Habitat fragmentation decouples fire-stimulated flowering from plant reproductive fitness

Abstract

Many plant species in historically fire-dependent ecosystems exhibit fire-stimulated flowering. While greater reproductive effort after fire is expected to result in increased reproductive outcomes, seed production often depends on pollination, the spatial distribution of prospective mates, and the timing of their reproductive activity. Fire-stimulated flowering may thus have limited fitness benefits in small, isolated populations where mating opportunities are restricted and pollination rates are low. We conducted a 6-y study of 6,357 Echinacea angustifolia (Asteraceae) individuals across 35 remnant prairies in Minnesota (USA) to experimentally evaluate how fire effects on multiple components of reproduction vary with population size in a common species. Fire increased annual reproductive effort across populations, doubling the proportion of plants in flower and increasing the number of flower heads 65% per plant. In contrast, fire’s influence on reproductive outcomes differed between large and small populations, reflecting the density-dependent effects of fire on spatiotemporal mating potential and pollination. In populations with fewer than 20 individuals, fire did not consistently increase pollination or annual seed production. Above this threshold, fire increased mating potential, leading to a 24% increase in seed set and a 71% increase in annual seed production. Our findings suggest that density-dependent effects of fire on pollination largely determine plant reproductive outcomes and could influence population dynamics across fire-dependent systems. Failure to account for the density-dependent effects of fire on seed production may lead us to overestimate the beneficial effects of fire on plant demography and the capacity of fire to maintain plant diversity, especially in fragmented habitats.

Masting, fire‐stimulated flowering, and the evolutionary ecology of synchronized reproduction

“…The separate study plots within each site are burned on different schedules (i.e., different years) years allowing us to distinguish fire effects on reproductive effort from other causes of interannual variation (Wagenius et al, 2020). Each year we counted flowering individuals as well as the number of flowering heads produced by individual plants to quantify interannual reproductive variation (see Wagenius et al, 2020 for detailed E. angustifolia methods and Beck et al, 2022 for data).…”

“…Our review encompassed research using synonymous terms (e.g., “mass flowering,” “mass seeding,” “post‐fire flowering,” “pyrogenic flowering”) as well as empirical studies examining interannual reproductive variation that did not self‐identify with the fields of masting or fire‐stimulated flowering. We relied on published compilations and additional sources cited in this paper to compile a database of 1870 plant species (Beck et al, 2022). This database includes species within the MASTREE+ database (Hacket‐Pain et al, 2022), the largest assemblage of reproductive time series that includes 973 taxa.…”

“…Data and code (Beck et al, 2022) are available in Figshare at https://doi.org/10.6084/m9.figshare.21568509.v2.…”

“…In addition to altering abiotic environmental conditions, fire-induced mortality among arthropods can reduce seed predation (Hiers et al, 2000;Vickery, 2002aVickery, , 2002bVlok, 2020)-a special case of environmental prediction distinct from predator satiation. This emphasis on seedling recruitment, the lack of a comprehensive framework that considers alternative hypotheses (Pyke, 2018), and the relative scarcity of empirical studies directly quantifying seed production (see Auld, 1987;Beck et al, 2023;Lamont & Runciman, 1993;Mark, 1965;Richardson & Wagenius, 2022;Taylor et al, 1998;Wagenius et al, 2020 for known exceptions) have obscured the potential importance of other adaptive explanations. Few fire-stimulated flowering studies have investigated the potential roles of predator satiation or pollination efficiency (but see Auld, 1987;Beck et al, 2023;Hiers et al, 2000;Richardson & Wagenius, 2022;Vickery, 2002b;Vlok, 2020;Wagenius et al, 2020).…”

“…Fire-stimulated species provide more tractable systems to experimentally manipulate plant density or the spatial scale of reproductive synchronization in natural populations to directly investigate fundamental questions about density-dependent processes. For example, in a recent study Beck et al (2023) experimentally demonstrated that synchronized post-fire reproduction contributes to greater pollination efficiency and seed production in large populations while synchronized reproduction does not have consistent fitness benefits in small populations. These empirical results directly parallel theoretical predictions about the density-dependent fitness benefits associated with pollination efficiency in wind-pollinated masting species (Kelly et al, 2001).…”