Biodiversity conservation in cities: Defining habitat analogues for plant species of conservation interest.

SYNTHESIS AND APPLICATIONS: The stepwise method was useful in producing informative plant lists and assemblages for planting designs and landscape management; it generated a plant selection palette that is not restrictive and does not enforce a native only policy. It also offered a wide range of potential habitat analogues for M. crassifolia.

Introduction

Novel ecosystems are human-modified ecosystems that have been irreversibly altered by intense impacts on abiotic conditions or biotic composition [1, 2, 3]. Novel ecosystems include urban green spaces that emerge mostly after built structures have replaced previously existing ecosystems. As such they include non native vegetation assemblages, consisting of native, spontaneous, naturalized, and invasive species [4]. Urban green spaces are sometimes abandoned after human disturbances or continue to experience disturbance regimes and consequently contain a range of both early- and late-succession vegetation.

Both unmanaged and managed green space can potentially contribute to urban biodiversity conservation. When unmanaged, urban green spaces are referred to as Informal Green Spaces (IGS) and can potentially contribute to urban biodiversity conservation [4]. IGS can provide valuable habitats [5, 6, 7, 8, 9, 10], and occasionally serve as a substitute for natural habitats [11, 12]. Certain cities are important for the conservation of threatened species [13]. Urban green spaces in Mediterranean cities, for instance, where plant diversity and endemism are high, offer a prospective of refuges to plant species regardless of whether the urban green spaces are semi-natural or anthropogenic [14]. However, despite the persistence of endangered species in cities [15], there are only few reported case studies of cities hosting viable populations of rare or endangered species, and thus directly contributing to conservation efforts [16].

Urban habitats tend to favor the persistence of plant species with particular trait combinations that appear well suited to the conditions [17]. Furthermore, certain plant functional traits tend to increase in response to urbanisation, while other traits have mixed responses [18]. For example, it has been shown that urbanized grid cells favor wind pollinated plants, plants with scleromorphic leaves, or plant seeds dispersed by animals, while other grid cells favor insect pollinated plants, plants with hygromorphic leaves, or plant seeds dispersed by wind [19]. Also, acidophiles may have disappeared in urban areas [20]. Identifying predictable relationships between plant traits and environmental conditions or disturbances is a promising approach for understanding how plant communities change in response to human land-use modification [21].

Many plant species can be found more or less regularly in various city habitats; the region of a habitat associated with a particular ecological community. For example, classification of urban habitat types inside the city of Berlin has revealed 19 habitats particularly worthy of protection and these were nominated as legally protected [22]. However, the classification of habitat types inside cities requires standard habitat classification systems which have not been developed in all countries, at least not in Lebanon [23]. Furthermore, the nomination of such habitat types becomes challenging when urban habitats are privately owned, as is the case of most informal green spaces in Beirut [24]. Another challenge is the protection of such habitats in cities like Beirut where law enforcement is weak and is unlikely to deter against infringement [25].

More relevant to cities like Beirut are urban biodiversity strategies that proposed to transform urban habitats into habitats suitable for native plant conservation [26]. One example of urban biodiversity strategy is the use of species-rich herbaceous communities to promote biodiversity in cities [27]. Another strategy, referred to as reconciliation ecology, proposes the conversion of spaces assigned to human activities into spaces that support the persistence of native species [28]. Identifying habitat analogues in this case is essential to guide reconciliation ecology strategy in cities [29]. If appropriate conservation targets are set, habitat analogues may dilute the distinction between disturbed and non-disturbed habitats as favorable sites for plant conservation [30, 31].

There are various methods that describe vegetation based on species identity and abundance, species functional traits, structural characteristics, or degree of naturalness. Floristic surveys are one of two main vegetation description methods used to collect data on native species of conservation interest, and to generate community classification schemes and structure patterns which vary predictably in response to external factors such as environmental stress and disturbance [32]. The floristic method uses taxonomic identification and species abundance to describe vegetation. From a floristics perspective, plant species found in an area are unique and capable of coexisting as distinct, recognizable units that are repeated regularly in response to biotic and environmental variations [33, 34, 35, 36, 37].

The other main vegetation description method, physiognomy, is frequently used to describe vegetation according to external morphology, life form, stratification, and size of each species [38, 39, 40, 41, 42, 43, 44, 45, 46, 47].

EcoVeg is a recent method that combines floristics and physiognomy, in addition to ecological descriptors, and that applies different rationales depending on whether the vegetation is natural or cultural [48]. Combining both approaches may be necessary to generate informative data from sites subjected to different disturbance conditions. The application of floristics in urban habitats may present a challenge when interpreting the data, since many studies reported an over-representation of ruderal species and high taxonomic diversity between relatively close sites [49, 50, 51, 52, 53, 54, 55, 56, 57, 58, 59]. In contrast, the application of physiognomic and structural vegetation description, may be more useful in urban habitats [18, 60] as the data informs about predominance of life strategies adopted by different life forms, and the method is applicable in highly modified sites, and at both, macro- and micro-climate conditions [61, 62].

A widely used functional type or physiognomic vegetation description system is the life form classification of Raunkiær [39]. Although physiognomic and structural vegetation description methodologies were developed to describe vegetation over large areas, these methods have been considered as potentially more useful tools than floristics in highly modified sites because they better reflect life strategies, for example, the ruderal strategy, encompassed by certain life forms [61]. Down (1973) resorted to life-form in studying reclamation of spoil heaps [62].

There is consensus that physiognomic and physiological characteristics of plants, including species life-history strategies and population biology, are also important descriptors of vegetation communities [63, 64, 65, 66, 67, 68, 69, 70]. Plant communities were shown to be important indicators to determine suitable habitats for rare species [71], and for ecologically and economically important species [72]. Some of these studies, however, deliberately exclude disturbed areas from sampling [72].

One aspect of urban vegetation that might challenge classification is the abundance of ruderal plant species which, benefit from the absence of interspecific competition that normally occurs in later successional stages, and colonize bare and disturbed land [61]. By spreading from nearby semi-natural vegetation, ruderals contribute to high variability in urban plant diversity, even between close sites, limiting the value of vegetation classification using floristic methods [32]. Some of these ruderal species may be distantly related to agricultural weeds and others to plant species found across transportation networks [73]. Ruderals are also populating green walls in cities [74]. The overrepresentation of ruderals and the haphazard management of green spaces in Beirut make vegetation classification difficult due to the small scale of associated biotopes and abundance of structured biotope complexes.

The success of plant conservation strategies is highly influenced by perceptions and social preferences which should be taken into consideration in addition to field assessment challenges in cities. For example, studies have shown that spontaneous ‘unmanaged’ vegetation may not appeal to residents as aesthetically pleasing nor is it perceived as acceptable ‘urban nature’ by decision-makers [75, 76, 77]. This is further complicated by the fact that plant selection and management, is driven by landscape architects and landscape contractors who have limited experience with native species, and do not have clear guidelines on how to contribute to biodiversity conservation in cities [78, 79].

While several studies show how vegetation description using floristic assessments in urban areas is limited by over-representation of ruderal species, abundance of exotic plants, and a high taxonomic diversity between relatively close sites [49, 50, 51, 52, 73, 54, 55, 58, 80, 81], other studies suggest that descriptions of functional types, such as life form, may permit ecological comparisons among areas of similar ecology on a more general scale than would be possible when using a taxonomic approach [82, 83, 84]. For instance, structural and adaptation characteristics of beach and dune vegetation were found similar, even if their taxonomic spectrum differed [85]. Furthermore, life-form, among other descriptions of functional types, were associated with plant responses to environmental change, to plant competitive strength, and to plant effects on biogeochemical cycles and disturbance regimes [86]. Recently, life form and life history were found to be stronger predictors of underlying population processes than native status [87]. The first meta-analysis on intra-urban biodiversity variation worldwide showed that patch area and corridors have the strongest positive effects on biodiversity, and that vegetation structure, local scale, biotic factors, and management habitat variables, are significantly more important than landscape scale, abiotic factors, or design related variables [88].

The objective of this study was to define urban habitat analogues for a plant species of conservation interest, Matthiola crassifolia, which has persisted in varying abundance in the Mediterranean city of Beirut. M. crassifolia is a rare Lebanese steno-endemic, it is only present in urban habitats, and its largest population in Beirut is decreasing. As the natural habitat of M. crassifolia is described as coastal area rocks [89], we hypothesize that the expected habitat analogues for the target species will include urban green space typologies that include significant percent of bareground, minimal presence of plant litter, and vegetation that does not significantly produce shade.

Materials and methods

Study location

Located along the Eastern shores of the Mediterranean, Lebanon is a predominantly mountainous country consisting of five geomorphological regions namely, a narrow coast along the length of the country, two mountain ranges that run parallel to the sea, and a fertile high plain that separates the two mountain chains. Lebanon possesses botanical elements from temperate, arid and subtropical biomes.

Species of conservation interest and its distribution

There are four Matthiola species recorded in Lebanon, two of which are either national or regional endemics. The Species-Group Ovatifolia is represented by the regional endemic Matthiola damascena Boiss. The Species-Group Longipetala is represented by Matthiola tricuspidata and Matthiola longipetala. Species-Group Iincana is represented by the national endemic Matthiola crassifolia Boiss. & Gaill which is restricted to a few locations along the highly urbanized Lebanese coast and is the subject of this study. M. crassifolia is a taxon of conservation interest as the species is recognized as an endemic of Lebanon. However, Gowler (1998) has questioned the taxonomic status of the species proposing that it should be considered subspecies of Matthiola sinuata [90]. Even if future molecular analyses support this preference, the taxon will remain an endemic of Lebanon yet at the intra-specific level.

