Ecology, 86(1), 2005, pp. 106–115
q 2005 by the Ecological Society of America
COLONIZATION–EXTINCTION DYNAMICS OF AN EPIPHYTE
METAPOPULATION IN A DYNAMIC LANDSCAPE
TORD SNÄLL,1,3 JOHAN EHRLÉN,2
AND
HÅKAN RYDIN1
1Department
of Plant Ecology, Evolutionary Biology Centre, Uppsala University, Villavägen 14,
SE-752 36 Uppsala, Sweden
2Department of Botany, Stockholm University, Lilla Frescativägen 5, SE-106 91 Stockholm, Sweden
Abstract. Metapopulation dynamics have received much attention in population biology and conservation. Most studies have dealt with species whose population turnover
rate is much higher than the rate of patch turnover. Models of the dynamics in such systems
have assumed a static patch landscape. The dynamics of many species, however, are likely
to be significantly affected by the dynamics of their patches. We tested the relative importance of local conditions, connectivity, and dynamics of host tree patches on the metapopulation dynamics of a red-listed epiphytic moss, Neckera pennata, in Sweden. Repeated
surveys of the species and its host trees were conducted at three sites over a period of six
years. There was a positive effect of connectivity, and colonizations mainly occurred in
the vicinity of occupied trees. Colonizations were also less likely on strongly leaning trees.
Local extinctions sometimes occurred from small trees with low local abundances but were
most often caused by treefall. Simulations of the future (100 years) dynamics of the system
showed that the metapopulation size will be overestimated unless the increased local extinction rate imposed by the dynamics of the trees is accounted for. The simulations also
suggested that local extinctions from standing trees may be disregarded in dynamic models
for this species. This implies that the dynamics of N. pennata can be characterized as a
patch-tracking metapopulation, where local extinctions are caused by patch destruction.
Key words: boreo-nemoral; colonization; dynamic landscape; epidemiology; epiphytic moss;
extinction; Neckera pennata; parameterization; patch-tracking metapopulation; single-tree patch; Sweden.
INTRODUCTION
Extensive empirical and theoretical work on metapopulations has increased our understanding of the dynamics of species in highly fragmented landscapes
(Hanski and Gaggiotti 2004). Most studies have concerned short-lived animals with a high colonization–
extinction rate. Important conclusions are that longterm persistence increases with increasing amounts of
habitat and connectivity, and that large and well-connected patches are most important for species persistence. High turnover rates imply that species can be
assumed to be in equilibrium with the landscape structure (Hanski 1998). In the long term, landscapes
change, e.g., through succession, and this must be accounted for in predicting species dynamics (Thomas
1994). The short-term dynamics of these species can
therefore often be predicted using population models
that assume that the landscape is static, but the changing number of patches must be accounted for when
predicting long-term dynamics (Thomas and Hanski
1997). In many other species, even the short-term extinction rate is potentially determined by patch destruction (Snäll et al. 2003). For such species, we also need
Manuscript received 17 March 2004; revised 8 June 2004;
accepted 22 June 2004. Corresponding Editor: T. P. Young.
3 E-mail: [email protected]
to account for patch dynamics for short-term predictions. In empirical studies where patch destruction has
been seen to cause local extinctions, the local extinction rate is still primarily set by stochastic extinctions
within intact patches (Sjögren-Gulve 1994, Nilsson
1997, Stelter et al. 1997, Wahlberg et al. 2002).
Several theoretical studies have investigated the importance of the dynamics of the patches on metapopulation dynamics or persistence. Patch longevity can
be more important than distance between patches (Fahrig 1992), and even more important than overall patch
amount for species persistence (Keymer et al. 2000).
Johnson (2000) examined in more detail how the time
to deterministic patch destruction influenced metapopulation persistence. The time that a patch is unsuitable
has also been shown to be important (Ellner and Fussman 2003). Spatially correlated patch destruction can
be detrimental, because it increases the temporal fluctuations in the regional carrying capacity of the metapopulation (Johst and Drechsler 2003).
The lack of empirical studies of metapopulations in
systems with dynamic patches can be explained by the
great difficulties and resource requirements involved
in data collection. Not only metapopulation data, but
also data on patch dynamics are required. As a consequence, most studies have guessed parameter values
(Stelter et al. 1997). However, attempts to make the
106
January 2005
EPIPHYTE METAPOPULATION DYNAMICS
107
TABLE 1. Simulation scenarios used to investigate the effect of connectivity and dynamics of the trees on future metapopulation size of Neckera pennata.
