Sequential decline in allocation among flowers within inflorescences: Proximate mechanisms and adaptive significance

Flowering plants often exhibit declining investment in gametes, seeds, and floral organs among sequentially blooming flowers within inflorescences. However, few experimental studies have determined the relative importance of proximate underlying causes such as architectural constraints or resource competition among flowers, and fewer still have identified likely selective factors that favor sequential variation in allocation. By combining observational and experimental studies in natural populations of Aquilegia canadensis, we showed that ovule and pollen production declined with flower sequence by 9% and. 18%, respectively, due to architectural effects. However, a much stronger decline in fruit set (27%) and seeds per fruit (58%) was mediated entirely by competition for resources among flowers. Reducing resources by defoliation greatly reduced fruit set (-37%) and seeds per fruit (-61%) and increased the severity of the decline in fruit set. Experimentally alleviating resource preemption by first flowers greatly increased the seed production of later flowers (+39%) to the extent that fourth flowers on manipulated plants set as many seeds as first flowers on control plants. In contrast, aspects of floral morphology including sepal size, nectar spur length, and herkogamy showed little or no sequential variation and were relatively insensitive to experimental manipulation of resources. We also investigated whether the positional decline in allocation was adaptive. Disproportionate investment in early flowers was not associated with a seasonal decline in important environmental factors (e.g., light, water, soil nutrients) or cross-pollination. Marker-gene assays also failed to show that early flowers consistently produced a greater proportion of high-quality outcrossed progeny. All flowers had a high probability of being eaten by herbivores (mean = 70%). However, the risk of herbivory was lower for early flowers (64%) than later flowers (79%). Herbivory may, therefore, select for higher allocation to early flowers as well as flexible investment mediated by interflower competition because it allows the reallocation of resources to later flowers when early flowers are lost to herbivores. This adaptive hypothesis is further supported by comparative data from closely related A. caerulea, which differs from A. canadensis in the nature of herbivory as well as the pattern and mechanism of sequential variation in reproductive allocation.