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. 2024 Feb 22;12(1):coae009. doi: 10.1093/conphys/coae009

Same, same, but different: dissimilarities in the hydrothermal germination performance of range-restricted endemics emerge despite microclimatic similarities

Rajapakshe P V G S W Rajapakshe 1,2,3, Sean Tomlinson 4,5,2,✉, Emily P Tudor 6,7, Shane R Turner 8,9, Carole P Elliott 10,11, Wolfgang Lewandrowski 12,13
Editor: Steven Cooke
PMCID: PMC10939308  PMID: 38487732

Tetratheca spp. are herbaceous shrubs notable for their allopatric speciation over short distances in Western Australia. We compared the germination responses of four species of Tetratheca under combined water and temperature stress with the environmental conditions found where these plants grow. Despite similar environments, their germination niches are subtly different.

Keywords: Hydrothermal performance, physiological seed dormancy, seed biology, Tetratheca, threatened species conservation

Abstract

Seed germination responses for most narrow-range endemic species are poorly understood, imperilling their conservation management in the face of warming and drying terrestrial ecosystems. We quantified the realized microclimatic niches and the hydrothermal germination thresholds in four threatened taxa (Tetratheca erubescens, Tetratheca harperi, Tetratheca paynterae subsp. paynterae and Tetratheca aphylla subsp. aphylla) that are restricted to individual Banded Ironstone Formations in Western Australia. While T. aphylla subsp. aphylla largely failed to germinate in our trials, all other species demonstrated extended hydrothermal time accumulation (186–500°C MPa days), cool minimum temperatures (7.8–8.5°C), but broad base water potential thresholds (−2.46 to −5.41 MPa) under which germination occurred. These slow germination dynamics are suggestive of cool and wet winter months, where soil moisture is retained to a greater capacity in local microsites where these species occur, rather than the warmer and drier conditions in the surrounding arid environment. Hydrothermal time-to-event modelling showed that each species occupied unique hydrothermal germination niches, which correspond with the microclimatic differences the species are exposed to. Our results provide a baseline understanding for environmental and germination thresholds that govern the recruitment, and ultimately the population structure and persistence, of these short-range endemic plants. In addition, our results can aid future conservation, as well as restoration actions such as translocation to bolster population numbers and to mitigate against losses due to anthropogenic disturbance and global environmental change.

Introduction

Rare and threatened species are often considered at most risk of decline, especially when their distribution is range-restricted or geographically isolated, and where significant dispersal barriers exist due to their specific environmental requirements such as unusual substrates, stochastic moisture regimes or extreme conditions between refugia (Byrne,et al., 2019). However, short-range endemic species, those that occur only in very specific habitats (Lavergne,et al., 2004), may not be necessarily associated with numerical rarity, nor intrinsic extinction risk (Murray,et al., 2002). Nevertheless, conserving short-range endemic species is challenging where their only known habitat is vulnerable to anthropogenic alteration (Lande,et al., 1999), especially where their capacity to disperse in the face of changing conditions is limited. In situations where whole biogeographic regions and taxonomic groups are defined by species with ranges ~10–100 km2 (Markey,et al., 2012), specialization to cryptic environmental conditions is often assumed to drive speciation and persistence of diverse short-range endemic taxa (Lavergne,et al., 2004). Under such conditions, investigating the link between biogeography and the environmental conditions that are critical to species' persistence can be particularly revealing of population dynamics, species distributions and management initiatives underpinning conservation and restoration (Pironon,et al., 2018). Understanding species’ physiological thresholds is required to inform management actions, particularly in the face of current global change impacts driven by increasing average temperatures and evaporation, and decreasing rainfall (Tomlinson,et al., 2021; Speißer,et al., 2022). Moreover, it is important to quantify the impact of environmental change on species' performance at key stages of the life cycle as population persistence can be constrained by ontogenetic-specific requirements (Warren,et al., 2011; Merow,et al., 2014; Pascual,et al., 2022).

Seed germination is a crucial stage of the life cycle of plants during which new seedlings are highly susceptible to environmental stressors (Larson,and,Funk, 2016; Gremer, 2023). Recruitment strategies, such as ‘bet-hedging’, where average fitness is sacrificed to minimize variance in fitness, and ‘risk avoidance’, where fitness is maximized by preventing germination in unfavourable conditions, can help mediate against seedling losses by optimizing germination to milder, and more favourable periods for seedling establishment (Baskin,and,Baskin, 2014; Duncan,et al., 2019; Gremer, 2023). Ecophysiological constraints on germination therefore represent one of the main contributors to plants’ geographical distributions (Fernández-Pascual,et al., 2017; del,Vecchio,et al., 2020), with success or failure at this critical point profoundly impacting all following life stage transitions (Donohue,et al., 2010).

