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Received: 6 March 2020    Accepted: 13 April 2021

DOI: 10.1111/1365-2745.13677

RESEARCH ARTICLE

Closing the life cycle of forest trees: The difficult dynamics

of seedling-­to-­sapling transitions in a subtropical rainforest

Chia-­Hao Chang-­Yang1  | Jessica Needham2  | Chia-­Ling Lu3 | Chang-­Fu Hsieh3  |

I-­Fang Sun4  | Sean M. McMahon5

1
Department of Biological Sciences, National
Sun Yat-­Sen University, Kaohsiung, Taiwan Abstract
2
Climate and Ecosystem Sciences Division, 1. Experimental and observational studies on seedling dynamics posit mechanisms
Lawrence Berkeley National Lab, Berkeley,
that can influence forest diversity, structure and function. However, high mor-
CA, USA
3
Institute of Ecology and Evolutionary
tality and slow growth of seedlings make it difficult to evaluate the importance
Biology, National Taiwan University, Taipei, of this life-­history filter to total tree life history. Quantifying the duration and
Taiwan
4
transition of the seedling phase would help us understand this ‘black box’ in tree
Center for Interdisciplinary Research on
Ecology and Sustainability, National Dong population biology.
Hwa University, Hualien, Taiwan 2. We used a 16-­year dataset of comprehensive seedling-­to-­sapling demography
5
Forest Global Earth Observatory,
from a subtropical rainforest to construct population models that capture tem-
Smithsonian Environmental Research
Center, Edgewater, MD, USA poral demographic fluctuations for eight major tree species. We used data-­driven
demographic models and simulations to estimate the transition ratios from newly
Correspondence
Chia-­Hao Chang-­Yang recruited seedlings to saplings of 2-­m height and the time taken to attain 2-­m
Email: changyang@mail.nsysu.edu.tw
height for a newly recruited seedling conditional on its survival.
Funding information 3. Projections among species estimated that as few as 57 to more than 40,000 seed-
Taiwan Forestry Research Institute, Grant/
lings (with a median of 2,087) were required to make a single 2-­m high sapling.
Award Number: 93AS-­2.4.2-­FI-­G1(2)
and 94AS-­11.1.2-­FI-­G1(01)-­1; Taiwan Furthermore, it would take 22–­200  years (with a median of 47) for a newly re-
Forestry Bureau, Grant/Award Number:
cruited seedling to become a 2-­m high sapling. We found that temporal variation
104AS-­13.7.5-­FB-­e 4, 105AS-­12.7.4-­FB-­e3,
92-­0 0-­2-­06, 95-­0 0-­2-­05, 96-­0 0-­2-­02, in demographic rates could greatly reduce the number of seedlings per estab-
97-­0 0-­2-­01, tfbc-­1070219 and tfbk-­990207;
lished sapling, but not passage times (PTs). We also identified the importance of
Ministry of Science and Technology, Taiwan,
Grant/Award Number: MOST 104-­2621-­B-­ consistently fast growth rates for seedlings to escape the high mortality of early
259-­0 01 and MOST 104-­2917-­I-­564-­019
stages.
Handling Editor: Xiaojuan Liu 4. Synthesis. Our findings demonstrate that high mortality in the very early seedling
stage severely limits the probability that a newly recruited seedling will transition
to the sapling stage. Although the PTs vary, we found this to be true across spe-
cies with a range of life-­history strategies. Only seedlings with consistently fast
growth rates are expected to pass through this life-­history filter. Findings from
seedling studies should consider how short-­term studies of seedling demography
might capture the rare exceptional individuals and exceptional conditions that
might define the dynamics of this seedling bottleneck.

KEYWORDS

community assembly, Fushan forest dynamics plot, hierarchical Bayesian model, life-­history
strategy, non-­random ecological process, species coexistence, stochastic simulation

Journal of Ecology. 2021;109:2705–2716. wileyonlinelibrary.com/journal/jec© 2021 British Ecological Society     2705 |


