J Appl Ecol. 2020;57:1581–1592.
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1581wileyonlinelibrary.com/journal/jpe
Received: 2 March 2020
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Accepted: 8 April 2020
DOI: 10.1111/1365-2664.13661
RESEARCH ARTICLE
Plant traits, biotopes and urbanization dynamics explain the
survival of endangered urban plant populations
Greg Planchuelo1 | Ingo Kowarik1,2 | Moritz von der Lippe1,2
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium,
provided the original work is properly cited.
© 2020 The Authors. Journal of Applied Ecology published by John Wiley & Sons Ltd on behalf of British Ecological Society
1Department of Ecology, Ecosystem
Science/Plant Ecology, Technische
Universität Berlin, Berlin, Germany
2Berlin-Brandenburg Institute of Advanced
Biodiversity Research, Berlin, Germany
Correspondence
Greg Planchuelo
Email: greg.planchue[email protected]
Funding information
DAAD / Technische Universität Berlin; Hans
Böckler Stiftung, Grant/Award Number:
398226
Handling Editor: Peter Manning
Abstract
1. With accelerating urbanization, the urban contribution to biodiversity conservation
becomes increasingly important. Previous research shows that cities can host
many endangered plant species. However, fundamental questions for urban na-
ture conservation remain open: to what extent and where can endangered plant
species persist in the long term and which mechanisms underlie population
survival?
2. We evaluate the survival of 858 precisely monitored populations of 179 endan-
gered plant species in Berlin, Germany, by assessing population survival through-
out different urban ecosystems over a period of 7.6 years on average. By linking
population survival to various landscape variables and plant traits, we unravel the
underlying drivers.
3. More than one–third of populations went extinct during the observation period.
Population survival was inversely correlated to the increase in impervious sur-
faces in the vicinity following the first 11 years after the fall of the Berlin wall.
Additionally, populations in semi-natural habitats like forests and bogs were sur-
prisingly more prone to local extinction than populations in anthropogenic habi-
tats. Survival was highest for competitive species with a preference for drier soils
(Ellenberg indicator for soil humidity).
4. Synthesis and applications. Considerable levels of local population extinction dem-
onstrate that the presence of endangered plants cannot be directly linked with
their long-term survival in cities. However, the survival of remaining populations
indicates opportunities for urban biodiversity conservation both within and out-
side conservation areas. The elucidated links between population survival, ur-
banization dynamics, biotope class and species traits support urban conservation
strategies that reduce the proportion of impervious surface, prioritize conserva-
tion management in forests and grasslands and explore the opportunities of green
spaces and built-up areas.
KEYWORDS
anthropogenic biotopes, biodiversity conservation, endangered plant species, plant traits,
population monitoring, population persistence, urban ecosystems, urbanization changes
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1 | INTRODUCTION
As urbanization accelerates globally, the question of the urban
contribution to biodiversity conservation is becoming increasingly
important (Kowarik & von der Lippe, 2018; McKinney, 2002; Nilon
et al., 2017; Parris et al., 2018). The number of urban conservation
studies has risen sharply in recent years (Shwartz, Turbé, Julliard,
Simon, & Prévot, 2014) and indicate considerable opportunities for
biodiversity conservation. Indeed, cities can be very rich in native
species (Aronson et al., 2014), including a considerable richness of
endangered plant species as reported from cities in Africa (Rebelo,
Holmes, Dorse, & Wood, 2011), Asia (Wang et al., 2007), Australia
(Ives et al., 2016), Europe (Kowarik & von der Lippe, 2018) and North
America (Lawson, Lamar, & Schwartz, 2008). From these insights, a
narrative regarding cities' contribution to biodiversity conservation
has developed, and with this several strategies to promote urban
biodiversity have been suggested. Classical approaches such as the
designation of protected areas are increasingly complemented by
integrative approaches arguing for a biodiversity-friendly manage-
ment of green spaces (Aronson et al., 2017; Chollet, Brabant, Tessier,
& Jung, 2018), a reconciliation of urban land use and biodiversity
conservation (Elmqvist et al., 2013), the integration of biodiversity in
urban design (Garrard, Williams, Mata, Thomas, & Bekessy, 2018) or
the promotion of urban wilderness (Hwang, Yue, Ling, & Tan, 2019;
McKinney, Kowarik, & Kendal, 2018).
However, strategies to promote urban biodiversity in general
may not specifically support the protection of endangered plant
species. While target species conservation is a major motive for
urban biodiversity conservation (Dearborn & Kark, 2010), the meta-
analysis by Shwartz et al. (2014) revealed that empirical evidence
for the effectiveness of urban conservation strategies is lacking. It
therefore remains unclear which criteria should guide the allocation
of scarce resources for urban nature conservation or whether the
contribution of cities to the conservation of biodiversity is generally
overestimated (Shwartz et al., 2014). An assessment of the long-term
survival of endangered plant species in cities is currently hampered
by knowledge deficits in three key areas.