Metapopulation dynamics
Extinction rate
Scenario
Tree network
S1
S2
S3
S4
S5
static
static
dynamic†
dynamic, direct tree replacement‡
dynamic†
Colonization rate
fixed
depends
depends
depends
depends
on
on
on
on
From
standing trees
As
trees fall
fixed
fixed
fixed
fixed
no
yes
yes
yes
connectivity
connectivity
connectivity
connectivity
† Trees regenerate, grow, and fall.
‡ Trees fall at observed rates but are directly replaced; there is no growth and no other regeneration.
parameterization less subjective have been made
(Wahlberg et al. 2002; Snäll et al., in press), based on
simulations of the past landscape dynamics.
Single trees are patches for a large number of organisms in forest landscapes (Lowman and Nadkarni
1995, Palmer et al. 2000). They are dynamic patches
in that they emerge, grow, and fall. Furthermore, the
patch quality changes with the age of trees. Epiphytes,
which depend on the dynamics of the trees, can therefore increase our understanding of metapopulation processes in dynamic landscapes. Many epiphytes are confined to easily defined patches, trees, surrounded by an
inhospitable matrix, and have a restricted dispersal
(Overton 1996, Sillett et al. 2000, Gu et al. 2001, Walser et al. 2001, Dettki and Esseen 2003). Epiphytes
also can be negatively affected by modern forestry
(Gärdenfors 2000).
The dynamics of trees are largely determined by
small- and large-scale disturbances in the boreo-nemoral vegetation zone. This zone is dominated by coniferous trees but, in addition to typical boreal broadleaved trees, e.g., Betula spp., also includes more luxurious tree species such as ash tree Fraxinus excelsior
and Quercus robur (Engelmark and Hytteborn 1999).
Fires or human activities can affect the dynamics of
trees at a scale of several thousands of hectares (Dobson et al. 1997, Niklasson and Granström 2000). At a
smaller scale, interspecific interactions between trees
are important (Engelmark and Hytteborn 1999). The
typical successional trend of the boreal and boreo-nemoral landscape is from broad-leaved trees, establishing in great numbers, to conifers (Engelmark and Hytteborn 1999). A forest landscape thus consists of a
mosaic of different successional stages. At smaller
scales, up to hundreds of hectares, successional trends
in the numbers of trees of different species can be
observed. However, at a scale of thousands of hectares,
and at a constant disturbance regime, equilibrium in
number of trees of different species is expected.
The aims of this paper are twofold: first, we test the
relative importance of local factors, dispersal, and tree
dynamics on colonization and extinction dynamics of
the red-listed epiphytic moss Neckera pennata, whose
patches are broad-leaved trees in the boreo-nemoral
forest landscape. Based on our findings, we construct,
to our knowledge, the first parameterized simulation
model for a system consisting of a metapopulation and
its dynamic patches. Data from repeated surveys of the
metapopulation and its patches are utilized. Second,
we investigate the importance of the dynamics of the
trees on future N. pennata metapopulation size by simulating five scenarios that differ in assumptions regarding the dynamics of the metapopulation and its
patches (Table 1).
METHODS
Study system and empirical data
We studied the epiphytic moss Neckera pennata
Hedw. Its male and female organs are situated on the
same shot (autoicous), and it is dispersed by spores
(sized 24 mm) from frequently encountered sporophytes, or by stoloniform branches (Nyholm 1960). The
species is red-listed (Vulnerable), mostly found in old
forests (Gärdenfors 2000). Its host trees are the broadleaved trees, ash (Fraxinus excelsior), elm (Ulmus glabra), maple (Acer platanoides), aspen (Populus tremula), rowan (Sorbus aucuparia), lime (Tilia cordata),
oak (Quercus robur), and bird-cherry (Prunus padus).
The moss is considered a good indicator of occurrence
of other red-listed species (Nitare 2000).
A thorough survey of N. pennata at our study sites
revealed that it only grew on five individual trees with
a diameter at breast height (1.3 m; dbh henceforth) of
.5 cm. Hence, this diameter sets the lower limit of
what is considered a patch for N. pennata. On trees,
the abundance of N. pennata increases by radial growth
of single turfs (Wiklund and Rydin 2004) or by establishments of new turfs from spores, stoloniferous
branches, or fragments, originating from turfs on the
focal tree or a surrounding tree. The genetic structuring
suggests a metapopulation structure because different
turfs on a single tree are more similar than turfs on
different trees, although immigration from surrounding
trees occurs (Appelgren and Cronberg 1999). The probabilities of moss occurrence and abundance increase
TORD SNÄLL ET AL.
108
Ecology, Vol. 86, No. 1
TABLE 2. Dynamics of Neckera pennata and its host trees, host tree characteristics, and soil moisture conditions at the
studied sites.