The most comprehensive record of the distribution and status of M. crassifolia prior to this study was by Rteil (2002) who performed a systematic survey of the Lebanese coast and recorded the presence of the species in three out of five previously reported sites, Beirut, Ras Beirut and Byblos [91]. In this study, Ras Beirut and Beirut were considered a single locality. Subsequent field investigations by added Sidon, Khaldeh and Amchit as localities for M. crassifolia [89]. Our field survey to all reported localities confirmed the extinction of M. crassifolia in Sidon and its continued presence in Khaldeh, Beirut, Amchit and Byblos [92].

Study area

Beirut (33.8869° N, 35.5131° E), the capital of the Republic of Lebanon, is located on the eastern coast of the Mediterranean. Archeological evidence shows that humans have continuously occupied Beirut for the last 5000 years [93, 94]. Today, the city of Beirut has one of the highest urban densities in the Middle East with an area roughly over 20 km2, population density is estimated at 21,000 people per sq. km [95, 96]. The topography of the city includes two hills, Achrafieh (100 m asl) and Mousseitbeh (80 m asl) [97]. Paul Mouterde, who conducted floristic studies in Beirut in the 20th century, reported 1200 floral species including native and non-native species [98].

Our study site, Beirut, is defined by a 6 km long and 2 km wide cape [99]. Today, this area consists of densely populated neighborhoods interspersed with managed landscapes and zones with spontaneous naturalized vegetation occurring within geographically adjacent lots. Recent floristic studies of semi natural areas of Beirut revealed low community similarity, patchy species distribution, and predominance of habitat non-specific species [81]. Green spaces in the southern part of the promontory of Beirut fall under two broad categories; managed landscapes, dominated by exotic ornamental species planted in raised beds with reconstructed soil, and spontaneous landscapes where spontaneous floral communities survive along with casual non-native species, in coastal cliffs, along the rocky water front, and in un-built/abandoned lots [100].

The study location, particularly the southern part of the promontory of Beirut, can be considered a type III city that is likely to be carrying an extinction debt because extensive landscape transformations occurred after initial floristic surveys [80]. Although the expansion of the city started in 1840, the city passed through five stages of transformation when the southern part of the promontory consisted mostly of semi-natural areas until 1943 [101]. The earliest botanical studies in the region took place in the mid-1800 [102] and continued giving considerable focus to Beirut and its environments till the 1930s [103; 104].

Concurrent with early botanical studies of semi natural areas in Beirut, since 1840, Beirut has passed through five phases of transformation which extensively altered its landscape (Fig 1) [101]. Today, Beirut still harbors significant remnant native vegetation, especially the southern side of the promotary where urban expansion took place after 1970.

Fig 1

Beirut phases of urbanisation (From “Beirut,” by N. Yassin, 2010, Cities, 29, p. 64–73. Reprinted with permission.).

Field data collection

Baseline data collection was initiated in 2012, three years before the start of the study, to ensure comprehensive coverage of all informal green space locations. During 2012, all informal green spaces in the study location were surveyed to locate all spaces where M. crassifolia was present. In subsequent years (2013 and 2014), during flowering season of the target species, annual visits were made to all identified green spaces, regardless of whether the species was present or not. In 2015, sites were selected according to management intensity (high or low management intensity) of anthropogenic sites, and to levels of diversity of semi-natural habitats. Fig 2 presents the distribution of M. crassifolia in Beirut as well as the location of the selected sites for the study. All visited sites were either accessible public spaces or abandoned private lots. No permits were needed as no plant material was collected from study sites: only plant voucher specimens were collected from the field for taxonomic identification.

Fig 2

The distribution of M. crassifolia in Beirut and selected sites for the study.

As our objective is to capture habitat diversity of a rare species in small plots,we used a deliberate biased method to select study locations and to lay out sampling quadrats [71]. In their attempt to compare the effects of random to non-random sampling on patterns of species abundance, species richness and vegetation-environment relationships, Diekmann et al. (2007) concluded that random sampling resulted in a larger number of common species, and a smaller number of rare species when compared to non-random sampling. They also found that for small plots, the number of species in the non-randomly placed plots was higher than in the randomly placed plots, and that in random sampling, there was considerable redundancy [105].

We set a total of 78 quadrats in 12 sites. In vegetation patches with clearly visible boundaries, one to two 1 m × 1 m quadrats were placed [32]. We placed larger quadrats, 2 m × 2 m, in locations where shrubs are present [32]. As in Dinsdale, deliberate bias method consists of placing quadrats in areas judged representative of the selected location and for capturing the maximum observed variation [71,106]. We made three modifications to the sampling technique to address site-specific challenges. First, when the boundary of a plant assemblage was not clearly defined due to site disturbance, we placed quadrats in locations where the target species was highly represented and at least one quadrat where the target species was minimally represented assuming that this location constitutes the boundary of the sampled plant assemblage. Second, when species had an ‘individualistic’ distribution pattern, we increased the number of quadrats, up to six, to capture the observed variation and compensate for the difficulty to define the boundaries of the plant assemblage [107]. Third, when the target species was consistently not present in a given vegetation assemblage, we placed one quadrat.

We divided each quadrat into a grid of 100 subunits to ensure speed of measurement and relative accuracy [108, 109, 110, 111]. In every quadrat, we determined percent cover using the 11-point Domin cover scale by visually assessing subunits as: fully covered, empty, and partially covered for each species and each life form [32]. Data obtained from all subunits within a quadrat was then added to determine Domin cover per quadrat.

As the analysis of non-randomly placed plots such as phytosociological quadrats may be biased, especially regarding estimates of species abundance and species richness patterns [105] ordination was not attempted to analyse vegetation-environment relationships in this study.

Taxonomic and life form identification

We identified each plant specimen by consulting published floras, voucher specimens at the American University of Beirut Herbarium (Post Herbarium), and photographic floras [104, 98, 89]. All identified species were described by their life form according to Ellenberg and Mueller-Dombois, with amendment to include bunched shoot arrangement in reptant hemicryptophytes which forms a partially decomposed thick mat and causes peat accumulation [40]. We then pooled species that shared the same life form under the one category and estimated area cover for each life form accordingly.

Analysis

Based on the 11-point Domin cover scale, we analyzed floristic data, species and percent species cover, using TWINSPAN [112]. Also called dichotomized ordination analysis, the Two Way INdicator SPecies ANalysis is a method for classifying communities according to hierarchical divisions based on progressive refinement of a single ordination axis of a (sites × species) data matrix [113]. Using the same tool, TWINSPAN, we analyzed the life form data, life-form categories and percent cover (as relative abundance of each life form within each quadrat). In the TWINSPAN, the cut levels 0-3-4-5-6-8 were applied. The TWINSPAN groups were characterized by constancy-percentage, average cover, and representation of target species. A matrix, integrating floristic and physiognomic TWINSPAN findings, was then created to find intersections between quadrat groups defined by classifying life form and floristic data sets. This process led to the identification of new classification that consisted of quadrat groups that share similar life form and species composition. The full dataset can be found in [92]. A conceptual extrapolation of these findings allowed us to define landscape plant typologies with vegetation assemblages similar to quadrat groups in which the target species is highly represented and we considered these typologies as suitable locations for the introduction of M. crassifolia.

Results

M. crassifolia is most widely distributed in Beirut; based on our field surveys its presence was confirmed in 73 sites of which only one site, Pigeon Rock, is protected by law, and another site, the limestone cliff facing Pigeon Rock, is almost inaccessible and may be considered de facto protected. The remaining 71 sites offer highly diverse habitats and are not protected [92]. In remnant semi-natural sites, M. crassifolia is found in, spiny Mediterranean heaths, screes, sea cliffs and rocky offshore islands, growing on both sandstone and limestone formations and on (stabilized) coastal sand dunes. In anthropogenic sites, it grows near open sewers, in abandoned dump sites, through cracks in concrete walls and asphalt, on heaps of gravel, in street medians and on two occasions, almost epiphytically, out of the trunks of date and fan palms. The species’ tendency to utilize modified habitats reflects its partial behavior as a ruderal [61]. During the course of this study, M. crassifolia was lost in 20 sites to urban development including one site which harbored the largest clump count, and only four of these sites were recolonized. As a result, the plant species’ range in Beirut was reduced by 17% between 2012 and 2015 [92].

We recorded the presence of 124 plant species belonging to 107 genera and 40 families in the 78 sampled quadrats [92]. Plant species co-occurring with M. crassifolia included 16% non-native species. Analysis of floristic data by TWINSPAN clustered the 78 quadrats under 17 quadrat groups labeled af to qf. M. crassifolia had the highest constancy and abundance in three groups, df, gf and if. In contrast, the species was not present in eight groups, cf, ff, kf, mf, nf, of, pf and qf. The low community similarity, patchy species distribution, and predominance of habitat non-specific species reported by Talhouk et al. (2005) in their study of the floristics of the Lebanese coast was confirmed in this study [81]. High floristic variability between and within different sites resulted in more than half the quadrat groups (58.8%) consisting of no more than two quadrats. Only one group (ef) consisted of a large number of quadrats and represented a perceptible community of sparse vegetation on sandstone outcrops. Other groups were not site specific, but included quadrats exposed to similar disturbance; for example, in group gf the nine quadrats were sampled from street medians and side walks and consisted of a combination of evergreen exotic ornamental species such as Agave americana, Agave attenuata, and Lampranthus multiradiatus. Similarly, tf included quadrats characterized by a high representation of graminoids, Cyperus rotundus and Cynodon dactylon, which often grow in gardens and street medians under and around evergreen ornamentals such as the shrub Pittosporum tobira, and the creeping herbaceous forb Sphagneticola trilobata.

One problem we encountered with floristics based TWINSPAN analysis is that many groups did not represent actual communities i.e. plant species in an area that are unique and capable of coexisting as distinct, recognizable units that are repeated regularly in response to biotic and environmental variations [33, 34, 35, 36]. For example, group ef, which included about 28% of sampled quadrats, consisted of several distinct vegetation assemblages that occur in different habitats, both semi-natural and anthropogenic, and the target species, a stress-tolerant ruderal, was the only common indicator species between these assemblages.