1.1 | Population persistence
The occurrence of species of conservation concern in cities does not
necessarily indicate their effective protection (Shwartz et al., 2014).
Environmental constraints due to urban land use, fragmentation or
novel environmental stressors represent significant limitations on
plant dispersal and recruitment (Kowarik & von der Lippe, 2018;
McDonnell & Hahs, 2015; Williams et al., 2009), while habitat loss
and change can be responsible of local plant extinctions (Duncan
et al., 2011; Knapp, Kühn, Stolle, & Klotz, 2010). Thus, population
persistence is a key issue for sustainable target species conserva-
tion in cities, as there is evidence for decreasing population sizes
in urban plants over time (Chocholoušková & Pyšek, 2003; Knapp
et al., 2010), and remaining populations of a species can thus mask
future extinction debts (Hahs & McDonnell, 2014). However, most
urban biodiversity studies report as snapshot studies the occurrence
of species at a certain point in time, but do not allow conclusions
to be drawn about the persistence of urban populations (but see
Lawson et al., 2008; Schwartz, Smith, & Steel, 2013).
1.2 | Type of habitat
While the occurrence of target species of conservation concern
across different habitats in cities has often been described, the
relative importance of different urban habitats for such species is
not fully understood (Shwartz et al., 2014). Species of conserva-
tion concern have been reported from very different habitat types
within cities (Planchuelo, von der Lippe, & Kowarik, 2019), for ex-
ample, forests (Godefroid & Koedam, 2003), brownfields (Bonthoux,
Brun, Di Pietro, Greulich, & Bouché-Pillon, 2014), parks (Cornelis &
Hermy, 2004) or cemeteries (Kowarik, Buchholz, von der Lippe, &
Seitz, 2016; Löki, Deák, Lukács, & Molnár, 2019). However, an im-
portant bias is that populations of endangered species have not been
studied equally across all urban habitat types. Rather, most urban
conservation studies address larger habitats (roughly >2 ha), with
natural remnants and large green spaces being overrepresented
(Shwartz et al., 2014). Moreover, species inventories of urban nature
reserves are likely better known than those of unprotected land use
types.
1.3 | Environmental and urbanization predictors
Which species occur in urban habitats not only depends on local
habitat features such as patch size but also on features of the sur-
rounding urban matrix as indicated by urbanization parameters (e.g.
the proportion of impervious surface, human population density)
or the vicinity to (semi-)natural ecosystems. Previous urban studies
have revealed the relative importance of many potential predictors
of species richness (e.g. Anderson & Minor, 2019; Beninde, Veith,
& Hochkirch, 2015; Westermann, von der Lippe, & Kowarik, 2011;
Williams, Morgan, McCarthy, & McDonnell, 2006). However, results
based on total species richness cannot necessarily be generalized
to endangered plant species, as shown for urban grassland re-
serves in Prague (Jarošík, Konvička, Pyšek, Kadlec, & Beneš, 2011).
Specific analyses for endangered plant species are rare and yielded
ambiguous results: studies at larger national scales revealed posi-
tive relationships between urbanization parameters and species of
conservation concern (Kühn, Brandl, & Klotz, 2004; Lenzen, Lane,
Widmer-Cooper, & Williams, 2009; Shwartz, Muratet, Simon, &
Julliard, 2013), while studies at smaller city scales yielded contrast-
ing results (Schmidt, Poppendieck, & Jensen, 2014). However, many
studies rely on heterogeneous urban landscapes (e.g. grids) without
specifying the habitat scale, that is, the specific locations of endan-
gered plant populations. Moreover, dynamics of urban environments
are an important features of cities (Ramalho & Hobbs, 2012). Change
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PLANCHUELO Et AL.
rates of urbanization measures (e.g. impervious surface, population
size) can determine urban biodiversity patterns (Fischer, Rodorff,
von der Lippe, & Kowarik, 2016). Such measures are rarely incorpo-
rated into analyses of the long-term survival of endangered species,
although dynamic changes of urban environments can potentially
threaten population survival, for example, by loss of open spaces, or
indirect urbanization effects.
1.4 | Species traits
Besides characteristics of a population's environment, species iden-
tity or more generally, species traits, are held responsible for the vul-
nerability to local extinction in cities (Duncan et al., 2011). Although
several studies have indicated shifts in specific plant traits due to
urbanization, there was only a marginal impact of species traits on
plant extinctions in another study (Duncan et al., 2011). However,
higher frequency in urban habitats has been linked to competitive
traits (e.g. plant height; Fischer, von der Lippe, & Kowarik, 2013) or
strategies (Chocholoušková & Pyšek, 2003), and to preference for
nutrient-rich sites (Knapp et al., 2009), while lower frequencies in
cities are reported for species with high water requirements (Knapp
et al., 2010).
