Elsevier

Ecological Indicators

Volume 117, October 2020, 106517
Ecological Indicators

Ecological drivers of plant life-history traits: Assessment of seed mass and germination variation using climate cues and nitrogen resources in conifers

https://doi.org/10.1016/j.ecolind.2020.106517Get rights and content

Highlights

  • Climates in prior-years and N were key to seed mass; crop-year climate important to germination.

  • Climate variables were inversely correlated with the same trait between species.

  • Ecological trade-offs differed in precipitation-based variables.

  • Both traits become spatially homogenous towards intermediate-low levels under climate change.

  • Such tendencies cascade to affect plant fitness, community assemblies and population dynamics.

Abstract

Understanding plant-environment interactions is an important link to studying the impact of climate change on community assemblies and population dynamics, especially for tree species that define the ecosystem they occupy. Based on seed mass and germination data of three conifers over six decades (1955–2015) across British Columbia, Canada, we performed pairwise correlation analysis between focal traits and the environment (climates in crop year and four prior-years and nitrogen resources). Using key environmental correlates, we constructed a linear mixed model to assess both traits and performed linear discrimination analysis to predict trait tendencies under future climate scenarios. Findings showed that seed mass variation was considerably ascribed to nitrogen deposition and climate in prior-years preceding seed crop. Climate in crop year had higher correlations with seed germination than in prior-years, but germination-climate correlations were much weaker than seed mass-climate counterparts. Both seed mass and germination had high correlations with temperature-based climate variables, such as evapotranspiration, degree-days above 5 °C (positive) and below 18 °C (negative); however, some climate variables had high but opposite correlations with the same trait between species. Across the study region, ecological trade-offs between species were similar for the aspect of temperature but differed between precipitation-based variables, indicating the important role of precipitation in ecological constraints. Finally, we predicted that climate change would result in more spatially homogeneous traits and make them shift towards intermediate or low levels. These results have important implications for the natural seedling regeneration of forest trees under climate change, which potentially cascades to influence trait expression, plant fitness and population persistence.

Introduction

In the face of ongoing rapid climate change, many species are expected to respond by tracking ecological niche through their historical climate envelopes. Most forecasts of trait redistribution under climate change mainly consider trait-climate relationships through time (Angert et al., 2011, Banta et al., 2012, Wang et al., 2006). In practice, assisted migration has been proposed as part of regular reforestation programs and conservation efforts (Pedlar et al., 2012, Vitt et al., 2009). To date, studies on assisted migration in forest trees have focused on traits of economic values, such as growth, wood properties, and cold-hardiness [e.g., (Aitken and Bemmels, 2016, Schreiber et al., 2013)]. However, shifts in environmental conditions aroused by climate change can alter the availability and reliability of environmental cues to life-history timing. Species can increase persistence by altering key life-history events, as shown by shifts to earlier spring growth in deciduous trees (Chmielewski and Rotzer, 2001). On the other hand, insufficient seedling recruitment (i.e., extinction debt; (Hanski and Ovaskainen, 2002)) likely begets forest decline in many forest tree species under climate change (Talluto et al., 2017). Hence, extending the consideration of assisted migration to life-history traits would improve understanding of the multiple factors that influence adaptation and foster conservation strategies based on holistic scenarios.

Life-history traits, known as fitness components, are related to the timing and success of development, reproduction, and senescence throughout the plant life cycle (Stearns, 1999). Since they govern the timing and allocation of resources to different portions of the life cycle, they influence organisms’ response to climate change by re-allotting resources (e.g., shifting seed mass mean) or rescheduling life-history events (e.g., seed emergence timing). Seed mass is the most common life-history trait used in ecology due to its wide availability in trait databases and has demonstrated its importance to plant functions such as seed dispersal, recruitment, competition, colonization, stress tolerance, and plant growth rates (Díaz et al., 2015, El-Kassaby and Barclay, 1992, Moles and Westoby, 2006). Seed mass variation often has concomitant effects on seed dormancy (i.e., delayed onset of germination) [e.g., reviews in (Baskin and Baskin, 2014)]. Germination is an irreversible process and therefore timed to avoid unfavorable environmental conditions for subsequent plant establishment and growth (Donohue et al., 2010). Both seed mass and germination covary and may evolve in a coordinated manner [e.g., (Liu et al., 2017a, Liu et al., 2016)]; however, their ecological trade-offs are found to be inconsistent between species [e.g., review (Liu et al., 2017b)]. As resource allocation conflicts have been shown to drive life-history trade-offs (Agrawal et al., 2010), such inconsistencies likely reflect different adaptive constraints on fitness (i.e., fitness trade-offs) for traits between species (Futuyma and Moreno, 1988). As such, critical environmental cues affecting life-history traits represent their ecological drivers, leading to ecological trade-offs.