Temperature and water stress are two major environmental factors that regulate the success of seed germination, particularly in water-limited ecosystems (Duncan,et al., 2019). Both temperature and water stress interact to define a bivariate space within which seeds can germinate upon the alleviation of seed dormancy (Bradford, 2002; Onofri,et al., 2018), but quantitative studies accounting for hydrothermal interactions are often understudied for short-range endemics (Rajapakshe,et al., 2020; Tomlinson,et al., 2021). The hydrothermal time concept establishes thresholds for temperature, as well as moisture availability, that regulate the germination of a seed population over time (Bradford, 2002; Onofri,et al., 2018). Within specific temperature and moisture thresholds, seeds will accumulate hydrothermal time and progress towards germination (Bradford, 2002). The germination limits for temperature are defined between the minimum (Tb, base) and maximum (Tc, ceiling) temperatures, and the base water potential threshold (Ψb) for moisture availability (Bradford, 2002). These thresholds are defined by both the dormancy state of the seeds and the specific physiological tolerance to both temperature and water stress for any given species (Alvarado,and,Bradford, 2002; Baskin,and,Baskin, 2014; Lewandrowski,et al., 2017). Quantifying the hydrothermal germination niche, the hygric and thermal requirements necessary for seed germination, can provide important insights into the roles of these environmental variables in structuring populations and recruitment events, as well as shaping biogeographical patterns of rarity and endemism; critical information when planning future conservation actions such as translocation or assisted migration (Rajapakshe,et al., 2020).

Banded ironstone formations (BIFs) are widely distributed in the semi-arid and arid Yilgarn region of Western Australia, characterized by shallow, skeletal soils, emergent rock surfaces and often substantial topographical variability at small spatial scales (Gibson,et al., 2012). The seeds of range-restricted taxa living on shallow-soil habitats such as outcrop surfaces can have narrower hydrothermal germination norms (i.e. germinate under a narrower range of hygric and/or thermal conditions) compared to widely occurring sympatric species (Donohue,et al., 2010). However, there is a scarcity of data on how closely related short-range endemic species vary in their adaptation to hydrothermal stress, especially where non-overlapping distributions can be quite close together (<50 km) but are separated by different landforms and vegetation communities (Gibson,et al., 2010; Yates,et al., 2011; Elliott,et al., 2019), essentially forming isolated islands of endemism (Byrne,et al., 2019).

Several studies have highlighted the importance of assessing the role of different environmental variables on the germination response of range-restricted taxa and the implications for their distributional extent (Vincent,et al., 2015; Cochrane, 2020). We quantified the hydrothermal germination niches of a guild of closely related Tetratheca Sm. species, each highly restricted (area of occupancy <50km2) to geographically separate BIF ranges. Though the species occur on isolated, yet adjacent ranges (Fig. 1), we hypothesized that due to the highly localized range of each species, each species may display subtle differences in their hydrothermal germination envelope that reflects subtle site-specific differences in their microclimate envelope. We also expected the environmental factors most strongly associated with each species’ biogeography to reflect hydrothermal germination niches that are more aligned with cooler and reliably wetter germination windows that reflect the unique capacity for BIFs to retain water for longer periods compared to the surrounding landscape (Byrne,et al., 2019).

Figure 1.

Figure 1

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Distributional extents of the Tetratheca spp. studied here all fall within an area ~20 × 20 km, located 370 km north-east of Perth, Western Australia (a). The study region is characterized by relatively uniform soil temperatures (b, c) and soil water potentials (d, e). Even in the coolest and wettest periods (b, d) soils in the region are relatively warm and very dry. The points on the maps (b–e) indicate the known populations of our four study species T. paynterae subsp. paynterae, T. harperi, T. aphylla subsp. aphylla and T. erubescens (north to south).

Materials and Methods

Study species, seed collection and processing

The distributions of Tetratheca Sm. (Elaeocarpaceae) species in the semi-arid and arid regions of Western Australia (WA) represents an intriguing display of short-range endemism and diversification, where a number of unique species are confined to rocky habitats for reasons that are not obvious (Di,Virgilio,et al., 2018; Byrne,et al., 2019). Tetratheca species in the region very rarely inhabit more than one outcrop (Yates,et al., 2011), and neighbouring outcrops often support different species that have been separated for substantial periods of time (Butcher,et al., 2007).

We compared four species of Tetratheca that are geographically restricted to BIF habitats in the Yilgarn region of WA in this study (Fig. 1, Supplementary Table S1). The distribution of each species is restricted to one of four BIF ranges (Fig. 1) that are within ~100 km of each other, though separated by different edaphic conditions and floristic communities (Butcher,et al., 2007; Gibson,et al., 2010). Tetratheca aphylla F.Muell. subsp. aphylla inhabits the relatively deep skeletal soils of lower slopes, hill crests and cliffs of the Helena and Aurora Range (Yates,et al., 2011). Tetratheca erubescens J.P.Bull is found in rock fissures and crevices associated with cliffs, hill crests and steep slopes of the Koolyanobbing Range (Krauss,and,Anthony, 2019). Tetratheca harperi F.Muell. inhabits hill crests, cliffs and cliff slopes of the Mt. Jackson Range (Yates,et al., 2011). Tetratheca paynterae Alford subsp. paynterae is restricted to fissures on steep cliffs and tors of the Windarling Range (Ladd,et al., 2019). All four taxa are of high conservation concern and have been gazetted as threatened flora in Western Australia (Herbarium, 1998).