We aimed to elucidate the persistence of endangered plant spe-
cies in cities—and underlying mechanisms—by evaluating a unique
dataset from Berlin. These data contained long-term monitoring
results of a large number of precisely mapped plant populations
(n = 858) belonging to 179 endangered plant species. These plant
species have been identified as priority species of conservation
concern in Berlin's Flora Protection Program and the extant popu-
lations of these species have been subjected to a repeated monitor-
ing (Meißner & Seitz, 2010). Therefore, information was available on
which populations have survived or have gone locally extinct at the
respective sites since the first survey.
To unravel mechanisms that might underpin population survival,
we assigned each of the originally mapped populations (a) to a spe-
cific biotope type and (b) characterized the site occupied by each
population by a range of urban landscape variables whose funda-
mental relevance has been shown previously and that were related
to habitat features, the urbanization of the surroundings and the
vicinity of (near)-natural ecosystems. Additionally, we linked popu-
lation survival to plant traits that have been shown to be relevant to
plant performance in previous urban studies.
We expected population survival rates to decrease with increas-
ing urbanization or rapid changes in the areas surrounding each pop-
ulation and to differ significantly among biotope types. We assumed
a positive correlation between population survival and an increasing
proximity to natural remnants or large forest and grassland areas,
which might act as propagule sources. Furthermore, we expected
a positive relationship between plant traits related to competitive
ability and population survival.
In detail, we addressed the following research questions: How is
the survival rate of populations of endangered plant species in Berlin
related to (a) features of the respective habitats (e.g. type of biotope,
patch size, legal conservation status); (b) the degree and dynamics
of urbanization of the surrounding urban matrix (e.g. current share
and change in impervious surface area, human population density);
(c) to the vicinity of (near)natural ecosystems (e.g. distance to natural
remnants, proportion of forests in buffer around the sites) and (d)
plant functional traits of the respective endangered plant species
(e.g. Ellenberg indicators, CSR strategy).
2 | MATERIALS AND METHODS
2.1 | Study area
This study was carried out in Berlin, the largest city of Germany, with
3.6 million inhabitants in 2017. Berlin is a typical large European
city, including a wide range of ecosystems ranging from remnants
of semi-natural and agrarian landscapes or urban greenspaces with
different land use histories to novel ecosystems in vacant urban-
industrial land. Green and blue spaces make up 41% of the total
area of Berlin, which is 891 km2; the remaining 59% is covered by
built-up and traffic areas (SenStadtUm, 2016). Red lists of endan-
gered species were established in the 1980s and updated several
times since. From today's perspective, we thus know that 17% of
Berlin's flora has gone extinct since the mid-19th century, and 29%
is currently being endangered (Seitz, Ristow, Meißner, Machatzi, &
Sukopp, 2018).
2.2 | Population data
We used an extensive monitoring dataset from Berlin's Flora
Protection Program (Berliner Florenschutzkonzept) on the precise
geographical location of 858 populations of 179 endangered plant
species in Berlin (see Appendix S1). From these, 72.5% of the spe-
cies are herbaceous, 20.6% geophytes, 3.5% shrubs, 1.9% hydro-
phytes and 1.5% trees (Table 1). The 10 most populous plant families
are, in decreasing order, Rosaceae, Cyperaceae, Caryophyllaceae,
Asteraceae, Poaceae, Orchidaceae, Ranunculaceae, Iridaceae and
Fabaceae (Table 1). The monitored species have the highest con-
servation priority because they are threatened locally and/or at
regional, national or global scales (Meißner & Seitz, 2010). A popula-
tion was discerned from another when individuals where separated
at least 30 m or when populations were clearly separated by roads
or paved paths. We used the dataset in previous studies (Planchuelo,
Kowarik, & von der Lippe, 2020a; Planchuelo et al., 2019) but here
include for the first time information on population survival. The first
inventory of populations was compiled from several expert surveys
after 1990. On the basis of the georeferenced locations of this initial
dataset, a re-mapping project took place between 2009 and 2014,
aiming to relocate all previously mapped populations. The average
period of time between the first and second mapping of a population
was 7.6 (±0.2) years. This allowed us to differentiate persistent from
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locally extinct populations of those recorded in the initial dataset.
To avoid methodological bias, we excluded all populations from the
initial compilation with imprecise information on the spatial location,
and populations in open waters, due to difficulties in relocating and
resurveying them.
2.3 | Habitat features
To evaluate the role of different biotope types for population sur-
vival, we intersected the location of each mapped population with
the respective biotope class from the Berlin biotope mapping
(SenStadtUm, 2014). Terrestrial populations of endangered plant
species were present in eight major biotope classes (Figure 1): for-
ests, grasslands, ruderal sites, built-up areas, bogs and marshes,
groves and hedges, green spaces and agricultural fields. We calcu-
lated the area of the respective biotope patches to elucidate the role
of patch size for population survival.
