van Schaik, Jaap

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Author's Bibliography

Non-invasive investigation of Polychromophilus parasite infections in bat populations in Serbia using bat flies

Bajić, Branka; Werb, Oskar; Budinski, Ivana; Blagojević, Jelena; Schaer, Juliane; van Schaik, Jaap

(Springer Nature, 2023)

TY  - JOUR
AU  - Bajić, Branka
AU  - Werb, Oskar
AU  - Budinski, Ivana
AU  - Blagojević, Jelena
AU  - Schaer, Juliane
AU  - van Schaik, Jaap
PY  - 2023
UR  - http://radar.ibiss.bg.ac.rs/handle/123456789/5768
AB  - Background

Haemosporidian parasites of the genus Polychromophilus infect bats worldwide. They are vectored by obligate ectoparasitic bat flies of the family Nycteribiidae. Despite their global distribution, only five Polychromophilus morphospecies have been described to date. The two predominant species, Polychromophilus melanipherus and Polychromophilus murinus, are broadly distributed and mainly infect miniopterid and vespertilionid bats, respectively. In areas where species from different bat families aggregate together, the infection dynamics and ability of either Polychromophilus species to infect other host families is poorly characterized.

Methods

We collected 215 bat flies from two bat species, Miniopterus schreibersii and Rhinolophus ferrumequinum, which sometimes form mixed clusters in Serbia. Miniopterus schreibersii is known to be frequently infected with P. melanipherus, whereas R. ferrumequinum has been observed to be incidentally infected with both Polychromophilus species. All flies were screened for Polychromophilus infections using a PCR targeting the haemosporidian cytb gene. Positive samples were subsequently sequenced for 579 bp of cytochrome b (cytb) and 945 bp of cytochrome oxidase subunit 1 (cox1).

Results

Polychromophilus melanipherus DNA was detected at six out of nine sampling locations and in all three examined bat fly species collected from M. schreibersii (Nycteribia schmidlii, n = 21; Penicillidia conspicua, n = 8; Penicillidia dufourii, n = 3). Four and five haplotypes were found for cytb and cox1, respectively. Evidence for multiple Polychromophilus haplotypes was found in 15 individual flies. These results point to a high diversity of P. melanipherus parasites in Miniopterus hosts and efficient transmission throughout the study area. A single Phthiridium biarticulatum bat fly collected from R. ferrumequinum screened positive for P. melanipherus, but only yielded a partial cox1 sequence fragment. Nevertheless, this result suggests that secondary hosts (both bat and fly species) are regularly confronted with this parasite.

Conclusions

The results of this study provide new insights into the prevalence and distribution of Polychromophilus parasites in European bats and their nycteribiid vectors. The use of bat flies for the non-invasive investigation of Polychromophilus infections in bat populations has proven to be efficient and thus represents an alternative for large-scale studies of infections in bat populations without the need to invasively collect blood from bats.
PB  - Springer Nature
T2  - Parasites & Vectors
T1  - Non-invasive investigation of Polychromophilus parasite infections in bat populations in Serbia using bat flies
IS  - 16
DO  - 10.1186/s13071-023-05786-1
SP  - 170
ER  - 
@article{
author = "Bajić, Branka and Werb, Oskar and Budinski, Ivana and Blagojević, Jelena and Schaer, Juliane and van Schaik, Jaap",
year = "2023",
abstract = "Background

Haemosporidian parasites of the genus Polychromophilus infect bats worldwide. They are vectored by obligate ectoparasitic bat flies of the family Nycteribiidae. Despite their global distribution, only five Polychromophilus morphospecies have been described to date. The two predominant species, Polychromophilus melanipherus and Polychromophilus murinus, are broadly distributed and mainly infect miniopterid and vespertilionid bats, respectively. In areas where species from different bat families aggregate together, the infection dynamics and ability of either Polychromophilus species to infect other host families is poorly characterized.

Methods

We collected 215 bat flies from two bat species, Miniopterus schreibersii and Rhinolophus ferrumequinum, which sometimes form mixed clusters in Serbia. Miniopterus schreibersii is known to be frequently infected with P. melanipherus, whereas R. ferrumequinum has been observed to be incidentally infected with both Polychromophilus species. All flies were screened for Polychromophilus infections using a PCR targeting the haemosporidian cytb gene. Positive samples were subsequently sequenced for 579 bp of cytochrome b (cytb) and 945 bp of cytochrome oxidase subunit 1 (cox1).

