Density and behavior of capybara (Hydrochoerus hydrochaeris) ticks (Acari: Ixodidae) Amblyomma sculptum and Amblyomma dubitatum with notes on Rickettsia bellii infection: Assessing human exposure risk

IF 3.1 2区 医学 Q2 INFECTIOUS DISEASES
Matias P.J. Szabó , Caroline Lopes Queiroz , Adriane Suzin , Vinicius da Silva Rodrigues , Raíssa Brauner Kamla Vieira , Maria Marlene Martins , Lais Miguel Rezende , Ana Carolina P. Sousa , Vanessa do Nascimento Ramos , Fernanda Marinho Muraro , Lais Keocheguerian Fernandes , Lorena C.M. Santos , Rodrigo da Costa Maia , Amanda Ferreira Rezende
{"title":"Density and behavior of capybara (Hydrochoerus hydrochaeris) ticks (Acari: Ixodidae) Amblyomma sculptum and Amblyomma dubitatum with notes on Rickettsia bellii infection: Assessing human exposure risk","authors":"Matias P.J. Szabó ,&nbsp;Caroline Lopes Queiroz ,&nbsp;Adriane Suzin ,&nbsp;Vinicius da Silva Rodrigues ,&nbsp;Raíssa Brauner Kamla Vieira ,&nbsp;Maria Marlene Martins ,&nbsp;Lais Miguel Rezende ,&nbsp;Ana Carolina P. Sousa ,&nbsp;Vanessa do Nascimento Ramos ,&nbsp;Fernanda Marinho Muraro ,&nbsp;Lais Keocheguerian Fernandes ,&nbsp;Lorena C.M. Santos ,&nbsp;Rodrigo da Costa Maia ,&nbsp;Amanda Ferreira Rezende","doi":"10.1016/j.ttbdis.2024.102330","DOIUrl":null,"url":null,"abstract":"<div><p>In several urban and peri‑urban areas of Brazil, populations of <em>Amblyomma sculptum</em> and <em>Amblyomma dubitatum</em> ticks are maintained by capybaras (<em>Hydrochoerus hydrochaeris</em>). In some of these areas, this host and these tick species are associated with Brazilian spotted fever (BSF), a lethal human disease caused by the bacterium <em>Rickettsia rickettsii</em>. In this work, we evaluated the risk of human exposure to these tick species using four collection techniques to discern host-seeking behavior. The study was carried out in 10 urban sites inhabited by capybaras in Uberlândia, a BSF-free municipality in southeastern Brazil. Ticks were collected in areas of 400 m<sup>2</sup> at each site and at three seasons. Within the same municipality, the distance and speed of <em>A. sculptum</em> nymphs moving towards the CO<sub>2</sub> traps were evaluated. In a sample of ticks <em>Rickettsia</em> DNA was investigated. During the study period, 52,953 ticks were collected. Among these, 83.4 % were <em>A. sculptum</em> (1,523 adults, 10,545 nymphs and 32,104 larvae) and 16.6 % were <em>A. dubitatum</em> (464 adults, 2,153 nymphs and 6,164 larvae). An average annual questing tick density of 4.4/m² was observed, with the highest density recorded at one site in autumn (31.8/m²) and the lowest in summer at another site (0.03/m²). The visual search yielded the highest proportion of <em>A. sculptum</em> larvae, constituting 47 % of the total and 63.6 % of all <em>A. sculptum</em> larvae. In contrast, CO<sub>2</sub> traps collected a greater proportion of nymphs and adults of <em>A. sculptum</em> ticks. In the case of <em>A. dubitatum</em>, the CO<sub>2</sub> trap was the most efficient technique with 57.7 % of captures of this species, especially of nymphs (94.5 % of captures) and adults (97.8 % of captures). Ticks' ambush height on vegetation (9 to 77 cm), observed by visual search 30 times, yielded a total of 20,771 ticks. Of these, 28 (93 %) were <em>A. sculptum</em> ticks, with only two (7 %) identified as <em>A. dubitatum</em> ticks. Among <em>A. sculptum</em> ticks, the nymph was the most attracted stage to humans and larva in the case of <em>A. dubitatum. Amblyomma sculptum</em> adults and nymphs were significantly more attracted to humans than those of <em>A. dubitatum,</em> but <em>A. dubitatum</em> larvae were significantly more attracted than the same stage of <em>A. sculptum</em>. The maximum distance and speed of horizontal displacement for <em>A. sculptum</em> nymphs were five meters and 2.0 m/h, respectively. The only species of <em>Rickettsia</em> detected in ticks, exclusively in <em>A. dubitatum,</em> was <em>R. bellii</em>. Importantly, it was observed that the higher the proportion of <em>A. sculptum</em> in the community of ticks, the lower the rate of infection of <em>A. dubitatum</em> by <em>R. bellii</em>. In conclusion, host-seeking behavior differed between the two tick species, as well as between stages of the same species. A greater restriction of <em>A. dubitatum</em> ticks to the soil was observed, while larvae and nymphs of <em>A. sculptum</em> dispersed higher in the vegetation. The behavior presented by <em>A. sculptum</em> provides greater opportunities for contact with the hosts, while <em>A. dubitatum</em> depends more on an active search for a host, the hunter behavior. Taken together, these observations show that a human being crossing an area infested with <em>A. sculptum</em> and <em>A. dubitatum</em> ticks will have almost exclusive contact with <em>A. sculptum</em> larvae and/or nymphs. Humans in a stationary position (sitting, lying or immobile) are exposed to both tick species, but they are more attractive to adults and mainly nymphs of <em>A. sculptum</em> compared to the corresponding stages of the tick <em>A. dubitatum</em>. The negative effect of <em>A. sculptum</em> on <em>A. dubitatum</em> infection by <em>R. bellii</em> deserves further studies.