Defining the pyro-thermal niche: do seed traits, ecosystem type and phylogeny influence thermal thresholds in seeds with physical dormancy?

Abstract

Introduction

Regeneration of plants from seeds is fundamental for species persistence and population expansion (Nolan et al., 2021). Seeds are one of the key pathways for plant populations to recover following disturbances and are essential both for dispersal and as a means for adaptation to environmental conditions (Baskin & Baskin, 2001). At a population level, seed dormancy enables the formation of soil seed banks, allowing for the emergence of seedlings in response to ecosystem disturbances, including fire (Baskin & Baskin, 2001; Penfield, 2017). Seed dormancy is a critical mechanism for species persistence in ecosystems that experience sporadic ecological disturbances, for example fire, as it ensures seeds germinate at the most opportune time to maximise recruitment success (Ooi et al., 2022). Understanding how seed traits and dormancy mechanisms differ between species can allow us to predict species responses to disturbances such as fire (Saatkamp et al., 2019), which are projected to become more frequent and severe under global climate change (Boer et al., 2016).

Seed dormancy is common amongst vascular plants, occurring in > 50% of all wild species globally (Baskin & Baskin, 2001; Kildisheva et al., 2020). Seeds with physical dormancy (PY) are released from the mother plant with a water-impermeable seed coat which restricts their ability to hydrate and thus germinate (Baskin & Baskin, 2004), but once the seed coat is ruptured, hydration can occur, and germination will proceed given suitable moisture and temperature conditions. Physical dormancy is a derived trait, having evolved relatively recently (Willis et al., 2014), and is known to occur in at least 18 families of angiosperms (Baskin et al., 2000, 2006), including Fabaceae, Rhamnaceae, Sapindaceae and Malvaceae (Baskin, 2003; Baskin et al., 2006). Dormancy loss in PY seeds represents a critical life stage transition for plants, as the process of dormancy break is often irreversible (Baskin & Baskin, 2001) and usually results in seeds germinating quickly once hydrated (Ryan et al., 2023). Therefore, the mechanisms responsible for the alleviation of PY are fine-tuned to ensure germination occurs when seedling emergence and survival are most likely optimal for that population of seeds (Overton et al., 2024).

Seed dormancy is particularly common among species in fire-prone ecosystems, with germination cues aligned with fire-derived stimulants (Collette & Ooi, 2021; Pausas & Lamont, 2022), and fire promoting a pulse of seedling emergence for many species. Fire creates a unique window in time, providing conditions for dormancy loss, germination and subsequent emergence, in conjunction with a postfire period optimal for seedling recruitment in which abundant light and ample space mean competition for resources are at its lowest (Pausas et al., 2022). Emergence immediately following fire provides seedlings the longest period before the next fire event, which maximises the likelihood of maturation and replacement potential. Conversely, interfire seedling emergence may be disadvantaged in fire-prone ecosystems because germination during these periods is less conducive to persistence (Ooi et al., 2022), with an increased likelihood of recruits experiencing fire before reaching maturity. One of the primary cues for PY release in fire-prone ecosystems is elevated soil temperatures, often referred to as ‘heat-shock’, resulting from the consumption of surface fuels during fire (Moreira & Pausas, 2012), potentially in conjunction with increased postfire solar radiation in some vegetation types (Santana et al., 2012; Hill & Auld, 2020). At the population scale, the soil seed bank is impacted by soil heating, characterised along a temperature continuum marked by critical thresholds corresponding to significant irreversible events (Fig. 1).

Fig. 1

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Conceptual figure describing the continuum between loss of dormancy and subsequent lethal temperature for seeds exposed to high temperatures. This continuum is punctuated by critical thresholds corresponding to significant ecologically irreversible events, and here, we define these three thresholds as the limits that shape the pyro-thermal niche, adapted from Martin et al. (1975) with permission.

Soil heating during fire is mediated by the structure and quantity of biomass that is in direct contact with the soil surface (henceforth surface fuels). These fuels can include, but are not limited to, duff, fallen leaves, fine twigs and branches from elevated layers, herbaceous ground covers and grasses, prefire woody debris and trees and branches, which fall during fire. The quantity of surface fuels, combined with the extent of surface fuel consumption during the fire event (Tangney et al., 2020), shapes soil heating dynamics. Soil temperatures decline rapidly with soil depth and are affected by soil moisture and texture (Bradstock & Auld, 1995). Consumption of a large quantity of surface fuels can generate soil temperatures exceeding 200°C in the upper soil profile, while lower levels of consumption generate temperatures as low as 40°C (Tangney et al., 2018). As different vegetation types generate different arrays of surface fuels, and as these vary spatially at small scales within ecosystems, variation in soil heating dynamics differs between and within ecosystems (Schwilk & Ackerly, 2001; Pausas & Moreira, 2012). The composition and characteristics of surface fuel beds are a function of leaf traits and include litterbed density and moisture (Scarff & Westoby, 2006; Cornwell et al., 2015), the habit of species that are supported within that ecosystem and the prevailing climate of the ecosystem (Grant et al., 1997; Dimitrakopoulos, 2002). How seeds differ in their response to high soil temperatures may also vary between ecosystems, as seed thermal requirements and tolerances may be under selection pressures unique to each ecosystem.