Life form description of plant species yielded 55 different life forms. Results revealed that more than half of all recorded species were therophytes with a total of 64 autotrophic therophyte and two heterotrophic annual vascular parasites. The high representation of therophytes reflects high disturbance of study sites [61].

Fig 3 presents the life-form spectrum of all species recorded in the 78 plots. Chamaephytes constituted the most prominent perennial life form and included 24 species. Over half of all chamaephytes were either regional or national endemics and only three were not native. Phanerophytes were represented by 14 species, 10 of which were not native. Perennials characterized by a periodic shoot reduction were represented by 15 hemicryptophytes and six geophytes.

Fig 3

Raunkiaer life-form spectrum of plant species recorded in 78 quadrats in 12 sites in Ras Beirut.

Analysis of life form data by TWINSPAN clustered the 78 quadrats under 11 quadrat groups labeled

Al to Kl (Table 1). M. crassifolia was highly represented in three of these groups (Cl, Dl, and El) with a percent cover ranging between 11% and 25% in almost all quadrats within these groups. Examples of life forms in these three groups include, unbranched dwarf palm like trees (Phanerophyte08), typical and tall evergreen dwarf-shrubs (Chamaephyte03 & Chamaephyte04), low reptant evergreen succulents (Chamaephyte14), tall drought-deciduous hemicryptophytes (Hemicryptophyte01) and small reptant evergreen hemicryptophytes (Hemicryptophyte03) were common. Ornamental examples of these life forms include Agave and Yucca species (Phanerophyte08), cultivated Sea Lavender species (Chamaephyte03 and Chamaephyte04), and Lampranthus multiradiatus (Chamaephyte13).

Table 1

TWINSPAN analysis of life form data set collected in Ras Beirut.

(Alphabetical naming of quadrat groups by floristic and life form classification are not related.).

	Quadrat groups (A to K) resulting from life form classification (l)
	Al	Bl	Cl	Dl	El	Fl	Gl	Hl	Il	Jl	Kl
Phanerophyte08	_	_	IV 5	_	_	_	_	_	_	_	_
Phanerophyte09	_	V 5	II 1	_	_	_	_	_	_	_	_
Phanerophyte10	_	III 5	II 3	_	_	_	_	_	_	_	_
Chamaephyte13	_	III 6	IV 5	_	_	_	_	_	_	_	_
Hemicryptophyte12	_	III 1	II 1	_	II 1	_	_	_	_	_	_
Hemicryptophyte05	_	_	II 1	_	I 2	_	_	_	_	_	_
Chamaephyte05	_	_	_	II 6	_	_	_	_	_	_	_
Chamaephyte14	_	_	_	II 6	_	_	_	_	_	_	_
Hemicryptophyte03	_	_	_	III 4	II 3	_	_	_	_	_	_
Therophyte03	_	_	_	IV 2	I 1	_	_	_	_	_	_
Therophyte08	_	_	II 1	V 3	I 1	_	_	_	_	_	_
Therophyte02	_	_	_	IV 2	III 1	_	_	_	_	_	_
Phanerophyte07	_	_	_	_	I 6	_	_	_	_	_	_
Phanerophyte11	_	_	_	_	I 3	_	_	_	_	_	_
Phanerophyte12	_	_	_	_	II 6	_	_	_	_	_	_
Chamaephyte02	_	_	_	_	I 5	_	_	_	_	_	_
Chamaephyte09	_	_	_	_	I 1	_	_	_	_	_	_
Hemicryptophyte02	_	_	_	_	II 2	_	_	_	_	_	_
Hemicryptophyte06	_	_	_	_	I 6	_	_	_	_	_	_
Hemicryptophyte08	_	_	_	_	III 3	II 1	_	_	_	_	_
Hemicryptophyte09	_	_	_	_	III 2	_	_	_	_	_	_
Hemicryptophyte10	_	_	_	_	I 2	_	_	_	_	_	_
Geophyte01	_	_	_	_	I 2	_	_	_	_	_	_
Therophyte06	_	_	_	III 1	IV 3	II 1	_	III 2	_	_	_
Chamaephyte06	_	_	_	III 4	II 4	_	III 2	_	_	_	_
Therophyte01	VI 1	_	_	II 2	I 2	_	_	_	_	_	_
Therophyte04	_	_	III 1	VI 3	IV 2	III 1	_	_	VI 2	_	_
Hemicryptophyte01	_	_	II 1	II 2	II 2	_	III 2	_	_	_	_
Geophyte04	_	_	III 3	III 1		_	_	_	IV 3	_	_
Therophyte11	_	V 2	V 2	V 2	IV 3	IV 1	_	_	_	_	_
Chamaephyte08	_	VI 2	VI 4	V 4	VI 4	V2	IV 3	_	_	_	_
Hemicryptophyte11	_	_	_	II 1	IV 2	III 2	_	_	_	_	_
Therophyte10	_	_	_	VI 2	IV 2	IV 1	_	_	_	_	_
Phanerophyte04	_	_	_	II 6	I 3	_	_	_	IV 6	_	_
Phanerophyte05	_	_	_	_	II 5	II 5	_	_	_	_	_
Chamaephyte01	_	_	_	III 4	II 4	II 3	IV 4	_	_	_	_
Chamaephyte04	_	V 4	_	II 4	III 3	III 3	VI 6	_	_	_	_
Chamaephyte07	_	_	_	_	I 2	II 1	_	_	_	_	_
Geophyte02	_	_	_	_	III 2	II 1	_	III 6	_	_	_
Therophyte05	_	_	_	IV 1	IV 3	V 3	III 3	VI 4	_	_	_
Therophyte09	_	_	_	II 2	I 1	_	III 3	_	_	_	_
Chamaephyte03	_	_	_	_	I 3	VI 4	III 2	III 3	_	_	_
Chamaephte12	_	_	_	_	I 2	II 1	_	_	IV 6	_	_
Geophyte03	_	_	_	_	_	II 2	_	_	_	_	_
Phanerophyte03	_	_	_	_	_	_	_	_	_	IV 6	_
Phanerophyte06	_	_	_	_	_	II 2	_	_	_	IV 6	_
Chamaephyte11	_	_	_	_	I 1	II 1	III 2	VI 6	VI 3	VI 3	_
Hemicyptophyte04	VI 6	_	_	_	_	_	_	_	_	_	_
Chamaephyte10	_	_	_	_	_	_	_	III 4	_	_	VI 2
Phanerophyte01	_	_	_	_	_	_	_	_	_	_	VI 6

The Roman number corresponds to species constancy within each TWINSPAN group (I = 5% or less; II = 6–20%; III = 21–40%; IV = 41–60%; V = 61–80%; VI = 81–100%). The Arabic number indicates average species abundance for each group on the domin scale (1 = less than 1%; 2 = 1–4%; 3 = 5–10%; 4 = 11–25%; 5 = 26–50%; 6 = 51–100%). Life-form of M. crassifolia is presented in bold and it is the only species under Chamaephyte08.

Five groups (Al, Hl, Il, Jl, Kl) excluded the target species and the dominant life form in these groups was mostly phanerophytes. These groups include mesophyllous large evergreen trees with spherical crown restricted to their upper half (Phanerophyte01), mesophyllous normal-sized evergreen shrubs with spherical crown extending to near their base (Phanerophyte04), microphyllous normal-sized evergreen shrubs with spherical crown extending to near their base (Phanerophyte03), and mesophyllous tall deciduous shrub with spherical crown extending to near the base of the shrub (Phanerophyte07). Ornamental examples of these life forms include various shade trees (Phanerophyte01), and shrubs used as hedges such as Pittosporum tobira (Phanerophyte04 and Phanerophyte03). They also include typical evergreen reptant herbaceous chamaephytes (Chamaephyte12) and ornamental plant species belonging to this life form and similar life forms such as turfgrass species and the Singapore Daisy, Sphagneticola trilobata.

The integration of floristic and life-form classification results into one matrix to identify quadrats at the intersection of both classifications generated a new set of quadrat groups that shared similar life form and species composition, and where M. crassifolia presented similar constancy and abundance (Table 2). This stepwise approach generated 30 quadrat groups, 8 which were highly favorable to M. crassifolia, and 12 which excluded it. We then proceeded to describe life form and species prevalent in these groups.

Table 2

Matrix of floristic and life-form classifications of quadrats from plant data set collected in Ras Beirut and southern part of the promontory of Beirut.

Intersections show M. crassifolia represented by constancy and abundance and help define favorable and unfavorable vegetation assemblages.

Quadrat groups (Al to Kl) resulting from life form classification; Quadrat groups (af to gf) resulting from floristic classification	Al	B l	C l	D l	E l	F l	G l	H l	I l	J l	K l
af	_	_	_	0	VI 4	_	0	_	_	_	_
bf	_	_	_	_	VI 3	_	_	_	_	_	_
cf	_	_	_	_	0	_	_	_	_	_	_
df	_	_	_	_	VI 4	VI 4	_	_	_	_	_
ef	_	VI 2	_	_	IV 3	V 2	_	_	_	_	_
ff	_	_	_	_	_	_	_	_	0	_	_
gf	_	VI 3	VI 4	_	_	_	_	_	_	_	_
hf	_	_	_	_	_	_	VI 2	_	_	_	_
if	_	_	VI 5	VI 4	VI 4	VI 4	VI 3	_	_	_	_
jf	0	_	_	VI 5	VI 3	_	_	_	_	_	_
kf	_	_	_	_	0	_	_	_	_	_	_
lf	_	_	_	VI 3	_	_	0	_	_	_	_
mf	_	_	_	_	_	_	_	_	_	0	_
nf	_	_	_	_	_	_	_	0	_	_	_
of	_	_	_	_	_	_	_	_	_	0	_
pf	_	_	_	_	_	_	_	_	0	_	_
qf	_	_	_	_	_	_	_	_	_	_	0

Quadrat groups: Al to Jl and af to Qf, f = floristic, l = life form (Alphabetical naming of quadrat groups by floristic and life fom classification are not related), constancy (I = 5% or less; II = 6–20%; III = 21–40%; IV = 41–60%; V = 61–80%; VI = 81–100%), average cover (1 = less than 1%; 2 = 1–4%; 3 = 5–10%; 4 = 11–25%; 5 = 26–50%; 6 = 51–100%).

