j.g. pausas' blog

The increasing availability of global-scale data on plant traits, species distribution (e.g. GBIF), climate variables, sophisticated numerical methods (e.g. machine learning tools, R packages) and computing power (e.g. cloud computing) has enabled researchers to understand our biosphere in an unprecedented manner. However, these techno-scientific advances come with a cost. Researchers with sufficient technical skills in data management can now study global patterns and produce numerically sophisticated and apparently robust papers, without a clear hypothesis to test nor attempt to interpret any patterns from a mechanistic perspective. In addition, these broad-scale analyses tend to use the most readily available data rather than necessarily the most relevant data. This is further fuelled by the growing culture that values ‘fast’ science over research that may take years to complete (the publish-or-perish culture). As a consequence, there is an increase in research based on correlating ‘everything’ to see if any patterns emerge, instead of a hypothesis-driven approach. An outcome for plant ecology is that key factors in determining plant fitness, such as fire regime, light availability, herbivory, pollinator availability and other biotic interactions, are underconsidered in broad-scale studies, as they are less available than climate information, in particular. This is exacerbated by the long-standing belief that climate is the major factor shaping ecological patterns [1]. Studying global-scale patterns also tends to hide biological mechanisms, as these act at local scales and may vary across environments; thus, broad-brush approaches may mask key local processes.

In this letter [2], we highlight the potential for broad-scale correlative studies that ignore mechanisms to hinder progress in ecology. We first present examples related to seed dormancy [3], and then a few other recent examples to illustrate that this is currently a general problem in ecological studies. We end by emphasizing the importance of mechanistic understanding in ecology. Global analyses are an ambitious endeavour to find universal rules, but it needs to be appreciated that such rules may fail at identifying mechanisms that create broad-scale patterns if likely causal variables are not included in the first place. Such a broad-scale approach may even hide key local ecological processes; more integration between broad-scale description and hypothesis-based studies is needed. Furthermore, hypothesis-driven science cannot be replaced by computer mining of immense databases; the scientific method can be enriched by the use of large databases but not replaced by it. If ecology aims to be a predictive science, we should focus more on a mechanistic understanding than on describing correlations with vast amounts of data [2].

I would rather discover one cause than gain the kingdom of Persia.

Democritus (460–370 BC)

References

[1] Pausas J.G. & Bond W.J. 2019. Humboldt and the reinvention of nature. J. Ecol. 107: 1031-1037.  [doi | jecol blog | jgp blog | pdf]

[2] Pausas JG, Lamont BB, Keeley JE, Bond WJ. 2024. The need for mechanistic explanations in (seed) ecology. New Phytol. 242: 2394-2398.  [doi | wiley | pdf]

[3] Pausas JG, Lamont BB, Keeley JE., Bond, WJ. 2022. Bet-hedging and best-bet strategies shape seed dormancy. New Phytol. 236: 1232-1236. [ doi | wiley | pdf]

In Mediterranean ecosystems, fire breaks the dormancy in many species and stimulates germination in the postfire environment [1]. Both the smoke and the heat of the fire may be responsible for breaking dormancy [1]. Cistaceae species are typical examples of species with this heat-released dormancy [1, 2], together with many legumes. Despite fire is a much more powerful driver of dormancy release than the summer heat (figure 9 in [1] and figure 2 in [2]), there are still people aiming to demonstrate the role of summer temperatures in dormancy release in Cistaceae. A recent research team studied the germination of 12 Cistacea species and compared the effect of fire-type heat in seeds submitted to a summer heat treatment (50/20^o C for a month) and in seeds without this summer treatment [3]. They concluded that high summer temperatures are needed for maximum germination in the presence of fire [3]. A reanalysis of their data suggests that not only are summer temperatures inefficient at releasing dormancy, but they also reduce postfire germination [4]. The applied summer heat treatment reduced the germination (%) in the control (H-) and in all fire treatments, and for all species (Fig. 1 below). And for the seeds that germinate, those under summer heat tended to germinate slower than those that did not suffer the summer heat (Fig. 2 below). In conclusion, fire increases the germination of Cistaceae seeds in contrast to summer-type heat, i.e., the great fitness benefits of fire are unmatched by the summer heat [4].

Fig. 1. Germination with no summer heat (x-axis; ~ 20^o C for a month) and with summer heat (y-axis, 50/20^o C altering for 12 h, and during a month) in 12 Cistaceae species with different fire treatments. All fire heat treatments were 100^o C for 10 min applied as follows: H-, no fire heat (black); HB, fire heat before summer (green); HA, fire heat treatment after summer (red); HBA, fire heat before and after the summer (unrealistic scenario; blue). The results suggest that applying a strong summer heat treatment (52/20^o C for a month) reduces the germination (%) in the control (H-) and in all fire treatments and for all species. From [4].