Seeds were harvested from wild populations of all four species in 2019 (license numbers SW019800 and DRF7789) and once collected were cleaned, processed (Supplementary Table S2) and stored at 15°C and 15% relative humidity (controlled environment room) at the Kings Park Science laboratories, Western Australia for 15 months. These conditions both enhance seed longevity and suppress physiological dormancy loss, maintaining the physiological state of the seeds, including their dormancy status, for several years following collection (Turner,et al., 2009; Turner,et al., 2013). Prior to experimentation, seeds were assessed by X-Ray (MX-20 digital X-Ray cabinet, Faxitron, USA), to identify filled seeds. Filled seeds contained fully formed embryos and endosperm, with these anatomical features identified by the presence of uniform white shading of internal tissues. Seeds deviating from this visual appearance were determined to be non-viable and discarded (Erickson,and,Merritt, 2016).

Microclimatic conditions of seed sources

The hydrothermal correlates of the realized niche of each study species were quantified using species occurrence data sourced from records maintained by the Herbarium of Western Australia (Herbarium, 1998), supplemented by extensive unpublished surveys by stakeholders from the mineral extraction industry. These known locations were intersected with spatial data describing elevation; aspect and slope (Gallant,et al., 2011; Gallant,and,Austin, 2012a; Gallant,and,Austin, 2012b); edaphic data describing clay, sand and silt percentage composition Viscarra,Rossel,et al.(2018a, 2018b, 2018c) and soil depth interpolated from national soil data provided by the Australian Collaborative Land Evaluation Program (ACLEP), endorsed through the National Committee on Soil and Terrain (NCST; www.clw.csiro.au/aclep). We incorporated these spatial data into soil types using a soil textural triangle (Gerakis,et al., 1999) to inform the ‘micro_global’ algorithm in the ‘NicheMapR’ package (Kearney,and,Porter, 2017) to estimate microclimatic details that are most relevant to seed germination (Tomlinson,et al., 2020). These specific parameters were chosen to capture the most extreme hydrothermal dynamics experienced by each species, where high water availability at the warmest temperatures may offset thermal stress, and warmer temperatures in the wettest months may promote more rapid germination, given that winter is relatively cold in this region (Supplementary Fig. S1). Higher average soil water availability was thought to represent a less challenging germination environment generally. These data were then averaged between sunrise and sunset at each location to generate daily temperatures and water stress levels 2.5 cm below the soil surface. We used these microclimate estimates to model a 3D environmental niche model built around the annual average soil water potential (SWP), the SWP in the warmest quarter (hottest SWP) and the soil temperature in the wettest quarter (wettest temperature) for each species separately using a Monte Carlo approach, using the ‘hypervolume’ function of the ‘hypervolume’ R package (Blonder,et al., 2018). The construction function for the hypervolume was a Gaussian kernel density estimation (KDE), where the bandwidth was estimated using a Silverman estimator. The resulting 3D hypervolumes (Fig. 2) were used to define a range of experimental hydrothermal regimes. Hypervolumes of each of the four species were also compared in n-dimensional space to assess overlap using the ‘hypervolume_overlap_statistics’ function of the ‘hypervolume’ package (Blonder,et al., 2018). The findings of this comparison were used to guide our expectations of likely species hydrothermal performance, in that species with high microclimatic overlap should have highly congruent population performance means (Carscadden,et al., 2020).

Figure 2.

Figure 2

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Microclimate hypervolumes constructed using the hydrothermal conditions (average temperature of the wettest quarter; annual average soil water potential; soil water potential of the warmest quarter) of the known occurrence locations for each Tetratheca species. The combined hypervolume (a) shows substantial overlap between all four species. Individual hypervolumes (b–e) show more clearly the niche space occupied by each species relative to the constraining parameters. The black points represent the conditions characterizing the known locations of all species combined. The scales on each axis are Euclidean distances of centred and scaled environmental variables.

Germination requirements and hydrothermal thresholds

Prior to incubation, seeds were surface sterilized with a solution of 2% (w/v) calcium hypochlorite (Ca[OCl]2) infused with detergent (Tween 80) for 30 minutes under vacuum (−70 kPa), followed by rinsing with sterile deionized water three times. Seeds were placed inside 90-mm plastic Petri dishes that were lined with moist (9 ml of water per Petri dish) 84-mm germination papers (Advantec, Dublin, CA, USA). The Petri dishes were sealed with plastic wrap to prevent desiccation and covered with aluminium foil to minimize the impact of light, which has a potential confounding effect on germination (Bell, 1994; Ruiz-Talonia,et al., 2018). Before commencing hydrothermal germination experiments, seeds were exposed to a warm stratification treatment that, based on previous research, was assumed to be appropriate for dormancy alleviation in all test species (Elliott,et al., 2019). These seeds were stratified at 30°C for 28 days, then removed from Petri dishes and dried at 15°C and 15% RH (cool dry storage) for 1 week prior to starting the hydrothermal experiments. A random subsample of seeds was also immediately moved from 30°C to 15°C while maintaining their hydration status to confirm the effectiveness of this stratification approach. Seeds were maintained for 4 weeks at 15°C to assess germination after the application of the warm stratification treatment (Supplementary Table S2).