The intersections that resulted in quadrat groups with the highest representation of M. crassifolia belonged to 4 out of 11 quadrat groups that were derived from the classification of the life form data set (Cl, Dl, El and Fl) and 4 out of 17 quadrat groups that were derived from the classification of the floristic data set (af, df, gf and if) (Table 3).

Table 3

Description of urban plant habitat analogues (habitat condition, life forms, plant habitat, and species) for M. crassifolia in Beirut following a stepwise approach that intersects floristic and life form data classifications.

Floristic classification	Life form classification	Average constancy and cover of target species	Habitat conditions	Description of urban habitat analogue: life form	Description of urban habitat analogue: Plant habitat and species
if	Cl	VI 5	Semi-natural vegetation, mostly occupying coastal cliffs	Quadrat groups dominated solely by suffruticose chamaephytes, the life form of the target species, at an average cover of 11–50%, sometimes including fruticose chamaephytes or caespitose nanophanerophytes with scale like leaves, both at average cover of 26–50%.	The highest representation of the target species was only revealed through the matrix. The quadrat group shows that the target species probably prefers to be alone.
af	El	VI 4			Species poor quadrat group. M. crassifolia was the only species consistently common between the quadrats. Perennials that less significantly occurred included Thymbra capitata and Thymelaea hirsuta.
gf	Cl	VI 4	Quadrat groups describing managed artificial vegetation of street medians	Low lying spreading succulent chamaephytes, at average cover of 26–50%, growing spontaneously or used as ground cover, sometimes interspersed by rosulate nanopherophytes, at average cover of 26–50%. Semi-rosette therophytes, at an everage cover of 1–4%, behaved as consistent ruderals.	Dominated by palm-like species of Agave and Yucca. Lampranthus multiradiatus used as ground cover. Several annuals, most notably Urospermum picroides, and Matthiola crassifolia behaved as ruderals.
if	Dl	VI 4			Polycarpon tetraphyllum and Crepis aculeata were common ruderals—besides Matthiola crassifolia. Carpobrotus edulis dominated—Pittosporum tobira dominated once, but in that case, its canopy was disturbed.
df	El	VI 4	Semi-natural vegetation, mostly occupying spontaneous urban wastelands	Very tall drought-deciduous scapose hemicryptophytes, at an average cover of 5–10%, as well as small and very tall scapose therophytes, at a cover that did not exceed 14%, were consistent ephemeral elements of this quadrat group. Shrubs such as tall evergreen semi-woody dwarf-shrubs and low (3–10 cm) creeping deciduous semi-woody dwarf-shrubs creeping along the ground were sometimes present at an average cover of 11–25%. Nanophyllous (usually less than 1 cm2) normal-sized evergreen shrubs sometimes dominated at an average cover exceeding 51%.	Sandy soil with small rock fragments sometimes alternatively dominated by Dittrichia viscosa, Thymaleae hirsuta or Convulvulus secundus, among other perennials and annuals, but consistently including the target species as well as Alcea setosa
if	El	VI 4	Quadrat groups of samples collected from minimally managed artificial vegetation of street medians and highly disturbed semi-natural patches	Drought deciduous semi-rosette scapose hemicryptophytes at an average cover of 5–10% and tall scapose therophytes at an average cover of 5–10% were regular features in this group of quadrats. Besides graminoid phanerophytes being seldom present at an average cover exceeding 50% and thus behaving as dominant evergreen perennial elements, suffrutescent chamaephytes were consistently present at an average that did not exceed 25%.	This quadrat group included both anthropogenic and disturbed semi-natural habitats. Sparse vegetation composed of evergreen ornamentals and ruderals growing on a mostly bare sandy soil mixed with gravel in a minimally managed street median or cracks in concrete. Vegetation growing on slightly stabilized sands of a sandy beach; meeting line of sandstone formation with pedestrian path, abandoned dump site; mostly bare ground on wet sandstone cliff occupied by sparse vegetation; mostly bare ground on wet sandstone cliff occupied by sparse vegetation; part of steep sandstone cliff dominated by Galium canum; sandy soil with small rock fragments and cement dominated with Arundo donax
if	Fl	VI 4	Abandoned anthropogenic structures	Typical or tall caespitose and tall scapose suffrutescent chamaephytes codominating vegetation at an average abundance of 26–50%.	Crack in concrete through which few perennial species grow; A bolder protruding from a sandstone cliff allowing for both Limonium mouterdei and Matthiola crassifolia to grow on it; Part of steep sandstone cliff dominated by Galium canum
df	Fl	VI 4	Abandoned part of public beach		Dittrichia viscosa and Matthiola crassifolia dominating vegetation growing on slightly stabilized sands of a sandy beach

Alphabetical naming of quadrat groups by floristic and life form classification are not related.

The intersections that resulted in quadrat groups with the lowest representation of the target species belonged to 8 out of 11 quadrat groups that were derived from the classification of the life form data set and 11 out of 17 quadrat groups that were derived from the classification of the floristic data set (Table 4).

Table 4

Description of urban plant habitats (habitat condition, life forms, plant habitat, and species) unsuitable for M. crassifolia in Beirut following a stepwise approach that intersects floristic and life form data classifications.

Quadrat Group by Floristic Classification	Quadrat Group by Life form Classification	Description of the intersecting groups that exclude M. crassifolia	Description of habitats and species of the intersecting groups that exclude M. crassifolia
af	Gl	Natural assemblages dominated by suffruticose chamaephytes at an average cover exceeding 51%, sometimes also dominated by fruticose chamaephytes	Galium canum growing as clumps on steep sandstone cliff
lf	Gl		Crithmum maritimum growing on slightly stabilized sand beach
af	Dl		Thymbra capitata dominating a limestone formation
jf	Al	Natural and artificial assemblages dominated by thick mat-forming reptant herbaceous hemicryptophytes or chamaephytes at an average cover exceeding 91%; sometimes geophytes were significantly present	Phyla nodiflora growing as thick mat
cf	El		Sandy soil ground covered with some sandstone pebels and a thick layer of reptant herbaceous plants such as Polygonum equisetiforme among which many annuals.
ff	Il		Street median dominated by Sphagneticola trilobata
nf	Hl		Sandy soil and degraded limestone or sandstone dominated by dense creeping Sporobolus pungens and Cynodon dactylon, sometimes high Oxalis pes-caprae
pf	Il	Artificial and spontaneous vegetation assemblages dominated with microphyllous and mesophyllous mostly evergreen normal-sized and tall shrubs as well as large sized trees at an average cover exceeding 91%.	Hedge of Pittosporum tobira in garden of a residential building
mf	Jl		Lantana camara in residential gardens
of	Jl		Street median entirely covered with Carissa macrocarpa
kf	El		Paritaria judaeca and Ricinus communis growing as understory of Ficus carica along an open sewer
qf	Kl		Tufts of Piptatherum miliaceum growing on sandy soil and rubble under a canopy of Ficus microcarpa

Alphabetical naming of quadrat groups by floristic and life form classification are not related.

Discussion

The similarity in the infrastructure of a city may explain homogeneity of urban ruderal species, which out-compete sown species [114]. For example, a 30-year green roof study concluded that spontaneous colonization should be accepted and considered as a design factor; and regional plant communities could serve as a model for seed recruitment and installations [114]. However, preventing a rapid loss of area-sensitive species necessitates large sites greater than 50 ha [88]. Such areas are absent in Beirut, and the loss of Matthiola crassifolia in the city is highly likely. Utilizing habitat analogues to increase the area of habitat patches and create a network of corridors is the most plausible strategy to ensure the persistence of this narrow endemic.

Urban environments share many features in common because they are designed to perform standard functions to meet human needs [115]. Such an environment, common to cities around the world, might be expected to select for species with a similar suite of traits favouring persistence in highly disturbed and human-modified habitats. Indeed the process of urbanization has been conceptualized as a series of filters acting on an existing species pool and selectively removing those species with traits unfavourable for persistence in this new environment [59].

The peculiarity of our study is that, not only is classification influenced by ruderals, but the species of conservation interest M. crassifolia also behaves as a ruderal. Considering the diversity of habitats occupied by M. crassifolia, it was not possible to resolve this lack of location specificity with floristic assessments, which in turn did not allow us to develop an understanding of urban habitat analogues. Instead, the number of quadrat groups generated by the floristic analysis was large, and some of these clusters did not represent actual plant community assemblages. Although the natural habitat of the target species is described as coastal area rocks [89], the behavior of the target species as a ruderal led to TWISPAN quadrat groups of highly variable species constituency and quadrat locations ranging from highly managed street medians to semi-natural coastal cliffs and including commercially introduced species and native ones.

Classifying life form data by including percent cover for each category helped specify which life forms and their respective abundance were positively or negatively associated with M. crassifolia. Our findings are in line with Kent [32], who emphasized that physiognomy might be more useful as a tool than floristics in highly modified habitats at different scales due to the responses of plant species to macro- and micro-climate conditions. Life history and life form are stronger predictors of underlying population processes than native status [87,116].