References

[1] Pausas J.G. & Lamont B.B. 2022. Fire-released seed dormancy – a global synthesis. Biological Reviews 97: 1612-1639.  [doi | pdf | supp. mat. | data (figshare)]

[2] Moreira B. & Pausas J.G. 2012. Tanned or burned: The role of fire in shaping physical seed dormancy. PLoS ONE 7(12): e51523. [doi | plos | pdf]

[3] Luna B, Piñas-Bonilla P, Zavala G, Pérez B. 2023. Timing of fire during summer determines seed germination in Mediterranean Cistaceae. Fire Ecology 19: 52.

[4] Lamont BB, Burrows GR, Pausas JG 2024. Fire-type heat increases the germination of Cistaceae seeds in contrast to summer heat. Fire Ecology 20:14 [doi | pdf]

More on seed dormancy: A review | a glossary | bet-hedging & best-bet | smoke-released dormancy 

We have recently reviewed concepts related to seed dormancy and the mechanism of dormancy release (see references 1, 2, 3 below). Here we summarize the main definitions considered.

Seed dormancy: delayed germination even when conditions are favorable. It is a state of metabolic inactivity in the seed that prevents the embryo from growing and thus the seed from germinating. There are two major classes of seed dormancy, inherent dormancy and imposed dormancy.

• Inherent (or innate) dormancy: dormancy is an internal response through retarded embryo maturity or metabolic inactivity. This is often called just ‘dormancy’; it has also been called primary dormancy, but this name is not appropriate (see Secondary dormancy below). There are three basic types of inherent dormancy, depending on the mechanism of release: morphological, physical and physiological dormancy. Some seeds may have multiple mechanisms where they combine physiological and either morphological or physical dormancy.

• • Physical dormancy (PY): a type of inherent dormancy where the seed coat is impermeable to water and/or oxygen such that metabolism cannot occur and the seed cannot germinate even if hydrothermal conditions are suitable. Physical dormancy is typically released by heat, or by physical or chemical scarification: 
    • • Heat-released dormancy: seeds require a heat pulse for breaking physical dormancy that exceeds soil temperatures experienced during summer and is comparable with fire heat.
      • Scarification-released dormancy: seeds require a physical or chemical scarification (different from heat) for breaking physical dormancy (e.g., scratching the surface of the seed coat). Scarification may be a convenient tool for breaking dormancy in horticulture, but its ecological role in the soil is not well known; it may be related to seed coat decays over time through temperature fluctuations or microbial processes. Scarification-released dormancy also occurs in species that do not form a seed bank: seeds of fleshy-fruited species are typically dormant, and scarification (chemical or mechanical) through the guts of frugivorous vertebrates releases their dormancy; in that case, dormancy is a strategy for long distance dispersal [2].

• • Physiological dormancy (PD): a type of inherent dormancy in which metabolic requirements have yet to be met and germination cannot proceed even if hydrothermal conditions are suitable. Some examples of physiological dormancy are:
    • • Smoke-released dormancy: a type of physiological dormancy that is maintained until chemical byproducts in smoke or ash from the combustion of plant matter (collectively termed ‘smoke’) breaks dormancy by catalysing production of enzymes required for initiating metabolic activity and germination.
      • Inhibitor-released dormancy: a type of physiological dormancy where chemical inhibitors must be removed to allow germination. It has been observed in some seeds that germinate only when removed from the fruit, or in mistletoes, when the mucilage is removed (by frugivorous birds). [3].
      • Cold-released dormancy: a type of physiological dormancy that is maintained until the seed is exposed to periods of cold (e.g., ~5°C for two months) that promotes production of cofactors required for initiating metabolic activity [3].
      • Light/dark-released dormancy: a type of physiological dormancy that is maintained until the seed is exposed to periods light-dark that promotes production of specific cofactors required for initiating metabolic activity (photoperiod-controlled dormancy or photodormancy).

• • Morphological dormancy (MD): Dormancy is maintained in an underdeveloped embryo which requires a period of post-dispersal maturation (after-ripening) before the seed is ready to germinate. Morphological dormancy due to immature embryos is neither environmentally controlled nor metabolically inactive and might be better considered as post-release embryo maturation and only apparently dormant (pseudodormancy) [3].