The germination response of seeds to hydrothermal stress was assessed with three replicates of 15 seeds per species, which were incubated at one of 30 hydrothermal stress regimes (water stress levels of 0.0, −0.2, −0.4, −0.6, −0.8 and − 1.2 MPa at temperatures of 10, 15, 20, 22 and 25°C). These hydrothermal regimes encompass a broad range of the hydrothermal conditions constructed for the habitats of the test species (see above; Fig. 2). Seeds were placed on 84-mm germination paper (Advantec, Dublin, CA, USA) moistened with either distilled water or polyethylene glycol 8000 (PEG) solution (of different concentrations) to generate the range of water potentials outlined above for each incubation temperature (Michel, 1983). These solutions had 2% (v/v) PPM (Plant Preservation Mixture, Austratec Pty Ltd, Bayswater, Victoria Australia) added to minimize microbial contamination during stratification and incubation treatments. Nine millilitres of this solution was added per 90-mm Petri dish for all species, except Petri dishes containing T. aphylla subsp. aphylla. These were instead irrigated with the addition of 1 μM karrikinolide (KAR1—Flematti,et al.(2004); Chiwocha,et al.(2009)) for the duration of the incubation period as preliminary data found an improved germination response for this species following the application of KAR1 (Supplementary Table S2). All Petri dishes were sealed with plastic wrap and aluminium foil. During the incubation period, iButton data loggers (Maxim Integrated™, San Jose, USA) were placed in the middle of each set of Petri dishes, which were subjected to the same treatment regime to record the temperature that seeds were exposed to within each incubator while the germination trial was underway (Supplementary Table S3). Germination was identified when the radicle emerged >2 mm from the testa and was scored 3 days per week for 56 days.

Statistical analysis

Germination modelling

The germination responses of each species, except T. aphylla subsp. aphylla, which failed to germinate beyond 27% in any given treatment, were characterized by a hydrothermal time-to-event (HTTE) model (Onofri,et al.(2018)). HTTE models are well-grounded in physiological theory and work on the assumption that germination does not occur outside certain temperature or water stress thresholds and parameterize the hydrothermal germination niche by a function of time (Onofri,et al.(2018)). Preliminary assessments of a global model compared five defined HTTE models with selection based on graphical inspection of goodness of fit and Akaike’s Information Criterion (AIC; Akaike,(1974)). The model selected was a six-parameter log-logistic cumulative distribution function (HTTEM; Mesgaran,et al., 2017, Onofri,et al., 2018, Onofri,et al., 2022), defined as:

graphic file with name DmEquation1.gif

With three distinct sub-models:

graphic file with name DmEquation2.gif
graphic file with name DmEquation3.gif
graphic file with name DmEquation4.gif

Where germination proportion is dependent upon time (t), temperature (T) and base water potential (Ψ); the model is computed by the reciprocal of time to the 50th percentile of the germinated fraction (Inline graphic) GR50HTTE, maximum germination proportion (G; while accounting for possibility that PmaxHTTE may not reach 1 under any condition); median base water potential limiting to germination in the seed lot (Ψb); variability of median base water potential (Inline graphic); base or minimum temperature for germination (Tb); hydrothermal time constant (θHTT; MPa °C days; the hydrothermal time required for germination in the seed population), slope of the linear increase in Ψb when temperature increases (Kt); and the slope of the germination curve in the FHTTE distribution (b). The model is only defined under the conditions between which germination occurs (i.e. between Tb and Tc; maximum temperature for germination) and is equal to 0 for temperatures TInline graphicTb or TInline graphicTc, and water potentials Inline graphic < Inline graphic. Models were fitted using the drcte function of the ‘drcte’ statistical package (Onofri,et al., 2022) with hydrothermal time to event model coded in the ‘drcSeedGerm’ package (Onofri,et al., 2022) using the R statistical environment (version 4.2.3) and RStudio Version 2023.03.0 (R,Development,Core,Team, 2022).

After global model selection, we constructed a species-specific model, and determined if the delineation identified responses that were significantly different to the ‘global model’ via an F-test using the anova function in the ‘stats’ package (R,Development,Core,Team, 2022). Post hoc comparisons of parameter estimates were conducted with the compParm function in the ‘drc’ package (Ritz,and,Streibig, 2012) with significance established at P < 0.05. However, we do not report on comparisons for b, as it is a shape parameter that is regarded as independent from the environmental covariates, or Inline graphic, due to insignificant fit and parameterization in the global model. After the hydrothermal time distributions were modelled, using equation 1.3, hydrothermal germination responses were plotted at 15, 30 and 60 days to quantify the changes in germination behaviour for each species. Maximum germination proportions (Gmax) and thresholds for Tb and Tc, as well as Ψb were derived from the predictions at each increment, defining the breadth of the hydrothermal germination niche as it changes over time.

