regressions, together accounting for 20-43% of the variation in measures of parasitism. Lack of correlation between proxies of distribution and abundance with parasitism is taken to indicate that proximate factors such as host-as-habitat, social groupings, and roost microhabitat take precedence over species-wide attributes like commonness and ubiquity.     

Morphology and Postnatal Development of Lower Hindlimbs in Desmodus rotundus (Chiroptera: Phyllostomidae): A Comparative Study

The hindlimbs in bats are functionally adapted to serve as a hook to attach to the mother from birth, and to roost during independent life. Although bats exhibit different terrestrial locomotion capabilities involving hindlimbs, hindlimb morphology and postnatal development have been poorly studied. We describe in detail the postnatal development and bone morphology of hindlimbs of the nimble walker vampire bat, Desmodus rotundus, and compare adult characters with the insectivorous Molossus molossus (erratic walker) and the frugivorous Artibeus lituratus (non‐walker). The advanced ossification of most hindlimb elements of D. rotundus at the newborn stage is consistent with the functional role of this structure at birth in bats. The development completion events of hindlimb bone elements and bone processes in D. rotundus coincide with the cranial bone processes completion and suture closure events. Those events occur when individuals begin to feed by themselves. There are differences in the number and position of bone processes and sesamoids in adults among the compared species, most of which are described for the first time, and in the case of D. rotundus and M. molossus mostly related to a greater and tight articulation between elements. These facts seem to be closely associated with the different terrestrial locomotion capabilities, and in the case of the exclusively sanguivorous D. rotundus with specializations for obtaining food. Anat Rec, 300:2150–2165, 2017. © 2017 Wiley Periodicals, Inc.     

The virome of the white-winged vampire bat Diaemus youngi is rich in circular DNA viruses

In the Neotropical region, the white-winged vampire bat (Diaemus youngi) is the rarest of the three species of vampire bats. This bat species feeds preferentially on bird blood, and there is limited information on the viruses infecting D. youngi. Hence, this study aimed to expand the knowledge about the viral diversity associated with D. youngi by sampling and pooling the lungs, liver, kidneys, heart, and intestines of all animals using high-throughput sequencing (HTS) on the Illumina MiSeq platform. A total of three complete and 10 nearly complete circular virus genomes were closely related to gemykrogvirus (Genomoviridae family), smacovirus (Smacoviridae family), and torque teno viruses (TTVs) (Anelloviridae family). In addition, three sequences of bat paramyxovirus were detected and found to be closely related to viruses reported in Pomona roundleaf bats and rodents. The present study provides a snapshot of the viral diversity associated with white-winged vampire bats and provides a baseline for comparison to viruses detected in future outbreaks.

     

Angiotensin-converting enzyme 2 (ACE2) proteins of different bat species confer variable susceptibility to SARS-CoV entry

The discovery of SARS-like coronavirus in bats suggests that bats could be the natural reservoir of SARS-CoV. However, previous studies indicated the angiotensin-converting enzyme 2 (ACE2) protein, a known SARS-CoV receptor, from a horseshoe bat was unable to act as a functional receptor for SARS-CoV. Here, we extended our previous study to ACE2 molecules from seven additional bat species and tested their interactions with human SARS-CoV spike protein using both HIV-based pseudotype and live SARS-CoV infection assays. The results show that ACE2s of Myotis daubentoni and Rhinolophus sinicus support viral entry mediated by the SARS-CoV S protein, albeit with different efficiency in comparison to that of the human ACE2. Further, the alteration of several key residues either decreased or enhanced bat ACE2 receptor efficiency, as predicted from a structural modeling study of the different bat ACE2 molecules. These data suggest that M. daubentoni and R. sinicus are likely to be susceptible to SARS-CoV and may be candidates as the natural host of the SARS-CoV progenitor viruses. Furthermore, our current study also demonstrates that the genetic diversity of ACE2 among bats is greater than that observed among known SARS-CoV susceptible mammals, highlighting the possibility that there are many more uncharacterized bat species that can act as a reservoir of SARS-CoV or its progenitor viruses. This calls for continuation and expansion of field surveillance studies among different bat populations to eventually identify the true natural reservoir of SARS-CoV.     