While timing of phenologies (e.g., bud burst and bud set) is crucial to apical meristem damaging avoidance (i.e., survival) in late-spring and early-fall frosts in conifers (Bigras and Colombo, 2001), pollen and seed development are directly linked to seed filling and maturation (pollen clouds in Fig. 1A). Important external climatic factors during pollination and seed development should be important to final seed mass and germination. The amount of nutrient reserves (e.g., N) during the seed provisioning determines seed mass. As nitrogen is the main component of proteins and seeds with copious proteins germinate quickly (Ching and Rynd, 1978, Lowe and Ries, 1972), high nitrogen concentration is found to promote rapid germination (Hara and Toriyama, 1998) possibly through increased ribosomal activities (Elser et al., 2000, Makino et al., 2003). Hence, niches with high emission nitrogen deposition are supposed to have high soil nitrogen resource, resulting in elevated seed mass (net increase of plant internal source and seed provisioning) and possibly high final germination fraction. High seed mass often correlates with large seedling size (Chaisurisri et al., 1992, Kidson and Westoby, 2000), and large seedlings are better able to compete for light and nutrients due to their fast growth, leading to greater adult fitness (Moles and Westoby, 2006).

Whilst seedling recruitment is a primary determinant of the long-term dynamics of plant populations, life-history traits that govern propagule production and dispersal, germination, and establishment are crucial to community assemblies, in addition to functional traits (e.g., plant height) [illustration in Fig. 1B; (Huang et al., 2016, Jiménez-Alfaro et al., 2016, Larson et al., 2015)]. For example, one case in a Sonoran Desert winter annuals community demonstrated that species with early reproduction and germination had less interannual demographic variability (Kimball et al., 2011). The persistence or spread of tree species may be influenced by temporal trends in seed production which, in turn, controls population maintenance, demography, fitness, and consumer (predation) dynamics [e.g., (Archibald et al., 2012, Janzen, 1971)]. As such, if environmental changes considerably alter life-history traits, community and population outcomes are necessary to consider the influences of these traits (Cochrane et al., 2015, Saatkamp et al., 2019).

In this study, we use conifers as a study system, contrasting with previous studies in this taxonomic group (Liu and El-Kassaby, 2018, Mathys et al., 2017, Wang et al., 2006). Conifers are wind-pollinated gymnosperms, and female cones (seed cones hereafter) are usually restricted to the distal region of the shoot and their reproductive cycles vary among conifer species. Typically, there are two most common reproductive cycles in conifers (illustration in Fig. 1C). For instance, spruce (Picea spp.) and Douglas-fir (Pseudotsuga spp.) follow a two-year reproductive cycle (Allen and Owens, 1972, Owens, 1973, Owens and Molder, 1984a). Given a cone crop year i, bud completes differentiation (pollen or seed) in the year i-1. Pollination occurs in the spring or early summer of the year i. The time between pollination and fertilization is brief and usually completed within a few weeks. Following fertilization, embryo and seed development are rapid and continuous and then seeds mature and are released as early as late summer. The three-year reproductive cycle is characteristic of most pine species (Pinus spp.) (Owens and Molder, 1984b). Pollen and seed cones initiate in the year i-2. Pollination occurs in the early spring or summer of the year i-1, halts in the mid-summer, and resumes in the following spring (year i). Then, fertilization occurs and embryos and seeds mature by the fall. Seeds usually do not shed in the year when they mature (year i). Instead, mature serotinous seed cones [e.g., in lodgepole pine (Pinus contorta)] remain closed for many years and release of seeds, usually occurring after natural disturbances (e.g., fire), results in a massive shedding at one time. In addition to reproductive cycles, the three study species have different maturity ages of 16–25, 12–15, and 10–15 years for white spruce, Douglas-fir, and lodgepole pine, respectively (Allen and Owens, 1972, Owens and Molder, 1984a, Owens and Molder, 1984b).