</p></div>","PeriodicalId":49320,"journal":{"name":"Ticks and Tick-borne Diseases","volume":"15 3","pages":"Article 102330"},"PeriodicalIF":3.1000,"publicationDate":"2024-03-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.sciencedirect.com/science/article/pii/S1877959X24000232/pdfft?md5=0a3c0c205f4bef6c950aedc17eb4710f&pid=1-s2.0-S1877959X24000232-main.pdf","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Ticks and Tick-borne Diseases","FirstCategoryId":"3","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S1877959X24000232","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"INFECTIOUS DISEASES","Score":null,"Total":0}
引用次数: 0

Abstract

In several urban and peri‑urban areas of Brazil, populations of Amblyomma sculptum and Amblyomma dubitatum ticks are maintained by capybaras (Hydrochoerus hydrochaeris). In some of these areas, this host and these tick species are associated with Brazilian spotted fever (BSF), a lethal human disease caused by the bacterium Rickettsia rickettsii. In this work, we evaluated the risk of human exposure to these tick species using four collection techniques to discern host-seeking behavior. The study was carried out in 10 urban sites inhabited by capybaras in Uberlândia, a BSF-free municipality in southeastern Brazil. Ticks were collected in areas of 400 m2 at each site and at three seasons. Within the same municipality, the distance and speed of A. sculptum nymphs moving towards the CO2 traps were evaluated. In a sample of ticks Rickettsia DNA was investigated. During the study period, 52,953 ticks were collected. Among these, 83.4 % were A. sculptum (1,523 adults, 10,545 nymphs and 32,104 larvae) and 16.6 % were A. dubitatum (464 adults, 2,153 nymphs and 6,164 larvae). An average annual questing tick density of 4.4/m² was observed, with the highest density recorded at one site in autumn (31.8/m²) and the lowest in summer at another site (0.03/m²). The visual search yielded the highest proportion of A. sculptum larvae, constituting 47 % of the total and 63.6 % of all A. sculptum larvae. In contrast, CO2 traps collected a greater proportion of nymphs and adults of A. sculptum ticks. In the case of A. dubitatum, the CO2 trap was the most efficient technique with 57.7 % of captures of this species, especially of nymphs (94.5 % of captures) and adults (97.8 % of captures). Ticks' ambush height on vegetation (9 to 77 cm), observed by visual search 30 times, yielded a total of 20,771 ticks. Of these, 28 (93 %) were A. sculptum ticks, with only two (7 %) identified as A. dubitatum ticks. Among A. sculptum ticks, the nymph was the most attracted stage to humans and larva in the case of A. dubitatum. Amblyomma sculptum adults and nymphs were significantly more attracted to humans than those of A. dubitatum, but A. dubitatum larvae were significantly more attracted than the same stage of A. sculptum. The maximum distance and speed of horizontal displacement for A. sculptum nymphs were five meters and 2.0 m/h, respectively. The only species of Rickettsia detected in ticks, exclusively in A. dubitatum, was R. bellii. Importantly, it was observed that the higher the proportion of A. sculptum in the community of ticks, the lower the rate of infection of A. dubitatum by R. bellii. In conclusion, host-seeking behavior differed between the two tick species, as well as between stages of the same species. A greater restriction of A. dubitatum ticks to the soil was observed, while larvae and nymphs of A. sculptum dispersed higher in the vegetation. The behavior presented by A. sculptum provides greater opportunities for contact with the hosts, while A. dubitatum depends more on an active search for a host, the hunter behavior. Taken together, these observations show that a human being crossing an area infested with A. sculptum and A. dubitatum ticks will have almost exclusive contact with A. sculptum larvae and/or nymphs. Humans in a stationary position (sitting, lying or immobile) are exposed to both tick species, but they are more attractive to adults and mainly nymphs of A. sculptum compared to the corresponding stages of the tick A. dubitatum. The negative effect of A. sculptum on A. dubitatum infection by R. bellii deserves further studies.