Results

Niche overlap in microclimatic conditions

The highest degree of microclimatic niche overlap (70%) was between T. paynterae subsp. paynterae and T. aphylla subsp. aphylla and between T. paynterae subsp. paynterae and T. harperi, with all four species sharing at least 50% of their 3D microclimatic niche space with each other (Table 1; Fig. 2). The percentage of unique space a species had was complex, as different species nested within each other’s realized niches in different ways. The main patterns were that T. erubescens consistently had the lowest percentage of unique space (11–23%) compared to the other three (i.e. had a realized niche that mostly nested within the other three). This was followed by T. aphylla subsp. aphylla (10–18%) compared to T. paynterae subsp. paynterae and T. harperi, except when compared to T. erubescens. Compared to T. erubescens, T. aphylla subsp. aphylla had a higher percentage (45%) of unique space that mainly related to having a broader envelope of soil temperature in the wettest quarter (wettest temperature), where the known occurrence locations are found. Leaving T. paynterae subsp. paynterae and T. harperi to both retain ~30% of the combined niche space uniquely to themselves (Table 1), that related to also having a broader microclimatic envelope across all three hydrothermal conditions, albeit both dominating the opposite ends of this envelope. Tetratheca harperi uniquely occupied microclimates characterized by higher temperatures than any other species, while T. paynterae subsp. paynterae occupied microclimates characterized by the coolest and wettest conditions (Fig. 2).

Table 1.

Patterns of niche overlap between pairs of Tetratheca species. The Sorenson overlap indicates the proportion of the combined niche space that the two species share, while the Fraction Unique columns indicate what proportion of that combined niche space is occupied by only the indicated species (Sp. 1 or Sp. 2)

Species 1 Species 2 Sorensen overlap Fraction unique (Sp. 1) Fraction unique (Sp. 2)
T. aphylla T. erubescens 0.64 0.45 0.23
T. harperi 0.66 0.18 0.44
T. paynterae 0.70 0.10 0.43
T. harperi 0.56 0.15 0.58
T. erubescens T. paynterae 0.55 0.11 0.60
T. harperi T. paynterae 0.70 0.27 0.33
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Hydrothermal time-to-event germination modelling

The global HTTE model resolved significant fits for each parameter (P < 0.001), excluding Inline graphic. As such, we conducted no further interrogation or post hoc comparison of Inline graphic. The global model had an AIC index of 16 052.54 and log-likelihood of −2153.27. The species-specific model significantly improved model parsimony and reduced the AIC to 15 769.0 and log-likelihood of −2025.75 (F14,5859 = 26.34, P < 0.001), indicating species-level differences in hydrothermal performance.

Species-level differences in hydrothermal performance occurred for all parameters excluding Inline graphic and b (Table 2). The projected mean maximum germination (Gmax) proportion was significantly lower for T. paynterae subsp. paynterae (0.21 ± 0.03) than T. erubescens (0.64 ± 0.16; t = 2.18; P = 0.02) or T. harperi (0.56 ± 0.03; t = 3.15; P = 0.002). However, T. paynterae subsp. paynterae required significantly less hydrothermal time (186.8 ± 34.1 MPa °C days) to reach maximum germination compared to T. erubescens (421.4 ± 40.5 MPa °C days; t = 2.25; P = 0.006) or T. harperi (499.9 ± 46.3 MPa °C days; t = 3.05; P = 0.002). Base temperature for germination (Tb) was significantly lower in T. harperi (7.82 ± 0.22°C) compared to T. erubescens (8.50 ± 0.17°C; t = 2.21; P = 0.027), but statistically indistinguishable from T. paynterae subsp. paynterae (8.51 ± 0.45°C; t = −1.45; P = 0.145). There were significant differences between Kt parameter estimates only between T. erubescens (0.34 ± 0.04) and T. paynterae subsp. paynterae (0.16 ± 0.02; t = 3.01; P = 0.002). Lastly, median base water potential was significantly less negative (i.e. requires more water availability) in T. paynterae subsp. paynterae (−2.47 ± 0.18 MPa) compared to both T. erubescens (−5.41 ± 0.57 MPa; t = 4.19; P < 0.001) and T. harperi (−4.61 ± 0.54 MPa; t = 3.34; P < 0.001).

Table 2.

Hydrothermal time parameters of T. erubescens, T. harperi and T. paynterae subsp. paynterae. Population differences for HTTE-parameters are summarized with the F-value, and specific parameter comparisons summarized with letters in superscript (at P < 0.05). Tetratheca aphylla subsp. aphylla did not germinate in this study

Parameter T. erubescens T. harperi T. paynterae
G 0.65 ± 0.16 a 0.56 ± 0.03 a 0.21 ± 0.04 b
b [MPa] −5.41 ± 0.57a −4.61 ± 0.54 a −2.46 ± 0.19 b
Kt 0.34 ± 0.05 a −0.24 ± 0.04 ab −0.16 ± 0.02 b
Tb [°C] 8.51 ± 0.45 a 7.82 ± 0.23 b 8.51 ± 0.45 ab
σ 1.21 ± 0.76 a 0.14 ± 0.34 a 0.09 ± 0.12 b
θHTT [MPa °C days] 421 ± 40.5 a 500 ± 46.3 b 186 ± 34.1 b
b 4.99 ± 0.38 a 6.81 ± 0.57 a 3.78 ± 0.61 b
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Population difference F-value: 26.34***