By employing a climatological approach to uncover a six-decadal trend (1955–2015) for seed mass and germination in conifers across British Columbia, Canada, and their association with climatic variables and atmospheric nitrogen deposition, this retrospective study seeks to investigate two questions:

(1) Given species in a close phylogenetic status (e.g., conifers) and exposed to similar environmental conditions (i.e., individuals inhabiting overlapped niches), are their life histories driven by similar climatic variables in the same manner? In addition to climate, is the pattern of trait variation in concert with that of nutrient resources (e.g., nitrogen)? The answer to the question informs the traits sensitivity to the environment and provides insights into environmental influences on life-history traits at reproduction. Environmental variables key to life-history traits (key events marked in Fig. 1C) represent important cues driving resource allocation trade-offs. Understanding such trade-offs is crucial for understanding how organisms acquire and utilize resources through their lifetime, and why they form species with distinct ecological niche breadth over long timescales (Agrawal et al., 2010, Futuyma and Moreno, 1988).

(2) Based on trait prediction models fitted with key climatic drivers from (1) under future climate scenarios, what is the impact of climate change on trait variability? By addressing this question, this study further ascertains climatic influences on conifer seed mass and germination and evaluates the strength and stability of the relationship between focal traits and climates under changing scenarios. The outcome of these prediction models allows to answer whether predicative changes in life-history traits would mitigate or intensify the impact of climate change on species distribution predicted through functional traits-climate relationships, and whether the deployment of assisted migration needs considering the aspect of life-history strategies. The answer to this question also has implications for the impact of climate change on seedling regeneration, which potentially has cascading influences on community assemblies and population dynamics.

Section snippets

Study system and data compilation

In total, we used 1,314, 1,070 and 3,458 seed mass and final germination fraction data of white spruce, Douglas-fir, and lodgepole pine, respectively, over the period 1955–2015 across British Columbia (a climatically heterogeneous region), Canada, in which 24 locations were overlapped for the three studied conifers (species distribution ranges in Fig. 2A). Seed mass unit was gram per 1,000 seeds averaged over 3–5 replicates and seed weight per 1 K seeds was used as seed mass throughout this

Relationship between seed mass/ germination and the environment

In a hypervolume analysis based on records in species’ overlapping habitats, estimated kernel bandwidth vector for seed mass in Spruce, Fir, and Pine was 0.33, 0.62, and 0.42, respectively (Fig. S1) and the bandwidth for final germination fraction was 3.24, 3.14, and 1.11, respectively (Fig. S1). This showed that Fir had a high hypervolume space in both traits while Pine had a low one, indicating that the two traits were more variable in Fir, followed by Spruce and least variable in Pine. Seed

Discussion

In this retrospective study, we synthesized six-decadal data on seed mass and germination records in three conifer species (white spruce, Douglas-fir, and lodgepole pine) across British Columbia, Canada, and extensively searched for seed mass records of the three genera from databases and the literature. We used these three species’ seed mass and germination to unfold their ecological drivers and future tendencies as leveraged by climate and nutrient resources. The outcome of this study

CRediT authorship contribution statement

Yang Liu: Conceptualization, Data curation, Resources, Formal analysis, Investigation, Methodology, Software, Validation, Visualization, Writing - original draft. Yousry A. El-Kassaby: Conceptualization, Data curation, Resources, Funding acquisition, Project administration, Supervision, Writing - review & editing.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

We are grateful to the staff affiliated to British Columbia Tree Seed Centre (TSC; Surrey, Canada) for providing their long-term historical records, to Mr. J. Woods (Forest Genetics Council of British Columbia) for providing pollen clouds photos, to TRY database custodians for providing their publicly unreleased data upon our request, and to the scientists who contributed to the data on which this global meta-analysis is based. We also thank the Editor, X. Moreira, and two anonymous referees

Funding

This project was funded by the Johnson’s Family Forest Biotechnology Endowment and the National Science and Engineering Research Council of Canada Discovery and Industrial Research Chair to Y.A.E.

Data availability

All relevant data contained within this article can be requested from the corresponding author. TSC reserves the ownership of the original seed data and access to the original data needs TSC’s permission. For reproducibility, the scaled seed trait data and all the other data can be provided upon request.

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