• Imposed dormancy: environmentally-imposed dormancy is the state where metabolic activity continues to be suppressed as external conditions remain unsuitable for germination. Some times it is called secondary dormancy but this term is inappropriate because it may be the only form of dormancy among many seeds, so it cannot be considered secondary in a temporal sense nor minor in a functional sense [3]. In species with heat-released dormancy, this state is maintained between the fire event and the first substantial postfire rains but may be minimal among smoke-responsive seeds if the chemicals are only absorbed once the seeds have imbibed. [1,3]

Dormancy syndrome: A correlated suite of traits that is coordinated to maintain seed dormancy during storage, execute seed dormancy release in response to a specified stimulus, and respond quickly to favorable germination conditions when they become available [1]. In fire-prone ecosystems, we defined four dormancy syndromes: Heat-released dormancy, Smoke-released dormancy, Non-fire-released dormancy, Non-dormancy [1]. Fire-released dormancy is a concise term for heat-released and smoke-released dormancy syndromes [1]

Heat-stimulated germination: Heat per se does not stimulate germination but breaks dormancy that allows germination to proceed later, i.e. once suitable hydrothermal conditions are met. Thus, this term refers to the heat-released dormancy syndrome [1].

Secondary dormancy: under some conditions seeds may return to a dormant state following the introduction of earlier or new inhibitory conditions that re-impose seed dormancy. Dormancy cycling may occur when seeds that have previously broken inherent or imposed dormancy return several times to that state (secondary inherent or imposed dormancy) following conditions that annul the current dormancy-release state.

Smoke-stimulated germination: In physiologically dormant seeds, specific smoke chemicals break dormancy and allow germination to proceed. These chemicals may be absorbed by dry seeds but, once the wet season begins, they are more likely to be absorbed dissolved in the soil solution during imbibition so that germination proceeds without further delay. Thus, this term is equivalent to the smoke-released dormancy syndrome [1]. Smoke chemicals may also hasten the rate of germination of non-dormant seeds among some species.

Dormancy-released pathways:  There are at least three ways by which seeds release dormancy [3]:

• Pathway 1 (inherent/imposed dormancy release pathway): First inherent dormancy is broken, but for germination to proceed, imposed dormancy must also be broken at some later stage, that is, when suitable hydrothermal conditions prevail. E.g., the heat of a fire may break (inherent) physical dormancy, but seeds will not germinate until the first significant rainfall events (breaking environmental imposed dormancy).
• Pathway 2 (imposed dormancy release pathway): seeds that lack inherent dormancy (non-dormant) may still encounter an environment that does not meet their germination requirements, so that they remain under imposed dormancy until the appropriate hydrothermal conditions are met.
• Pathway 3 (imposed/inherent dormancy release pathway): first imposed dormancy is broken before inherent (physiological) dormancy release is possible. Some seeds must already be imbibed before the inherent physiological dormancy is released, e.g, before the seed is receptive to light/dark or to cold that breaks inherent dormancy (light/dark-dormancy release or cold-dormancy release).

Bet-hedging vs best-bet strategies: In unpredictable arid ecosystems, seed dormancy is a bet-hedging strategy, as it favours spreading the risk of recruitment failure over many years. In seasonal environments where fires are predictable, seed dormancy is a best-bet strategy as seed dormancy maximizes germination in a single year when conditions are optimal, following the first substantial rains after fire [2] (this best-bet strategy is also termed environmental matching [1]). Serotiny (seeds stored in the canopy seed bank with delayed seed release and dispersal [link]) is usually not considered within the concept of dormancy, but it certainly fits the best-bet strategy [2].

References

[1] Pausas JG. & Lamont BB. 2022. Fire-released seed dormancy – a global synthesis. Biol. Rev. 97: 1612-1639. [doi | pdf | supp. mat. | data (figshare)] (highlighted in plant.org)

[2] Pausas JG, Lamont BB, Keeley JE., Bond, WJ. 2022. Bet-hedging and best-bet strategies shape seed dormancy. New Phytol. 236: 1232-1236. [doi | wiley | pdf]

[3] Lamont BB & Pausas JG 2023. Seed dormancy revisited: dormancy-release pathways and environmental interactions. Funct. Ecol. [doi | pdf | data: dryad | plain language summary]

 

Seed dormancy is a key plant characteristic that occurs among many species worldwide. One mechanism that select for seed dormancy is the bet-hedging strategy. In unpredictable environment (i.e., with high interannual variability) there is a benefit in spreading the germination over a number of years to reduce year-to-year variation in fitness but taking advantage of exceptionally good years for establishment. In those environments, seed dormancy is adaptive; each year there is a small fraction of the seed crop that germinates and the other seeds remain dormant in the soil. Because the environmental conditions of most years are poor, successful establishment only occurs in good (wet) years. Thus bet-hedging selects for seed dormancy and it is a mechanism for living in highly unpredictable environments such as arid ecosystems [1]