Characteristic
Erken
Rörmyran
Valkrör
Number of host trees in 1997
Number of tree falls, 1997–1999
Number of tree falls, 1999–2001
Number of tree falls, 2001–2003
Number of new trees between 1997 and 2003
Number of trees occupied by N. pennata in 1997
Occupancy of N. pennata in 1997
Number of N. pennata colonizations, 1997–1999
Number of N. pennata colonizations, 1999–2001
Number of MP-extinctions, 1997–1999
Number of DET-extinctions, 1997–1999
Number of MP-extinctions, 1999–2001
Number of DET-extinctions, 1999–2001
Number of host tree species
Mean diameter of host trees (cm)
Mean depth of bark crevices of host trees (mm)
Mean tree inclination (8)
Proportion of host trees touched by spruce branch
Mean moisture value recorded at host trees
108
2
1
6
···
36
0.33
2
3
1
0
1
1
5
19.4
2.5
9.2
0.2
3.6
234
0
0
0
···
113
0.48
7
4
0
0
0
0
7
32.5
4.8
4.6
0.0
2.9
489
3
5
8
6
131
0.27
14
8
0
2
1
2
8
15.3
3.2
10.4
0.2
3.7
Notes: MP-extinction refers to an extinction of N. pennata from a tree that remains standing; DET-extinction refers to a
tree fall of a tree occupied by N. pennata.
with increasing tree diameter (Snäll et al. 2004b). As
an occupied tree falls, the local N. pennata population
usually, deterministically, goes extinct. Two years after
tree fall, the population is lost or in markedly bad condition.
The empirical data were collected at three sites in
the boreo-nemoral zone of Sweden (Rydin et al. 1999):
Erken (0.6 ha; 59852940 N, 188309160 E), Rörmyran (2.2
ha; 60859120 N, 188179580 E), and Valkrör (2.4 ha;
60839250 N, 18826980 E). At Erken and Valkrör, the host
trees for N. pennata were intermingled with other
broad-leaved trees and with Norway spruce (Picea abies). The approximate basal area proportions were 0.15,
0.35, and 0.50, for host species, other broad-leaved
trees (e.g., Alnus glutinosa), and Norway spruce, respectively. At Rörmyran, the corresponding basal area
proportions were 0.45, 0.10, and 0.45, but Norway
spruce trees almost exclusively occurred in the outer
part of the area. At all sites, ash was the most common
host tree, and the field layer indicated productive soil
conditions. The soil was drier at Rörmyran than at the
other sites (Table 2). Forestry had been conducted in
all sites, but Valkrör is a nature reserve at a late-successional stage.
In the autumn of 1997, we mapped all potential host
trees for N. pennata with a dbh $5 cm. We recorded
occurrence and local abundance (in square centimeters)
of N. pennata on each tree. The abundance is the total
moss cover, made up by one or several ramets or genets
(Appelgren and Cronberg 1999). It thus represents the
local population size. In the autumns of 1999 and 2001,
we again recorded occurrence of N. pennata on all host
trees. The local abundance on newly colonized trees
was usually ;2 cm2 (this value was assumed in fitting
the statistical models, see ‘‘21local abundance’’ in Statistical analysis). There is a well known problem in
metapopulation studies of detecting all occurrences,
and failing to do so can strongly affect parameter estimates (Moilanen 2002, MacKenzie et al. 2003). However, because our study species rarely occurs above a
height of 3m (Snäll et al. 2004b), and because it has
a protruding growth form, it is easily surveyed from
the ground. Based on measurements of growth rates
(Hagström 1998) and studies of turf growth (Wiklund
and Rydin 2004), we concluded that six recorded colonizations must, in fact, have been present and overlooked in 1997, and we corrected the data accordingly.
Data from the previous surveys were always brought
into the field.
In the autumn of 1999, 2001, and 2003, we recorded
which trees had fallen, and in 2003, we mapped all new
patches, i.e., trees that had grown to 5 cm in dbh since
1997. By coring them and measuring diameter growth
during the preceding six years (after soaking the cores
in water for 15 minutes), we were able to confirm that
these trees were ,5 cm in 1997.
For each host tree, we recorded the following independent variables that were used in the statistical
analysis: study site, species, dbh (in centimeters), the
depth of bark crevices (in millimeters) 50 cm above
the ground, and tree inclination (in degrees). We noted
if a branch from a spruce touched the host tree, because
rainwater percolating through coniferous tree branches
might affect host tree bark chemistry and bryophyte
viability (Gustafsson and Eriksson 1995). We estimated
soil moisture for a 2 m radius zone around each host
tree on a four-level ordinal scale (Anonymous 1997):
1, dry (ground water level .2 m below soil surface);
2, mesic (groundwater level 1–2 m below soil surface);
3, mesic-moist (ground water level ,1 m below soil
surface, flat ground); and 4, moist (ground water level
,1 m below soil surface, visible in hollows).