Dormancy and dormancy release dynamics play an important role in determining species distribution, population structure and persistence within many ecosystems (Willis et al., 2014), as seeds must first germinate and establish. When attempting to determine the drivers of dormancy release, the heat requirement for dormancy break for PY species in fire-prone systems provides additional complexity. For example, soil heating varies with differing fire intensities, and dormant seeds need to be located within the soil profile at depths below those that experience lethal temperatures (LT₅₀s), but not so deep that temperature cues are missed, or where emergence is limited by internal seed resources (Tangney et al., 2020). Maximum seedling emergence depth is related to seed mass (Bond et al., 1999; Liyanage & Ooi, 2018), with larger seeds able to emerge from deeper within the soil profile due to proportional increases in energy reserves (Leishman et al., 2000; Hanley et al., 2003). However, as soil depth increases, the heat generated by a passing fire is buffered, drastically reducing heat penetration into the soil (Tangney et al., 2020). For some seeds that need high temperatures to release dormancy, being too deep in the soil may reduce their ability to receive dormancy release cues. The process of dormancy release during fire is made even more complex by the high degree of heterogeneity present in both the spatial and temporal domains of soil heating (Odion & Davis, 2000; Pingree & Kobziar, 2019). The degree or intensity of soil heating, seed burial depth and heating duration are all critical factors in determining whether a seed or a population of seeds loses dormancy, and all operate at fine-scale resolutions (Paula & Pausas, 2008; Tangney et al., 2020).

Duration of soil heating during fire is a critical component for understanding the process of dormancy release in PY seeds yet may be the most difficult aspect to quantify due to the complicated nature of recording the spatial and temporal dynamics of soil temperatures during fire (Tangney et al., 2018). Nonetheless, the duration of heating holds significant influence over the patterns of postfire emergence from soil seed banks (Tyler, 1995). Short durations of high temperatures may be insufficient to release seed dormancy in PY seeds, while prolonged exposures of high temperature may lead to significant mortality of seeds in soil seed banks (Auld & O'Connell, 1991). Critically, however, the relationship with heating duration may be species-specific, and how duration of heating interacts with temperature thresholds remains an important element to examine.

Here, we introduce the concept of the pyro-thermal niche – the thermal niche occupied by seeds during exposure to high temperatures. It is defined by a collective of three thermal thresholds: dormancy release temperature (DRT₅₀), optimal temperature (T_opt) and lethal temperature (LT₅₀, Fig. 1), all of which may be influenced by heating duration. The pyro-thermal niche provides a pathway and statistical framework, with which we can conduct comparative studies across species and reveal lesser studied aspects of seed ecology across the entire thermal domain. Dormancy release temperature (Fig. 1) is defined as the temperature in which half of the viable dormant seeds within the population are released from dormancy (Moreira & Pausas, 2012; Ooi et al., 2014), accounting for any significant nondormant fraction within the population (Overton et al., 2024). T_opt is defined as the temperature that aligns with the highest germination proportion of all viable seeds within a population (Zomer et al., 2022), inclusive of the nondormant fraction (Fig. 1). Lastly, LT₅₀ is defined as the temperature in which half of the germinable seeds within a population are killed and align with a 50% reduction in germination from T_opt (Martin et al., 1975; Tangney et al., 2019). Here, the reduction in germination as a result of heat shock higher than the seed lot or species-specific T_opt is associated with increased mortality within the seed lot as seeds increasingly reach their individual physiological temperature limits (Tangney et al., 2019; Overton et al., 2024) and cellular machinery becomes increasingly damaged (Cox et al., 2010). Therefore, LT₅₀ represents the collective decline in germination of the seed lot below optimum germination for that species at that heating duration because of increased mortality of individual seeds. In seeds with PY, low relative humidities (e.g. < 12%) associated with high temperatures can induce temporary secondary dormancy in some rare cases. However, as seed coat permeability is irreversibly alleviated following heat shock, any secondary dormancy would be overcome during imbibition and subsequent germination (Jaganathan, 2022).

Seed response to temperature may vary across all three of these thresholds, driven by both ecological and evolutionary mechanisms. Furthermore, characterising diversity in the pyro-thermal niche requires components of phylogenetic and functional diversity to be considered. For example, all thresholds may be negatively correlated with seed size (Liyanage & Ooi, 2018). Small seeds must be near the soil surface to successfully emerge (Bond et al., 1999; Tangney et al., 2020), but consequently can experience high levels of ambient soil heating due to proximity to the soil surface. To avoid dormancy loss during unsuitable periods for establishment, DRT₅₀ in smaller seeds may be relatively higher than co-occurring larger seeded species (Liyanage & Ooi, 2018).

The aim of this study was to assess variation in thermal thresholds between species with seeds that have PY, to understand how the pyro-thermal niche is aligned with seed mass and vegetation type, and whether it is constrained across phylogeny. We directly address four questions:

1. Are the metrics of the pyro-thermal niche dependent on the duration of heat exposure?;
2. Is variation in the pyro-thermal niche associated with seed mass?;
3. Do species from the same vegetation community share similar pyro-thermal niches, given that they are likely to experience the same fire regimes?; and
4. Is there evidence for fire acting as an evolutionary pressure shaping the pyro-thermal niche in PY species?

To achieve this, we set out to define and model critical life stage thresholds in PY seeds. We compiled experimental heat-shock and subsequent germination data from previously published research and combined it with newly acquired data for a total of 58 species from Rhamnaceae and Fabaceae across Australia. We defined the DRT₅₀, T_opt and LT₅₀ (Fig. 1) for each species. This allowed us to understand the diversity and dynamics of the pyro-thermal niche and how it differs between species and whether patterns of variation in the pyro-thermal niche differ between ecosystems and across phylogenies.