水豚(Hydrochoerus hydrochaeris)蜱(Acari: Ixodidae)Amblyomma sculptum 和 Amblyomma dubitatum 的密度和行为,以及有关 Rickettsia bellii 感染的说明:评估人类接触风险
在巴西的一些城市和城郊地区,水豚(Hydrochoerus hydrochaeris)维持着Amblyomma sculptum和Amblyomma dubitatum蜱的种群。在其中一些地区,这种宿主和这些蜱类与巴西斑疹热(BSF)有关,这是一种由立克次体细菌引起的致命性人类疾病。在这项工作中,我们使用四种采集技术来评估人类接触这些蜱虫物种的风险,以辨别寻找宿主的行为。研究在巴西东南部无 BSF 的乌贝兰迪亚市的 10 个水豚栖息的城市地点进行。在三个季节中,在每个地点 400 平方米的区域内采集了蜱虫。在同一城市中,还评估了雕蜱若虫向二氧化碳诱捕器移动的距离和速度。对蜱虫样本中的立克次体 DNA 进行了调查。在研究期间,共收集到 52 953 只蜱虫。其中 83.4% 为雕蜱(1,523 只成虫、10,545 只若虫和 32,104 只幼虫),16.6% 为蜱螨(464 只成虫、2,153 只若虫和 6,164 只幼虫)。观察到的蜱虫年平均密度为 4.4/m²,其中一个地点秋季的密度最高(31.8/m²),另一个地点夏季的密度最低(0.03/m²)。肉眼观察到的雕尾蚜幼虫比例最高,占总数的 47%,占所有雕尾蚜幼虫的 63.6%。相比之下,二氧化碳诱捕器收集到的雕蜱若虫和成虫比例更高。对于 A. dubitatum,二氧化碳诱捕器是最有效的技术,捕获了该种蜱虫的 57.7%,尤其是若虫(捕获率 94.5%)和成蜱(捕获率 97.8%)。通过目测观察蜱在植被上的埋伏高度(9 至 77 厘米)30 次,共发现 20 771 只蜱。其中有 28 只(93%)是 A. sculptum蜱,只有 2 只(7%)被鉴定为 A. dubitatum蜱。在A. sculptum蜱中,若虫是最吸引人类的阶段,而A. dubitatum则是幼虫。Amblyomma sculptum成虫和若虫对人类的吸引力明显高于A. dubitatum成虫和若虫,但A. dubitatum幼虫对人类的吸引力明显高于同一阶段的A. sculptum幼虫。A.sculptum若虫的最大水平位移距离和速度分别为5米和2.0米/小时。在蜱虫体内检测到的唯一立克次氏体是贝氏立克次氏体(R. bellii),而且仅在 A. dubitatum 身上检测到。重要的是,据观察,蜱群中 A. sculptum 的比例越高,R. bellii 对 A. dubitatum 的感染率就越低。总之,两种蜱之间以及同一物种不同阶段的蜱寻找宿主的行为是不同的。据观察,A. dubitatum蜱更多地局限于土壤中,而A. sculptum的幼虫和若虫则更多地分散在植被中。雕蜱的行为提供了更多与宿主接触的机会,而杜比他蜱则更依赖于主动寻找宿主,即猎人行为。综上所述,这些观察结果表明,人类在穿越有 A. sculptum 和 A. dubitatum 虱子出没的地区时,几乎只能接触到 A. sculptum 幼虫和/或若虫。处于静止状态(坐着、躺着或不动)的人类会接触到这两种蜱虫,但与蜱虫 A. dubitatum 的相应阶段相比,他们对 A. sculptum 的成虫和主要是若虫更有吸引力。A. sculptum 对 R. bellii 感染 A. dubitatum 的负面影响值得进一步研究。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 求助全文
来源期刊
Ticks and Tick-borne Diseases
Ticks and Tick-borne Diseases INFECTIOUS DISEASES-MICROBIOLOGY
CiteScore
6.90
自引率
12.50%
发文量
185
审稿时长
6-12 weeks
期刊介绍: Ticks and Tick-borne Diseases is an international, peer-reviewed scientific journal. It publishes original research papers, short communications, state-of-the-art mini-reviews, letters to the editor, clinical-case studies, announcements of pertinent international meetings, and editorials. The journal covers a broad spectrum and brings together various disciplines, for example, zoology, microbiology, molecular biology, genetics, mathematical modelling, veterinary and human medicine. Multidisciplinary approaches and the use of conventional and novel methods/methodologies (in the field and in the laboratory) are crucial for deeper understanding of the natural processes and human behaviour/activities that result in human or animal diseases and in economic effects of ticks and tick-borne pathogens. Such understanding is essential for management of tick populations and tick-borne diseases in an effective and environmentally acceptable manner.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术官方微信