EPIPHYTE METAPOPULATION DYNAMICS
January 2005
For parameterizing a tree growth model, we cored
host trees at breast height at Erken and Valkrör. Their
diameter growth during the last 10 years was measured
(after soaking the cores in water for 15 minutes). The
growth rate model was based on these measurements
and therefore reflects the recent late-successional conditions.
Statistical analysis
We identified variables that significantly affected the
probabilities of local colonization of N. pennata and
probability of tree fall using generalized linear models
(GLM; McCullagh and Nelder 1989) with binomial error distribution and logit link (logistic regression). We
also built the dynamic N. pennata metapopulation model and the dynamic tree fall model using GLMs. We
did not analyze which factors affected local extinctions
because of the low number recorded.
The analysis of the effects of local conditions and
connectivity on colonization probability of a tree was
based on trees that were not occupied by N. pennata
in 1997 and 1999, recording colonization in 1999 and
2001, respectively. The binary dependent variable included the outcomes colonization (1) or no colonization
(0). We choose this type of state-transition type model
because a successional change of the system was expected on the spatial scale studied. Using logistic regression, we first tested single variables for local conditions one by one, and selected those with P values
,0.40 in likelihood ratio tests (McCullagh and Nelder
1989). Next, we built a multiple-start model with these
selected variables and included biologically reasonable
two-way interactions and squared variables. We furthermore added a connectivity measure (Hanski 1999)
to the GLM, which corresponds to fitting the dispersal
kernel for N. pennata. We choose a lognormal function
that is intermediate, in terms of thickness of the tail,
between the negative exponential and the power function. Functions similar to the lognormal have been
found to fit better to the dispersal of plants (Clark et
al. 1999), and our preliminary analysis confirmed this.
The full start model with the connectivity measure
included nonlinear parameters and was therefore a generalized nonlinear model (GNLM) given by
logit(Ci ) 5
Ob x
m im
1b
|
O p exp{2a[ln(d )] }Ab
j±i
j
ij
|
2
g
j
|
Si
where, for the ith tree, the binomial parameter Ci is the
probability of colonization, xim is the value of the mth
local variable assumed to affect Ci, and bm is the associated regression parameter. The second term, connectivity Si with regression parameter b, accounts for
the relation between Ci of the ith tree, and the occurrence of the epiphyte on the surrounding source trees
( j). The variable pj 5 1 if N. pennata occurs on tree
j; otherwise pj 5 0. The influence of each surrounding
109
potential source tree j is quantified by the lognormal
function of the distance dij in meters between the trees
i and j. The rate of decay is controlled by a, a parameter
to be estimated from the data. For trees that could potentially become colonized in 1999, Abj is local abundance of N. pennata in 1997, and for trees that could
potentially become colonized in 2001, Abj is local
abundance of N. pennata in 1997 1 2 (see Study system
and empirical data for an explanation of ‘‘21local
abundance’’). The exponent g scales local abundance
to rate of emigration.
The full start model was simplified by manual removal of single variables (backward elimination). The
criteria for stopping the removal of variables was AIC,
Akaike’s Information Criterion, (Akaike 1974, McCullagh and Nelder 1989), defined as AIC 5 22l 1
2p, where l is the maximized likelihood and p is the
number of parameters.
We did not calculate a P value for the connectivity
measure (Snäll et al. 2003). Because the confidence
intervals for the parameters of the GLMs and the
GNLM are asymmetric, we estimated them based on
the likelihood profile (Hudson 1971, Venables and Ripley 1999).
We identified variables that significantly affected the
probability of tree fall following the stepwise GLM
approach just described but without the connectivity
measure in the start model.
Parameterization of the simulation models,
and simulated scenarios
In order to investigate the importance of connectivity
and the dynamics of the trees on the predicted future
N. pennata dynamics and metapopulation size, we simulated five future scenarios of the N. pennata metapopulation at the old-growth Valkrör site. The scenarios
differed in assumptions regarding the dynamics of N.
pennata and its host trees. We chose the Valkrör site
because it was least affected by human land use.
All simulations were started at the conditions prevailing in 1997, in terms of spatial structure of the trees
and the epiphyte (Fig. 1). Each time step was two years.