Two novel adenoviruses found in Cave Myotis bats (Myotis velifer) in Oklahoma

Bats are carriers of potentially zoonotic viruses, therefore it is crucial to identify viruses currently found in bats to better understand how they are maintained in bat populations and evaluate risks for transmission to other species. Adenoviruses have been previously detected in bats throughout the world, but sampling is still limited. In this study, 30 pooled-guano samples were collected from a cave roost of Myotis velifer in Oklahoma. A portion of the DNA polymerase gene from Adenoviridae was amplified successfully in 18 M. velifer samples; however, DNA sequence was obtained from only 6 of these M. velifer samples. One was collected in October 2016, one in March 2017, and 4 in July 2017. The October and March samples contained viral DNA that was 3.1% different from each other but 33% different than the novel viral sequence found in the July 2017 samples. Phylogenetic analysis of these fragments confirmed our isolates were from the genus Mastadenovirus and had genetic diversity ranging from 20 to 50% when compared to other bat adenoviruses.

     

Mitochondrial DNA and morphology show independent evolutionary histories of bedbug Cimex lectularius (Heteroptera: Cimicidae) on bats and humans

The bedbug, Cimex lectularius, is a well-known human ectoparasite that is reemerging after a long absence of several decades in developed countries of North America and Western Europe. Bedbugs' original hosts were likely bats, and the bedbugs are still common in their roosts. Using morphometry and sequences of mitochondrial cytochrome oxidase subunit I and 16S genes, we showed that the populations on bats and humans are largely isolated and differ in morphology. The character of the morphological difference suggests it to be due to adaptation to different hosts, namely adaptations to different sensory, feeding, and dispersal needs. Using the molecular data, we estimated the time of splitting into bat- and human-parasitizing groups using the isolation-with-migration model. The estimate is surprisingly long ago and seems to predate the expansion of modern human from Africa. The gene flow between bat- and human-parasitizing bedbugs is limited and asymmetric with prevailing direction from human-parasitizing populations to bat-parasitizing populations. The differentiation of the populations fits the concept of host races and supports the idea of sympatric speciation. Furthermore, our findings contradict recently formulated hypotheses suggesting bat roosts as a source of bedbug's resurgence as a human pest. Also, we extend the known host range of the bedbug by two bat species.     

Variation in ectoparasite load in the Mehely’s horseshoe bat, Rhinolophus mehelyi (Chiroptera: Rhinolophidae) in a nursery colony in western Iran

We studied variation of ectoparasite load in a free ranging populations of Mehely’s horseshoe bat (Rhinolophus mehelyi) on five successive occasions in a nursery roost in western Iran. In total, 87 Rhinolophus mehelyi were captured. The patterns of abundance differed greatly among parasite species but total parasite load was markedly higher in pregnant females in spring and early summer and lower in solitary males. On average, 90% of bats were infested by Eyndhovenia sp. with a mean intensity of 13.79 individuals per bat. Penicillidia sp. and one species from Streblidae were found in 66.7% and 11.49% of bats with parasite load of 2.31 and 1.8 parasite per bat, respectively. Using ratio of forearm length to body mass as an indication of bat health the correlation coefficient between parasite load and the health indicator was 0.002 for males and 0.06 for females indicating that parasite load has no apparent impact on bat’s health.     

Comparative ultrastructure study of lamellar gastrodermal projections in Echinostoma paraensei, E. caproni, and E. trivolvis (Trematoda: Echinostomatidae)

A comparative ultrastructure study using transmission electron microscopy (TEM) of ultrathin sections, freeze-fracture replication, and scanning electron microscopy (SEM) was conducted on the gastrodermal lamellar microvilli in adults of Echinostoma paraensei, E. caproni, and E. trivolvis. Lamellar projections observed by SEM were mainly planiform and rhomboidal or paddle-shaped, and they were commonly seen in the three species. The distal margins of these lamellae were mainly smooth in E. paraensei, whereas filiform or digitiform extensions in the margins occurred occasionally in E. caproni and frequently in E. trivolvis. Freeze-fracture TEM elucidated significant interspecific differences in the numbers of intramembranous particles (IMP) per square micrometer; the numbers of IMP were significantly lower in E. trivolvis than in either E. caproni or E. paraensei. Thus, ultrastructural differences in the gastrodermal lamellae of adult echinostomes will be a taxonomically useful criterion for distinguishing species of Echinostoma. Received: 8 March 1999 / Accepted: 25 March 1999