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2706      
Journal of Ecology
1 |  I NTRO D U C TI O N
Trees are thought to have long life spans, but only a small frac-
tion of individuals in a population that reach maturity contributes
to this reputation. The majority of individual stems in a population
are seedlings (here defined as being between a new germinant and
2  m in height). The relatively high mortality in this stage means
that although seedlings may reflect only a fraction of the full life
span of any tree species, the individuals that survive this bottle-
neck may define many important characteristics of the juvenile and
adult populations of a species (Green & Harms, 2018; Harper, 1977;
Poorter,  2007). Important mechanisms, such as ontogenetic vari-
ations in trait-­mediated demography (Green & Harms,  2018) and
episodic recruitment events driven by climatic oscillations (Brown
& Wu, 2005; Pederson et al., 2014), have been identified that may
determine both the percentage of survivors of the seedling phase
and the amount of time it takes to pass through this phase, criti-
cal to how we anticipate the temporal scales in forest regeneration.
These life-­history processes make the demographic behaviour of
species' seedling populations an important focus for explaining spe-
cies coexistence and forest dynamics (Comita et  al.,  2010; Green
et al., 2014), density-­dependent processes (Comita et al., 2014), the
role of pests and pathogens in defining tree communities (Bagchi
et al., 2014; Chen, Swenson, et al., 2019; Chen, Wang, et al., 2019),
the spatial influence of forest structure on populations (Comita &
Engelbrecht, 2009; Johnson et al., 2017) and trait-­based life-­history
strategies (Jia et al., 2020; Umaña et al., 2017).
A gap remains, however, between inference from seedling stud-
ies and their quantitative integration into the complete tree life
history. This gap results in part from the fact that seedling stems
can still be long-­lived, fluctuate widely in abundance over time and
respond to multiple biotic and abiotic drivers. Few studies include
seedlings that span all sizes from germinant up to the size of sapling
and adult inventory protocols, and even long-­running observational
studies cannot capture the range of climatic and demographic fea-
tures that link seedlings to larger patterns observed in forests (but
see Connell & Green,  2000; Green et  al.,  2014). Previous studies
have shown that tree seedlings may spend decades in the forest un-
derstorey (Antos et al., 2005; Delissio et al., 2002; Hubbell, 1998),
but estimates of the retention time at the seedling stage are rare
for a number of reasons. High temporal variation in seedling density
is often observed at both population and community levels (Chang-­
Yang et  al.,  2013; Connell & Green,  2000; Metz et  al.,  2008), and
seedling demography is associated with environmental fluctuations
(Bachelot et al., 2015; Ibáñez et al., 2007). The robust estimates of
demographic rates rely on long-­term observations made at adequate
intervals (Connell & Green,  2000), but most of the seedling stud-
ies last only 3–­5 years. Finally, relatively few records document the
full transition from seedling to sapling, leaving potentially important
gaps in inference about whole life-­history rates. Therefore, although
comparisons between discrete stages designated as seedlings and
those designated as sapling or later offer important insights into
ontogeny (e.g. Green et  al.,  2014), the ‘black box’ of demographic
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CHANG-­YANG et al.
impact of seedlings on forest dynamics remains. Quantifying the full
development of seedling demography from germinants to saplings
stage will ground inference about the impacts of specific mecha-
nisms on forest communities.
Seedling growth and survival, which co-­determine the seedling-­
to-­sapling transition, vary among individuals. Rapid growth at
early stages is crucial for seedlings to reach later stages (Metcalf
et al., 2009; Snyder & Ellner, 2016; Zuidema et al., 2009), and these
persistently fast-­growing individuals may make a disproportionate
contribution to population growth (Jansen et  al.,  2012; Zuidema
et al., 2009). Tree demographic rates also change over time (Bachelot
et al., 2015; Connell & Green, 2000; Ibáñez et al., 2007). The tem-
poral variation in tree demography, driven by multiple external forc-
ings at different spatial and temporal scales, may play an important
role in community assembly (Chesson,  2000; Wright,  2002). For
example, small-­scale events, like gap dynamics, can enhance the
growth of suppressed seedlings or recruitment of light-­demanding
species, contributing to the maintenance of forest composition and
structure (McCarthy,  2001; Runkle,  1982; Yamamoto,  1992). Over
longer temporal scales, climatic shifts and/or disturbances may pro-
vide occasional periods that facilitate tree recruitment and impart a
legacy in forest communities centuries after their occurrence (Baker
et al., 2005; Brown & Wu, 2005; Hoffmann et al., 2020; Pederson
et al., 2014; Vlam et al., 2014). Understanding the effects of tempo-
ral variation in seedling vital rates on the seedling-­to-­sapling transi-
tion will help evaluate the importance of the seedling stage for the
entire tree life history.
In 2003, in a 25-­ha forest dynamics plot (FDP) in Fushan, Taiwan,
three hundred and eighteen 1-­m2 seedling plots were established
where all stems between germinants to 2-­m height (roughly the 1-­cm
size class from the FDP) were measured subannually (Chang-­Yang
et  al.,  2013). Despite the identification and monitoring of 13,818
stems from 40 tree species, as of 2019, 14 individuals achieved the
1-­cm cut-­off for the FDP, and only one of them was from the newly
recruited seedlings during the study period. There were 5,165 and
2,838 sapling recruits in the 2009 and 2014 FDP full censuses, re-
spectively, but only three of them occurred in the ~0.1% of the FDP
area comprising the seedling experiments. This disconnect between
the dynamics of seedlings and their rare success in becoming sap-
lings suggested a need for a theoretical model to explore the con-
straints and potential developmental paths that could lead to sapling
recruitment.
Demographic process models based on simple biological rules
and with parameters estimated from data can provide a robust,
qualitative and quantitative assessment of the black box of tree-­
seedling life history. We are using a model developed specifically
for the challenges of interpreting rare life-­history events that
compound to define distributions of forest tree species (Needham
et  al.,  2018). This model overcomes some of the basic challenges
that statistical approaches to seedling life history are vulnera-
ble to. First, seedling demographic data are usually concentrated
with small individuals with high mortality, limiting inference from
short-­term observations on the full life cycle of trees. Second,

