Department of Biology, Emory University, Atlanta, GA, USA.
Odum School of Ecology, University of Georgia, Athens, GA, USA.
J Anim Ecol. 2022 Apr;91(4):780-793. doi: 10.1111/1365-2656.13678. Epub 2022 Mar 7.
Insect-pathogen dynamics can show seasonal and inter-annual variations that covary with fluctuations in insect abundance and climate. Long-term analyses are especially needed to track parasite dynamics in migratory insects, in part because their vast habitat ranges and high mobility might dampen local effects of density and climate on infection prevalence. Monarch butterflies Danaus plexippus are commonly infected with the protozoan Ophryocystis elektroscirrha (OE). Because this parasite lowers monarch survival and flight performance, and because migratory monarchs have experienced declines in recent decades, it is important to understand the patterns and drivers of infection. Here we compiled data on OE infection spanning 50 years, from wild monarchs sampled in the United States, Canada and Mexico during summer breeding, fall migrating and overwintering periods. We examined eastern versus western North American monarchs separately, to ask how abundance estimates, resource availability, climate and breeding season length impact infection trends. We further assessed the intensity of migratory culling, which occurs when infected individuals are removed from the population during migration. Average infection prevalence was four times higher in western compared to eastern subpopulations. In eastern North America, the proportion of infected monarchs increased threefold since the mid-2000s. In the western region, the proportion of infected monarchs declined sharply from 2000 to 2015, and increased thereafter. For both eastern and western subpopulations, years with greater summer adult abundance predicted greater infection prevalence, indicating that transmission increases with host breeding density. Environmental variables (temperature and NDVI) were not associated with changes in the proportion of infected adults. We found evidence for migratory culling of infected butterflies, based on declines in parasitism during fall migration. We estimated that tens of millions fewer monarchs reach overwintering sites in Mexico as a result of OE, highlighting the need to consider the parasite as a potential threat to the monarch population. Increases in infection among eastern North American monarchs post-2002 suggest that changes to the host's ecology or environment have intensified parasite transmission. Further work is needed to examine the degree to which human practices, such as mass caterpillar rearing and the widespread planting of exotic milkweed, have contributed to this trend.
昆虫-病原体动态变化具有季节性和年际变化的特点，与昆虫丰度和气候的波动有关。长期分析对于跟踪迁徙昆虫中的寄生虫动态变化尤为重要，部分原因是它们广阔的栖息地范围和高度的流动性可能会削弱密度和气候对感染率的局部影响。帝王蝶 Danaus plexippus 通常会感染原生动物 Ophryocystis elektroscirrha（OE）。由于这种寄生虫降低了帝王蝶的存活率和飞行能力，而且迁徙的帝王蝶在最近几十年经历了数量下降，因此了解感染的模式和驱动因素非常重要。在这里，我们汇总了 50 年来在美国、加拿大和墨西哥夏季繁殖、秋季迁徙和越冬期间采集的野生帝王蝶的 OE 感染数据。我们分别研究了北美东部和西部的帝王蝶，以了解丰度估计、资源可用性、气候和繁殖季节长度如何影响感染趋势。我们还评估了迁徙时的密集淘汰强度，即在迁徙期间从种群中剔除感染个体的行为。与东部亚种群相比，西部亚种群的平均感染率高出四倍。在北美东部，自 21 世纪中期以来，感染帝王蝶的比例增加了两倍。在西部地区，2000 年至 2015 年期间，感染帝王蝶的比例急剧下降，此后又有所上升。对于东部和西部亚种群，夏季成虫数量较多的年份预测感染率较高，这表明随着宿主繁殖密度的增加，传播也会增加。环境变量（温度和 NDVI）与成年感染率的变化无关。我们发现了迁徙时淘汰感染蝴蝶的证据，这表明寄生虫在秋季迁徙期间的寄生率下降。我们估计，由于 OE，到达墨西哥越冬地的帝王蝶减少了数千万，这凸显了有必要将寄生虫视为帝王蝶种群的潜在威胁。2002 年后，北美东部帝王蝶的感染率增加表明，宿主生态或环境的变化加剧了寄生虫的传播。需要进一步研究人类行为（如大规模饲养毛毛虫和广泛种植外来乳草）在多大程度上促成了这一趋势。
