Different factors limit early- and late-season windows of opportunity for monarch development

Seasonal windows of opportunity are intervals within a year that provide improved prospects for growth, survival, or reproduction. However, few studies have sufficient temporal resolution to examine how multiple factors combine to constrain the seasonal timing and extent of developmental opportunities. Here, we document seasonal changes in milkweed (Ascelpias fascicularis) – monarch (Danaus plexippus) interactions with high-resolution throughout the last three breeding seasons prior to a precipitous single-year decline in the western monarch population. Our results show early- and late-season windows of opportunity for monarch recruitment that were constrained by different combinations of factors. Early-season windows of opportunity were characterized by high egg densities and low survival on a select subset of host plants, consistent with the hypothesis that early-spring migrant female monarchs select earlier-emerging plants to balance a seasonal trade-off between increasing host plant quantity and decreasing host plant quality. Late-season windows of opportunity were coincident with the initiation of host plant senescence and caterpillar success was negatively correlated with heatwave exposure, consistent with the hypothesis that late-season windows were constrained by plant defense traits and thermal stress. Throughout this study, climatic and microclimatic variation played a foundational role in the timing and success of monarch developmental windows by affecting bottom-up, top-down, and abiotic limitations. More exposed microclimates were associated with higher developmental success during cooler conditions and more shaded microclimates were associated with higher developmental success during warmer conditions, suggesting that habitat heterogeneity could buffer the effects of climatic variation. Together, these findings show an important dimension of seasonal change in milkweed-monarch interactions and illustrate how different biotic and abiotic factors can limit the developmental success of monarchs across the breeding season. These results also suggest the potential for seasonal sequences of favorable or unfavorable conditions across the breeding range to strongly affect monarch population dynamics.

季节机遇窗口（seasonal windows of opportunity）指一年中为生物生长、存活或繁殖提供更佳前景的时段区间。然而，鲜有研究具备足够高的时间分辨率，以解析多重因素如何共同制约发育机遇的季节时序与范围。本研究针对北美西部帝王蝶（Danaus plexippus）种群单年度骤降前的最后三个繁殖季，以高分辨率记录了马利筋（Ascelpias fascicularis）与帝王蝶的互作季节动态。研究结果显示，帝王蝶种群补充存在季初与季末两个机遇窗口，二者分别受不同组合的因素制约。季初机遇窗口的特征为：寄主植物子集上的卵密度较高，但幼虫存活率较低，这与"早春迁飞的雌性帝王蝶会选择萌发更早的寄主植物，以平衡寄主植物数量增加与品质下降之间的季节权衡"的假说相符。季末机遇窗口与寄主植物衰老启动的时段重合，且幼虫发育成功率与热浪暴露程度呈负相关，这与"季末机遇窗口受植物防御性状与热胁迫共同制约"的假说相符。本研究表明，气候与微气候变异通过调控上行效应（bottom-up）、下行效应（top-down）与非生物限制因子，对帝王蝶发育窗口的时序与成功率起到了基础性作用。在温度较低的环境中，更暴露的微生境与更高的发育成功率相关；而在温度较高的环境中，更遮阴的微生境则与更高的发育成功率相关，这表明生境异质性能够缓冲气候变异带来的影响。综上，本研究结果揭示了马利筋-帝王蝶互作季节动态的重要维度，并阐明了在整个繁殖季中，不同生物与非生物因子如何制约帝王蝶的发育成功率。本研究结果还表明，在整个繁殖分布区内，有利或不利条件的季节序列，有可能对帝王蝶的种群动态产生强烈影响。