Hydrothermal threshold variation over a 60-day window

Maximum germination (Gmax) proportion after a 15-day window was 0.12 in T. erubescens, in contrast to 0.04 and 0.05 in T. harperi, and T. paynterae subsp. paynterae, respectively. These proportions increased progressively in all species, although variation was characterized by overall lower germination performance in T. paynterae subsp. paynterae (Gmax < 0.21, after 60 days), in contrast to T. erubescens and T. harperi (Gmax > 0.5 after 60 days). The lower germination performance of T. paynterae subsp. paynterae was also matched by the narrowest hydrothermal ranges for germination in T. paynterae subsp. paynterae (see Tb, Tc and Ψb, Fig. 3). While all species were constrained to germinate between 10 and 25°C, T. harperi had the broadest range over time (Fig. 3). There was progressive broadening of Ψb thresholds in all species, with T. erubescens characterized by the lowest Ψb over the time-course (refer to Fig. 3 for all Tb, Tc and Ψb parameter estimates).

Figure 3.

Figure 3

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Modelled hydrothermal germination windows of T. erubescens, T. harperi and T. paynterae subsp. paynterae for 15, 30 and 60 days across a simulated temperature, water potential gradient. Colour scale bar represents germination proportion.

Discussion

In natural environments, successful seedling establishment is reliant on the duration of the window of opportunity for germination (Gremer, 2023). Hydrothermal stress is a major selective pressure that restricts that window of opportunity, particularly in semi-arid ecosystems where water availability can be extremely variable from year to year due to the dynamic nature of these extreme environments (Huang,et al., 2016). To our knowledge, our results are the first to characterize the hydrothermal germination niche for Tetratheca species, using a contemporary HTTE modelling approach (Onofri,et al., 2018). The cool thermal thresholds quantified from our hydrothermal time modelling are consistent with reports in the region (Dalziell,et al., 2022) that all four species tend to germinate during the cooler winter months, and the HTTE models explained slowed germination, along with a gradual widening of hydrothermal thresholds over a 60-day germination window. Despite substantial overlap in the realized microclimatic niche estimated from known occurrence locations, subtle interspecific differences were evident in the hydrothermal niche consistent with the specific biogeography of each species.

Microclimatic niche and germination strategy

The high degree of overlap between the microclimatic niches and the hydrothermal optima of the Tetratheca species (Fig. 2, Fig. 3) suggests that similar selection pressures have optimized their hydrothermal niches, despite their geographic and genetic isolation (Byrne,et al., 2019). The locations where these species occur are less stressful at critical times by comparison to the surrounding landscape, with SWPs higher than −1.2 MPa and soil temperatures between 5 and 25°C occur during a potential germination window over the winter rainfall period for the region (Supplementary Figure S1). As demonstrated by the HTTE models, the three modelled Tetratheca species require long periods of hydrothermal time accumulation to germinate, with germination constrained to comparatively cooler and wetter conditions (Table 2; Fig. 3).

Despite the narrow temperature range (10–25°C), all species included in the analysis demonstrated remarkably wide base water potentials for germination, suggesting that a proportion of the seed population may be capable of germinating into significant water stress. Collectively, these observations suggest that different outcrop-endemic Tetratheca species may be differently adapted to cope with limited water availability. This interpretation is at odds with that which may be drawn when considering the high degrees of microclimatic niche overlap between the species (see above). However, despite the similarities present in the microclimatic niche, each species inhabits some unique microclimatic niche space, which correspond with their dissimilarities in hydrothermal niches. For example, T. erubescens inhabits the core of the microclimate envelope shared by all species, defined by moderately broad thermal conditions and SWPs (Fig. 2), and germinates relatively well across a wide combination of water stress and thermal stress (Fig. 3). It is also the youngest species in a phylogenetic sense (Byrne,et al., 2019), and thus may not have specialized to microclimatic conditions unique to Koolyanobbing Range. Where T. harperi occurs uniquely, this microclimatic space is principally defined by warmer temperatures (Fig. 2), and the species has the broadest tolerance to thermal stress of any of the species studied (Fig. 3). Finally, T. paynterae subsp. paynterae occurs more in cooler and wetter microclimate space than any of the other species (Fig. 2) and has the lowest germination success of the three species that we characterized here, and only at cooler temperatures and lower water stress compared to either T. harperi or T. erubescens. The more limited germination success could be attributed to seeds of T. paynterae subsp. paynterae that remained in a conditional dormancy state at the time of the germination study, which explains the limited and narrow optimal conditions for germination, in contrast to the other species (Baskin,and,Baskin, 2014).