By using a stepwise approach which combines the two methods, floristics and physiognomy, we were able to minimize the masking effect of ruderal species and to identify life form similarities within distinct vegetation assemblages. In the last decade, researchers have combined life form and floristic vegetation description methods to overcome difficulties in analyzing data in disturbed habitats. For example, Vestergaard [117] generated quadrat groups based on floristic data through TWINSPAN and then described the life-form spectra in each to investigate the relationship between plant diversity and artificial dune development processes. Although similar to our methodology, Vestergaard did not use this combined methodology to define habitat analogues for target plant species. In 2014, a new vegetation classification approach that relies on both physiognomy and floristics over large areas was published under the name EcoVeg [48]. Our approach, however, differs from EcoVeg in that we first mathematically classify physiognomic data and later sort the classifications according to a specific floristic trend. In addition, we base our study on field data collected from small urban habitat sites while EcoVeg uses map data and is meant to classify vegetation over large natural landscapes.

More recently, several studies have sought to explore the potential of light detection and ranging (LiDAR) to inform landscape biodiversity assessments. In fact, the utilization of this technology has developed from quantification of gaps (above bare ground, low vegetation and medium vegetation), canopy cover and its vertical density in open landscapes [118] to mapping tree cover and vegetation spatial and vertical structure in cities and estimating above ground biomass despite particular challenges posed by urban areas [119,120].

Furthermore, accurate mapping of vegetation communities within highly disturbed urban landscapes was recently achieved through incorporating a hierarchical object-based image analysis (OBIA) approach with high-spatial resolution imagery and canopy height surfaces derived from LiDAR data [121]. Provided the range of outputs these recent methods are producing, LiDAR technology may serve for rapid indentification of potential locations for habitat analogues and the exclusion of areas that are known not to be favorable to the target species, for example canopy cover in the case of M. crassifolia.

Improving the quality of existing green spaces throughout the entire urban matrix has been suggested as an effective approach to enhancing biodiversity experience [122]. The information we generated using a stepwise approach integrating floristics and physiognomy, may serve as blueprints for planting designs; it offers a plant selection palette that is not restrictive and does not enforce a native only policy. The habitat conditions in quadrat groups of high representation of the target species were not the same and reflected a wide range of potential habitat analogues for M. crassifolia. These varied from abandoned buildings to highly managed street medians.The urban habitat analogues that we identified include green spaces dominated by palms, low-lying succulents, or shrubs with scale-like leaves. In contrast, the species does not seem to persist in green spaces dominated by turf grass, canopy trees, or vegetation that produces a significant litter. Furthermore, since knowledge of a target species’ preferred physiognomies includes an understanding of its position in the vertical stratification of its ecological community [32], we were able to identify additional habitats suitable for the introduction of M. crassifolia. Streetscapes, such as street medians, sidewalks and street tree planters, that lack both peat accumulating ground cover and canopy species, ubiquitous throughout the city, provide patches of optimal vegetation composition that could potentially accommodate M. crassifolia. Such streetscapes that can function as habitat analogues for M. crassifolia are illustrated in Fig 4 ana Fig 5. A change in landscape management strategy, however, needs to preceed design and development of habitat analogues. At the end of the four-year study, M. crassifolia was no longer seen in 16 out of 73 sites. Our field observations, revealed that management strategies such as the intentional uprooting of M. crassifolia considered by gardeners as a weed led to the disappearance of the species from these locations. On the other hand, there are locations where the species persists probably due to the fact that in these sites gardeners remove plants during their dieback stage, which includes seed-bearing silique fruits, but they keep seedlings and flowering plants.

Fig 4

Illustrated scene for a planted street median functioning as a habitat analogue for M. crassifolia.

Rosulate phanerophytes and reptant succulent chamaephytes, often used as ornamentals in green spaces in Beirut, dominate the street median without excluding the target species.

Fig 5

Illlustrated scene for sidewalk functioning as a habitat analogue for M. crassifolia.

The cracks in the concrete of the sidewalk due to poor management and the adjacent sandstone wall resemble coastal cliffs occupied by the species. Small and medium-sized therophytes like Plantago coronopus L. abd Polycarpon tetraphyllum are often observed occupying such spaces.

In the case where more than one species is a conservation target, then a conservation strategy conducive to the persistence of both species. In our study, we found that M. crassifolia persisted as part of the low shrub layer under taller nanophyllous shrubs like the Shaggy sparrow-wort, Thymalea hirsuta, another species of conservation interest in Lebanon. M. crassifolia also thrived in the understory of tuft-trees like the fan palm, Washingtonia robusta, an introduced species, and within groves of the giant reed, Arundo donax, a spreading native. Species belonging to these life forms, or similar ones, dominate many sites in Beirut including street medians and could serve as favorable habitats for M. crassifolia. Our findings also show that some exotic invasive species impacted M. crassifolia positively. M. crassifolia grew in sites dominated by Carpobrotus edulis, a potentially invasive in Lebanon, planted at the edge of pedestrian paths. Pedestrians avoided stepping onto these areas, maybe due to their appreciation of C. edulis as an evergreen ground cover [123]. As a result, this plant assemblage protected M. crassifolia and allowed C. edulis to spread constrained by water availability. Removal of invasive plant species should be determined based on its impact on endemic and rare vegetation present in a given region, and eradication should focus on those invasive species that compete with endemic species in general and those of conservation interest especially [124]. Huenneke and Thomson [125] suggest criteria for determining whether such species pose problems for specific rare native taxa and indicated the possibility that some species may be beneficial to endemics.

Equipped with the findings above, landscape designers, architects, and managers can better reconcile between desired conservation targets and, socio-behavioral, and aesthetic outcomes by including M. crassifolia in an aesthetically pleasing setting. They can design urban habitat analogues that promote the persistence of M. crassifolia by excluding from the plant palette native or non-native species belonging to life forms associated with its low representation as reported in this study. Alternatively, they can design an urban habitat analogue using a vegetation architecture conducive to the persistence of M. crassifolia. In the case of established green spaces, they can manage the space to become suitable for M. crassifolia by selectively removing species with a life form that is incompatible or that restricts its abundance. In some situations, horticultural techniques, such as pruning, can modify the micro environment without changing species existing on site, to create suitable urban habitat analogues; for example, improving light conditions in cases where species of conservation interest is shade intolerant.

Identifying predictable relationships between plant traits and environmental conditions provides a promising framework for understanding how vegetation responds to environmental change in a variety of ecosystems [21].

Conclusion

Given the rate of expansion of urban landscapes [126, 127, 128, 129], increasing a target species’ site area in a city is highly desired [28]. Our findings may serve as guidance on how to create or modify, through landscape planting designs, suitable habitats for species of conservation interest. By understanding the physiognomy and structure, and environmental conditions in which a species occurs, green areas may be designed to suit the requirements of a target species while established areas may be surveyed for candidate sites suited for the introduction of a target species. Our stepwise approach offers a detailed field assessment tool for urban plant habitat analogue characterization.

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17 Jan 2020

PONE-D-19-19705

Biodiversity conservation in cities: Defining habitat analogs for plant species of conservation interest

PLOS ONE

Dear Professor Talhouk,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

Most importantly, the study should be better linked to recent concepts and results of urban ecology, thereby making use of the broad literature in this field of research. For instance, this includes current knowledge about conservation in urban areas, applying the concept of novel ecosystems, using plant functional traits, and referring to approaches for classification of habitat types in other cities. Many of your statements are not supported by literature, e.g. why vegetation physiognomy or structure should be more useful for urban biodiversity research than floristics.

One important methodological question is why you did not take into account local habitat conditions when assessing habitat analogues for a species of conservation concern; it would be important to include, for instance, abiotic site conditions or management intensity at these sites. Another methodological issue refers to the non-random location of plots, which will have major implications for the interpretation of data. Likewise, the target species’ habitat preference can hardly be assessed if it occurs on nearly all sites.

In general, some basic information is missing in the Materials and Methods chapter, including the criteria used for site selection and how you identified the additional habitats. The reviewers also provide a range of recommendations regarding the presentation of results. For instance, a more consistent coding of life-form types has to be used and definitions of life-form types has to be added; the number of tables should be reduced; some results may be shown using graphical presentations.

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Reviewer #1: The manuscript includes a novel stepwise approach in identifying habitats suitable for target species. The use of a combination of lifeform spectrum snd physiognomic characteristic and floristic identity has helped in proposing management strategies for Matthiola crassifolia. I admire the approach

Reviewer #2: INTRODUCTION

1. The introduction is missing citations, as many statements are not supported by literature.

2. I would only use the world “artificial” (e.g. line 76) to describe urban habitats that have been deliberately designed by man with a specific purpose. Not all urban habitats should be classified as such.

3. Before introducing Table 1, the authors mention that current data collection methods are designed for non-urban contexts. However, they should be aware that very important work has been done to classify the urban habitats inside the city of Berlin. This project lasted several years and was done by the Senate Department for Urban Development and Housing of Berlin (more info here: http://www.stadtentwicklung.berlin.de/umwelt/umweltatlas/ed508_03.htm). They differentiated more than 7000 different urban biotopes/habitats inside the city of Berlin.

4. I would include in the introduction an hypothesis stating what kind of analogue habitats the authors expect to find for M. crassifolia.

5. In general, I have the feeling that this section could profit from a deeper insight into current findings in urban ecology. This is a non-exhaustive list of some important literature that could help:

• Anderson, EC & Minor, ES (2019) Assessing social and biophysical drivers of spontaneous plant diversity and structure in urban vacant lots. Sci Total Environ, 653, 1272-1281.

• Beninde, J, Veith, M & Hochkirch, A (2015) Biodiversity in cities needs space: a meta-analysis of factors determining intra-urban biodiversity variation. Ecol Lett, 18, 581-592.

• Chocholoušková, Z & Pyšek, P (2003) Changes in composition and structure of urban flora over 120 years: a case study of the city of Plzen. Flora, 198, 366-376.

• Duncan, RP et al. (2011) Plant traits and extinction in urban areas: a meta-analysis of 11 cities. Global Ecology and Biogeography, 20, 509-519.

• Ives, CD et al. (2016) Cities are hotspots for threatened species. Global Ecology and Biogeography, 25, 117- 126.

• Knapp, S et al. (2008a) Urbanization causes shifts of species' trait state frequencies. Presilia, 80, 375-388.