To test for the role of the legal protection status of an area on
population survival, we attributed the site of each population to
one of the following categories: nature reserve (Naturschutzgebiet),
Natura 2000 site, protected landscape (Landschaftsschutzgebiet)
and unprotected sites. The first three categories represent legally
protected areas, with decreasingly strict protection status and man-
agement measures. We also assessed whether the populations were
located in former East Berlin or West Berlin to evaluate if the differ-
ent patterns of urban development in both parts of the city had an
effect on population survival.
2.4 | Landscape variables
We determined several characteristics of the urban matrix surround-
ing the populations of endangered plants and used them to reveal the
effects of urbanization on population survival (see Appendix S2 for
parameters and sources). We calculated data on the proportion of
impervious surface, the mean floor space index (a measure of urban
TABLE 1 Number of populations and species belonging to
different life forms and to the 10 most populous plant families of
the endangered plants used in our study
Number of
populations
Number of
species
Life form
Herbaceous perennial 566 66.0% 101 56.4%
Geophyte 177 20.6% 30 16.8%
Herbaceous annual 56 6.5% 23 12.8%
Shrub 30 3.5% 15 8.4%
Hydrophyte 16 1.9% 95.0%
Tree 13 1.5% 10.6%
Plant family
Rosaceae 96 11.2% 13 7.3%
Cyperaceae 89 10.4% 15 8.4%
Caryophyllaceae 84 9.8% 11 6.1%
Asteraceae 83 9.7% 21 11.7%
Poaceae 73 8.5% 13 7.3%
Orchidaceae 47 5.5% 84.5%
Ranunculaceae 44 5.1% 10 5.6%
Iridaceae 35 4.1% 10.6%
Fabaceae 28 3.3% 63.4%
FIGURE 1 Location of populations
(n = 858) of endangered plant species in
Berlin that survived (blue dots) or did not
survive (red dots) during the monitoring
period. The category ‘open land’ includes
biotope classes that were further
differentiated in the analyses
Water bodies
Forests
Built up areas
Open land
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density, i.e. the ratio of a buildings total floor area and its lot area),
human population density and the length of the road network in a
500 m radius buffer surrounding each population of endangered plant
species. To account for effects of spatial isolation from (near)natural
ecosystems, we calculated the proportion of forests and grasslands
for a 500 m radius buffer around each population, based on informa-
tion from the Berlin biotope map (SenStadtUm, 2014).
To account for urbanization dynamics throughout the monitor-
ing period, we calculated the changes in the proportion of imper-
vious surface area throughout two periods of time (i.e. 1990–2001
and 2005–2016) for a 500 m radius buffer around each population.
These periods reflect different phases of urbanization: the first de-
cade after the fall of the Berlin Wall in 1989, and a period of less dy-
namic but progressive urban development. Both periods are covered
by citywide measurements of the impervious surface area using the
same method. As a measure of socioeconomic change, we compiled
mean human population constancy (i.e. the percentage of residents
living at least 5 years in the same address) in the same buffer from
the Berlin map of land use (SenStadtUm, 2016).
To calculate the average values of each parameter, we spatially inter-
sected the corresponding map with each individual buffer in QGIS (2019)
and then used the plugin ‘Dissolve with Stats’ to obtain the average val-
ues for each buffer. The distance of each population to the nearest road
and to the nearest natural remnant was calculated in QGIS (2019) with
the ‘NN Join’ plugin. We addressed those biotopes as natural remnants
if they corresponded to historical natural ecosystems, being only slightly
affected by human impacts, following the classification by Kowarik and
von der Lippe (2018). Such remnants include mires, wetlands, semi-nat-
ural forests and some semi-natural grasslands. Spatial information on
natural remnants was derived from Planchuelo et al. (2019). Appendix
S3 summarizes the methodological approach of the study.
2.5 | Plant traits
Plant traits, CSR strategy types (Grime, 1977) and Ellenberg indica-
tors (Ellenberg, Weber, Düll, Wirth, & Werner, 1991) have been suc-
cessfully linked to urban biodiversity patterns in previous studies
(Williams, Hahs, & Vesk, 2015). We thus included these parameters
as predictors of population survival in our analyses (Appendix S4).
Information on plant morphological traits (SLA, plant height) and the
CSR strategy of the species was gathered from the BIOFLOR database
(Klotz, Kühn, Durka, & Briemle, 2002). For information on the realized
niche of a species, we used indicator values for the soil humidity, soil
nitrogen and soil acidity requirements, and for light and temperature
requirements of each species from Ellenberg et al. (1991).
2.6 | Statistical analyses
To relate population survival to habitat characteristics and
landscape variables (Appendix S2), we used a GLMM (R func-
tion glmer; Bates, 2010). We coded population survival as a
binomial response and corrected for spatial and phylogenetic
dependence by including the spatial coordinates of their loca-
tions (longitude and latitude) and plant genus as random fac-
tors. Plant genus has been included as a random factor in GLMM
models to successfully account for phylogenetic dependencies
(e.g. Pandit, White, & Pocock, 2014). Because of the varying pe-
riod between the first and the second monitoring of the popu-
lations, this time span in years was also included as a random
effect in our model. All habitat and landscape variables were
tested for intercorrelation and as no correlations higher than
|r| < 0.7 appeared, all of them were included as fixed effects in
a full model (Dorman et al., 2013). A minimal adequate model
was chosen by stepwise backward selection of the predictors
based on minimal AIC. Random variable selection was done
separately with the entire set of variables prior to backward
selection of the fixed effects. We evaluated the prediction ac-
curacy of the model by calculating the area under the receiver
operating curve (AUC) with the package pROC in R (Robin et al.,
2011).
