Herbarium specimens reveal the footprint of climate change on flowering trends across north-central North America

Abstract

Shifting flowering phenology with rising temperatures is occurring worldwide, but the rarity of co-occurring long-term observational and temperature records has hindered the evaluation of phenological responsiveness in many species and across large spatial scales. We used herbarium specimens combined with historic temperature data to examine the impact of climate change on flowering trends in 141 species collected across 116,000 km(2) in north-central North America. On average, date of maximum flowering advanced 2.4 days °C(-1), although species-specific responses varied from - 13.5 to + 7.3 days °C(-1). Plant functional types exhibited distinct patterns of phenological responsiveness with significant differences between native and introduced species, among flowering seasons, and between wind- and biotically pollinated species. This study is the first to assess large-scale patterns of phenological responsiveness with broad species representation and is an important step towards understanding current and future impacts of climate change on species performance and biodiversity.

Keywords: Climate change; invasive species; life history; phenological responsiveness; phenology; pollination syndrome.

Figure 1

Spring temperature trends across the state of Ohio (a) and in Trumbull County (b). Yearly spring (February to May) temperature anomalies were calculated by subtracting the 115-year (1895–2009) average for these four months from yearly averages. Simple linear regression lines were added to determine shifts in spring temperatures over the 115-year period. Trumbull Co. has experienced a 2.0 °C average spring temperature increase compared with the state-wide 0.9 °C average increase.

Figure 2

Variation in phenological responsiveness to changing temperature among 141 species of plants in Ohio. (a) For each species, the day of year of maximum flowering (D_xi) was regressed against the average temperature from the average month of flowering and the 3 months prior . The slope of each line quantifies the phenological responsiveness for each species. (b) Rank order of each species’ phenological responsiveness is represented by a point ± SE bars. Closed points show a significant (P ≤ 0.05) phenological response to temperature, while open points designate no significant change. The dashed line indicates 0, or no phenological response. A negative phenological responsiveness indicates earlier flowering with warming while a positive shift represents delayed flowering with warming.

Figure 3

Phenological responsiveness to increasing temperature within different plant functional groups. Mean ± 1 SE with the number of species per group indicated in parentheses. Asterisks indicate a significant difference from the reference group, which is the topmost group in a sub-panel (P = 0.05).

Figure 4

Phenological responsiveness to rising temperature among spring flowering species separated by functional group. Points indicate group mean phenological responsiveness with standard error bars; the number of species included in a group is given in parentheses. Groups that are significantly different from the reference group (the topmost group in a sub-panel) are shown with asterisks (P = 0.05).

Figure 5

Differing phenological responsiveness to temperature based on origin among differing growth forms. Group mean phenological responsiveness is indicated by points and ± 1 SE bars. Species numbers per group are given in parentheses; significant differences between groups are indicated with asterisks (P = 0.05).