Results

Polychromophilus melanipherus DNA was detected at six out of nine sampling locations and in all three examined bat fly species collected from M. schreibersii (Nycteribia schmidlii, n = 21; Penicillidia conspicua, n = 8; Penicillidia dufourii, n = 3). Four and five haplotypes were found for cytb and cox1, respectively. Evidence for multiple Polychromophilus haplotypes was found in 15 individual flies. These results point to a high diversity of P. melanipherus parasites in Miniopterus hosts and efficient transmission throughout the study area. A single Phthiridium biarticulatum bat fly collected from R. ferrumequinum screened positive for P. melanipherus, but only yielded a partial cox1 sequence fragment. Nevertheless, this result suggests that secondary hosts (both bat and fly species) are regularly confronted with this parasite.

Conclusions

The results of this study provide new insights into the prevalence and distribution of Polychromophilus parasites in European bats and their nycteribiid vectors. The use of bat flies for the non-invasive investigation of Polychromophilus infections in bat populations has proven to be efficient and thus represents an alternative for large-scale studies of infections in bat populations without the need to invasively collect blood from bats.",
publisher = "Springer Nature",
journal = "Parasites & Vectors",
title = "Non-invasive investigation of Polychromophilus parasite infections in bat populations in Serbia using bat flies",
number = "16",
doi = "10.1186/s13071-023-05786-1",
pages = "170"
}
Bajić, B., Werb, O., Budinski, I., Blagojević, J., Schaer, J.,& van Schaik, J.. (2023). Non-invasive investigation of Polychromophilus parasite infections in bat populations in Serbia using bat flies. in Parasites & Vectors
Springer Nature.(16), 170.
https://doi.org/10.1186/s13071-023-05786-1
Bajić B, Werb O, Budinski I, Blagojević J, Schaer J, van Schaik J. Non-invasive investigation of Polychromophilus parasite infections in bat populations in Serbia using bat flies. in Parasites & Vectors. 2023;(16):170.
doi:10.1186/s13071-023-05786-1 .
Bajić, Branka, Werb, Oskar, Budinski, Ivana, Blagojević, Jelena, Schaer, Juliane, van Schaik, Jaap, "Non-invasive investigation of Polychromophilus parasite infections in bat populations in Serbia using bat flies" in Parasites & Vectors, no. 16 (2023):170,
https://doi.org/10.1186/s13071-023-05786-1 . .
7

Molecular investigation of Polychromophilus parasites –data from infections in bat flies of Miniopterus bats in Serbia and in Scotophilus bats in Thailand

Werb, Oskar; Bajić, Branka; van Schaik, Jaap; Chumnandee, Chatree; Pha-obnga, Nawarat; Schaer, Juliane

(Bielefeld: Deutsche Forschungsgemeinschaft, 2022)