To estimate the effect of plant traits on population survival
and to account for possible nonlinear effects, we calculated the
relative importance of each variable through a conditional ran-
dom forest and successively performed a conditional inference
tree analysis. For both, we used the same response as in the
GLMM (binomial population survival) and the set of predictors
related to the morphological plant traits of the species, their
CSR strategy and their realized niche as expressed through
Ellenberg indicator values (Ellenberg et al., 1991; Appendix S4).
A variable selection through a conditional random forest is a
machine learning technique that is able to estimate the relative
importance of highly correlated predictors (Strobl, Boulesteix,
Kneib, Augustin, & Zeileis, 2008). A conditional inference tree
is a non-parametric type of decision tree where the dataset is
recursively split into dichotomous subsets, which are discrim-
inated by the most significant predictor (Hothorn, Hornik, &
Zeileis, 2006). We chose these models because of their ability
to display interactions between different traits and their flexible
handling of categorical data.
All analyses were performed with the statistical and program-
ming software R version 3.5.2 (R Core Team, 2018).
3 | RESULTS
3.1 | Survival rate
Almost two-thirds of the populations of endangered plant species
(64%) mapped in the first monitoring were confirmed in the second
monitoring (551 populations). Thus, more than one-third of all popu-
lations became locally extinct during the period between the two
monitoring dates, which averaged 7.6 years. During that time, from
a total of 179 endangered species, 49 (27%) went extinct for the
study sites.
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3.2 | Landscape predictors
In the binomial GLMM, changes in the proportion of impervious
surface between 1990 and 2001 in a 500 m radius surrounding the
populations was the variable with the strongest effect on the sur-
vival of endangered plant species, followed closely by the biotope
class. Additionally, the minimal model with the best fit based on AIC
selection also included distance to the nearest natural remnant as
predictor, which had a negative, but non-significant effect (Table 2).
Population survival was negatively affected by changes in the
proportion of impervious surface between 1990 and 2001 (Figure 2).
Notably for those populations where the proportion of impervious
surface decreased, population survival was considerably higher and
no populations became locally extinct when impervious surface de-
creased below −1.6%.
The biotope class in which populations were situated was also
a significant predictor of population survival. Survival rates were
highest in green spaces (0.90) and built-up areas (0.78) and lowest
in forests (0.58) and ruderal sites (0.61). While the first two biotope
types only housed a few populations, the last two biotope types
had significantly more populations. Forests hosted the majority of
populations of endangered plants but had the lowest survival rate
(Figure 3). Grasslands, with the second highest number of popula-
tions (261), showed an intermediate survival rate of 0.69.
The distance to a natural remnant was also a variable selected by
the GLMM model as a predictor of population survival. However, mod-
elled estimates of population survival only showed a marginal decrease
on average from 0.63 at 0 m in a remnant patch to 0.59 at 1,500 m.
3.3 | Plant traits as predictors
Calculating the relative importance of each variable through a con-
ditional random forest revealed indicator values for soil humidity
requirements and CSR strategy as most important plant traits in
predicting population survival (Figure 4). In a subsequent conditional
TABLE 2 Analysis of deviance table (Type II Wald Chi square
Test) of the effects of predictor variables on population survival
of endangered plant species from the minimal GLMM model
after backward selection (prediction accuracy of AUC = 0.872).
Statistically significant p values are marked in bold. Random
effects of genus and monitoring duration of the endangered plant
populations were retained in the minimal model
Variable Chi square df p value
Changes in impervious surface
1990–2001 (500 m buffer)
4.96 10.026
Biotope class 15.30 70.032
Distance to natural remnants 2.70 10.100
FIGURE 2 Effect of change (period 1990–2001) in the
proportion of impervious surface in a 500 m buffer around 858
populations of endangered plant species on their survival rate. Dots
represent actual data, while the trend line represents the predicted
probabilities
−30−20 −100 10 20
0.00.2 0.40.6 0.8 1.0
Changes in impervious surface 1990−2001 (%)
Survival rate
FIGURE 3 Survival rate of populations of endangered plant
species (n = 858) across different biotope classes in Berlin over an
average period of 7.6 years; n above the bars indicates the total
number of populations in each class
n = 21
n = 27
n = 10 n = 261 n = 37
n = 31
n = 67
n = 404
0.45
0.50
0.55
0.60
0.65
0.70
0.75
0.80
0.85
0.90
0.95
Populaon survival rate
Biotope class
FIGURE 4 Plant traits and Ellenberg indicator values arranged
by their relative importance as predictors of population survival
of endangered plant species in a conditional random forest model.