The simulated unit was the single tree. We simulated
tree fall, tree dbh growth, and generation of new trees
in the described order. The N. pennata dynamics took
place after the tree processes had been simulated. For
each unoccupied tree, N. pennata colonization was simulated. Two types of local extinctions from an occupied
tree were simulated: stochastic extinction from a standing tree or deterministic extinction as an occupied tree
fell. We simulated 100 years, and for each scenario we
ran 1000 replicates. For each time step, we calculated
the mean of the replicates and constructed 95% confidence envelopes for the predictions by plotting the
upper and lower 2.5% percentiles of the simulated values. We report number of occupied trees, number of
trees, and occupancy (number of occupied trees/number of trees).
TORD SNÄLL ET AL.
110
Ecology, Vol. 86, No. 1
ing to the empirically observed rates. The tree network
was thus dynamic; trees fell, were generated, and grew.
Tree fall probability was affected by tree diameter according to the following model (null deviance 5 117.1,
df 5 754) fitted to our empirical data
logit(Fi) 5 b0 1 b1dbhi 1 b2 dbhi2
where Fi is the probability that tree i falls, dbhi is the
diameter of tree i, and b0 5 22.763 (95% CI, 21.401–
4.097), b1 520.126 (95% CI, 20.265 to 20.021), and
b2 5 0.001 (95% CI, 0.0002–0.0023).
Tree diameter growth (in centimeters per time step)
was simulated according to the fitted model (R2 5 0.50,
df 5 61)
Growthi 5 b0 1 b1dbhi
FIG. 1. The distribution pattern of the epiphytic moss
Neckera pennata and its host trees at the Valkrör site in Sweden, 1997. Each open circle represents an unoccupied tree,
and each solid circle represents a tree occupied by N. pennata.
Scenario 1.—In the first scenario (S1, Table 1), the
tree network was kept static. We kept the extinction
(Ei) and colonization (Ci) probabilities fixed (i.e., independent of connectivity) at their empirically observed mean values, Ei 5 3/575 5 0.0052 and Ci 5
38/1077 5 0.0353 (Table 2).
Scenario 2.—In the second scenario (S2, Table 1),
we investigated the effect of connectivity-dependent
colonizations, which is a commonly adopted assumption in models for classic metapopulation dynamics
(Hanski 1994, Harrison and Taylor 1997, Hanski 2001).
The tree network was kept static. Colonization probability
of N. pennata was affected by connectivity according to
the following colonization model (null deviance 5 328.4,
df 5 1070) fitted to our empirical data:
logit(Ci ) 5 b0 1 b1
O p exp{2a[ln(d )] }dbh .
j±i
j
ij
2
g
j
Here Ci is probability of colonization, b0 524.59 (95%
CI , 25.37 to 2 3.87), b 1 5 0.03 (95% CI, 0.02–0.05),
a 5 0.29 (95% CI, 0.14–0.49), and g 5 0.71 (95% CI,
20.03–1.65). We chose dbhj instead of Abj because we
lacked data on the rate of abundance increase on the
trees. The choice of dbh was based on an established
correlation between local abundance of N. pennata and
dbh of occupied trees (R2 5 0.10, df 5 278, P , 0.001).
In the classic metapopulation model, local extinctions are usually assumed to be dependent on local
population size, often estimated from patch area. We
observed only three extinctions and could not find support for local abundance or any local environmental
variable influencing the local extinction probability;
therefore we fixed it at the observed mean probability
(0.0052).
Scenario 3.—In the third scenario (S3, Table 1), tree
and metapopulation dynamics were simulated accord-
where b0 5 0.197 (SE 5 0.030, P ,0.001), b1 5 0.009
(SE 5 0.001, P ,0.001). We assumed that trees with
a dbh larger than the maximum observed among trees
used for fitting the model (65 cm), grew at a the same
rate (0.76 cm per time step) as this largest tree.
Trees were generated according to a Poisson process
with a mean of two trees per two years, which corresponds to the observed rate of tree regeneration (Table
2), and were assigned the start diameter 5 cm. It has
been found that the spatial pattern of patches can affect
metapopulation dynamics (Hanski and Ovaskainen
2000, Flather and Bevers 2002). Therefore, we retained
the observed (Fig. 1) aggregated pattern of trees over
time by first fitting a statistical model (Poisson cluster
process) to the empirical tree pattern and then locating
new trees using the fitted model (Appendix). Locating
the trees according to a random Poisson process provided similar simulation results (not shown).
The local colonization probability was affected by
connectivity, as in Scenario 2. Local extinctions occurred with the fixed probability (0.0052, Scenario 2),
or deterministically as a tree fell.