By capturing the time element of the germination window, we have shown differences in how divergent species respond to ephemeral conditions. The modelled Tetratheca species require hydrothermal time accumulation between 186 and 500 MPa °C days to complete germination of the seed population, which could be attributed to dormant proportions in the seed cohort (Baskin,and,Baskin, 2014), or being intrinsically slow-germinating species. Slow germination has been reported in many taxa endemic to mesic habitats of Western Australia (Vincent,et al., 2015; Cochrane, 2020; Dalziell,et al., 2022). However, slow germination is potentially risky as it could compromise seedling survival in microhabitats if they fail to retain moisture for a sufficient period following rainfall episodes. This supports contentions that the study species may have contracted to microhabitats on outcrops that can retain high soil moisture for sufficient time to support germination beyond what would normally be expected in surrounding environments (Gibson,et al., 2010; Yates,et al., 2011). The extended hydrothermal germination requirement may be a common characteristic of floristic endemism in the inselberg communities of the Yilgarn region (Gibson,et al., 2012), and likely influences the biogeography of other BIF-restricted species such as Ricinocarpos brevis, Darwinia masonii and Lepidosperma gibsonii (Byrne,et al., 2008). While the hydrothermal requirements for seed germination are largely unexplored for many BIF-restricted species, understanding these dynamics could provide critical insight into the constraints and requirements driving recruitment events in these floristically diverse ecosystems.

Seed dormancy and ‘bet-hedging’

The specialization of Tetratheca species to slow germination in relatively cool and wet conditions is also likely enhanced by the presence of physiological dormancy, as seeds are cued for germination via warm stratification as soil temperatures gradually drop, leading into the cooler relatively wetter winter season (Turner,et al., 2006; Just,et al., 2023). Previous studies on several BIF-endemic species suggest that in physiologically dormant, range-restricted species, the windows of opportunities for seedling establishment are rare, unpredictable and perhaps only occur every few years (Yates,et al., 2011; Elliott,et al., 2019). Although not an essential trait in the formation of a soil seedbank (Gioria,et al., 2020), dormant seeds are likely to persist in the soil seedbank while conditions are not conducive to germination and seeding recruitment, and seed dormancy can leave ungerminated or dormant seeds exposed to long periods between recruitment events (Long,et al., 2015; Miller,et al., 2019). Indeed, warm stratification is a relatively uncommon dormancy release treatment (Just,et al., 2023), allowing seeds to retain a slow germination pattern in cool moist conditions as gradual dormancy release occurs in response to an initial warmer, moist soil environment. This gradual drop in soil temperature acts as an initial environmental filter to cue seeds for seasonal germination, rather than opportunistic, aseasonal germination (Vincent,et al., 2015). As such, any given hydrothermal window could stimulate the germination of only a proportion of the available soil seed bank, minimizing the risk of unsuccessful germination in dynamic and unpredictable environments. While we cannot conclusively demonstrate this for the Tetratheca species studied here, other short-range endemic species in the region, such as Darwinia masonii and Lepidosperma gibsonii possess physiological seed dormancy and form long-lived soil seed banks (Elliott,et al., 2019; Miller,et al., 2019). The mechanisms underpinning the alleviation of seed dormancy under natural conditions are often difficult to unravel (Merritt,et al., 2007), and additional research is necessary to understand the nuances of dormancy loss and germination stimulation in these species more broadly.

Limitations to model interpretations

While the applied dormancy alleviation treatments resulted in varied degrees of germination success across the studied species, the low germination rates seen for T. aphylla subsp. aphylla may be a result of physiological dormancy that was not adequately overcome. This suggests that an extended stratification period may be required, in addition to the stimulus applied (KAR1). Moreover, the germination responses here may still encapsulate some component of seed dormancy, which would account for the generally much lower germination success that we also found for T. paynterae subsp. paynterae across all hydrothermal conditions (Fig. 3). In general, exposure to KAR1 enhanced the germination success of these species, potentially indicating that exposure to smoke represents a critical environmental stimulus that defines the germination requirements of those taxa, particularly under conditions where disturbance events (e.g. fire) may occur (Turner,et al., 2018). As such, dormancy alleviation and the hydrothermal niche require further attention to provide a comprehensive understanding of the drivers of in situ recruitment beyond the fundamental microclimatic elements that we have reported here.

The capacity of range-restricted taxa to persist in the face of changing conditions is dependent on the influence of interacting niche dimensions on population demographics (Pironon,et al., 2018). Our study captured the performance norms of seeds collected under current climatic conditions but offers little direct insight into phenotypic flexibility in these norms. The extent to which climate change can affect the physiological limits and optima of range-restricted taxa in terms of altered rainfall patterns and temperature, as well as dormancy cycling, must also be quantified (Walck,et al., 2011; Cochrane,et al., 2014; Cochrane, 2017). However, a greater suite of species should be compared including both range-restricted taxa as well as those with wide distributions to gain useful insights into how hydrothermal germination niche affects patterns of species distribution. Collectively, this can help determine whether range-restricted species display attributes not typically observed with more broadly occurring sympatric species (Byrne, 2019).