CHANG-­YANG et al.
the majority of seedlings have very slow growth rates. This is be-
cause most seedlings are in deep shade, and are in competition
for nutrients and water with each other and adult trees. They
have also been shown to be more vulnerable to herbivores, pests
and pathogens than later life-­c ycle stages (Bagchi et  al.,  2014;
Barton & Hanley, 2013; Chen, Swenson, et al., 2019; Chen, Wang,
et al., 2019). Rare access to resources, such as light through open-
ings in canopy or understorey vegetation can substantially increase
the growth rates of a relatively small number of seedlings for brief
periods in their lives (Brokaw & Busing, 2000; Denslow et al., 1990;
George & Bazzaz, 1999). Such rare beneficial conditions can com-
pound over time, such that growth begets larger size which begets
potential greater access to resources. Although rare, such events,
when frequent enough for an individual, can offer a path to demo-
graphic success (Snyder & Ellner, 2016).
This study extends the demographic process model explained
in Needham et al. (2018) and applied in Needham et al. (2016) and
Johnson et  al.  (2018) to explore the broader life-­history context
of seedling growth. We parameterize this model using data from
16 years of seedling growth and mortality data that include all stems
of tree species from germination to 2-­m height in the Fushan sub-
tropical rainforest in Taiwan (Chang-­Yang et al., 2013). We perform
our model runs using parameterizations from eight major species
that reflect a range of life-­history strategies. Our model runs were
designed to answer the following questions for each species: (a) If
a seedling successfully recruits to 2  m in height, how many years
on average does this take (hereafter denoted ‘passage time’ [PT])?;
(b) on average, how many seedlings does it take in order to pro-
duce a single 2-­m tall sapling? and (c) how do different patterns of
resource acquisition (i.e. canopy openings) determine both of these
life-­history metrics?
2 | M ATE R I A L S A N D M E TH O DS
2.1 | Study site
This study was conducted in the 25-­ha Fushan FDP (24°45′N,
121°35′E; 600–­733 m a.s.l.) in northeastern Taiwan (Su et al., 2007),
where all free-­standing woody individuals ≥1-­cm DBH (measured at
130 cm along the tree stem from the ground) within the plot were
tagged, mapped, measured, identified to species. A full census is re-
peated at approximately 5-­year intervals. A total of 111 species were
found in the FDP, including 84 tree species and 27 shrub species. The
climate at the Fushan is warm and humid (Lu et al., 2000, 2009), sup-
porting an evergreen broadleaf forest in the Machilus-­Castanopsis
zonation (Su, 1984). The mean annual temperature is 18.1°C, ranging
from 11.6°C in January to 24.2°C in July. The annual precipitation
ranged from 1,783 to 7,437 mm, with a mean of 4,059 mm, between
1991 and 2015. The average relative humidity is >90% throughout
the year. Typhoons are frequent between July and September. Frost
and snow are rare in this forest, but occurred once in March, 2005
(frost) and once in January, 2016 (snow).
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Journal of Ecology |
      2707
2.2 | Seedling censuses and study species
Our process model was parameterized with data from a long-­term
seedling dynamics study, where three hundred and eighteen 1-­m2
seedling plots along four 400-­m trails within the Fushan FDP were
monitored according to the protocol that had been used in the FDP
on Barro Colorado Island, Panama (Harms et al., 2000). For extensive
information on the dataset, see Chang-­Yang et al. (2013). These data
span from February 2003 to February 2019. In February 2003, all
seedlings of tree species <1-­cm DBH within the plots were tagged
with a unique number, measured for height to the apical bud and
identified to species. In subsequent censuses, surviving seedlings
were measured and new recruits were tagged, measured and iden-
tified to species. Although this study recorded these data every
3  months from February 2003 to May 2010, and every 6  months
thereafter until February 2019, we annualized the data for use in our
demographic model, which we ran on an annual time step. The de-
tails of the data annualization procedure are described in the follow-
ing paragraphs. As the seedling abundances in Fushan were highly
concentrated within a few species (Chang-­Yang et al., 2013), we se-
lected eight species with more than 100 seedlings (Table 1) and that
account for 88% of individuals found in the seedling census, and also
ranked as the top 20 in basal area among the 84 tree species found in
the Fushan FDP. Of importance to our demographic process model,
these species also span a continuum of life-­history strategies: they
include three light-­demanding and five shade-­tolerant species, and
reflect both canopy and subcanopy life-­forms (Table 1). The selected
group also captures the range of demographic diversity exhibited by
the community of tree saplings at Fushan (Figure S1).
2.3 | The demographic process model adapted to
seedling stage of trees
Our demographic model extends Needham et  al.  (2018), which al-
though designed for simulating sapling to adult life histories, ad-
dresses two key challenges that also exist in seedling data: (a) stem
growth is modelled to reflect the rare acquisition of resources and
autocorrelation in acquisition, and (b) survival is modelled as a logis-
tic function that increases with size to an asymptote. This approach
allows growth to create heterogeneity in size trajectories over a life
span, creating ‘lucky’ individuals which define the successful recruits
(Snyder & Ellner,  2016). We model survival as size dependent, be-
cause the seedling stage can show radically different survival prob-
abilities across size depending on species strategies and resource
access, which are well-­represented as continuous functions of size.
Our model does not directly link survival to growth. Although slow
growth may be associated with lower survival probabilities at in-
traspecific level, our model does not include this interaction explic-
itly, as this is difficult to quantify. Most individuals that survive grow
slowly, and deaths include non-­growth-­dependent mechanisms (i.e.
physical damage from treefall). There is an emergent correlation,
however, as slow growth lengthens the years spent as a seedling or
 13652745, 2021, 7, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/1365-2745.13677 by Readcube (Labtiva Inc.), Wiley Online Library on [13/07/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
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2708      
Journal of Ecology CHANG-­YANG et al.

in the highest risk regions of the survival curve, and stem shrinkage

height (m)
can lead to much higher mortality probabilities. The model struc-

TA B L E 1   Species name, code, dispersal mode, light strategy, life-­form, sample size and major functional traits of eight study species. Detailed descriptions of measurement protocol for
ture is presented in Figure 1. The details of the model parameteriza-

Max.

24.2

12.8

18.8
16.8
21.3

27.6

17.0
24.4
tion follow. For detailed description of model design, see Needham
et al. (2018), with applications in Needham et al. (2016) and Johnson
Wood density et al. (2018).
(g/cm3)

0.466
0.550

0.738
0.793
0.371
0.524
0.518

0.474
2.3.1 | Survival: Linking seedling and sapling stages
with different data sources
(cm2/g)

114.2
166.8

138.3
105.3
240.3
148.3

156.6
207.6
SLA

The survival component uses a logistic function to parameterize the

relationship between seedling survival and stem height. For each
Seed mass

study species, we used a hierarchical Bayesian model of survival

probability to describe the size-­dependent changes in seedling sur-
4.8
21.0

300.6

4.4
255.4

26.7
102.9

125.1
(mg)

vivorship with two data sources. We assumed that the seedling sur-
vival followed a Bernoulli distribution with the survival probability S
Initial height

over a time interval. S was predicted as a function of seedling height

using a three-­parameter logistic function:
8.5
4.5
3.5

2.5
11.5

3.0
10.4
14.1
(cm)

( )t
K (1)
S= ,
1 + exp( − r(x − p))
saplings
No. of

2,601

591
690
214
498
523
1,077
529

where x is the seedling height in cm, t is the time interval between

annual censuses in years for each seedling, K is the upper asymp-
seedlings

tote of survival probability, p is the inflection point of the logistic

No. of

863

388
7,116
130
800
1,494
900
261

curve and r is the rate of change in survival probability with seedling

height. The rapid increase (p and r) and plateau (K) in seedling sur-
vival were parameterized from both seedling survival data and FDP
Subcanopy
Subcanopy
Subcanopy
Life-­form

small stem data. Because the seedling size distribution was highly
Canopy

Canopy
Canopy
Canopy
Canopy

right-­skewed, K would tend to be underestimated due to the nu-

merical dominance of small individuals (seedlings of <30 cm height)
and the lack of large individuals. We therefore determined a K value
Light demanding

