Seasonal Dynamics of Phlebotomine Sand Fly Species Proven Vectors of Mediterranean Leishmaniasis Caused by Leishmania infantum

BackgroundThe recent geographical expansion of phlebotomine vectors of Leishmania infantum in the Mediterranean subregion has been attributed to ongoing climate changes. At these latitudes, the activity of sand flies is typically seasonal; because seasonal phenomena are also sensitive to general variations in climate, current phenological data sets can provide a baseline for continuing investigations on sand fly population dynamics that may impact on future scenarios of leishmaniasis transmission. With this aim, in 2011–2013 a consortium of partners from eight Mediterranean countries carried out entomological investigations in sites where L. infantum transmission was recently reported.Methods/Principal FindingsA common protocol for sand fly collection included monthly captures by CDC light traps, complemented by sticky traps in most of the sites. Collections were replicated for more than one season in order to reduce the effects of local weather events. In each site, the trapping effort was left unchanged throughout the survey to legitimate inter-seasonal comparisons. Data from 99,000 collected specimens were analyzed, resulting in the description of seasonal dynamics of 56,000 sand flies belonging to L. infantum vector species throughout a wide geographical area, namely P. perniciosus (Portugal, Spain and Italy), P. ariasi (France), P. neglectus (Greece), P. tobbi (Cyprus and Turkey), P. balcanicus and P. kandelakii (Georgia). Time of sand fly appearance/disappearance in collections differed between sites, and seasonal densities showed variations in each site. Significant correlations were found between latitude/mean annual temperature of sites and i) the first month of sand fly appearance, that ranged from early April to the first half of June; ii) the type of density trend, varying from a single peak in July/August to multiple peaks increasing in magnitude from May through September. A 3-modal trend, recorded for P. tobbi in Cyprus, represents a novel finding for a L. infantum vector. Adults ended the activity starting from mid September through November, without significant correlation with latitude/mean annual temperature of sites. The period of potential exposure to L.infantum in the Mediterranean subregion, as inferred by adult densities calculated from 3 years, 37 sites and 6 competent vector species, was associated to a regular bell-shaped density curve having a wide peak center encompassing the July-September period, and falling between early May to late October for more than 99% of values. Apparently no risk for leishmaniasis transmission took place from December through March in the years considered. We found a common pattern of nocturnal females activity, whose density peaked between 11 pm and 2 am.ConclusionsDespite annual variations, multiple collections performed over consecutive years provided homogeneous patterns of the potential behavior of leishmaniasis vectors in selected sites, which we propose may represent sentinel areas for future monitoring. In the investigated years, higher potential risk for L. infantum transmission in the Mediterranean was identified in the June-October period (97% relative vector density), however such risk was not equally distributed throughout the region, since density waves of adults occurred earlier and were more frequent in southern territories.

背景 地中海次区域内婴儿利什曼原虫（Leishmania infantum）的白蛉媒介（phlebotomine vectors）近期出现地理扩张，这一现象被归因于持续的气候变化。在该纬度带内，白蛉的活动通常具有季节性；由于季节性现象同样对气候的整体变化敏感，现有物候数据集（phenological data sets）可为后续关于白蛉种群动态的研究提供基准基线，而这些动态可能影响利什曼病传播的未来情景。基于此目标，2011至2013年间，来自8个地中海国家的合作联盟在近期有婴儿利什曼原虫传播报道的地点开展了昆虫学调查（entomological investigations）。方法/主要结果 白蛉采集采用统一方案：多数调查点使用CDC光诱捕器（CDC light traps）每月进行捕获，并辅以粘虫诱捕器（sticky traps）。为降低局地气象事件的影响，采集工作在多个季节进行重复。每个调查点的诱捕强度在整个调查期间保持一致，以保证季节间比较的合理性。研究对99000份采集标本的数据进行了分析，明确了广泛地理范围内隶属于婴儿利什曼原虫媒介物种的56000只白蛉的季节动态，涉及的媒介物种包括：菲氏白蛉（P. perniciosus，分布于葡萄牙、西班牙与意大利）、阿里亚斯白蛉（P. ariasi，分布于法国）、淡漠白蛉（P. neglectus，分布于希腊）、托氏白蛉（P. tobbi，分布于塞浦路斯与土耳其）、巴尔干白蛉（P. balcanicus）以及坎德拉基白蛉（P. kandelakii，分布于格鲁吉亚）。不同调查点的白蛉出现与消失时间存在差异，且各调查点的季节密度均存在波动。研究发现，调查点的纬度/年平均气温与以下两项指标存在显著相关性：① 白蛉首次出现的月份，范围为4月初至6月上旬；② 密度趋势类型，从7月/8月的单峰格局，到5月至9月间幅度逐渐增大的多峰格局不等。在塞浦路斯记录到的托氏白蛉三峰密度趋势，为婴儿利什曼原虫媒介物种的相关研究提供了全新发现。白蛉成虫的活动终止期为9月中旬至11月，该指标与调查点的纬度/年平均气温无显著相关性。基于3年、37个调查点以及6种有效媒介物种（competent vector species）的成虫密度数据推断，地中海次区域内婴儿利什曼原虫的潜在暴露期符合典型的钟形密度曲线：峰值中心覆盖7月至9月，99%以上的密度值集中于5月初至10月下旬。在本研究涉及的年份中，12月至次年3月无利什曼病传播风险。研究还发现了雌性白蛉夜间活动的共同模式：其密度峰值出现在23:00至次日02:00之间。结论 尽管存在年度波动，但连续多年开展的多次采集工作在选定调查点中均呈现出利什曼病媒介潜在行为的一致性模式，我们建议这些区域可作为未来监测的哨点区域（sentinel areas）。在本研究涉及的年份中，地中海区域婴儿利什曼原虫传播的潜在高风险期为6月至10月（相对媒介密度占比达97%），但该风险在区域内分布不均：南部区域的成虫密度高峰出现更早且更为频繁。