TY  - CONF
AU  - Werb, Oskar
AU  - Bajić, Branka
AU  - van Schaik, Jaap
AU  - Chumnandee, Chatree
AU  - Pha-obnga, Nawarat
AU  - Schaer, Juliane
PY  - 2022
UR  - http://radar.ibiss.bg.ac.rs/handle/123456789/6688
AB  - Polychromophilus parasites infect bats in temperate as well as in tropical regions and are
phylogenetically close related to Plasmodium species of ungulates. The haemosporidian
parasites are vectored by ectoparasitic bat flies (Nycteribiidae) and five to seven
Polychromophilus morphospecies have been described to date.
Here we present data of Polychromophilus parasites of both temperate and tropical bat
species. Polychromophilus parasites in Palearctic (Serbian) bat flies and in blood samples
from bats in Thailand were investigated. Mitochondrial, apicoplast and nuclear genes
were analyzed for molecular characterization of the parasites.
The study provides the first information of Polychromophilus parasites in the lesser Asiatic
yellow bat (Scotophilus kuhlii) in Thailand, a common vespertilionid bat species distributed
in South and Southeast Asia. The gametocyte blood stages of the parasites could not be
assigned to a described morphospecies and the molecular analysis revealed that these
parasites might represent a distinct Polychromophilus species.
Further, Polychromophilus melanipherus infections were detected in different nycteribiid
bat fly genera collected from 216 bat individuals of the bat species Miniopterus
schreibersii and Rhinolophus ferrumequinum in Serbia. A high prevalence of P.
melanipherus infections was recorded in the bat fly association Penicillidia/Miniopterus
(60%) and lower prevalences in Nycteribia/Miniopterus (15%) and
Phthiridium/Rhinolophus (1.5%). The nucleotide sequence comparisons of these parasites
revealed evidence of mixed infections with different P. melanipherus haplotypes.
Infections were detected in 7/9 sampling locations which points to a high transmission of
infections across Miniopterus bats and the bat flies in this region of Serbia.
The results of this study provide new insights into the distribution and phylogenetic
relationships of Polychromophilus parasites in bats and their nycteribiid vectors. The use
of bat flies to non-invasively investigate Polychromophilus infections in bat populations
has proven to be very efficient.
PB  - Bielefeld: Deutsche Forschungsgemeinschaft
C3  - Fifth International Conference on Malaria and Related Haemosporidian Parasites of Wildlife; 2022 Sep 5-8; Bielefeld, Germany
T1  - Molecular investigation of Polychromophilus parasites –data from infections in bat flies of Miniopterus bats in Serbia and in Scotophilus bats in Thailand
SP  - 82
UR  - https://hdl.handle.net/21.15107/rcub_ibiss_6688
ER  - 
@conference{
author = "Werb, Oskar and Bajić, Branka and van Schaik, Jaap and Chumnandee, Chatree and Pha-obnga, Nawarat and Schaer, Juliane",
year = "2022",
abstract = "Polychromophilus parasites infect bats in temperate as well as in tropical regions and are
phylogenetically close related to Plasmodium species of ungulates. The haemosporidian
parasites are vectored by ectoparasitic bat flies (Nycteribiidae) and five to seven
Polychromophilus morphospecies have been described to date.
Here we present data of Polychromophilus parasites of both temperate and tropical bat
species. Polychromophilus parasites in Palearctic (Serbian) bat flies and in blood samples