Light demanding
Light demanding

using sapling survival data from the 25-­ha Fushan FDP and then fit-
Shade tolerant
Shade tolerant
Shade tolerant
Shade tolerant
Shade tolerant
Light strategy

ted p and r using seedling survival data with the estimated K value.
Specifically, we estimated K as the average annual survival rate of
trees of 1-­to 2-­cm DBH from the 2004 to 2009 census data of the
Fushan FDP.
Because there is considerable temporal variation in seedling
Dispersal

Animal
Animal
Animal
Animal
Animal
Animal
Animal

survival, we added a year random effect for parameter p (inflection

mode

Wind

point) to estimate the year-­by-­year p. Our preliminary analysis sug-

gested that the survival model with random effect on p performed
functional traits, see Lasky et al. (2013)

better than the one with random effect on r (Appendix S1). Further,

MACHTH
MACHZU

PRUNPH
ENGERO
GLOCAC

SCHEOC
MYRSSE
Species

LITSAC

although there were multiple FDP censuses, K differed little across

code

them and so K remained a constant asymptote. Since most seed-

ling studies in other tropical forests were conducted at an annual
Engelhardia roxburghiana

(or greater) interval, including all census data would give lower es-
Glochidion acuminatum

timates of seedling survival than other seedling studies (Sheil &

Schefflera octophylla
Machilus zuihoensis
Machilus thunbergii

Prunus phaeosticta

May, 1996), as nearly 50% of newly recruited seedlings died within

Litsea acuminata

Myrsine seguinii

6  months in Fushan (Chang-­Yang et  al.,  2013). We therefore used

census data from February (or data from May if February data were
Species

not available in that year) for seedling survival analysis to avoid the
peak germination season.
 13652745, 2021, 7, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/1365-2745.13677 by Readcube (Labtiva Inc.), Wiley Online Library on [13/07/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
CHANG-­YANG et al. Journal of Ecology |
      2709

F I G U R E 1   Seedling survival and

growth models for Litsea acuminata (a)
(LITSAC, Lauraceae). (a) Size-­dependent
survival model: A three-­parameter logistic
function is fitted. Blue line shows the
estimated parameter, and grey lines
around it show estimates for each year.
Black and red rugs along the top and
bottom axes show survival and mortality
data respectively. (b) Mixture-­distribution
growth model: Slow and fast growth
groups are fitted by normal (blue) and
gamma distribution (red) respectively.
(b)
The insets show the mixture distribution,
with the dashed vertical line representing
the 0.9 quantile of growth increment. (c)
Size-­dependent growth transition models:
Blue (left) and red (right) lines denote the
population-­level estimates for slow-­to-­fast
and fast-­to-­fast transitions, respectively,
and grey lines around it show estimates
for each year (year random effect)
a
(c)
f f

2.3.2 | Growth: Heterogeneity in individual growth
In order to capture autocorrelation in growth that can lead to rare ex-
ceptional performance over many years (Clark et al., 2010), two pro-
cesses must be captured: the distributions of slow and fast growth
and the rules under which an individual stem transitions between
those rates over their life span. Because fast growth is rare due to
the highly skewed nature of growth in the understorey, where most
individuals are suppressed, fast growth must be represented by an
upper quantile of observations: we chose 90% as the cut-­off for this
difference, allowing sufficient data to support the fast distribution,
but retaining the distinction between the rates. The transition prob-
ability between slow and fast growth and the reverse begins at a
minimum value and increases as the stem grows, to a maximum level,
representing the potential to gain more resources (e.g. light) as the
stem grows. This function also reflects autocorrelation in growth
(e.g. where an individual has access to light for a period before the
canopy closes).
Although most seedlings grew very little each year and some-
times had negative growth (shrinkage in height due to stem break-
age), a few seedlings had much larger height increments (Figure 2a).
In addition, same-­sized seedlings exhibited large variation in their
growth (Figure  2b). We parameterized a distributional model that
describes this crucial individual-­level variation in seedling growth for
each study species. The growth data of each species were separated
into two different groups: fast and slow growth (again, defined as
the fastest 10% and the remaining 90% of the growth data respec-
tively). A gamma and a normal distribution were then fitted to the
fast and slow growth data respectively:
⎧ 2
⎪ Normal(𝜇, 𝜎 ) when Z ≤ q
Z∼⎨ , (2)
⎪ Gamma(𝛼, 𝛽) when Z > q
⎩
where Z is the growth increment change per year (cm/year) and q
is the 0.9-­quantile threshold for inclusion in the fast growth distri-
bution. The normal distribution fit the more symmetric distribution
of the slow growth group with parameters μ (mean) and σ (variance)
and allowed for negative growth, while the gamma distribution of-
fers a flexible way to fit the right-­skewed distribution of the fast
growth group with only two parameters (distribution shape, α, and
rate, β). Z was calculated as the difference in height measurements
of surviving individuals between seedling censuses. If a seedling
had more than one growth measurement in a year, we calculated