• Knapp, S et al. (2009) How species traits and affinity to urban land use control large-scale species frequency. Diversity and Distributions, 15, 533-546.

• Kowarik, I & von der Lippe, M (2018) Plant population success across urban ecosystems: A framework to inform biodiversity conservation in cities. Journal of Applied Ecology, 55, 2354-2361.

• Planchuelo, G, von der Lippe, M & Kowarik, I (2019) Untangling the role of urban ecosystems as habitats for endangered plant species. Landscape and Urban Planning, 189, 320-334.

• Schmidt, KJ, Poppendieck, HH & Jensen, K (2014) Effects of urban structure on plant species richness in a large European city. Urban Ecosystems, 17, 427-444.

• Shwartz, A et al. (2014) Outstanding challenges for urban conservation research and action. Global Environmental Change, 28, 39-49.

METHODS

6. From my perspective, the description of the genus and the whole range of species beyond M. crassifolia is not necessary.

7. In lines 131 to 135, I would state that the mentioned sites are cities. Many readers might not be familiar with the geography of Lebanon. Additionally, I would use the English instead of the local name of the city (i.e. Sidon instead of Saida) for international readers.

8. I don’t fully understand what the authors wanted to achieve with point 3 starting in line 170. Where was the second quadrat placed and why?

RESULTS

9. I would argue that this section in general needs to be easier to interpret and more visual. I think most tables don’t necessarily need to be included in the results. Perhaps I would include them as an annex and only represent a summary of some of them in the results. For example, Table 2 could be summarized showing only the genus that co-occur with M. crassifolia, not all the species, or Table 4 could be easily summarized with a pie chart showing the different proportion of each life-form. Additionally, some data mentioned in the text could be represented visually in a graph or similar (i.e. the proportion of M. crassifolia found in remnant sites vs. anthropogenic areas, or a map showing the location of these 20 sites where M. crassifolia was lost)

DISCUSSION

10. I think the authors should discuss about their own results earlier in this section. Perhaps some of the text between lines 353-396 could go to the introduction.

11. It could be interesting to include some discussion about the characteristics of the sites where M. crassifolia was lost.

12. I think it could be interesting to discuss about the ecological reasons explaining why there is a difference in the presence of M. crassifolia in remnant sites vs. anthropogenic sites.

13. Regarding the non-random design of this study, it might be interesting if the authors would consider this paper when interpreting their results: Diekmann, M., Kühne, A. & Isermann, M. Folia Geobot (2007) 42: 179. https://doi.org/10.1007/BF02893884. It shows that in small plot sizes like the ones used in this study, non-randomly placed plots result in general in higher species richness than if they were randomly distributed.

14. As a general comment for this section, I would argue that in order to develop a methodology to assess the habitat analogues of a species, the authors should consider including an assessment of not only floristics and physiognomy, but also of the local habitat conditions. As an example, we could reflect on the areas where M. crassifolia thrives (those with palms, succulents or dry shrubs) - perhaps there is something in these locations beyond the species assemblages that can explain why the target species is performing favorably. Are these locations the least managed? Are they in spontaneous urban wastelands? I think it is very important that the authors include an additional assessment of the local habitat conditions in their study.

GENERAL REMARKS

I think more work is needed to improve the scientific quality of this paper. The authors should make use of the broad literature available in the field of urban ecology and their methodology should include an assessment of the local habitat conditions when assessing habitat analogues for a species of conservation concern.

Reviewer #3: Dear authors of „Biodiversity conservation in cities: Defining habitat analogs for plant species of conservation interest“,

The idea of identifying habitat analogs for species of conservation interest within human-dominated landscapes is an interesting idea for improving species conservation and, in your case, for improving the contribution of urban areas to the protection of biological diversity.

After reviewing your manuscript, I have a number of concerns that in my opinion should be solved before the manuscript is ready for publication. I will describe my concerns below, point by point.

Abstract:

- Line 28: I am not sure what you want to express with the first sentence of the abstract. Do you want to express that urban environmental conditions change the composition of species assemblages or that species in urban areas interact differently with each other than they do within non-urban habitats? If you mean the latter, is there proof for it? For example, would two species interact differently with each other depending on whether they occur in an urban or in a non-urban area?

- You distinguished among native, naturalized, ornamental garden escapes and invasive plant species (e.g., lines 29/30, 73, 145). Could you state more precisely that these are native and non-native species, with the three latter groups comprising non-native species? Also, I’d rather talk about casual non-native species than about ornamental garden escapes because usually, non-naturalized non-native species in urban areas do not only (although to a large share) include ornamental garden escapes but also other introduced species that have not naturalized (yet), such as species accidentally introduced.

- Line 34: Where are these 12 study sites located? Please say so in the abstract and consider adding a figure to the manuscript that depicts the location of sites.

Introduction: The introduction would benefit from better linking it to recent urban biodiversity research, especially to our knowledge about species conservation in urban areas, to the concept of novel ecosystems, and to functional traits and functional groups:

- The persistence of species of conservation interest within urban areas is not in general unlikely (and thus I do not completely agree with your sentence in lines 75/76). A range of threatened species can occur within urban areas (see Ives et al. 2016, Global Ecology and Biogeography 25, 117-126). Whether a species will be able to persist within urban environmental conditions does depend on its functional traits (cf. Williams et al. 2015, Perspectives in Plant Ecology, Evolution and Systematics 17, 78–86).

- Introduction, lines 73/74: Well-established standard classifications of urban habitats exist, such as the four types of urban nature by Kowarik (1992 – cited e.g. in Kowarik 2018 Urban Forestry & Urban Greening 29, 336-347). You do not necessarily need to refer to one of these classifications, but please note that urban areas usually not only comprise artificial habitats but also remnants of natural habitats.

- Lines 84-86: I do not see why the methods used to describe vegetation that you present should only work in natural areas. I guess that what you want to express is that the TWINSPAN-classification of groups does not work that well because, as you wrote later, there are many unique co-occurrences of plant species at different urban sites. However, the methods you present in Table 1 can be applied in all kinds of terrestrial plant communities, including urban ones. It’s just that the results differ among urban and non-urban habitats. Concerning the many unique co-occurrences of plant species at different urban sites, I suggest that you refer to the concept of novel ecosystems (see Hobbs et al. 2006, Global Ecology and Biogeography 15, 1-7 for the overall concept and Kowarik 2011, Environmental Pollution 159, 1974-1983 for a review on novel urban ecosystems) because what you describe – untypical, unique species assemblages – might exactly be this – novel urban ecosystems.

- Table 1: How did you collect / choose these methods? Did you perform some kind of literature review to do so? If not, how do you know that the overview is complete? Also, I do not see much use in presenting all this detailed information. The table occupies a lot of space but the basic message could be wrapped into one or two sentences: The methods you present in Table 1 describe vegetation based on species identity and abundance, species functional traits, structural characteristics or degree of naturalness. All other details are not necessary for understanding your study and interested readers can refer to the literature cited. So, my suggestion is to delete Table 1 and to wrap its most important content into one or two sentences with references. (cf. Discussion, line 353 where you wrote about “two main vegetation description methods” – so, this can be nicely wrapped)

- Citations in lines 94/95 – a lot. Maybe it is not necessary to cite all of these 17 references. Rather choose some and provide them as example references.

- Lines 95/96: please, do provide references for the statement that physiognomic and structural vegetation description may be a more useful tool for urban biodiversity than floristics. To better link your manuscript to recent urban biodiversity research, I think it is useful to refer to functional plant traits. The physiognomic characteristics that you look at equal functional traits and functional groups. (See e.g. Williams et al. 2015, Perspectives in Plant Ecology, Evolution and Systematics 17, 78–86 and Lavorel et al. 1997, Trend in Ecology and Evolution 12, 474-478). Especially, to relate species to environmental conditions or their ability to co-occur with other species, trait-based approaches (or physiognomic approaches, as you call them) are indeed more helpful than floristic approaches.

- In addition, some information on the target species and why it is the target species of your study should be added to the Introduction. From all the data that you present, I got the impression that Matthiola crassifolia performs reasonably well in the urban area of Beirut. So, is it really threatened by urbanization? Also, in which natural habitats does the target species usually occur? Please, add this information to the description of the study species as it seems basic to understanding habitat analogs (as these will be analog to the natural habitats of the target species, won’t they?)

Materials and Methods:

- The identification of habitat analogs for the target species is solely based on the identification of species and life form types it occurs with. No abiotic conditions (temperature, soil type, soil moisture, pH, nutrients, surrounding land cover, …) have been taken into account although the occurrence and abundance of a species is not only determined by its biotic interactions but also, to a major extent, by abiotic conditions. Why haven’t abiotic conditions been taken into account?

- How were the 12 study sites selected? Was selection based on specific criteria? Which data (such as habitat or land-use maps) were used to select sites? I do understand the method that you used, still, it does not explain to me how sites were selected, i.e.: Were all anthropogenic and semi-natural habitats that occur in Ras Beirut taken into account or were specific anthropogenic and semi-natural habitats selected? This question is crucial because in the end, there are 78 plots and in 73 of these plots, the target species occurs. How can you, statistically sound, assess the preference of the target species for specific species assemblages if you have hardly any sites where it does not occur?

- Basic temporal information is missing in the Materials and Methods chapter: How long did the study last? When did the study start? When did the study end?

- Lines 122-124: Why are the species group names written in large letters?

- Line 127: add “should” among “species proposing that it” and “be considered”

- Line 133: “three out of five previously reported sites, Beirut and Byblos”. These are just two sites, not three. What’s the third one?

- Lines 134/135: What about Amchit? Has it been extirpated there as well or does it still occur there?

- Lines 142: With 20 km², you refer to the city, not to the total metropolis of Beirut, right? Please specify.

- Lines 156: Is there a reference for the early botanical studies of semi natural areas in Beirut? Also, when did these studies take place?