from bats in Thailand were investigated. Mitochondrial, apicoplast and nuclear genes
were analyzed for molecular characterization of the parasites.
The study provides the first information of Polychromophilus parasites in the lesser Asiatic
yellow bat (Scotophilus kuhlii) in Thailand, a common vespertilionid bat species distributed
in South and Southeast Asia. The gametocyte blood stages of the parasites could not be
assigned to a described morphospecies and the molecular analysis revealed that these
parasites might represent a distinct Polychromophilus species.
Further, Polychromophilus melanipherus infections were detected in different nycteribiid
bat fly genera collected from 216 bat individuals of the bat species Miniopterus
schreibersii and Rhinolophus ferrumequinum in Serbia. A high prevalence of P.
melanipherus infections was recorded in the bat fly association Penicillidia/Miniopterus
(60%) and lower prevalences in Nycteribia/Miniopterus (15%) and
Phthiridium/Rhinolophus (1.5%). The nucleotide sequence comparisons of these parasites
revealed evidence of mixed infections with different P. melanipherus haplotypes.
Infections were detected in 7/9 sampling locations which points to a high transmission of
infections across Miniopterus bats and the bat flies in this region of Serbia.
The results of this study provide new insights into the distribution and phylogenetic
relationships of Polychromophilus parasites in bats and their nycteribiid vectors. The use
of bat flies to non-invasively investigate Polychromophilus infections in bat populations
has proven to be very efficient.",
publisher = "Bielefeld: Deutsche Forschungsgemeinschaft",
journal = "Fifth International Conference on Malaria and Related Haemosporidian Parasites of Wildlife; 2022 Sep 5-8; Bielefeld, Germany",
title = "Molecular investigation of Polychromophilus parasites –data from infections in bat flies of Miniopterus bats in Serbia and in Scotophilus bats in Thailand",
pages = "82",
url = "https://hdl.handle.net/21.15107/rcub_ibiss_6688"
}
Werb, O., Bajić, B., van Schaik, J., Chumnandee, C., Pha-obnga, N.,& Schaer, J.. (2022). Molecular investigation of Polychromophilus parasites –data from infections in bat flies of Miniopterus bats in Serbia and in Scotophilus bats in Thailand. in Fifth International Conference on Malaria and Related Haemosporidian Parasites of Wildlife; 2022 Sep 5-8; Bielefeld, Germany
Bielefeld: Deutsche Forschungsgemeinschaft., 82.
https://hdl.handle.net/21.15107/rcub_ibiss_6688
Werb O, Bajić B, van Schaik J, Chumnandee C, Pha-obnga N, Schaer J. Molecular investigation of Polychromophilus parasites –data from infections in bat flies of Miniopterus bats in Serbia and in Scotophilus bats in Thailand. in Fifth International Conference on Malaria and Related Haemosporidian Parasites of Wildlife; 2022 Sep 5-8; Bielefeld, Germany. 2022;:82.
https://hdl.handle.net/21.15107/rcub_ibiss_6688 .
Werb, Oskar, Bajić, Branka, van Schaik, Jaap, Chumnandee, Chatree, Pha-obnga, Nawarat, Schaer, Juliane, "Molecular investigation of Polychromophilus parasites –data from infections in bat flies of Miniopterus bats in Serbia and in Scotophilus bats in Thailand" in Fifth International Conference on Malaria and Related Haemosporidian Parasites of Wildlife; 2022 Sep 5-8; Bielefeld, Germany (2022):82,
https://hdl.handle.net/21.15107/rcub_ibiss_6688 .