Scenario 4.—In the fourth scenario, (S4, Table 1),
we examined the effect of extinctions caused by tree
fall only, by keeping patch configuration constant over
the simulation. Metapopulation dynamics were simulated as in Scenario 3. Tree fall was also simulated as
in Scenario 3, but fallen trees were directly replaced
by a new, unoccupied tree with the same dbh at the
same location. No other regeneration took place and
trees did not grow.
Scenario 5.—In the fifth scenario (S5, Table 1), we
investigated the effect of simplified metapopulation dynamics, as assumed in the patch-tracking metapopulation model (Snäll et al. 2003). Tree and metapopulation dynamics were thus simulated as in Scenario 3,
but local extinctions only occurred as trees fell.
Software
The statistical analyses and dynamic modeling were
performed with R 1.8.0 (R Development Core Team
2003), using the add-on libraries geoR 1.3.16 (Ribeiro
EPIPHYTE METAPOPULATION DYNAMICS
January 2005
TABLE 3.
111
Likelihood ratio tests of the effect of single variables on colonization probability of Neckera pennata.
Variable
N
Null
deviance
Deviance
reduction
df
P
Study site
Tree species
dbh
Bark†
Tree inclination
Spruce branch‡
Soil moisture
Connectivity (Si)
dbh squared
Bark squared
Tree inclination, squared
Tree species 3 bark
1070
1070
1070
1012
1028
976
1046
1070
1070
1012
1028
1012
328.4
328.4
328.4
324.1
325.3
321.3
326.6
328.4
328.4
324.1
325.3
324.1
1.1
5.1
1.1
2.7
2.2
1.2
1.5
19.5
1.5
1.6
2.9
1.8
2
7
1
1
1
1
4
3
1
1
1
6
0.57
0.65
0.30
0.10
0.14
0.27
0.83
···
0.22
0.21
0.09
0.94
Notes: The P value is based on the assumption that deviance reduction follows the x2 distribution. The P value for
connectivity (Si) was not calculated (see Statistical analysis for explanation). The three models with squared variables also
included the untransformed variables, and the model with the interaction also included the two single variables.
† Depth of bark crevices.
‡ Spruce branch touching the host tree.
and Diggle 2001), MASS 7.1.10 (Venables and Ripley
1999), spatstat 1.3.3 (Baddeley and Turner 2004), and
splancs 2.1.9 (Rowlingson and Diggle 1993), all freely
available online.4 We wrote our own R-code for fitting
the connectivity term, for estimating the confidence
envelopes for a and g, and for simulating the dynamics
of the system.
RESULTS
The number of trees occupied by Neckera pennata
increased during the study period (Table 2). We observed 38 colonizations of trees. Three local extinctions occurred from standing trees and five deterministic extinctions occurred as occupied trees fell. The
number of trees that fell differed between sites. At
Valkrör, where we had mapped tree recruitment, the
number of trees decreased during the study period.
Connectivity was the most important variable in explaining the colonization probability of trees, judged
by its large deviance reduction in the first tests of the
effect of single variables (Table 3). In the final multiple
model (null deviance 5 325.3, df 5 1028), the large
effect of connectivity remained (deviance reduction 5
19.1, P not calculated). Colonizations mainly occurred
in the vicinity of occupied trees, as given by a best fit
of a 5 0.25 (95% CI, 0.13–0.47), and g 5 0.44 (95%
CI , 20.40–1.12). Moreover, the final multiple model
showed that trees that leaned considerably had a low
probability of becoming colonized, which was evident
as a negative effect of inclination (squared) of the tree.
However, the relative effect of this second independent
variable was small, as judged by the low model deviance reduction (5.2, P 5 0.02). We therefore excluded this variable from the colonization function of
the metapopulation model.
Three local extinctions occurred, which give a mean
extinction probability of 0.0052. The abundances of N.
4
^http://www.r-project.org&
pennata occurrences that went extinct were of 0.5, 2,
and 4 cm2 prior to the extinctions, and the diameter of
these trees were 22, 7, and 12 cm, respectively.
In all scenarios, the metapopulation size of N. pennata was predicted to increase over the next century
(Fig. 2). Incorporation of tree dynamics into the model
resulted in decreases in tree number and in smaller
increases in moss metapopulation size 80 years from
now (S3–S5 vs. S2). The predicted metapopulation size
was similar in all scenarios that included tree dynamics.
Under the assumption of a static tree network, the model with a connectivity-dependent colonization probability (S2) predicted higher metapopulation size than
the one with a fixed colonization rate (S1). The latter
predicted the lowest future occupancy.
DISCUSSION
Our study highlights several important features of
metapopulation dynamics in epiphyte–tree systems as
compared with other types of metapopulation systems.