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2710      
Journal of Ecology
(a) (b)
year
the average growth rate for measurements within the same year.
Extreme growth increments (growth >100 or <−100 cm/year), pos-
sibly representing errors in the data, were excluded. We combined
the two distributions into a mixture distribution with a weighting of
90% and 10% for normal and gamma distributions respectively. We
then sampled the growth increment from the mixture distribution in
the population projections.
While fast growth in seedlings was rarely observed, fast growth
of a seedling often lasted for either a couple of months or a few
years, which further enhanced its probability of being fast growing,
as large individuals generally have increased access to resources
(such as light or soil nutrients). The growth transition models capture
the temporal correlation and size dependence in seedling growth.
We used GLMMs to estimate the size-­dependent transition proba-
bilities between growth groups. Two growth transition models were
constructed: slow-­to-­fast and remaining-­fast growth. Due to the rar-
ity of the transition event in some species, we pooled the species
data and performed the analysis at the community level. We esti-
mated the species-­specific coefficients by including species identity
as a random effect. In addition to the species random effect, we
included year as a crossed random effect to capture the temporal
variation in the transition probabilities. The random slope model can
be specified as:
[ ] [ ]
logit(P) = m0 + m1 x fixed_part + 𝛾 species x + uspecies + uyear random_part , (3)
where P is the transition probability either from the slow to the fast
group or remaining in the fast group, x is the seedling height, m0 rep-
resents the mean intercept, m1 represents the mean coefficient value
of the seedling height, γspecies and uspecies denote the random slope and
intercept, respectively, for each species and uyear denotes the random
intercept for each year.
Sampling from the posterior distribution of all survival and
growth parameters was performed using the Hamiltonian Monte
Carlo method with the ‘rstan’ package (https://mc-­stan.org) in r (R
Core Team, 2019). The probability samples were obtained from four
independent Markov chains, in which a total of 200 values were
sampled with 50 thinning intervals after a burn-­in of 10,000 iter-
ations (in total 20,000 iterations). The convergence of the Markov
chains was checked with the Gelman-­Rubin statistic (or potential
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CHANG-­YANG et al.
F I G U R E 2   (a) Annual seedling growth
data of the Fushan subtropical rainforest.
Data are sorted from small to big. Zero
growth data are indicated by open box
with dashed vertical lines, and top 10%
growth data are indicated by black
box with solid vertical lines. (b) Annual
seedling growth increment verses seedling
height. We excluded annual growth data
>100 or <−100 cm per year from the
seedling growth analysis
scale reduction statistic, R)
̂ and effective sample sizes for each pa-
rameter (Gelman et  al.,  2013). The GLMMs were fitted using the
‘lme4’ package (Bates et al., 2015). Full descriptions of the Bayesian
models and GLMMs are given in Appendix S1.
2.4 | Population projections with a process-­
based model
We used an individual-­based model (IBM) to simulate seedling co-
hort dynamics and estimate PTs and transition ratios (TRs) from
newly recruited seedlings to saplings of 2-­m height. In Fushan, a
sapling of 2-­m height generally has attained the 1-­cm DBH status
that would include it as a ‘sapling’ in the FDP census (and therefore
link the seedling analysis to the rest of the tree census and trait
data collected in the FDP). We started the IBM with 50,000 seed-
lings of species-­specific initial height: the average height of newly
recruited seedlings when they were first tagged and measured in
the seedling censuses (Table 1). In each year (iteration), the survival
of each seedling was determined by a random binomial draw with
a probability of success (survival) derived from the size-­dependent
survival probabilities given the fitted survival function (Equation
1). Surviving seedlings could then potentially move between slow
and fast growth groups according to the size-­dependent transition
probabilities (Equation 3; another binomial draw). We then sampled
a growth increment from above or below the increment threshold of
the mixture distribution according to the individual's growth group
(Equation 2). This is repeated for all living stems for 300 simulated
years or when all seedlings died in the simulation. We calculated the
ratios of seedlings to saplings and the PTs from first recruitment to
2-­m height.
To explore how temporal variation in seedling growth and sur-
vival influence PTs and ratios of seedlings to saplings, we designed
two types of individual-­based models: one with no temporal varia-
tion (using population-­level means of demographic parameters) and
the other with temporal variation in demographic parameters. For
the simulation with temporal variation, different degrees of tempo-
ral correlations in demographic rates were tested. In IBMs with tem-
poral variation but no temporal correlation, we randomly selected
the parameters values from all 16 annual estimates of each species.

