Temporal dynamics and biocontrol potential of a hyperparasite on coffee leaf rust across a landscape in Arabica coffee’s native range

Agroforestry systems can provide habitats for rich biodiversity including
multitrophic interactions, which presents opportunities to develop natural
pest control. Shade coffee systems in several coffee-growing areas of the
world host such unique habitats where pests and their natural enemies
interact. One of the major global challenges for coffee production, coffee
leaf rust caused by the fungal pathogen Hemileia vastatrix is attacked by
the fungal hyperparasite, Lecanicillium lecanii. However, we lack insights
in the dynamics and biocontrol potential of the hyperparasite on coffee
leaf rust from landscapes in Arabica coffee’s native range. To understand
the temporal dynamics across landscapes and environmental drivers of the
rust and hyperparasite, and the potential for biocontrol of the rust by
the hyperparasite, we studied the rust and hyperparasite during the dry
and wet seasons for three consecutive years at 60 sites across a gradient
of coffee management in southwestern Ethiopia. We found that coffee leaf
rust was more severe during the dry season, whereas the hyperparasite was
more severe during the wet season in two out of three years. The rust
growth rate from the wet to the dry season transition was negatively
related to the hyperparasite index during the wet season, implying a
potential top-down control. Coffee leaf rust was generally more severe at
lower altitudes in the dry season, whereas the hyperparasite was more
severe at high altitude. The rust incidence increased with management
intensity, while the hyperparasite was more common under less intensive
management. This study could be interesting in that it represents a
landscape where Arabica coffee originated and the rust and hyperparasite
might have a long co-evolutionary history. Our findings highlight the
potential of the hyperparasite to suppress the rust’s growth rate from the
wet to dry season transition when the rust severity could otherwise be at
its peak. We show that less intensively managed landscapes with dense
shade levels are likely to increase hyperparasite abundance and result in
an improved top-down control of the rust. However, more detailed knowledge
is needed on the interaction of these species to assess its importance for
reducing rust induced yield losses or the risk of rust outbreaks.

农林业（agroforestry）系统可为包括多营养级互作在内的丰富生物多样性提供栖息生境，这为开发自然害虫防治手段提供了契机。全球多个咖啡种植区的遮荫咖啡种植系统，便承载着这类独特生境，其中害虫与其天敌之间存在互作关系。咖啡生产面临的一项全球性重大挑战，当属由真菌病原菌咖啡驼孢锈菌（Hemileia vastatrix）引发的咖啡叶锈病（coffee leaf rust），而该病原菌可被真菌重寄生菌蜡蚧轮枝菌（Lecanicillium lecanii）寄生。然而，目前我们对阿拉比卡咖啡（Arabica coffee）原生分布区景观中重寄生菌对咖啡叶锈病的动态及其生防潜力仍缺乏深入认知。为明晰景观尺度下的时间动态、咖啡叶锈病与重寄生菌的环境驱动因子，以及重寄生菌对咖啡叶锈病的生防潜力，我们于埃塞俄比亚西南部60个沿咖啡管理强度梯度分布的样地中，连续三年在干湿两季对咖啡叶锈病与重寄生菌展开了调查。研究发现，在三年中的两年里，咖啡叶锈病在旱季更为严重，而重寄生菌则在雨季更为猖獗。从雨季向旱季过渡期间的锈病增长速率，与雨季的重寄生菌指数呈负相关，这暗示其存在潜在的下行控制效应。旱季时，咖啡叶锈病在低海拔地区通常更为严重，而重寄生菌则在高海拔地区更为高发。咖啡叶锈病的发病率随管理强度提升而升高，而重寄生菌在管理强度较低的生境中更为常见。本研究的独特之处在于，其研究区域正是阿拉比卡咖啡的原生分布区，咖啡叶锈病与重寄生菌或许拥有漫长的协同进化历史。我们的研究结果表明，在雨季向旱季过渡的阶段（此时锈病病害程度本可能达到峰值），重寄生菌可抑制锈病的增长速率。我们还发现，遮荫密度较高的低管理强度景观，有望提升重寄生菌的丰度，进而实现对锈病更有效的下行控制。不过，若要评估该互作关系在减轻锈病引发的产量损失或锈病爆发风险方面的重要性，还需要对这两个物种的互作机制开展更细致的研究。