It is the first empirical study demonstrating that connectivity has important effects on colonization probability in epiphyte metapopulations. We also found that
local conditions influenced colonization probability.
Local extinctions mainly occurred as trees fell, supporting the notion of a patch-tracking metapopulation.
Our simulations showed that failing to account for the
dynamics of the trees will overestimate future metapopulation size within one century.
The importance of connectivity on colonizations in
epiphytes, as in other metapopulations (Hanski 1998,
1999, 2001), is a consequence of restricted dispersal.
Our study confirms the steep dispersal functions, suggested by analyses of putative (rather than observed)
colonizations (Snäll et al. 2003; Snäll et al., in press),
and diaspore deposition patterns around known sources
(Overton 1996, Walser et al. 2001, Dettki and Esseen
2003). The restricted dispersal range has also been verified based on occupancy patterns (Gu et al. 2001, Hed-
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Ecology, Vol. 86, No. 1
FIG. 2. Five simulation projections of (A) the number of trees occupied by Neckera pennata, (B) the number of trees,
and (C) N. pennata occupancy (number of occupied trees/number of trees) at different times 0–100 years after 1997 at
Valkrör. The lines refer to the means of 1000 replicates. The error bars indicate the 95% confidence intervals at 20, 40, 60,
80, and 100 years.
enås et al. 2003, Johansson and Ehrlén 2003), spatial
genetic structure (Appelgren and Cronberg 1999, Snäll
et al. 2004a), and establishment experiments (Sillett et
al. 2000).
In our study system, the probability that a tree became colonized by N. pennata was lower on trees that
leaned strongly. This finding agrees with the increasing
number of studies that show significant effects of local
conditions on colonization probability in metapopulations (Moilanen and Hanski 1998, Hanski and Singer
2001, Fleishman et al 2002, Moilanen and Nieminen
2002). Colonizations may be hindered on leaning trees
by high abundance of competing bryophytes (T. Snäll,
personal observations), by less suitable bark chemistry
and moisture conditions, or because of lower tree vitality. In many studies of epiphyte occupancy, tree diameter has been found to be the most important predictor. Different mechanisms have been suggested
(Snäll et al. 2003). Our results suggest that diameter
reflects the time that the tree has been available for
colonization (Rose 1992, Kuusinen and Penttinen 1999,
Snäll et al. 2003) because diameter does not affect
colonization probability, but occurrence (Snäll et al.
2004b).
A few local extinctions did occur from trees that
remained standing; these trees were small and had low
moss abundances. However, local extinctions because
of tree fall were almost twice as common. Previous
studies have shown that extinctions caused by patch
destruction occur, but that stochastic extinctions are
more common in pool frogs (Sjögren-Gulve 1994), beetles (Nilsson 1997), grasshoppers (Stelter et al. 1997),
and butterflies (Wahlberg et al. 2002). Patch dynamics
are likely to be most important in sessile organisms,
such as epiphytic plants. Our results suggest that our
study system is different from classic systems in which
patch area, reflecting population size, has been put forth
as a first-order landscape feature explaining metapopulation dynamics (Hanski 1999). Dynamics as in our
system may also be common, for instance, in wooddecomposing fungi or invertebrates confined to rock
pools.
Our simulations predicted a decrease in numbers of
potential host trees in the coming century, yet the size
of the N. pennata metapopulation was predicted to increase (Fig. 2). The most realistic scenario is S3, because both tree and metapopulation dynamics were
simulated according to empirically observed rates. This
scenario predicted lower metapopulation size 80 years
from now than the scenario with classic metapopulation
dynamics in a static landscape (S2). This conclusion
was robust to doubling the local extinction rate (compared to the observed) in the simulations (not shown).
The scenario with direct replacement of fallen trees,
i.e., constant tree numbers (S4), predicted a metapopulation size similar to that of the other scenarios with
tree dynamics (S3, S5). This suggests that the smaller
metapopulation sizes in these three scenarios are
caused by the increased extinction rate imposed by falling trees, rather than an effect of decreasing tree num-
January 2005
EPIPHYTE METAPOPULATION DYNAMICS
bers. Both scenarios with a dynamic tree network, either accounting for (S3) or ignoring (S5) local stochastic extinctions from standing trees, predicted similar future metapopulation sizes. The result was robust
to doubling the local extinction rate (not shown). This
suggests that local stochastic extinctions may be disregarded in models of the dynamics of N. pennata, and
that its dynamics can be characterized by the patchtracking metapopulation model (Snäll et al. 2003). The
two scenarios with static landscapes (S1, S2) predicted
different future metapopulation sizes that approached
the equilibrium metapopulation levels given by the colonization and extinction rates. The scenario with constant colonization and extinction rates (S1) predicted
a lower metapopulation size than S2 and the lowest
occupancy, despite the assumption of a global dispersal. The explanation is that this scenario does not
permit the positive feedback on colonization rate, following from increasing connectivity as the number of
occupied trees increases.
