Plant traits, biotopes and urbanization dynamics explain the survival of endangered urban plant populations [original]

J Appl Ecol. 2020;57:1581–1592.

1581wileyonlinelibrary.com/journal/jpe

Received: 2 March 2020

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.

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);

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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PLANCHUELO Et AL.

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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