- Lines 157/158: Beirut as a type III-city according to Hahs et al. 2009: Hahs et al. refer to the year 1600 as a threshold (extensive transformations before or after 1600). As Beirut is a very old city, I guess that it might have experienced extensive transformations well before 1600. So, I am not convinced by your argument that Beirut is a type III-city – why not a type I-city? Please, be more precise in making your argument.

- Lines 180/181 University = American University of Beirut? Please, specify.

- Please, explain in more detail what TWINSPAN does, e.g. shortly mention what the cut levels are applied for. Also, please in the “Analysis” chapter, do explain how all this analysis is related to the target species. It is not mentioned at all how you identified habitat analogs for it.

Results:

- Line 207: What does “800 m” stand for?

- I think that in addition to (or instead of) Tables 3 and 5, ordination plots will be illustrative to show with which other species and with which life form types the target species preferentially occurs. The tables occupy a lot of space and are tedious to read.

- If you decide to stick with Tables 3 and 5, please define letters 1, 2, 3, … of the Domin-scale at the bottom of the tables.

- Line 244: add “as” between “around evergreen ornamentals such” and “the”.

- Line 246: Change “florsitics” to “floristics”

- Table 4: Three different codes (Life-form eight digit name, Abbreviated lifeform category, and Numeric code) are used here for the different life forms but no description/ definition is provided. Please, choose one out of three codes and add a description / definition of each life form type.

- Fig. 1: What exactly is shown here? Are these only the associates of M. crassifolia as stated in lines 263/264, i.e., species co-occurring with the target species, or are these all the species that you found across the 78 plots? As you worked with percent cover per species, it would as well be interesting to illustrate how the percent cover of the target species does change with the percent cover of specific life form types.

- Table 6: What does grey vs. no shade depict? What does “0” stand for?

- Lines 339/340: Rather “lowest representation” than “highest representation”? Otherwise, I do not understand how this is related to quadrat groups that excluded the target species.

- Table 8: Once, there is “chamaeophytes” written instead of “chamaephytes”. Please, correct.

Discussion:

- Parallel to the Introduction, the Discussion would benefit from better linking the study’s results to recent urban biodiversity research, especially to our knowledge about species conservation in urban areas, to the concept of novel ecosystems, and to functional traits and functional groups.

- Lines 365/366: “Such studies, however, are mostly conducted in natural habitats, and in many instances, deliberately exclude disturbed areas from sampling” – You do not compare natural to urban habitats, so why discuss this?

- Line 374: “aspect of urban vegetation that challenges field data analysis”: It might challenge classification but no analysis as such (see above). – same in line 384

- Line 387: How to develop an understanding of urban habitat analogs when there’s no description of natural habitats the target species usually occurs in (see above)?

- Lines 410-414: How to relate your method to LIDAR-data as long as herbaceous species cannot be distinguished by remote sensing (such as LIDAR)?

- Lines 422/423 “additional habitats”: You identified habitats where the target species occurs, habitats where it does not occur, and changes in percent cover of the target species across habitats. How did you identify additional habitats? Please explain in the Methods chapter.

- Lines 443: Add “of” between “case” and “established”.

- Lines 442-447: How would you manage a green space where several species of conservation interest are competing with each other? Would you selectively remove some of them?

**********

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Reviewer #1: Yes: Zerihun Woldu

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Reviewer #3: No

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4 Mar 2020

We have performed a major revision to the manuscript as suggested by the reviewers. We thank the reviewers for their thorough and constructive feedback and we agree with all the feedback and suggested changes. Considering that major changes were incorporated to the text of the manuscript there may be differences in the revised manuscript presented in 'track changes' and the version with no 'track changes' as it became difficult to read through the track changes. All the modifications, however, are clearly stated in the response to reviewers letter. Thank you for this opportunity.

Submitted filename: response to reviewers form feb 29 2020 SNT.docx

Click here for additional data file.

3 Apr 2020

PONE-D-19-19705R1

Biodiversity conservation in cities: Defining habitat analogues for plant species of conservation interest

PLOS ONE

Dear Professor Talhouk,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

The rather minor comments provided by the two reviewers mainly refer to terminology and phrasing, as well as to some improvements how references, figures and tables are presented. Please consider all of the reviewers' comments thoroughly when revising your paper. I think these recommendations can easily be implemented, and I'm looking forward to receiving a revised version of your manuscript soon.

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #2: All comments have been addressed

Reviewer #3: All comments have been addressed

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2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #2: Yes

Reviewer #3: Yes

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3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #2: Yes

Reviewer #3: Yes

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4. Have the authors made all data underlying the findings in their manuscript fully available?

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Reviewer #2: Yes

Reviewer #3: Yes

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Reviewer #3: Yes

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6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #2: The authors have made a good effort in addressing the points I mentioned in the last review and I see that the manuscript has considerably improved. I have still a few suggestions that I think might be interesting to consider in order to further improve the manuscript.

ABSTRACT

There have been numerous and interesting improvements in the manuscript in the last review, but the abstract has barely changed. In particular, I think it might be interesting to include a short sentence about the new information provided on the local habitat conditions of M. crassifolia (i.e. the it occurs throughout a wide range of potential urban habitats).

INTRODUCTION

In the introduction, the authors have now made good use of the current literature in urban ecology. This section has now improved considerably.

METHODS

The methods are more concise and clear now. I also find the new figures on Beirut’s historical development and particularly on the location of the sites very informative.

RESULTS

Regarding the results section, I would move Table 1 to the Appendix, as I think it might be too long and the authors have already made a good summary of it in lines 340-343.

Please check if all the figures are properly numbered when uploading, as some of the attached figures didn’t match the numbering in the text.

I am happy to see that table 4 has information about the local habitat conditions of the sites.

DISCUSSION

The discussion has substantially improved as well. The authors now added clarifications regarding the important local habitat conditions of M. crassifolia and about the reasons why the plant might be missing in some sites.

GENERAL REMARKS

I think the manuscript has now improved considerably and can be suitable for publication after the aforementioned improvements.

Reviewer #3: Dear Itani et al.

Thank you for considering my previous comments. I think that the manuscript has greatly improved. Still, some minor issues remain. Please, allow me to point these out:

- Abstract, line 45: add “of” between “design” and “urban habitat analogues”

- Lines 72 to 74: This sentence is misleading. It sounds as if novel ecosystems do include remnants of natural vegetation. Please, have a look at Kowarik & von der Lippe (DOI: 10.1111/1365-2664.13144) for definitions of natural remnants vs. novel ecosystems and do rephrase the sentence.

- Lines 74/75: Isn’t management something intentional? So why “unintentionally managed”?

- Lines 76/77: "When unmanaged, urban green spaces … can potentially contribute to urban biodiversity conservation" – does that mean, on the contrary, that when managed, urban green spaces cannot contribute to urban biodiversity conservation? It sounds like this but I do not think that this is what you wanted to say, especially as in the end of your manuscript you suggest the intentional design and management of habitat analogues for the conservation of the target species. Please, rephrase lines 76/77.

- Please note that habitat = biotope (the former is in English and the latter is derived from German, but basically, both mean the same). So, I suggest you only use the term habitat, e.g. from lines 92 on: “Many plant species can be found more or less regularly in various urban habitats. For example, classification of urban habitat types inside the city of Berlin has revealed 19 habitats particularly worthy of protection and these were nominated as legally protected [22]. However, the classification of habitat types inside cities requires standard habitat classification systems which have not been developed in all countries, at least not in Lebanon [23]. Furthermore, the nomination of such habitat types becomes challenging when [...]”

- In lines 141-149, also use the terms habitat and classification: lines 145 “vegetation classification” instead of “vegetation description”; line 148 “vegetation classification” instead of “biotope type mapping”; lines 148 and 149 “habitats” instead of “biotopes”. The way the text is written at the moment makes me feel that different terms are used for the same thing, that’s why I am suggesting these replacements.

- Lines 159/160, I suggest you write “[…] other studies suggest that descriptions of functional types, such as life form, may permit […]”. At the moment, it reads as if functional types are an example of life form – but rather, life forms are an example of functional types.

- Line 163: I do not know what you mean with “other physiognomic characters”. Can you use another term or provide an example?

- Lines 197 to 203 are confusing. There, it seems that Khaldeh, Beirut (including Ras Beirut), Amchhit and Byblos are your study sites. However, in lines 215 ff, you write that Ras Beirut is your study site. Please, be more precise in lines 197 – 203.

- References to Fig. 1, 2, and 3 in the text are mixed up. Fig. 1 in the text = Fig. 2 where the figure is shown; similarly Fig. 2 in the text = Fig 3 and Fig 3 in the text is Fig.1.

- Line 263 “we placed quadrats” – a certain number? Similarly, lines 266/267 “we increased the number of quadrats” – up to a maximum number of …?

- Lines 304/305, the site numbers “(Site 17)” / “(Site 16)” do not seem to occur anywhere else in the manuscript (at least, I could not find them). I think that it is not necessary to provide these numbers as long as they are not referred to anywhere else (e.g. tables or figures). Therefore, I suggest to delete the numbers.

- Lines 447: “is classification is” – delete one “is”

- Lines 488/489: Shwartz et al. warn against expanding cities and they suggest to improve the quality of urban green spaces. But they do not present these two points as opposing strategies. Therefore, I suggest you phrase the sentence like this: “Improving the quality of existing green spaces throughout the entire urban matrix has been suggested as an effective approach to enhancing biodiversity experience [122].”

- Lines 550-552: This (trash) comes surprisingly and in my opinion has no close relationship to the core topic of your paper. I would delete it.

- Line 556: “increasing species’ site area” – do you mean all species or do you mean specific species (e.g. rare species, endemic species, protected species)?

- In Fig. 2 it is very hard to visually distinguish between dots for Status = Extinct and dots for Status = Recolonized. Please, consider changing colors so that differences among the colors become more obvious (or check in the proof if quality go better than it is in the pdf-file that I got for review).

