Non-serotinous woody plants behave as aerial seed bank species when a late-summer wildfire coincides with a mast year

摘要

Abstract class="enumerated" style="list-style-type:decimal">Trees which lack obvious fire-adaptive traits such as serotinous seed-bearing structures or vegetative resprouting are assumed to be at a dramatic disadvantage in recolonization via sexual recruitment after fire, because seed dispersal is invariably quite constrained. We propose an alternative strategy in masting tree species with woody cones or cone-like structures: that the large clusters of woody tissue in a mast year will sufficiently impede heat transfer that a small fraction of seeds can survive the flaming front passage; in a mast year, this small fraction would be a very large absolute number.In Kootenay National Park in British Columbia, we examined regeneration by Engelmann spruce (Picea engelmannii), a non-serotinous conifer, after two fires, both of which coincided with mast years. Coupling models of seed survivorship within cones and seed maturation schedule to a spatially realistic recruitment model, we show that (1) the spatial pattern of seedlings on a 630 m transect from the forest edge into the burn was best explained if there was in situ seed dissemination by burnt trees; (2) in areas several hundred meters from any living trees, recruitment density was well correlated with local prefire cone density; and (3) spruce was responding exactly like its serotinous codominant, lodgepole pine (Pinus contorta).We conclude that non-serotinous species can indeed behave like aerial seed bank species in mast years if the fire takes place late in the seed maturation period. Using the example of the circumpolar boreal forest, while the joint probability of a mast year and a late-season fire will make this type of event rare (we estimate P = 0.1), nonetheless, it would permit a species lacking obvious fire-adapted traits to occasionally establish a widespread and abundant cohort on a large part of the landscape. class="kwd-title">Keywords: Adaptation, Engelmann spruce, fire, mass seeding, masting, regeneration, seed viability, serotiny class="head no_bottom_margin" id="__sec2title">IntroductionWoody plants in many parts of the world cope with a disturbance regime dominated by large, stand-replacing fires (e.g., Johnson ; Veblen et al. ; Peet ). Indeed, these fires are so large that, given dispersal constraints, species which must recolonize from the edge are at a tremendous disadvantage in the early recruitment phase (Greene and Johnson ). There are three fire-adaptive traits that permit in situ establishment and thus allow a species to circumvent this dispersal constraint (Keeley et al. ). The first is asexual reproduction. This is particularly advantageous, but much less common, when the perennating buds are located on widespread roots (e.g., in aspen, Populus tremuloides). More typically, angiosperms reliably sprout from the root collar (few gymnosperm species can do this), a trait often enhanced in fire-adapted species by the presence of lignotubers, storage organs at the root–shoot junction which contain numerous dormant buds (James ). The second trait is an aerial seed bank. Persistent ovulate cones or inflorescences ensure that a large proportion of seeds are on hand to disperse from burnt trees or shrubs onto the receptive seedbeds created by combustion of organic soil layers (Greene et al. ). Aerial seed banks are common among plants in many fire-prone areas, including several Pinus species in the Northern Hemisphere and Banksia species in Australia (Lamont et al. ). The third trait is a soil seed bank. Soil seed banks that can persist through fire, while common in Mediterranean and desert ecosystems, are, however, quite rare among species in the circumboreal forest where smoldering combustion of the deep organic layer typically kills all seeds (Johnson and Fryer ).How do species lacking these three traits persist in fire-prone environments? They must seed in from the fire edge or from residual stands within the burn; empirically, we find very few seedlings at distances greater than about 100 m from surviving seed sources (Zasada ; Greene and Johnson ). It remains a mystery how species without a strong asexual response or either aerial or soil seed banks can persist in a landscape dominated by stand-replacing fires (Greene and Johnson ). We hypothesize that under certain conditions, a species can respond to stand-replacing fire as if it possessed an aerial seed bank, dispersing viable seeds from dead or dying trees within the interior of the burn. Four conditions must be met for this hypothesis to be correct. First, seeds must be contained within structures that provide resistance to heat transfer from incident heat flux and can sufficiently insulate the seeds against lethal temperatures. Structures capable of insulating