DISCUSSION
Foundation species, by virtue of its special structural or functional
attributes, can create an entire ecological community or ecosystem,
sustain ecosystem functions and biodiversity; thus, the loss of
foundation species can induce broad consequences for associated biota
and ecosystem functions (Ellison et al., 2005; Schöb et al., 2012;
Thomsen et al., 2018). Thus, explicitly elucidating how foundation
species respond to climate warming and how the associated biodiversity
changes are crucial for robustly predicting changes in ecosystems, and
thus their long-term sustainable management.
As foundation species, cushion plants sustain a prominent proportion of
alpine biodiversity (Cavieres & Badano, 2009; Butterfield et al., 2013;
Chen et al., 2015a; Kikvidze et al., 2015). Thus, together with climate
change, their population dynamics may imply future biodiversity changes
in alpine ecosystems. We found that large numbers of cushion individuals
that once existed in low-elevation communities had been excluded, making
warmer populations now more fragmented than colder populations
(Figure 1). This was supported by
the facts that the warmer populations show lower population density but
more old individuals than those colder populations (Figure 1A-D; Figure
2A; Figure S2) which indicate a lower demographic rate in warmer
conditions. After exclusion from communities, the previously
cushion-dominated communities gradually turned to climax communities
that are overwhelmingly dominated by sedge species (Figure 3; Box 1).
All these results suggest that populations of the cushion A.
polytrichoides that are experiencing climate warming are simultaneously
experiencing degeneration, while populations under cold conditions are
maintaining recruitment and keep expanding (Chen et al., 2020a).
Newly established cushion populations in high-elevation habitats,
especially those newly uncovered by glacial retreat (Baker & Moseley,
2007), could facilitate the establishment of other species, thereby
increasing local plant diversity (Cavieres & Badano, 2009). In
contrast, population degeneration after climate warming could
potentially induce a thorough change in community
structures and (possibly reduced) biodiversity (Figure 3). In our study
sites, the mean annual temperature in the past decades has increased at
a rate of 0.06 oC yr-1, resulting inca. 70 m in elevation upward shift of the treeline (Baker &
Moseley, 2007), which could induce negative influences on high-elevation
vegetation (Grabherr et al., 1994). Moreover, upward shifts of lowland
species will inevitably induce increases in the diversity, cover and
productivity of alpine plant communities (Chen et al., 2011; Gottfried
et al., 2012; Steinbauer et al., 2018) which could impose strong
competition on cushion plants. Consequently, high-elevation populations
of the A. polytrichoides cushion plant would face the same
challenges that low-elevation populations face now. Thus, in the
long-term, low-elevation populations could become locally extinct and
there could be serious risks of degeneration of the high-elevation
populations. If cushion plants disappear, secondary extinctions are
likely to occur, especially of species exclusively sustained by cushion
plants (Losapio & Schöb, 2017). Furthermore, species interaction
networks that are now mainly sustained by cushion plants (Losapio &
Schöb, 2017; Losapio et al., 2019) would inevitably collapse.
Plants’ dynamics are influenced by ecological factors at different life
history stages (Gimenez-Benavides et al., 2008; Oldfather et al., 2021).
We found that all study populations except the Yulong population
produced sufficient seeds in a single growing season (Figure 2B),
suggesting that the species is not subject to seed limitation (Turnbull
et al., 2000). Thus, the seed germination and seedling establishment
rates in the following growing season could strongly affect recruitment
rates. We found that, generally, low temperature and light availability
can delay seed germination and reduce final germination percentages,
indicating that the frequently low temperatures in the early growing
season and cover by snow (Wang, 2006) or surrounding vegetation/litter,
may delay and/or reduce soil seed germination in the field. In addition,
very few seedlings survived for 17 weeks (Figure S4) which equals to the
length of the growing season in their natural alpine ecosystems. These
results imply large difficulties for A. polytrichoides seedlings
to establish successfully in situ .