CHANG-­YANG et al.
For IBMs with temporal correlations in demographic rates, we sim-
ulated seedling dynamics with different numbers of consecutive
good years at the beginning of simulations. We define a good year
as the year with highest survival (i.e. lowest p) and highest transition
probabilities to the fast growth group (i.e. highest m 0). We ran the
simulations with 0 to 20 consecutive good years (iterations). After
the duration of good years, we simulate the seedling dynamics with
annual estimates of demographic parameters selected randomly.
Previous studies have suggested that persistently rapid growth is
critical for small and young individuals to reach later stages for tree
species (Snyder & Ellner, 2016; Zuidema et al., 2009). We therefore
focused on how consistently high survival and growth at very early
stages influence seedling-­to-­sapling transition. We set the duration
of good years not for a specific environmental driver, but as a proxy
for potential drivers. The aim here was to test the number of consec-
utive good years that would be needed for a pulse of sapling recruit-
ment to occur that matched the observed population of 1-­cm DBH
stems in the larger FDP.
For each scenario of the IBM, we repeated the simulation
procedure 100 times to obtain the 95% confidence limits of the
population-­level statistics (PTs and TRs between seedlings and sap-
lings). We determined the number of repetitions based on the com-
putation power as the simulations were relatively time-­consuming.
We also compare the average growth rates between the seedlings
that reach 2-­m height and the ones that failed.
To explore how the uncertainty in parameter estimations influ-
ence the population-­level statistic, we perform the sensitivity analy-
sis of parameters of survival (r and p) and growth transition (m 0 and
m1) models and initial conditions. Initial conditions include initialized
growth groups (slow or fast) and seedling size (species-­specific initial
height or 50-­cm height) in the simulations. Further details on the
sensitivity analysis are provided in Appendix S3.
R scripts for the demographic process models and population
projections are provided in Appendix S4.
3 | R E S U LT S
3.1 | Demography of seedlings
All models (growth and survival for eight study species) converged
and were well mixed. Across all models, 184 estimated parameters
had R
̂ values  ≈  1 (Appendix  S2). All models also had sufficient ef-
fective sample sizes (Appendix  S2). We therefore extracted post-­
burn-­in mixes of the four chains for each model run and thinned the
values for posterior inference.
For most study species, the seedlings reached the upper asymp-
tote (K) of survival curve around 50-­cm height with considerable
temporal variation (Figure 1a; Figure S3). The mixture distributional
model was fit to the growth data of each species (Figure 1b; Figure
S5). The transition probabilities from slow-­to-­fast growth groups and
the probabilities of remaining in the fast group were positively cor-
related with seedling size for most study species (Figure 1c; Figure
13652745, 2021, 7, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/1365-2745.13677 by Readcube (Labtiva Inc.), Wiley Online Library on [13/07/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Journal of Ecology |
      2711
S6). In general, light-­demanding species tended to have relatively
low survival and high growth rates compared with shade-­tolerant
species, but with some exceptions (Appendix  S2). For example,
Schefflera octophylla (Araliaceae), a light-­demanding species, had
relatively low survival and growth rates among the study species.
3.2 | Population projections
Our demographic process model simulated population PTs and
TRs from newly recruited seedlings to saplings of 2-­m height. For
simulations with no temporal variation in demographic rates, PT
could be estimated for seven species and ranged from 22.3 to
200.1 years, with a median of 47 (Figure 3; Table S1). Species with
higher growth rates had shorter PTs. TR, however, depends both
on growth rates and survival functional form. TR numbers varied
by three orders of magnitude, with species requiring an average of
56 to more than 46,000 seedlings (with a median of 2,087) to make
a single sapling of 2-­m height (Figure 3; Table S1). Species with low
growth rates and low initial survival tended to have high TRs. The
results of sensitivity analysis are consistent with these findings. PT
is sensitive to the parameters of growth transition models, and is
less sensitive to the survival parameters and initial height in the
simulations (Appendix  S3). In contrast, TR is sensitive to initial
200 ● No temporal variation ●
With temporal variation MYRSSE
100
Passage time (year)
●
PRUNPH
●
50 GLOCAC
●
LITSAC
●
MACHTH ●
MACHZU
●
20 ENGERO
1 100 10,000
Transition ratio of seedlings to sapling
F I G U R E 3   Population-­level statistics estimated by 100
stochastic simulations of individual-­based models of 50,000
seedlings. Two types of IBMs were performed: With (solid circles)
or without (open triangles) temporal variation in demographic
rates. For IBMs with temporal variation, we started with a different
level of temporal correlation in demographic rates. In this figure,
we show the results of IBMs with 20 consecutive good years
as the starting condition. Solid lines represent 95% confidence
limits (CIs) of the estimates. The CIs for Litsea acuminata (LITSAC)
and Engelhardia roxburghiana (ENGERO) are too short to be
seen. The population-­level statistics for Schefflera octophylla
(SCHEOC) cannot be estimated because all of its seedlings died
before attaining 2-­m height
 13652745, 2021, 7, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/1365-2745.13677 by Readcube (Labtiva Inc.), Wiley Online Library on [13/07/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
2712       |
Journal of Ecology CHANG-­YANG et al.

height and the parameters of survival and the growth transition
models (Appendix S3), suggesting that the seedling-­to-­s apling tran-
sition was primarily limited by the low survival of early seedling
stages (<50-­cm high). The results of these simulations are also sup-
ported by field observations. In the 16 years of seedling monitor-
ing, none of the eight study species had newly recruited seedlings
reach 2-­m height.
In simulations with temporal variation in parameters, PTs and
TRs decreased as the period of consecutive good years increased
(Figure S2). TR was reduced more than 90%, while PT was only re-
duced between 10% and 20%. Compared with the simulations with
no temporal variation, a short period of high survival and growth
can greatly reduce TRs, while PTs only decrease marginally (Figure 3)
indicating the high sensitivity of mortality to annual variability.
Despite the low TRs for most study species, seedlings that attained
2-­m height had positive average growth rates that were faster than
seedlings that failed (Figure  4). These results suggest that consis-
tently fast growth rates at the early stage (i.e. seedlings <50-­cm
height) are critical to escape from the high mortality of this stage.
For S. octophylla, all seedlings died before attaining 2-­m height
in the simulations because of the low observed growth and survival
rates. The temporal variation in demographic rates was too low to
have a rescue effect. The sensitivity analysis showed that species
with low growth rates and survival were more sensitive to changes
in growth transition and survival parameters, indicating that some
species exist in a more fragile range of demographic space.
4 | D I S CU S S I O N
4.1 | The paths to the sapling stage that a new
seedling confronts
Studies that have investigated population dynamics of seedlings,
even when conducted longitudinally, offer limited snapshots of this
life-­history stage (Connell & Green, 2000). Our results demonstrate
that it might take decades for tree seedlings to attain 2-­m height,
and that the TRs from seedlings to saplings are low (Figure 3), further
emphasizing how short studies of seedling dynamics may not tell
the entire story of underlying ecological mechanisms. Survival and
growth combine to determine which seedlings successfully become
saplings, and how many individual stems in a population transition
per newly recruited seedling. Although components of these com-
bined dynamics are straightforward (e.g. faster growth increases the
rate at which a successful individual reaches sapling status [Figure 4]),
nonlinear features of survival rates combine with stochastic changes
in growth rates to create a more complex developmental landscape
between a seedling and its successful recruitment into the sapling
class. The influences of biotic and abiotic environmental variables on
both growth and survival further alter this developmental landscape.
We hope that understanding how features of a landscape of seed-
ling development determine population dynamics may guide future
research into specific mechanisms that forge this landscape, such as
pathogens, resources and disturbances.