Our simulations underline that it is important to account for the dynamics of the trees when predicting
future epiphyte metapopulation size. The present study
is, to our knowledge, the first comparison of predicted
metapopulation dynamics between models including,
or disregarding the dynamics of the patches, which
have been parameterized from empirical data. The large
importance of patch dynamics for long-term metapopulation dynamics previously has been demonstrated
only in spatially explicit simulations of hypothetical
species (Fahrig 1992, Johnson 2000, Keymer et al.
2000, Ellner and Fussman 2003, Johst and Drechsler
2003), or in simulations including many guessed parameter values (Stelter et al. 1997, Wahlberg et al.
2002; Snäll et al., in press).
Implications for long-term, large-scale dynamics
We expected the predicted increase in metapopulation size and decrease in number of host trees are in
the 2.4-ha old-growth successional forest of this study.
A metapopulation size as high as that predicted for N.
pennata has never been reported. However, even our
empirically observed metapopulation sizes are higher
than those previously reported. Possible explanations
are that cutting operations keep the number of suitable
trees down and do not allow the predicted metapopulation size to be attained (.95% of forest in this region
is managed for forestry), or simply that this is an overlooked species. In any case, our qualitative conclusions
of the importance of patch dynamics on metapopulation
dynamics are most probably robust to potential errors
in the predicted tree numbers and metapopulation sizes.
The explanation for the decreasing number of host
trees is competition from Norway spruce, which typically increases its dominance in these mesic-moist boreo-nemoral stands (Engelmark and Hytteborn 1999).
However, during this development toward increased
spruce dominance, small-scale gaps will be created in
113
which host trees for N. pennata may regenerate. The
final exclusion of the host trees therefore may take a
long time. The exclusion of the host trees will, of
course, shift the predicted increase in N. pennata metapopulation size to a decrease in the far future. The N.
pennata decrease will result from the overall decrease
in host tree numbers, but also from the increasing distance between trees, which leads to a lower colonization rate because of the restricted dispersal range. The
final metapopulation extinction from the stand will
probably take a long time because of the species’ inertia
to local extinctions on standing trees.
The long-term metapopulation persistence over large
spatial scales, thousands of hectares, depends on the
establishment of new host tree stands. Moreover, N.
pennata must colonize these stands at a rate that is
higher than the rate of disappearance of host tree stands
because of natural succession or forestry operations.
In natural boreo-nemoral landscapes, fire is the key
natural disturbance agent that facilitates establishment
of broad-leaved trees, because fire often kills spruce
and increase the probability of regeneration of broadleaved trees (Engelmark and Hytteborn 1999). In the
more northern boreal region, fires used to occur at time
intervals from 50 to .500 years (Niklasson and Granström 2000); in our more southern study region, the
mean frequency was higher (Granström 1993). During
the past century, the burned area, however, has been
very small. Past agricultural practices also favored the
host trees, notably Fraxinus, and many deciduous
stands are remnants from older managed wooded meadows (Diekmann 1999). In recent decades, forestry has
dramatically decreased the number of host trees (Snäll
et al. 2004b), rather than facilitating their establishment.
Our simulations have two important implications for
long-term conservation of N. pennata. First, management efforts should focus on the number of available
host trees and the creation of new host trees, rather
than on avoiding extinctions from trees in closed forest
stands. Second, to ensure a sufficient number of colonizations, trees should be allowed to become old
enough for N. pennata to colonize, produce, and disperse its diaspores, and new stands should be located
in the vicinity of stands occupied by N. pennata because of its restricted dispersal range.
ACKNOWLEDGMENTS
We thank Ilkka Hanski, Bob O’Hara, and Otso Ovaskainen
for valuable comments on the manuscript. Mats Niklasson
shared his experience in dendrochronology. Especially Anna
Hagström, but also Karin Andersson, Helena Persson, Jörgen
Rudolphi, and Camilla Wessberg, are thanked for help with
data collection. T. Snäll acknowledges financial support from
‘‘Bjurzons fond,’’ KVA, and Swedish Phytogeographical Society; J. Ehrlén from VR and FORMAS; and H. Rydin from
FORMAS.
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APPENDIX
A model for locating regenerated trees is available in ESA’s Electronic Data Archive: Ecological Archives E086-007-A1.