seeds from fire vary by species according to their thermophysical properties and can in some cases be single ovulate cones or fruits (Mercer et al. ; Michaletz et al. ) or, in other cases, dense clusters of many cones or fruits (Judd and Ashton ). Second, fire must occur when seeds are either mature or sufficiently advanced that they can finish maturation even when the tree is dead. Third, the fire must not occur so late in the year that the cones or fruits have begun to open; otherwise, the cones or fruits and any enclosed seeds will combust as fine fuels. For example, Michaletz et al. () concluded that the window between sufficient maturation and cone opening in the North American boreal species white spruce (Picea glauca) was, empirically, about 600 to 1180 degree days.The fourth requirement is that the species must be enjoying a mast year at the time of the fire (Koenig and Knops href="#b27" rid="b27" class=" bibr popnode">1998; Greene and Johnson href="#b13" rid="b13" class=" bibr popnode">2004). Masting is a condition in which individual plants of a species synchronously produce unusually high numbers of fruit or seeds over a wide region (Silvertown href="#b40" rid="b40" class=" bibr popnode">1980; Kelly href="#b26" rid="b26" class=" bibr popnode tag_hotlink tag_tooltip" id="__tag_422576285">1994). High production in one season (a mast year) is typically followed by several years of low seed production. We consider a mast year an additional requirement because high seed mortality will certainly occur during passage of the flaming front, and there will be therefore little in situ recruitment in a non-mast year. The coincidence of a mast year and a fire will have an augmenting effect from the living plants at the edge: The good seedbeds created by smoldering combustion are ephemeral, lasting only a few years before leaf accrual renders them poor substrates for small-seeded species (Greene and Johnson href="#b12" rid="b12" class=" bibr popnode">2000; Charron and Greene href="#b5" rid="b5" class=" bibr popnode">2002; Peters et al. href="#b39" rid="b39" class=" bibr popnode">2005), and thus, the edge trees would have a much stronger input (albeit still distance limited) in a mast year.Our objective is to formally model and test the hypothesis that a species can perform as if it had an aerial seed bank if a fire takes place late in the seed maturation period during a mast year. We focus on the conifer, Engelmann spruce (Picea engelmannii Parry ex Engelm.), in the southern Canadian Rockies following two late-summer fires. This is a masting species, with very little seed produced in inter-mast years (Fowler and Roche href="#b9" rid="b9" class=" bibr popnode">1976; Greene and Johnson href="#b13" rid="b13" class=" bibr popnode">2004). Both fires were selected for this study because they coincided with mast years. As Engelmann spruce is extremely closely related to, and hybridizes extensively with, white spruce (Daubenmire href="#b6" rid="b6" class=" bibr popnode">1974; Bouillé et al. href="#b3" rid="b3" class=" bibr popnode">2011), we can posit the same degree day window for seed maturation mentioned above. Likewise, reproductive potential and interannual variation in crop sizes are comparable between Engelmann and white spruce, with both species predictably showing a decrease in seed production with elevation (Owens and Molder href="#b35" rid="b35" class=" bibr popnode">1984; Greene and Johnson href="#b13" rid="b13" class=" bibr popnode">2004). Unpublished data collected by Greene and Pounden in consecutive years (2005 to 2013) show that the cone crops of the two species are indeed highly positively correlated.We will also compare recruitment of Engelmann spruce with the aerial seed bank species, lodgepole pine (Pinus contorta Dougl. ex Loud. var. latifolia Engelm.). We develop a general mechanistic model of sexual recruitment applicable to any species with or without aerial seed banks, or with a combination of the two responses. Our model makes two predictions for these late-summer fires. First, unlike the steep negative exponential decline in seeds or seedlings of wind-dispersed species from burn edges due to the dispersal constraint (Greene and Johnson href="#b10" rid="b10" class=" bibr popnode">1996) expected for species lacking reliable asexual reproduction or aerial seed banks, the decline in recruit density in a fire/mast year to a distance of about 200 m from the fire edge should be strongly moderated by input from dead spruce within the burn area, and beyond 200 m should be nonzero, yet quite flat, as effectively all seeds, as with lodgepole pine, are by that distance derived locally from dead spruce. Second, at distances greater than 200 m from an unburned edge, we expect spruce seedling density to be positively correlated with local burnt ovulate cone density (as it would be with lodgepole pine).