ENGERO GLOCAC
0.12 0.4
Density

Density

0.08 0.3
0.2
0.04
0.1
0.00 0.0
0 20 40 60 0 20 40 60
Averge growth rate (cm/year) Averge growth rate (cm/year)

LITSAC MACHTH
0.25
0.20 0.2
Density

Density

0.15
0.10 0.1
0.05
0.00 0.0
0 20 40 60 0 20 40 60
Averge growth rate (cm/year) Averge growth rate (cm/year)
F I G U R E 4   Probability density
MACHZU MYRSSE distributions of average growth rates of
10.0
0.3 seedlings that attain 2-­m height (reds) or
7.5
died before reaching this target (blues)
Density

Density

0.2
5.0
in individual-­based model (IBM) with
0.1 2.5
temporal variation in demographic rates.
0.0 0.0
0 20 40 60 0 20 40 60
Each of the 100 stochastic simulations
Averge growth rate (cm/year) Averge growth rate (cm/year) is represented by one density curve.
The dashed vertical lines denote zero
PRUNPH
growth rate. Note that densities are
0.5
0.4 relative to the separate results (success or
Density

0.3 failure) and are not comparable between

0.2 results, as many more stems failed than
0.1
0.0
succeeded (the success distribution
0 20 40 60 would not be visible if scaled to the total
Averge growth rate (cm/year) population)

CHANG-­YANG et al.
4.2 | Compounding survival
Tree survival probabilities are multiplicative. Thus slight changes in the
survival rate can have a large impact in overall chances of surviving long
time intervals. In fact, life expectancy is halved every time as mortality
rates are doubled (e.g. from 1.5% mortality to 3% mortality may af-
fect only a few stems every year, but the compounding nature of this
change doubles the turnover time of the population). In the context
of our findings, it means that periods of low survival, such as for small
individuals, can have a huge influence on the number of individuals that
survive the periods necessary to reach the relative ‘safety’ of larger life-­
history stages. For instance, L. acuminata and M. thunbergii show simi-
lar survival curves, but the minor difference in early seedling survival
results in a great difference in the TRs between seedlings and sapling.
4.3 | Interaction between growth and the
shape of the survival curve
There are two ways to facilitate recruitment, which are not mutually
exclusive: size-­dependent survival can increase (Figure 1a) or growth
rates can accelerate more rapidly with increases in size (Figure 1b,c).
The former alleviates the relatively low probabilities of successful
recruitment for individuals without changing their PTs, the latter ac-
celerates the PT to size classes with fewer or less severe risks.
Our estimates for the ratio of seedlings to saplings are similar to
the estimates from a tropical forest in Peru (Terborgh et al., 2014)
that looked only at the comparison of observed seeds and saplings
(i.e. they did not simulate a dynamic life history from data). We found
that the species with a high ratio of seedlings to saplings tended to
have long PTs. This finding seems to be counter-­intuitive to the ex-
pectation that there is a growth-­survival trade-­off: fast-­growing
species usually have lower survival rates than slow-­growing species,
and thus have short PTs and high TRs from seedlings to saplings.
However, while the PTs during seedling-­to-­sapling transitions were
primarily determined by growth rates, the ratio of seedlings to sap-
lings was driven by both growth and survival. For example, L. acum-
inata and M. seguinii had similar seedling survival but very different
growth rates, which resulted in large differences in the numbers of
seedlings per sapling. Slow-­growing species might spend more time
in the very early seedling stage and be exposed to higher mortality
risk longer than fast-­growing species (Moles & Westoby, 2006), and
thus increase the TRs from seedlings to saplings.
Under a closed forest canopy, seedlings can have extremely
low growth rates due to the low-­light environment, and thus might
persist decades in the understorey if mortality remains low enough
(Antos et  al.,  2005; Delissio et  al.,  2002). Considerable variation
has been observed in previous estimates on the PTs from newly
recruited seedlings to saplings of 1-­cm DBH. In a neotropical rain-
forest in Costa Rica, Clark and Clark (2001) showed that it might
take 4–­12 years for a seedling of 50-­cm high to attain 1-­cm DBH for
nine canopy or emergent tree species. Similarly, in a subalpine forest,
tree species may take 5–­20  years to achieve 1-­cm DBH (Landis &
13652745, 2021, 7, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/1365-2745.13677 by Readcube (Labtiva Inc.), Wiley Online Library on [13/07/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Journal of Ecology |
      2713
Peart, 2005). In contrast, in a tropical seasonal forest in Panama, tree
species, especially shade-­tolerant species, might spend decades in
these early life stages (Hubbell, 1998). In a temperate forest, Antos
et al. (2005) also showed that it might take more than a century from
germination to 1.3-­m height in the closed understorey for four co-
nifer species. Our findings align with these expectations of long PTs
from seedling-­to-­sapling stage.
Despite the relatively high-­light levels in the understorey of
the Fushan subtropical rainforest due to frequent typhoon distur-
bances (Lin et al., 2011; Yao et al., 2015), our findings suggest that
it might take many decades for a newly recruited seedling to reach
2-­m height (Figure 3). The high-­light environment in the forest floor
and moist climate in Fushan support a dense understoery of shrubs
and ferns (Su et al., 2007), which limit tree recruitment by reducing
light levels or hampering their establishment at small sizes (Beckage
et al., 2000; Harmon & Franklin, 1989; Nakashizuka, 1989; Yamamoto
et al., 1995). This also demonstrates that Fushan does indeed have
a critical size threshold (a ‘danger zone’) that seedlings must escape
in order to achieve the long-­term relatively higher survival rates that
allow them to persist in the understorey over the many decades it
takes to become a reproductive individual. The relatively long PTs
and high TRs during the seedling stage also suggest that the pro-
cesses which determine the long-­term survival and growth may be
critical to overall community dynamics. Considering how the tempo-
ral scales of different ecological processes match with the duration
of different life-­cycle stages can help us better evaluate their contri-
butions to community structure and composition.
4.4 | Processes that might change the
demographic landscape
Critically, a certain period (either sustained or intense) of fast growth
seems crucial for seedlings to escape from the early stage high mor-
tality evident across species regardless of their life-­history strate-
gies. Temporal variation in seedling demographic rates, especially
rare, exceptionally high growth rates, is an essential part of popula-
tion models if they are to accurately capture community assembly
and dynamics. Our study included species with varying life-­history
strategies (both light-­demanding and shade-­tolerant) as well as can-
opy and subcanopy life-­forms. Therefore, we believe the consider-
able temporal variation in seedling vital rates we observed indicate
broad patterns of the entire Fushan forest community.
Environmental fluctuations may drive temporal variation in seed-
ling demography, and in turn influence population dynamics (Bachelot
et al., 2015; Ibáñez et al., 2007; Valverde & Silvertown, 1998). Our
results indicated that a period of high seedling survival and growth
would substantially reduce the numbers of seedling per sapling and
decrease the PTs during the seedling-­to-­sapling transition for both
light-­demanding and shade-­tolerant species (Figure S2). Many stud-
ies suggest that the growth of suppressed seedlings can be released
after canopy gap formation, especially for gap-­dependent species
(e.g. Brokaw,  1985; Canham,  1985; Collet et  al.,  2001; Runkle &