Each percentage represents the variability in population survival
explained by each variable
0510 15 20
Temperature requirements
Plant height
Soil acidity requirements
Soil nitrogen requirements
Specific leaf area
Light requirements
CSR strategy
Soil humidity requirements
Relative variable importance (%)
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inference tree analysis, only these two predictors were retained
in the model as significant predictors of population survival of en-
dangered plants (Figure 5). Soil humidity requirements (p < 0.001)
caused the first split in the data, with an overall lower survival (0.16)
in populations with the highest soil humidity requirements (≥10).
Those with low to medium soil humidity requirements (<10) had
overall higher survival rates and were further split according to their
CSR strategy (p = 0.029), with populations of competitive species
(c, cs, csr) having higher survival rates (0.69) than those with ruderal
or stress tolerant (r, rs, rc, s) strategies (0.54).
4 | DISCUSSION
While cities can harbour many endangered plant species, their impor-
tance for biodiversity conservation has been challenged (Shwartz et al.,
2014). This study addressed one critically understudied key question:
the extent to which endangered species not only occur in cities but also
survive under urban conditions. To our knowledge, this is the first long-
term study to investigate the population survival for a large set of en-
dangered plant species (179) at their respective growth sites in a big city.
A key finding is that populations of endangered plant species
in urban settings can be highly dynamic and that there is a consid-
erable risk of local extinction within a period of <10 years. At the
second monitoring date, about two-thirds of the populations were
confirmed. Yet, population survival as reported in this study does
not necessarily relate to survival over longer periods of time, which
is generally challenging in urban environments as recently reported
from the low establishment rates of endangered plants in Berlin
(Kowarik & von der Lippe, 2018). Therefore, our results on popula-
tion survival may not reflect extinction debts—which should be ver-
ified by continued monitoring. Additionally, in the period between
the first and the second monitoring, some locally extinct species
may have colonized new sites due to meta-population dynamics
(Loreau, Mouquet, & Holt, 2003) or population establishment from
natural or human-mediated long-distance dispersal. However, our
study cannot consider newly established populations at locations
other than those originally surveyed. This could explain why ruderal
sites and species, with fast population dynamics and high dispersal
capacity, had lower than expected survival rates in our study.
As for the underlying factors of local extinction or survival of
populations, our study found significant differences with regard to
urbanization dynamics, biotope classes, proximity to semi-natural
areas and species traits.
4.1 | Urbanization dynamics
Previous studies have shown that high levels of urbanization relate
to higher risk of local extinction, as shown for native grassland plants
FIGURE 5 Effect of plant traits on the
survival rate of populations of endangered
plant species in Berlin (n = 858). The
conditional inference tree shows all
significant partitioning effects of plant
traits and Ellenberg indicator values on
population survival; n above the bars
indicates numbers of populations left in
each terminal node
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(Williams et al., 2006). In our study, the proportion of impervious
surface around the growing sites predicted population survival.
The risk of local extinction increases significantly with increasing
impervious surface for the period 1990–2001 but not for the later
2005–2016 period (Table 2). These periods differed in the pace of
urbanization in Berlin (SenStadtWo, 2019a). The first one covers the
decade after the fall of the Berlin Wall and thus a period of rapid
change, in which some old building structures were demolished and
some vacant land converted to new uses. The urban development
during the second period was less rapid, including a period of stagna-
tion at the beginning and a later focus on the development of exist-
ing built structures (densification). We expect that changes within
the first period affected populations of endangered species directly
by habitat loss, and indirectly by changing disturbance regimes at the
locations of the populations, for example, by changing recreational
pressure. In the same vein, a study from Buenos Aires revealed that
population growth, rather than human population density around
urban parks, negatively related to plant species richness within park
environments (Fischer et al., 2016). Missing significance of urbaniza-
tion dynamics for population survival during the second time-period
could mask extinction debts because the ecological consequences of
further development only take effect later.
Urbanization and socio-economic patterns differed between
West and East Berlin due to the political division of the city after
the Second World War. Correspondingly, distribution patterns for
fruit trees, for example, still differ today in both parts of the city
(Larondelle & Strohbach, 2016). Our study, however, found no cor-
responding legacy effects of Berlin's history as the location of the
populations in either East or West Berlin did not affect population
survival. This suggests that similar mechanisms operated in both
parts of the city.
