Lynn M. Osikowicz

Declines in large wildlife increase landscape-level prevalence of rodent-borne disease in Africa

Significance Understanding the effects of biodiversity loss on zoonotic disease is of pressing importance to both conservation science and public health. This paper provides experimental evidence of increased landscape-level disease risk following declines in large wildlife, using the case study of the rodent-borne zoonosis, bartonellosis, in East Africa. This pattern is driven not by changes in community composition or diversity of hosts, as frequently proposed in other systems, but by increases in abundance of susceptible hosts following large mammal declines. Given that rodent increases following large wildlife declines appear to be a widespread pattern, we suggest this relationship is likely to be general. Populations of large wildlife are declining on local and global scales. The impacts of this pulse of size-selective defaunation include cascading changes to smaller animals, particularly rodents, and alteration of many ecosystem processes and services, potentially involving changes to prevalence and transmission of zoonotic disease. Understanding linkages between biodiversity loss and zoonotic disease is important for both public health and nature conservation programs, and has been a source of much recent scientific debate. In the case of rodent-borne zoonoses, there is strong conceptual support, but limited empirical evidence, for the hypothesis that defaunation, the loss of large wildlife, increases zoonotic disease risk by directly or indirectly releasing controls on rodent density. We tested this hypothesis by experimentally excluding large wildlife from a savanna ecosystem in East Africa, and examining changes in prevalence and abundance of Bartonella spp. infection in rodents and their flea vectors. We found no effect of wildlife removal on per capita prevalence of Bartonella infection in either rodents or fleas. However, because rodent and, consequently, flea abundance doubled following experimental defaunation, the density of infected hosts and infected fleas was roughly twofold higher in sites where large wildlife was absent. Thus, defaunation represents an elevated risk in Bartonella transmission to humans (bartonellosis). Our results (i) provide experimental evidence of large wildlife defaunation increasing landscape-level disease prevalence, (ii) highlight the importance of susceptible host regulation pathways and host/vector density responses in biodiversity–disease relationships, and (iii) suggest that rodent-borne disease responses to large wildlife loss may represent an important context where this relationship is largely negative.

Prevalence and Diversity of Bartonella spp. in Bats in Peru

Bartonella infections were investigated in bats in the Amazon part of Peru. A total of 112 bats belonging to 19 species were surveyed. Bartonella bacteria were cultured from 24.1% of the bats (27/112). Infection rates ranged from 0% to 100% per bat species. Phylogenetic analyses of gltA of the Bartonella isolates revealed 21 genetic variants clustering into 13 divergent phylogroups. Some Bartonella strains were shared by bats of multiple species, and bats of some species were infected with multiple Bartonella strains, showing no evident specific Bartonella sp.-bat relationships. Rarely found in other bat species, the Bartonella strains of phylogroups I and III discovered from the common vampire bats (Desmodus rotundus) were more specific to the host bat species, suggesting some level of host specificity.

Bartonella spp. in Fruit Bats and Blood-Feeding Ectoparasites in Madagascar

We captured, ectoparasite-combed, and blood-sampled cave-roosting Madagascan fruit bats (Eidolon dupreanum) and tree-roosting Madagascan flying foxes (Pteropus rufus) in four single-species roosts within a sympatric geographic foraging range for these species in central Madagascar. We describe infection with novel Bartonella spp. in sampled Eidolon dupreanum and associated bat flies (Cyclopodia dubia), which nest close to or within major known Bartonella lineages; simultaneously, we report the absence of Bartonella spp. in Thaumapsylla sp. fleas collected from these same bats. This represents the first documented finding of Bartonella infection in these species of bat and bat fly, as well as a new geographic record for Thaumapsylla sp. We further relate the absence of both Bartonella spp. and ectoparasites in sympatrically sampled Pteropus rufus, thus suggestive of a potential role for bat flies in Bartonella spp. transmission. These findings shed light on transmission ecology of bat-borne Bartonella spp., recently demonstrated as a potentially zoonotic pathogen.

BARTONELLA ROCHALIMAE AND B. VINSONII SUBSP. BERKHOFFII IN WILD CARNIVORES FROM COLORADO, USA

Abstract Spleen samples from 292 wild carnivores from Colorado, US were screened for Bartonella infection. Bartonella DNA was detected in coyotes (Canis latrans) (28%), striped skunks (Mephitis mephitis) (23%), red foxes (Vulpes vulpes) (27%), and raccoons (Procyon lotor) (8%) but not in black bears (Ursus americanus), gray foxes (Urocyon cinereoargenteus), and mountain lions (Puma concolor). Two Bartonella species, B. vinsonii subsp. berkhoffii and B. rochalimae, were identified. All 10 infected striped skunks exclusively carried B. rochalimae while coyotes, red foxes, and raccoons could be infected with both Bartonella species. Five of seven infected coyotes carried B. v. berkhoffii whereas five of seven infected red foxes and 11 of 14 infected raccoons carried B. rochalimae. Further studies are needed to understand relationships between Bartonella species, wild carnivores, and their ectoparasites.

Molecular Survey of Bacterial Zoonotic Agents in Bats from the Country of Georgia (Caucasus).