Even worse, A. polytrichoides seeds cannot persist in the soil
for more than a year (Table S4; Figure S5), indicating that the species
has a transient soil seed bank. Thus, if seeds cannot germinate or
seedlings cannot survive through the first winter, population
recruitment will be extremely constrained. Moreover, extreme climate
events (e.g. , drought and coldness) frequently occur in our study
region (Wang, 2006). We found that short periods of extreme water stress
and low temperature can significantly reduce seedling survival (Figure
4A), but prior growth in mild conditions for sufficient time (90 to 120
days) significantly increases their ability to survive long-term extreme
climate events (simulating a long winter; Figure 4; Table S3). Thus,
timely germination early in the growing season and the occurrence of
extreme climate events during the growing season may be key determinants
of recruitment rates. These findings are consistent with expectations
that a sufficiently long growing season without damaging events could be
essential for seedlings to accumulate resources (e.g. ,
carbohydrates and various nutrients), allocate them
appropriately, and maintain a healthy physiological status, thereby
establishing high over-wintering capacity (Luscher et al., 2001). The
finding that all transplanted seedlings died by the end of the growing
season (Table S5) corroborates this conclusion, because the growing
season was too short (ca. 60 days) for them to develop
over-wintering capacity.
Furthermore, our transplantation experiment implied that inter-specific
competition can hinders seedlings’ establishment. This could be because
that other competitive species can delay seed germination and accelerate
the death of A. polytrichoides seedlings (Chen et al., 2020a). In
addition, surrounding vegetation may also impose certain allelopathic
constraints on seed germination and seedling growth (Table S6; Figure
S6).
Competitive stress imposed by beneficiary plants plays key role in the
decay of previously established individual cushions. Firstly,
beneficiary plants generally reduced the cushions’ nutrient contents and
two stable isotope (δ13C and δ15N)
ratios that provide information on plants’ water-use efficiency and
carbon, water and nitrogen balances (Table S7; Figure S7) (Dawson et
al., 2002). Secondly, beneficiary plants significantly constrain
physiological traits (SLA and LDMC) of cushion individuals (Table S8;
Figure S7A, C), which implies short leaf longevity and low resource use
efficiency (Wright et al., 2004). SLA is also positively correlated with
temperature, light availability (Poorter et al., 2009) and soil nitrogen
availability (Ordonez et al., 2009). High cover of beneficiary plants
can clearly reduce light availability on cushions’ surfaces, thereby
reducing SLA (Figure S8A). Thirdly, beneficiary species could generally
reduce the LDMC of individual cushions (Figure S7C), indicating that
they may inhibit cushion individuals partially through competition for
water and associated stress (Cornelissen et al., 2003). However, SLA
increases but LDMC decreases with increases in beneficiary cover (Figure
S7B, D). Nevertheless, the combined effects of high SLA and low LDMC
induced by increases in beneficiary species probably accelerate the
competitive exclusion process of individual cushions (Figure 5I-K) and
hence degeneration of cushion populations.
Furthermore, possibly due to the trophic and physiological constraints,
beneficiary species significantly reduced flower production of cushion
individuals (Figure 5A-H), and had context-dependent, but generally no
or slightly negative, effects on their fruit production (Figure 5A-H).
This may be partly because the vegetative growth of the beneficiary
plants hindered pollinators’ visitations of the flowers, and
consequently reduced pollination efficiency and fruit set. In addition,
increases in beneficiaries’ cover may induce changes in cushions’
resource allocation patterns, through competition-driven increases in
allocations to growth and/or defenses (Schöb et al., 2014b). These
results demonstrate that beneficiary species may constrain reproductive
functions of cushion plants, and hence future population recruitment.
In conclusion, taking communities
organized by typical foundational cushion species as a model system, we
here explicitly revealed that when foundation species degenerate due to
climate warming, the associated species composition and diversity both
change with a possible biodiversity collapse. Additionally, such
changing processes are influenced by the changes in series ecological
factors which are induced by climate warming. As a result, we strongly
suggest that to assess the processes of the dynamics of foundation
species and the associated biodiversity changes is critic and effective
for future biodiversity conservation concerns.