There is another environmental setting that also selects for seed dormancy: seasonal (predictable) climate with a dry season during which the vegetation is highly flammable and thus wildfires are frequent (e.g., mediterranean, savanna, warm temperate, and dry boreal ecosystems). In those ecosystems, seed dormancy is adaptive and fire provide both a mechanism for dormancy release (proximate cause) and conditions (postfire) optimal for germination and establishment (low competition, high resource availability, low predation, low pathogen load) that increase fitness and allow maintenance of the population (ultimate cause) [1,2]. Dormant seeds survive the passage of fire and the heat or the chemicals from the combustion (collectively called ‘smoke’ [2,3]) are the stimulus for the seed to recognize a fire gap to germinate. That is, postfire recruitment occurs in a single pulse after fire. Here selection does not favor spreading the risk of recruitment failure over many years (as in the bet-hedging strategy) but, instead, maximizes germination in a single year when conditions are optimal, after fire. We call this strategy the best-bet strategy [1] or environmental matching [2]. This strategy selects for seed dormancy to accumulates seeds in the soil seedbank but also selects for serotiny to accumulate seeds in the canopy seedbank [4]; in both cases, species recruit mostly after fire and not during the interfire period.

There is a further driver that selects for seed dormancy but it does not imply the formation of seed banks (in contrast with bet-hedging and best-bet). Many seeds have acquired seed dormancy to facilitate long-distance dispersal. The clearest example is dispersal by vertebrate frugivores (endozoochory). Frugivores consume the fruit pulp and defaecate or regurgitate the seeds far from the mother plant. This means that seeds need to resist passage through the gut and remain intact until arriving at a new microsite for germination. Thus, seeds of fleshy fruited species typically are dormant, and scarification through the gut releases their dormancy. While bet-hedging spreads germination of seeds over time, this strategy spread the seeds across the space and thus it could be viewed as a spatial bet-hedging strategy.

References

[1] Pausas JG, Lamont BB, Keeley JE., Bond WJ. 2022. Bet-hedging and best-bet strategies shape seed dormancy. New Phytol. [ doi | wiley | pdf]

[2] Pausas JG. & Lamont BB. 2022. Fire-released seed dormancy – a global synthesis. Biol. Rev. 97: 1612-1639. [doi | pdf | supp. mat. | data (figshare)] 

[3] Keeley JE & Pausas JG. 2018. Evolution of ‘smoke’ induced seed germination in pyroendemic plants. South African J. Bot. 115: 251-255. [doi | pdf]  

[4] Lamont BB, Pausas JG, He T, Witkowski, ETF, Hanley ME. 2020. Fire as a selective agent for both serotiny and nonserotiny over space and time. Critical Rev. Pl. Sci. 39:140-172. [doi | pdf | suppl.]

Many plants concentrate their seedling recruitment after the passage of a fire. This is because postfire conditions are especially optimal for germination and establishment of many species as fires create extensive vegetation gaps that have high resource availability, minimal competition, and low pathogen load. Thus we propose that fireprone ecosystems create ideal conditions for the selection of seed dormancy as fire provides a mechanism for dormancy release and optimal conditions for germination [1]. We compiled data from a wide range of fire-related germination experiments for species in different ecosystems across the globe and identified four dormancy syndromes: heat-released (physical) dormancy, smoke-released (physiological) dormancy, non-fire-released dormancy, and non-dormancy. In fireprone ecosystems, fire, in the form of heat and/or chemical by-products (collectively termed ‘smoke’), are the predominant stimuli for dormancy release and subsequent germination, with climate (cold or warm stratification) and light sometimes playing important secondary roles. Fire (heat or smoke)-released dormancy is best expressed where woody vegetation is dense and fires are intense, i.e. in crown-fire ecosystems (e.g., mediterranean-type ecosystems). In grassy fireprone ecosystems (e.g. savannas), where fires are less intense but more frequent, seed dormancy is less common and dormancy release is often not directly related to fire (non-fire-released dormancy). Fire-released dormancy is rare to absent in arid ecosystems and rainforests. Heat-released dormancy can be traced back to fireprone floras in the ‘fiery’ mid-Cretaceous, followed by smoke-released dormancy, with loss of fire-related dormancy among recent events associated with the advent of open savannas and non-fireprone habitats. Anthropogenic influences are now modifying dormancy-release mechanisms, usually decreasing the role of fire. We conclude that contrasting fire regimes are a key driver of the evolution and maintenance of diverse seed dormancy types in many of the world’s natural ecosystems.

References

[1] Pausas J.G. & Lamont B.B. 2022. Fire-released seed dormancy – a global synthesis. Biological Reviews  [doi | pdf | supp. mat. | data (figshare)]