Bats are important reservoirs for many zoonotic pathogens. However, no surveys of bacterial pathogens in bats have been performed in the Caucasus region. To understand the occurrence and distribution of bacterial infections in these mammals, 218 bats belonging to eight species collected from four regions of Georgia were examined for Bartonella, Brucella, Leptospira, and Yersinia using molecular approaches. Bartonella DNA was detected in 77 (35%) bats from all eight species and was distributed in all four regions. The prevalence ranged 6–50% per bat species. The Bartonella DNA represented 25 unique genetic variants that clustered into 21 lineages. Brucella DNA was detected in two Miniopterus schreibersii bats and in two Myotis blythii bats, all of which were from Imereti (west-central region). Leptospira DNA was detected in 25 (13%) bats that included four M. schreibersii bats and 21 M. blythii bats collected from two regions. The Leptospira sequences represented five genetic variants with one of them being closely related to the zoonotic pathogen L. interrogans (98.6% genetic identity). No Yersinia DNA was detected in the bats. Mixed infections were observed in several cases. One M. blythii bat and one M. schreibersii bat were co-infected with Bartonella, Brucella, and Leptospira; one M. blythii bat and one M. schreibersii bat were co-infected with Bartonella and Brucella; 15 M. blythii bats and three M. schreibersii bats were co-infected with Bartonella and Leptospira. Our results suggest that bats in Georgia are exposed to multiple bacterial infections. Further studies are needed to evaluate pathogenicity of these agents to bats and their zoonotic potential.

Exposure to Bat-Associated Bartonella spp. among Humans and Other Animals, Ghana

This is the author accepted manuscript. The final version is available from the Centers for Disease Control and Prevention via http://dx.doi.org/10.3201/eid2205.151908

Risk Factors for Human Lice and Bartonellosis among the Homeless, San Francisco, California, USA

Results suggest that body lice disproportionately affect certain demographic groups and those who sleep outdoors.

Prevalence, diversity, and host associations of Bartonella strains in bats from Georgia (Caucasus)

Bartonella infections were investigated in seven species of bats from four regions of the Republic of Georgia. Of the 236 bats that were captured, 212 (90%) specimens were tested for Bartonella infection. Colonies identified as Bartonella were isolated from 105 (49.5%) of 212 bats Phylogenetic analysis based on sequence variation of the gltA gene differentiated 22 unique Bartonella genogroups. Genetic distances between these diverse genogroups were at the level of those observed between different Bartonella species described previously. Twenty-one reference strains from 19 representative genogroups were characterized using four additional genetic markers. Host specificity to bat genera or families was reported for several Bartonella genogroups. Some Bartonella genotypes found in bats clustered with those identified in dogs from Thailand and humans from Poland.

Prevalence and Diversity of Bartonella Species in Rodents from Georgia (Caucasus)

Bartonella infections are widespread and highly prevalent in rodents. Several rodent-associated Bartonella species have been related to human diseases. Recently, Bartonella species was reported as the etiology of a human case in the country of Georgia (Caucasus). However, information on Bartonella in rodents in Georgia is absent. Rodent hearts were collected from Georgia to investigate the presence and diversity of Bartonella species. Bartonella bacteria were cultured from 37.2% (16/43) of rodents examined, while Bartonella DNA was detected in 41.2% (28/68) of rodents by polymerase chain reaction targeting citrate synthase (gltA) gene. Sequences of gltA showed that rodents in this region harbored multiple Bartonella strains, including Bartonella elizabethae, Bartonella tribocorum, Bartonella grahamii, and an unknown genogroup. The first three Bartonella species, known to be rat-associated and human cases linked, were commonly observed in wood mice (Apodemus [Sylvaemus] uralensis) (5/8 positive with B. elizabethae and B. tribocorum) and social voles (Microtus socialis) (4/6 positive with B. grahamii and B. elizabethae) in this study. The frequent distribution of these Bartonella species suggests that they may contribute to unidentified clinical infections. The unknown genogroup was observed in 24 Bartonella isolates and/or DNA extracts from heart tissues, all of which were obtained from Libyan jirds (Meriones libycus). Further characterization of the bacterial cultures based on sequence analysis of four additional genes (ftsZ, nuoG, rpoB, and ssrA) supported that the jird-associated Bartonella strains comprise a distinct monophyletic clade. The impact of this bacterium on wildlife and human health needs to be determined.

Bartonella species and trombiculid mites of rats from the Mekong Delta of Vietnam.

Abstract A survey of Bartonella spp. from 275 rats purchased in food markets (n=150) and trapped in different ecosystems (rice field, forest, and animal farms) (n=125) was carried out during October, 2012–March, 2013, in the Mekong Delta of Vietnam. The overall Bartonella spp. prevalence detected by culture and PCR in blood was 14.9% (10.7–19.1%), the highest corresponding to Rattus tanezumi (49.2%), followed by Rattus norvegicus (20.7%). Trapped rats were also investigated for the presence and type of chiggers (larvae of trombiculid mites), and Bartonella spp. were investigated on chigger pools collected from each rat by RT-PCR. A total of five Bartonella spp. were identified in rats, three of which (B. elizabethae, B. rattimassiliensis, and B. tribocorum) are known zoonotic pathogens. Among trapped rats, factors independently associated with increased prevalence of Bartonella spp. included: (1) Rat species (R. tanezumi); (2) the number of Trombiculini–Blankaartia and Schoengastiini–Ascoschoengastia mites found on rats; and (3) the habitat of the rat (i.e., forest/fields vs. animal farms). The prevalence of Bartonella infection among chiggers from Bartonella spp.–positive R. tanezumi rats was 5/25 (25%), compared with 1/27 (3.7%) among Bartonella spp.–negative R. tanezumi rats (relative risk [RR]=5.4, 95% confidence interval [CI] 0.68–43.09). The finding of Bartonella spp.–positive chiggers on Bartonella spp.–negative rats is strongly suggestive of a transovarial transmission cycle. Rats are ubiquitous in areas of human activity and farms in the Mekong Delta; in addition, trapping and trading of rats for food is common. To correctly assess the human risks due to rat trapping, marketing, and carcass dressing, further studies are needed to establish the routes of transmission and cycle of infection. The widespread presence of these zoonotic pathogens in rats and the abundance of human—rat interactions suggest that surveillance efforts should be enhanced to detect any human cases of Bartonella infection that may arise.