Conservation implications

This study highlights the significant role of hydrothermal stress on germination responses that are likely to influence population dynamics and distribution patterns of BIF specialist Tetratheca species. The high degree of overlap between the microclimatic niches, coupled with existing phylogenetic evidence, supports suggestions that these are allopatric species (i.e. localized speciation on extended time frames; Byrne,et al.(2019)) that have persisted on localized outcrops due to the relatively milder conditions they support compared to the surrounding semi-arid landscapes (Byrne,et al., 2018). The short-range endemic Tetratheca species are associated with such habitats (Butcher,et al., 2007; Byrne,et al., 2018), potentially because of a conserved germination strategy that is more aligned with cooler and reliably wetter regions in southwest Western Australia. This conserved germination strategy suggests that Tetratheca species endemic to BIFs may be more susceptible to environmental changes as the climate further warms and dries. Furthermore, other Tetratheca species endemic to granitic, sandstone and ironstone inselbergs throughout WA have unknown germination requirements, leaving uncertainties as to how they may respond to the unpredictable changes of climate likely to eventuate throughout the arid ecosystems of Australia (Lioubimtseva, 2004).

BIFs in the region are subject to extensive mineral exploitation (Gibson,et al., 2010). Management actions in response to mining disturbance often involve mitigation translocations (sensuBradley,et al.(2020)) to establish insurance populations. Underpinning these approaches is the recognition that there is often ‘uninhabited’ niche space in the distribution of short-range endemic flora (Byrne,et al., 2019), and that rapidly identifying this provides suitable recipient locations for translocated individuals. The data that we report here suggest that, while the Tetratheca species show high overlap in the microclimatic niches in which they occur, subtle interspecific differences in their germination performance norms are consistent with regions of the microclimatic niche that are uniquely occupied by each species. From the perspective of planning and executing mitigation translocations, while vacant habitats may appear suitable to Tetratheca spp. in a broad sense, the mechanistic drivers underpinning this vacancy can be complex, subtle and species-specific. Thus, introducing individuals into habitats without capturing these subtleties may result in suboptimal population performance in terms of form, function and fitness, thereby reducing long-term translocation success. Consequently, we believe that greater success in mitigation translocations is likely to result from greater investment in unravelling these critical drivers.

Supplementary Material

Web_Material_coae009
web_material_coae009.zip (572.9KB, zip)

Acknowledgments

The authors acknowledge the Wadjuk people of the Noongar nation, traditional owners of the land on which this work was undertaken and pay our respects to Elders past, present and emerging. We thank Kings Park Science for use of their equipment and facilities and Mineral Resources Ltd for providing site access during seed collections.

Contributor Information

Rajapakshe P V G S W Rajapakshe, ARC Centre for Mine Site Restoration, Curtin University, Bentley, 6102, Australia; School of Molecular and Life Sciences, Curtin University, Bentley, 6102, Australia; Kings Park Science, Department of Biodiversity, Conservation and Attractions, Kings Park, 6005, Australia.

Sean Tomlinson, School of Molecular and Life Sciences, Curtin University, Bentley, 6102, Australia; School of Biological Sciences, University of Adelaide, Adelaide, 5000, Australia.

Emily P Tudor, Kings Park Science, Department of Biodiversity, Conservation and Attractions, Kings Park, 6005, Australia; School of Biological Sciences, University of Western Australia, Crawley, 6009, Australia.

Shane R Turner, ARC Centre for Mine Site Restoration, Curtin University, Bentley, 6102, Australia; School of Molecular and Life Sciences, Curtin University, Bentley, 6102, Australia.

Carole P Elliott, Kings Park Science, Department of Biodiversity, Conservation and Attractions, Kings Park, 6005, Australia; School of Biological Sciences, University of Western Australia, Crawley, 6009, Australia.

Wolfgang Lewandrowski, Kings Park Science, Department of Biodiversity, Conservation and Attractions, Kings Park, 6005, Australia; School of Biological Sciences, University of Western Australia, Crawley, 6009, Australia.

Author Contributions

Conceptualization: R.P.V.G.S.W.R., S.R.T. and S.T. Methodology: R.P.V.G.S.W.R., S.R.T., S.T., C.P.E. and W.L. Resources: S.T., E.P.T., C.P.E. and W.L.. Investigation: R.P.V.G.S.W.R.. Data curation: R.P.V.G.S.W.R. Formal analysis: R.P.V.G.S.W.R., E.P.T., S.T. and W.L. Visualization: E.P.T. and S.T. Writing – original draft: R.P.V.G.S.W.R. Writing – review & editing: All authors. Project administration: S.T., S.R.T., C.P.E. and W.L. Supervision: S.T. and. S.R.T.

Conflicts of Interest

The authors have no conflicts of interest to declare.

Funding

This research was funded under the Australian Research Council Industrial Transformation Training Centre for Mine Site Restoration (ICI150100041) and the 2021 Curtin University Publication Grant. Open access publishing facilitated by Curtin University, as part of the Council of Australian University Librarians publication agreement.

Data Availability

The raw data underpinning the germination trials are provided as supplemental material. The location data underpinning the biogeographical analyses cannot be released for legislative reasons protecting rare species in Western Australia.

Supplementary Material

Supplementary material is available at Conservation Physiology online.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Web_Material_coae009
web_material_coae009.zip (572.9KB, zip)

Data Availability Statement

The raw data underpinning the germination trials are provided as supplemental material. The location data underpinning the biogeographical analyses cannot be released for legislative reasons protecting rare species in Western Australia.

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