4.2 | Biotope types
As assumed, biotope classes also had a pronounced effect on pop-
ulation survival (Table 2), with forests and grasslands hosting most
populations. Surprisingly, the survival rate was lowest in forests
(0.58; Figure 2a). The fact that 42% of populations of endangered
plants in forests were no longer present at the second monitoring is
alarming, as forests in Berlin are generally protected, that is, there
is no significant loss of forest area, and today's forest manage-
ment aim is to develop semi-natural forests in Berlin (SenStadtWo,
2019b). The low survival rates in forests likely relate to changes to
the vegetation structure. Many of Berlin's forests had sparse can-
opy and shrub layers with clearings within forest-heath complexes
as a consequence of being grazed for centuries until the mid-19th
century (Sukopp, 1990). Forest structures became denser with the
cessation of grazing, but a sparse canopy cover was preserved by
increased harvesting of timber and other destructive activities dur-
ing and after Second World War (Seidling, 1990). These settings
had supported many species with high light requirements, adapted
to the prevailing nutrient-poor sandy soils. However, during the
last decades, changes in forest management (Seidling, 1990) and
the establishment of native and alien species in the shrub layer
(Prunus serotina, Acer species; Kowarik, von der Lippe, & Cierjacks,
2013) made forest stands denser again. Comparing vegetation rel-
evés from 1955 and 1986 accordingly revealed a decline in many
species of semi-open forest habitats (Seidling, 1990). In the same
vein, mechanisms leading to denser forest structures can induce
local extinctions in this study—as indicated by species’ light re-
quirements as predictor of population survival (Figure 4). Indeed,
the species with the lowest survival rates in forests include Festuca
psammophila and Botrychium lunaria, species which are normally
missing in dense forests but that usually colonize nutrient-poor
sites in open forests or grasslands. Furthermore, the increasing
availability of nutrients due to influx from urban sources makes
these species even more vulnerable (Knapp et al., 2010; Williams
et al., 2015), exacerbating the negative effects of a lower light
availability.
Conversely, the survival rate was highest in the most anthro-
pogenic biotopes (i.e. green spaces: 0.90; built-up areas: 0.78).
However, only few species are found here. This pattern supports that
some highly endangered species are pre-adapted (sensu McDonnell
& Hahs, 2015) to intensively designed and novel urban biotope.
Examples of rare species that are adapted to highly disturbed sites
are Chenopodium murale, Filago minima and Sagina apetala.
Within the strongly anthropogenic biotope classes, ruderal
sites had the most populations but also the lowest population sur-
vival rate (0.61). While novel urban ecosystems harbour many en-
dangered plant species in Berlin (Kowarik & von der Lippe, 2018;
Planchuelo et al., 2019), population survival seems to be limited in
ruderal sites that are most prominent on vacant land. This may relate
to the increased construction activities in Berlin during the last de-
cades, which affect vacant land directly and indirectly. Alternatively,
succession towards forest in these biotope classes may impair the
habitats of rare ruderal species that usually rely on open habitats
(Kattwinkel, Strauss, Biedermann, & Kleyer, 2009).
Grasslands cover only 5% of the area of Berlin (SenStadtUm, 2014),
but hosted the second highest number of populations, with an inter-
mediate survival rate of 69%. This confirms the importance of urban
grassland for biodiversity conservation (Fischer et al., 2013; Kendal
et al., 2017; Klaus, 2013) at the population scale. Better survival
rates compared to forests may result from the long tradition of care
in grassland biotopes while appropriate measures for shaded forests
might be less commonly applied.
4.3 | Proximity to (semi-)natural ecosystems
The importance of natural remnants for urban biodiversity con-
servation is well established (e.g. Godefroid & Koedam, 2003).
Accordingly, it has been found that nearby conservation areas had
a positive effect on the occurrence of endangered plant species in
the city of Prague (Jarošík et al., 2011). Our findings build on this
by demonstrating that population survival of endangered plants is
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PLANCHUELO Et AL.
negatively related to the distance between the population and the
nearest natural remnant. Several complex interacting factors may
contribute to this finding. Assuming that remnant sites within pro-
tected areas harbour many endangered species, the probability of
successful dispersal increases with decreasing distance. These rem-
nant populations could serve as a source for external populations,
therefore reducing local extinctions. At closer distances to natural
remnants, there is a higher chance of having similar site conditions
(e.g. soils, hydrology), thus benefiting the endangered species de-
pendent on these environmental features. Indeed, a companion
study showed that populations of endangered plant species were
spatially dependent on natural remnants—except for populations in
novel ecosystems, that is, in settings with starkly differing site condi-
tions (Planchuelo et al., 2020a). Our findings thus support conserva-
tion strategies that encourage the protection of large areas around
natural remnants in formally protected areas—not only as a buffer
but also as potential habitats for endangered species.
4.4 | Species traits
While none of the metric plant traits were retained in the tree
model as predictors of population survival, indicator values for soil
humidity requirements and the CSR strategy types differentiated
three groups of species with distinct survival rates (Figure 3). The
first split of the model delineated a group of species with the high-
est requirements on soil humidity and a rather low population sur-
vival. This corroborates previous findings on low performance of
wetland species in urban areas (e.g. Knapp et al., 2010). In Berlin,
wetland species are particularly prone to extinction due to large-
scale groundwater subsidence caused by extensive sealing and
groundwater withdrawal (Seitz et al., 2018; Sukopp, 1990). One
example from our study is Ranunculus lingua—a highly endangered
wetland species with a low population survival (17%). Climate
change may further impair population survival of species that re-
quire high soil humidity as Berlin has increasingly experienced pe-
riods of higher temperatures and less precipitation over the past
20 years (Cubasch & Kadow, 2011), and future climates may con-
tinue this trend.