Sharing roosts but not ectoparasites: high host-specificity in bat flies and wing mites of Miniopterus schreibersii and Rhinolophus ferrumequinum (Mammalia: Chiroptera)

Bajić, Branka; Budinski, Ivana; van Schaik, Jaap; Blagojević, Jelena

(Oxford University Press, 2021)

TY  - JOUR
AU  - Bajić, Branka
AU  - Budinski, Ivana
AU  - van Schaik, Jaap
AU  - Blagojević, Jelena
PY  - 2021
UR  - http://radar.ibiss.bg.ac.rs/handle/123456789/4684
AB  - Schreiber’s bent-winged bat Miniopterus schreibersii and the greater horseshoe bat Rhinolophus ferrumequinum are widespread and common cavernicolous species across southern Europe that host numerous specialized ectoparasite species. The objective of this study was to characterize the species assemblage, genetic diversity, and host specificity of bat flies (Nycteribiidae, Diptera) and wing mites (Spinturnicidae, Acari) found on these bat hosts in Serbia and Bosnia and Herzegovina. Notably, while bat flies lay puparia on the cave walls and can thus be transmitted indirectly, wing mites require direct body contact for transmission. Morphological identification and sequencing of a 710-bp fragment of cytochrome oxidase I gene of 207 bat flies yielded 4 species, 3 on M. schreibersii and 1 on R. ferrumequinum. Sequencing of a 460-bp small subunit ribosomal RNA fragment, in all 190 collected wing mites revealed 2 species, 1 per host. In no case was a parasite associated with 1 host found on the other host. Species and genetic diversity of flies were higher in M. schreibersii, likely reflecting their host’s larger colony sizes and migratory potential. Mite species of both hosts showed similarly low diversity, likely due to their faster life history and lower winter survival.
Our findings highlight a remarkably high host-specificity and segregation of ectoparasite species despite direct contact among their hosts in the roost, suggesting a defined host preference in the investigated ectoparasite species. Furthermore, the differences in ectoparasite genetic diversity exemplify the interplay between host and parasite life histories in shaping parasite population genetic structure.
PB  - Oxford University Press
T2  - Current Zoology
T1  - Sharing roosts but not ectoparasites: high host-specificity in bat flies and wing mites of Miniopterus schreibersii and Rhinolophus ferrumequinum (Mammalia: Chiroptera)
DO  - 10.1093/cz/zoab086
ER  - 
@article{
author = "Bajić, Branka and Budinski, Ivana and van Schaik, Jaap and Blagojević, Jelena",
year = "2021",
abstract = "Schreiber’s bent-winged bat Miniopterus schreibersii and the greater horseshoe bat Rhinolophus ferrumequinum are widespread and common cavernicolous species across southern Europe that host numerous specialized ectoparasite species. The objective of this study was to characterize the species assemblage, genetic diversity, and host specificity of bat flies (Nycteribiidae, Diptera) and wing mites (Spinturnicidae, Acari) found on these bat hosts in Serbia and Bosnia and Herzegovina. Notably, while bat flies lay puparia on the cave walls and can thus be transmitted indirectly, wing mites require direct body contact for transmission. Morphological identification and sequencing of a 710-bp fragment of cytochrome oxidase I gene of 207 bat flies yielded 4 species, 3 on M. schreibersii and 1 on R. ferrumequinum. Sequencing of a 460-bp small subunit ribosomal RNA fragment, in all 190 collected wing mites revealed 2 species, 1 per host. In no case was a parasite associated with 1 host found on the other host. Species and genetic diversity of flies were higher in M. schreibersii, likely reflecting their host’s larger colony sizes and migratory potential. Mite species of both hosts showed similarly low diversity, likely due to their faster life history and lower winter survival.
Our findings highlight a remarkably high host-specificity and segregation of ectoparasite species despite direct contact among their hosts in the roost, suggesting a defined host preference in the investigated ectoparasite species. Furthermore, the differences in ectoparasite genetic diversity exemplify the interplay between host and parasite life histories in shaping parasite population genetic structure.",
publisher = "Oxford University Press",
journal = "Current Zoology",
title = "Sharing roosts but not ectoparasites: high host-specificity in bat flies and wing mites of Miniopterus schreibersii and Rhinolophus ferrumequinum (Mammalia: Chiroptera)",
doi = "10.1093/cz/zoab086"
}
Bajić, B., Budinski, I., van Schaik, J.,& Blagojević, J.. (2021). Sharing roosts but not ectoparasites: high host-specificity in bat flies and wing mites of Miniopterus schreibersii and Rhinolophus ferrumequinum (Mammalia: Chiroptera). in Current Zoology
Oxford University Press..
https://doi.org/10.1093/cz/zoab086
Bajić B, Budinski I, van Schaik J, Blagojević J. Sharing roosts but not ectoparasites: high host-specificity in bat flies and wing mites of Miniopterus schreibersii and Rhinolophus ferrumequinum (Mammalia: Chiroptera). in Current Zoology. 2021;.
doi:10.1093/cz/zoab086 .
Bajić, Branka, Budinski, Ivana, van Schaik, Jaap, Blagojević, Jelena, "Sharing roosts but not ectoparasites: high host-specificity in bat flies and wing mites of Miniopterus schreibersii and Rhinolophus ferrumequinum (Mammalia: Chiroptera)" in Current Zoology (2021),
https://doi.org/10.1093/cz/zoab086 . .
4
3

