Introduction
Seed mass, a key ecological trait that affects many aspects of plant
ecology (Moles et al., 2005a, b; Mason et al., 2008), has great
influences on the regeneration strategies of plants, including seed
output for a given amount of energy, seed dispersal and seedling
survival (Leishman et al., 2000). Variation in seed mass reflects the
fundamental trade-off between seed number and seed mass (Henery &
Westoby, 2001) and between seed mass and persistence in the seed bank
(Thompson et al., 1993). An increasing body of evidence has shown that
large-seeded species produce less seeds than those bearing small seeds
(Henery & Westoby, 2001; Moles et al., 2004). Compared to small-seeded
species, large-seeded species are more likely to produce large seedlings
that are supposed to survive better than small seedlings under a variety
of hazardous environments (Armstrong & Westoby, 1993; Leishman &
Westoby, 1994a, b; Burke & Grime 1996; Westoby et al., 1996, 2002;
Harms & Dalling, 1997; Leishman et al., 2000; Dalling & Hubbell, 2002;
Moles & Westoby, 2004; Dainese & Sitzia, 2013). Despite the advantages
associated with large seeds, seed masses of present-day species have
been observed to range over 11.5 orders of magnitude, from the 0.0001-mg
dust-like seeds of orchids to the 20-kg seeds of the double coconut
(Michelle et al., 1995). Therefore, to reveal the internal mechanism and
influencing factors of the changes in seed mass will help us to better
understand the ecological history of plants.
As proposed by the leaf-height-seed (LHS) scheme of plant ecology
strategy (Westoby, 1998), plant height and leaf area are closely
correlated with seed mass. As a crucial component of a plant species’
ecological strategy, plant height not only determines a plant’s ability
to compete for light but also a species’ carbon gain strategy, which is
supposed to play an important role in another life-history trait, seed
mass (Moles & Leishman, 2008). A pioneering study by Levin (1974) found
that the mean seed mass of 832 plant species increase along the growth
form: herbs, shrubs, vines, shrubby trees, and trees. Leishman et al.
(1995) showed that seed masses are consistently correlated with plant
height across 1659 species, representing a worldwide flora. Carly et al.
(2009) found positive linear correlations between plant height and seed
mass of 15 species at the community level in the northeast Galilee
region of Israel. Moles et al. (2004) analyzed the trait data of 2026
species across 150 families and revealed a positive correlation between
seed mass and plant height, representing large-scale evidence for the
relationship between seed mass and plant height. However, Grime et al.
(1997) found no significant correlation between plant height and seed
mass across 43 common British species. Thompson & Rabinowitz (1989)
analyzed 816 plant species around Sheffield and found significant
relationships between seed mass and plant height within some families
(Poaceae, Caryophyllaceae, Asteraceae and Fabaceae), but not in other
taxa like Scrophulariaceae, Apiaceae, Lamiaceae, Calophyllum ,Pinus , and Quercus . In a southeastern Sweden flora, seed
mass was only marginally correlated with plant height of 126 species
(Bolmgren & Cowan, 2007).
Rees
(1996) analyzed 382 species of Sheffield flora and found that the
relationship between seed mass and plant height is inconsistent and
dependent on dispersal modes. Therefore, much uncertainty still remains
to be tackled possibly due to the limitation of plant species sampled in
previous studies, although plant height has been considered one of the
strongest correlates of seed mass (Leishman et al., 1995; Moles et al.,
2004).
As the main organ of plants that contributes to photosynthesis (Bazzaz
et al., 2000), leaves act as a key determinant of the amount of energy
available for reproduction (Wright et al., 2004). Although leaves may
vary in their traits (e.g., area, morphology, anatomy, physiology and N
nutrition) in response to growing conditions (Givnish, 1987; Witkowski
& Lamont, 1991; Ackerly & Reich, 1999; Cornelissen et al., 2003;
McDonald et al., 2003; Xu et al., 2009; Milla & Reich, 2011), a strong
connection between total leaf mass and net annual reproductive biomass
has been observed (Niklas & Enquist, 2002, 2003). Therefore, the
ecological significance of leaf traits may relate to resource capture in
productive organs, implying that leaf area and seed mass should be
positively correlated (Westoby & Wright, 2003). Midgley & Bond (1989)
found that leaf area was positively correlated to cone size in 18
species from the Leucadendron genus in South Africa. Hodgson et
al. (2017) also found positive linear relationships between leaf area
and seed mass of 2400+ species from England and Spain. Although it was
not specifically stated in the studies by Laughlin et al. (2010), seed
mass appears to be positively correlated with leaf area of 133 plant
species in northern Arizona, USA. Rather than a linear relationship,
Cornelissen (1999) showed a triangular relationship between leaf area
and seed mass of 58 woody species from Europe. Recently, Santini et al.
(2017) showed that the triangular relationship also holds for 401 annual
plants belonging to 37 families from the United Kingdom. However,
Westoby & Wright (2003) failed to find the triangular relationship
between leaf area and seed mass as reported by Cornelissen (1999),
indicating that the pattern seems not universal between seed mass and
leaf area.
In addition, seed mass is not independent of growth form, which is often
a predictor of other plant traits (Moles et al., 2005a, b). Plant growth
form, like seed mass, may also be phylogenetically controlled (Li et
al., 2017). Evidence has shown that woody plants are more likely to have
larger seeds, while non-woody species are more likely to produce small
seeds (Jurado et al., 1991). Therefore, the phylogenetic conservatism of
plant growth form might have an indirect impact on the variations in
seed mass. Furthermore, genome size appears to be one of the most
studied factors that are related to variations in seed mass. Although
there is no significant linear regression relationship between genome
size and seed mass across 1222 species from 139 families and 48 orders
of seed plants, Beaulieu et al. (2007) found that species with very
large genome sizes never had small seeds. Therefore, apart from the
influence of plant height and leaf area, phylogeny, growth form and
genome size may also contribute to seed mass variations.
Phylogenetic conservatism in plant traits has been well studied (Wiens
et al., 2010; Baskin & Baskin, 2014; Cornwell et al., 2014; Tozer et
al., 2015) and such studies are helping to illuminate the role of the
evolutionary past in determining the characteristics of species. Seed
mass has been accepted as an ecologically important trait
phylogenetically constrained within local floras. This may also be true
for plant height and leaf area. Therefore, it should be obligatory to
extract variations in plant traits associated with phylogeny, before
analyzing relationships between seed mass and other plant ecological
attributes, e.g., growth form, plant height, and leaf area. However, the
potential influence of phylogeny on the leaf-height-seed (LHS) plant
ecology strategy scheme has not previously been well evaluated
(Cornelissen, 1999; Laughlin et al., 2010; Hodgson et al., 2017).
Despite previous data on the relationship between plant traits across
the world, published literature failed to incorporate phylogeny and
plant traits into the analysis of the variations in seed mass (Chase &
Pippen, 1990; Mustart & Cowling, 1992; Lord et al., 1995; Kang &
Primack, 1999; Zhang et al., 2004; Vandelook et al., 2018). The rapid
accumulation of databases on plant traits provides us an ideal
opportunity to illustrate a general pattern of the relationship between
plant traits, which helps us to have a better understanding of the
leaf-height-seed (LHS) plant ecology strategy scheme. In the present
study, we first used phylogenetic partial R2s (Ives,
2019) to tease apart the effects of multiple plant traits (plant height,
leaf area, genome size, growth form and leaf N) and phylogeny, to
quantify extent to which they contribute to variations in seed mass of
plant species when each predictor variable and the phylogeny is removed
one-by-one.