The second predictor in the model, CSR strategy, split the re-
maining species into two groups: one with medium survival rates,
characterized by ruderal and stress tolerant strategies, and a second
with the highest survival rates of species assigned to the competitive
strategy. While competitive species usually have higher prospects of
long-term survival (Chocholoušková & Pyšek, 2003; Knapp, Kühn,
Schweiger, & Klotz, 2008; Knapp, Kühn, Wittig, et al., 2008), it is
surprising that the ruderal strategy type does not promote survival
in urban environments. This is probably linked to the elevated risk
of local extinction in ruderal habitats that are often subject to hab-
itat transformation as described above and the fact that competi-
tive species are associated with locations with high nutrient levels
(Grime, 1977), a feature of many urban sites. Additionally, because
our methodology did not allow us to track the appearance of new
populations, ruderal plants that had dispersed into nearby sites
might have been recorded as extinct, thus biasing our results against
ruderal species.
4.5 | Practical implications
This study supports the role of cities for preserving biodiversity by
demonstrating opportunities for population survival of endangered
plants in different urban settings. Yet, we also revealed considerable
challenges since 36% of the populations of endangered plant species
went locally extinct during a period of <10 years. Moreover, negative
effects of urbanization dynamics (i.e. increasing impervious surface)
in adjacent areas indicate extinctions debts since urbanization is pro-
gressing in Berlin, as in many cities.
Importantly, population survival rate differed between biotope
classes, and with respect to some traits of the endangered species.
These results can support conservation policies, management and
research. Examples include the selection of species with particular
traits for re-introductions to suitable urban habitats and priority
setting in managing populations of target species in different urban
settings. Generally, our study illustrates the usefulness of allocating
limited conservation resources to population monitoring, more so
considering the recent claim on the importance of long-term monitor-
ing in anthropogenic systems (Haase et al., 2018; Pergl et al., 2019).
More specifically, the lowest survival rates in urban forests
challenges current policies in forest management that aim to sup-
port the species composition and structure of semi-natural forests
(SenStadtWo, 2019b). Our results support complementing strategies
of forest management with approaches that mimic historical land
uses to facilitate endangered species with high light requirements,
for example, by thinning the canopy and shrub layer in parts of the
forests.
The low population survival in bog- and wetland-species
points to challenges in maintaining hydrological systems despite
increasing constraints due to added effects of traditional driv-
ers of decline (e.g. drainage) and climate change impacts. Since
most wetlands are already protected areas in Berlin, our results
also indicate limits in conserving all endangered species in urban
environments.
Finally, the unexpectedly high population survival of a few en-
dangered species in green areas or built-up areas suggests unex-
ploited opportunities to re-introduce some pre-selected species to
public greenspaces (Klaus, 2013; Pan et al., 2019). In summary, our
study supports a wide range of conservation approaches within and
outside protected areas in cities that cover natural and anthropo-
genic ecosystem types.
ACKNOWLEDGEMENTS
We thank Justus Meißner and Stiftung Naturschutz Berlin for
providing monitoring data, Berlin's Senate Department of Urban
Development and Environment for sharing biotope and urbaniza-
tion data, and Elsa Anderson for comments on the manuscript. We
1590
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Journal of Applied Ecology
PLANCHUELO Et AL.
also thank Marc Cadotte, Peter Manning and anonymous reviewers
for their helpful comments. G.P. was funded by the Hans-Böckler
Foundation and the DAAD-STIBET program of the Technische
Universität Berlin.
AUTHORS' CONTRIBUTIONS
All persons entitled to authorship have been so named. All authors
conceived the ideas, designed methodology and contributed to writ-
ing; G.P. processed the data; G.P. and M.v.d.L. analysed the data. All
authors gave final approval for publication.
DATA AVAILABILITY STATEMENT
Data are available via the Dryad Digital Repository: https://doi.
org/10.5061/dryad.s1rn8 pk4v (Planchuelo, Kowarik, & von der
Lippe, 2020b).
ORCID
Greg Planchuelo https://orcid.org/0000-0003-0760-5478
Ingo Kowarik https://orcid.org/0000-0002-8251-7163
Moritz von der Lippe https://orcid.org/0000-0003-4760-1420
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SUPPORTING INFORMATION
Additional supporting information may be found online in the
Supporting Information section.
How to cite this article: Planchuelo G, Kowarik I, von der Lippe
M. Plant traits, biotopes and urbanization dynamics explain the
survival of endangered urban plant populations.
J Appl Ecol. 2020;57:1581–1592. https://doi.
org/10.1111/1365-2664.13661