|
2714      
Journal of Ecology
Yetter,  1987). However, unlike in most closed canopy forests, in
Fushan, the understorey light levels are relatively high and similar
in canopy gaps and non-­gaps (Yao et  al.,  2015). Thus it is unlikely
that the growth release of seedlings (switching to the fast growth
group) in Fushan is caused solely by canopy gaps. Instead, strong but
relatively short climate oscillations, such as prolonged dry or plu-
vial periods associated with El Niño-­Southern Oscillation (ENSO) or
Pacific Decadal Oscillations (PDO), may lead to a sustained period
of high seedling survival and growth, which could result in a pulse of
successful recruitment (Brown & Wu, 2005; Pederson et al., 2014).
More research should focus on these potential causes, especially
in forests with similar demographic dynamics but with different en-
vironmental constraints. Although biotic interactions also can have
important impacts on seedling demography (e.g. competition, her-
bivory or plant–­pathogen associations [Alexander et al., 2015; Chen,
Swenson, et al., 2019; Chen, Wang, et al., 2019; Ibáñez et al., 2013;
Uriarte et  al.,  2018]), these effects are largely negative (but see
Corrales et  al.  (2018) on mycorrhizal associations). Negative influ-
ences are implicitly captured by our model through the survival
functions, but fundamentally serve to remove individuals from the
population and not promote their transition to saplings. Regardless
of the specific mechanisms involved, we believe that it is clear that
sustained fast growth and high survival must occur to promote
seedlings to later life-­history stages, and therefore, these promot-
ing mechanisms may best explain the broad-­scale and long-­lasting
effects of seedling dynamics on forest communities.
5 |  CO N C LU S I O N S
The seedling stage marks the greatest reduction in population size
in tree life history. Despite a wealth of studies on seedling dynam-
ics, converting data collected from individuals into insights of for-
est community assembly and dynamics is still a great challenge. The
process-­based demographic models in this study capture the char-
acteristics of extensive seedling demographic data in a subtropical
cyclone forest. By integrating vital rate models through stochastic
simulations, we translated measurements of individual seedlings into
inference for population dynamics. The estimated PTs from newly
recruited seedlings to saplings of 2-­m height were surprisingly long
and the ratio of seedlings to saplings was high in Fushan. Consistently
fast growth is essential for tree species to go through this bottleneck
in their life cycle. Our results highlight the importance of conceptu-
alizing the seedling stage as a long part of the entire tree life cycle.
Considering how consequences of seedling survival and growth in-
teract far beyond the usual time that seedling studies are conducted
is important if the results of experimental and observational studies
on seedling demography are to be correctly interpreted and incorpo-
rated into larger models of forest dynamics.
AC K N OW L E D G E M E N T S
The authors thank the staff and student volunteers for the assis-
tance in the field work, and the Fushan Research Center, Taiwan
13652745, 2021, 7, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/1365-2745.13677 by Readcube (Labtiva Inc.), Wiley Online Library on [13/07/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
CHANG-­YANG et al.
Forestry Research Institute, for the long-­term logistic support.
This work was supported by grants from Taiwan Forestry Research
Institute to C.-­F.H., grants from Taiwan Forestry Bureau to C.-­F.H.
and I.-­F.S., and grants from the Ministry of Science and Technology
to I.F.S. and C.-­H.C.-­Y.
AU T H O R S ' C O N T R I B U T I O N S
C.-­H .C.-­Y. and S.M.M. conceived the research idea, analysed the
data and wrote the paper, with substantial feedback from J.N.;
C.-­H .C.-­Y., J.N. and S.M.M. designed the methodology; C.-­H .C.-­Y.,
C.-­L .L., C.-­F.H. and I.-­F.S. collected the data; all the authors con-
tributed critically to the drafts and gave their final approval for
publication.
PEER REVIEW
The peer review history for this article is available at https://publo​ns.​
com/publo​n/10.1111/1365-­2745.13677.
DATA AVA I L A B I L I T Y S TAT E M E N T
The data supporting the results are available from the Dryad Digital
Repository https://doi.org/10.5061/dryad.n5tb2​rbvr (Chang-­Yang
et al., 2021).
ORCID
Chia-­Hao Chang-­Yang  https://orcid.org/0000-0003-3635-4946
Jessica Needham  https://orcid.org/0000-0003-3653-3848
Chang-­Fu Hsieh  https://orcid.org/0000-0003-4165-8100
I-­Fang Sun  https://orcid.org/0000-0001-9749-8324
Sean M. McMahon  https://orcid.org/0000-0001-8302-6908
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S U P P O R T I N G I N FO R M AT I O N
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Supporting Information section.
How to cite this article: Chang-­Yang C-­H, Needham J, Lu C-­L ,
Hsieh C-­F, Sun I-­F, McMahon SM. Closing the life cycle of
forest trees: The difficult dynamics of seedling-­to-­sapling
transitions in a subtropical rainforest. J Ecol. 2021;109:2705–­
2716. https://doi.org/10.1111/1365-­2745.13677