- References: Please, do check references carefully as there are several typos within then. For example, journal names should be written with capital first letters (e.g. not Journal of applied ecology but Journal of Applied Ecology). Moreover, reference number 10 says “Doctoral dissertation” and “Master thesis” – it cannot be both a t once, can it? For reference number 19, rather cite the journal paper (Knapp, S., Kühn, I., Wittig, R., Ozinga, W.A., Poschlod, P. & Klotz, S. (2008) Urbanization causes shifts in species' trait state frequencies. Preslia 80, 375-388) than the book chapter, as the journal paper might be accessible to more readers. Also, in reference number 29, it should be “analogues” not “analogueues”. And with reference number 116, there’s an x after 116. There might be more typos as I did not look at them in detail.

**********

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If you choose “no”, your identity will remain anonymous but your review may still be made public.

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Reviewer #2: No

Reviewer #3: No

[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files to be viewed.]

While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email us at figures@plos.org. Please note that Supporting Information files do not need this step.

5 May 2020

PONE-D-19-19705

Biodiversity conservation in cities: Defining habitat analogs for plant species of conservation interest

PLOS ONE

RESPONSE TO REVIEWERS – SECOND FEEDBACK

Reviewer #2: The authors have made a good effort in addressing the points I mentioned in the last review and I see that the manuscript has considerably improved. I have still a few suggestions that I think might be interesting to consider in order to further improve the manuscript.

ABSTRACT

There have been numerous and interesting improvements in the manuscript in the last review, but the abstract has barely changed. In particular, I think it might be interesting to include a short sentence about the new information provided on the local habitat conditions of M. crassifolia (i.e. the it occurs throughout a wide range of potential urban habitats).

• As suggested by the reviewer we made major revisions to the abstract to reflect the revised version of the manuscript and to mention the new information on local habitat conditions of M. crassifolia

INTRODUCTION

In the introduction, the authors have now made good use of the current literature in urban ecology. This section has now improved considerably.

• We thank the reviewer for the positive feedback

METHODS

The methods are more concise and clear now. I also find the new figures on Beirut’s historical development and particularly on the location of the sites very informative.

• We thank the reviewer for the positive feedback

RESULTS

Regarding the results section, I would move Table 1 to the Appendix, as I think it might be too long and the authors have already made a good summary of it in lines 340-343.

• We moved Table 1 to the Appendix as suggested by the reviewer

Please check if all the figures are properly numbered when uploading, as some of the attached figures didn’t match the numbering in the text.

• We revised all figures and tables and made sure that their numbering is correct

I am happy to see that table 4 has information about the local habitat conditions of the sites.

• We thank the reviewer for his/her favorable comment

DISCUSSION

The discussion has substantially improved as well. The authors now added clarifications regarding the important local habitat conditions of M. crassifolia and about the reasons why the plant might be missing in some sites.

• We thank the reviewer for his/her favorable comment

GENERAL REMARKS

I think the manuscript has now improved considerably and can be suitable for publication after the aforementioned improvements.

Reviewer #3: Dear Itani et al.

Thank you for considering my previous comments. I think that the manuscript has greatly improved. Still, some minor issues remain. Please, allow me to point these out:

- Abstract, line 45: add “of” between “design” and “urban habitat analogues”

• We added “of” between “design” and “urban habitat analogues” as suggested by reviewer

- Lines 72 to 74: This sentence is misleading. It sounds as if novel ecosystems do include remnants of natural vegetation. Please, have a look at Kowarik & von der Lippe (DOI: 10.1111/1365-2664.13144) for definitions of natural remnants vs. novel ecosystems and do rephrase the sentence.

• The reference Kowarik and von der Lippe was consulted as suggested by reviewers and the sentence was revised for more clarification. “Novel ecosystems include urban green spaces that emerge mostly after built structures have replaced previously existing ecosystems. As such they include non native vegetation assemblages, consisting of native, spontaneous, naturalized, and invasive species [4]. ”

- Lines 74/75: Isn’t management something intentional? So why “unintentionally managed”?

• Sentence revised “Urban green spaces are sometimes abandoned after human disturbances or continue to experience disturbance regimes and consequently contain a range of both early- and late-succession vegetation. ”

- Lines 76/77: "When unmanaged, urban green spaces … can potentially contribute to urban biodiversity conservation" – does that mean, on the contrary, that when managed, urban green spaces cannot contribute to urban biodiversity conservation? It sounds like this but I do not think that this is what you wanted to say, especially as in the end of your manuscript you suggest the intentional design and management of habitat analogues for the conservation of the target species. Please, rephrase lines 76/77.

• Sentence in line 76/77 was rephrased to clarify that both unmanaged and managed green space can potentially contribute to urban biodiversity conservation. “Both unmanaged and managed green space can potentially contribute to urban biodiversity conservation.” added as introductory sentence.

- Please note that habitat = biotope (the former is in English and the latter is derived from German, but basically, both mean the same). So, I suggest you only use the term habitat, e.g. from lines 92 on: “Many plant species can be found more or less regularly in various urban habitats. For example, classification of urban habitat types inside the city of Berlin has revealed 19 habitats particularly worthy of protection and these were nominated as legally protected [22]. However, the classification of habitat types inside cities requires standard habitat classification systems which have not been developed in all countries, at least not in Lebanon [23]. Furthermore, the nomination of such habitat types becomes challenging when [...]”

• Habitat was used instead of biotope and sentence was changed as per reviewer suggestion

- In lines 141-149, also use the terms habitat and classification: lines 145 “vegetation classification” instead of “vegetation description”; line 148 “vegetation classification” instead of “biotope type mapping”; lines 148 and 149 “habitats” instead of “biotopes”. The way the text is written at the moment makes me feel that different terms are used for the same thing, that’s why I am suggesting these replacements.

• Terms were revised as suggested by reviewer

- Lines 159/160, I suggest you write “[…] other studies suggest that descriptions of functional types, such as life form, may permit […]”. At the moment, it reads as if functional types are an example of life form – but rather, life forms are an example of functional types.

• Sentence was revised as suggested by reviewer

- Line 163: I do not know what you mean with “other physiognomic characters”. Can you use another term or provide an example?

• We used another term as suggested by the reviewer “... life-form, among other descriptions of functional types, were associated with plant responses to environmental change...”

- Lines 197 to 203 are confusing. There, it seems that Khaldeh, Beirut (including Ras Beirut), Amchhit and Byblos are your study sites. However, in lines 215 ff, you write that Ras Beirut is your study site. Please, be more precise in lines 197 – 203.

• Lines 197 to 203 were revised to clarify that the study site was in Beirut

- References to Fig. 1, 2, and 3 in the text are mixed up. Fig. 1 in the text = Fig. 2 where the figure is shown; similarly Fig. 2 in the text = Fig 3 and Fig 3 in the text is Fig.1.

• References to figures were adjusted

- Line 263 “we placed quadrats” – a certain number? Similarly, lines 266/267 “we increased the number of quadrats” – up to a maximum number of …?

• Numbers were provided as suggested by the reviewer “In vegetation patches with clearly visible boundaries, one to two 1 m × 1 m quadrats were placed [32].” “... we increased the number of quadrats, up to six, … ”

- Lines 304/305, the site numbers “(Site 17)” / “(Site 16)” do not seem to occur anywhere else in the manuscript (at least, I could not find them). I think that it is not necessary to provide these numbers as long as they are not referred to anywhere else (e.g. tables or figures). Therefore, I suggest to delete the numbers.

• As suggested by reviewer sites 16 / 17 were deleted

- Lines 447: “is classification is” – delete one “is”

• Change made extra “is” removed

- Lines 488/489: Shwartz et al. warn against expanding cities and they suggest to improve the quality of urban green spaces. But they do not present these two points as opposing strategies. Therefore, I suggest you phrase the sentence like this: “Improving the quality of existing green spaces throughout the entire urban matrix has been suggested as an effective approach to enhancing biodiversity experience [122].”

• Sentence was rephrased as suggested by reviewer

- Lines 550-552: This (trash) comes surprisingly and in my opinion has no close relationship to the core topic of your paper. I would delete it.

• Sentence regarding trash deleted as suggested by reviewer

- Line 556: “increasing species’ site area” – do you mean all species or do you mean specific species (e.g. rare species, endemic species, protected species)?

• In this sentence we mean only the target species. The sentence was revised to clarify this. “... , increasing a target species’ site area in a city is highly desired ...”

- In Fig. 2 it is very hard to visually distinguish between dots for Status = Extinct and dots for Status = Recolonized. Please, consider changing colors so that differences among the colors become more obvious (or check in the proof if quality go better than it is in the pdf-file that I got for review).

• Color scheme was changed to better appear after publication

- References: Please, do check references carefully as there are several typos within then. For example, journal names should be written with capital first letters (e.g. not Journal of applied ecology but Journal of Applied Ecology). Moreover, reference number 10 says “Doctoral dissertation” and “Master thesis” – it cannot be both a t once, can it? For reference number 19, rather cite the journal paper (Knapp, S., Kühn, I., Wittig, R., Ozinga, W.A., Poschlod, P. & Klotz, S. (2008) Urbanization causes shifts in species' trait state frequencies. Preslia 80, 375-388) than the book chapter, as the journal paper might be accessible to more readers. Also, in reference number 29, it should be “analogues” not “analogueues”. And with reference number 116, there’s an x after 116. There might be more typos as I did not look at them in detail.

• We checked and corrected all references.

Submitted filename: RESPONSE TO REVIEWERS MAY 1 2020.docx

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21 May 2020

Biodiversity conservation in cities: Defining habitat analogues for plant species of conservation interest

PONE-D-19-19705R2

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28 May 2020

PONE-D-19-19705R2

Biodiversity conservation in cities: Defining habitat analogues for plant species of conservation interest

Dear Dr. Talhouk:

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