Genetic diversity of bat-flies and mites in two cave-dwelling bat species in Serbia

Vasiljević, Branka; Patenković, Aleksandra; Nikolić, Nađa; Bajić, Branka; van Schaik, Jaap; Budinski, Ivana; Blagojević, Jelena

(Belgrade: Serbian Genetic Society, 2019)

TY  - CONF
AU  - Bajić, Branka
AU  - van Schaik, Jaap
AU  - Budinski, Ivana
AU  - Blagojević, Jelena
PY  - 2019
UR  - https://radar.ibiss.bg.ac.rs/handle/123456789/4268
AB  - Bats (Chiroptera) can differ widely in their social organisaton, from living in small groups
to large colonies countng several thousands of individuals. Such ecological differences
can lead to drastc discrepancies in the populaton dynamics of parasites they carry.
European bat species are infected by a wide range of specialized ectoparasites. Bat flies
(Diptera: Hippoboscoidea – fam. Nycteribiidae) and wing-mites (Acari: Mesostgmata - fam.
Spinturnicidae) differ strongly in their phenology and life-histories. The objectve of this study
was to characterize the species assemblage, genetc diversity and host specifcity of bat flies
and mites collected from two cavernicolous bat species commonly found in Serbia, which
have different migraton potentals, and can be found both separate and in shared roosts.
A total of 219 flies and 205 mite specimens were collected from the common bentwing
bat (Miniopterus schreibersii) and greater horseshoe bat (Rhinolophus ferrumequinum) at
eight localites in Serbia and one in Bosnia and Herzegovina. Flies were morphologically
identfed and all samples were sequenced for a single mitochondrial gene (16S in mites
and COI in flies), allowing for a comparison of within and between-colony genetc diversity
among the dominant ectoparasite species in the sample (Nycteribia schmidlii, Phthiridium
biartculatum, Spinturnix psi and Eyndhovenia euryalis). Notably, all ectoparasite species
showed marked specifcity towards their primary hosts, even in roosts that were shared
by both bat host-species. Additonally, this data consttutes some of the frst reference
sequences for commonly used barcoding sequence fragments for several of the investgated
species.
PB  - Belgrade: Serbian Genetic Society
C3  - 6th Congress of the Serbian genetic society; 2019 Oct 13-17; Vrnjačka Banja, Serbia
T1  - Genetic diversity of bat-flies and mites in two cave-dwelling bat species in Serbia
SP  - 175
UR  - https://hdl.handle.net/21.15107/rcub_ibiss_4268
ER  - 
@conference{
editor = "Vasiljević, Branka, Patenković, Aleksandra, Nikolić, Nađa",
author = "Bajić, Branka and van Schaik, Jaap and Budinski, Ivana and Blagojević, Jelena",
year = "2019",
abstract = "Bats (Chiroptera) can differ widely in their social organisaton, from living in small groups
to large colonies countng several thousands of individuals. Such ecological differences
can lead to drastc discrepancies in the populaton dynamics of parasites they carry.
European bat species are infected by a wide range of specialized ectoparasites. Bat flies
(Diptera: Hippoboscoidea – fam. Nycteribiidae) and wing-mites (Acari: Mesostgmata - fam.
Spinturnicidae) differ strongly in their phenology and life-histories. The objectve of this study
was to characterize the species assemblage, genetc diversity and host specifcity of bat flies
and mites collected from two cavernicolous bat species commonly found in Serbia, which
have different migraton potentals, and can be found both separate and in shared roosts.
A total of 219 flies and 205 mite specimens were collected from the common bentwing
bat (Miniopterus schreibersii) and greater horseshoe bat (Rhinolophus ferrumequinum) at
eight localites in Serbia and one in Bosnia and Herzegovina. Flies were morphologically
identfed and all samples were sequenced for a single mitochondrial gene (16S in mites
and COI in flies), allowing for a comparison of within and between-colony genetc diversity
among the dominant ectoparasite species in the sample (Nycteribia schmidlii, Phthiridium
biartculatum, Spinturnix psi and Eyndhovenia euryalis). Notably, all ectoparasite species
showed marked specifcity towards their primary hosts, even in roosts that were shared
by both bat host-species. Additonally, this data consttutes some of the frst reference
sequences for commonly used barcoding sequence fragments for several of the investgated
species.",
publisher = "Belgrade: Serbian Genetic Society",
journal = "6th Congress of the Serbian genetic society; 2019 Oct 13-17; Vrnjačka Banja, Serbia",
title = "Genetic diversity of bat-flies and mites in two cave-dwelling bat species in Serbia",
pages = "175",
url = "https://hdl.handle.net/21.15107/rcub_ibiss_4268"
}
Vasiljević, B., Patenković, A., Nikolić, N., Bajić, B., van Schaik, J., Budinski, I.,& Blagojević, J.. (2019). Genetic diversity of bat-flies and mites in two cave-dwelling bat species in Serbia. in 6th Congress of the Serbian genetic society; 2019 Oct 13-17; Vrnjačka Banja, Serbia
Belgrade: Serbian Genetic Society., 175.
https://hdl.handle.net/21.15107/rcub_ibiss_4268
Vasiljević B, Patenković A, Nikolić N, Bajić B, van Schaik J, Budinski I, Blagojević J. Genetic diversity of bat-flies and mites in two cave-dwelling bat species in Serbia. in 6th Congress of the Serbian genetic society; 2019 Oct 13-17; Vrnjačka Banja, Serbia. 2019;:175.
https://hdl.handle.net/21.15107/rcub_ibiss_4268 .
Vasiljević, Branka, Patenković, Aleksandra, Nikolić, Nađa, Bajić, Branka, van Schaik, Jaap, Budinski, Ivana, Blagojević, Jelena, "Genetic diversity of bat-flies and mites in two cave-dwelling bat species in Serbia" in 6th Congress of the Serbian genetic society; 2019 Oct 13-17; Vrnjačka Banja, Serbia (2019):175,
https://hdl.handle.net/21.15107/rcub_ibiss_4268 .