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1. As human populations increasingly live in cities, urban floras and the ecosystem services they provide are under increasing threat. Understanding the effects of urbanization on plants can help to predict future changes and identify ways to preserve biological diversity. Relatively few studies document changes through time in the flora of a focal region and those that do primarily address European floras. They often rely on contemporary spatial gradient studies as surrogates for changes with time.
2. We compare historical species records (prior to 1940) with the current flora for Marion County, Indiana, USA, home to Indianapolis, the 13th largest city in the United States. Specimens from the Friesner Herbarium of Butler University and other vouchered records for the county provided the basis for historical records. Current records are derived from inventories of 16 sites conducted by Herbarium staff and other botanists over the past 15 years.
3. Physiognomic group, wetland classification and nativity (native vs. non-native) were determined for each species. Fidelity to high-quality habitat was quantified using coefficients of conservatism (C-values).
4. The last 70 years have seen a significant turnover in species presence, most notably a decrease in native plant species number (2.4 per year) and quality, with an accompanying increase in non-native plants of 1.4 per year. Loss of species has been non-random, with a disproportionate number of high-quality wetland plants lost. The signature of past land use can be seen in physiognomic changes in the composition of the flora that reflect the shift from agriculture to urban/suburban land use.
5. Many invasive non-native shrubs now present have escaped from cultivation, highlighting the combined threats of habitat conversion and human plant preference to native flora in cities. These invasives likely present the greatest threat to remaining biodiversity.
6. Synthesis. This study demonstrates the value well-documented historical records, such as those housed in herbaria, can have in addressing current ecological issues.
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It is estimated that for the first time in history more than half of the world’s people now live in cities (UNFPA 2007). Urbanization puts great pressure on natural resources needed to provide ecosystem services to support burgeoning human populations. Likewise, urban green spaces are becoming important refuges for native biodiversity (Goddard, Dougill & Benton 2009). At the same time, the social importance of urban floras has never been greater (Stenhouse 2004; Fuller et al. 2007). In the coming decades, most people’s contact with nature will be in urban settings (Thompson & McCarthy 2008).
The emerging field of urban ecology seeks to explore, document and understand the functioning of ecosystems in intimate association with humans and the built environment (Kaye et al. 2006; Shochat et al. 2006; Shen et al. 2008). A growing body of literature supports the notion that generalizations from studies of ecosystem processes in natural systems may not be applicable in human-dominated systems (Williams et al. 2009). For example, urban sites have altered disturbance regimes (Sukopp 2003) resulting in a perpetual state of disequilibrium. Theories of stability based on equilibrium are likely to be inadequate for urban ecosystems (Rebele 1994). Intentional and unintentional introductions of non-native species have degraded habitats and shift community composition in urban settings in ways that influence delivery of ecosystem services and habitat resiliency (Niinemets & Penuelas 2008; Walker et al. 2009). Finally, resource availability for co-evolved fauna, such as pollinators and seed dispersers, are likely to be greatly altered by urbanization (Burghardt, Tallamy & Shriver 2009).
Despite its potential to generate significant change, as noted by Tait, Daniels & Hill (2005), relatively few studies have investigated the effects of urbanization on flora. Studies examining biodiversity and richness of urban floras have typically found reduced overall biodiversity (Goddard, Dougill & Benton 2009) but greater species richness than surrounding rural areas (Wania, Kuhn & Klotz 2006; McKinney 2008). These results are usually attributed to the increased numbers of both native and non-native species (Sukopp 2003), most likely caused by cities having larger species pools due to landscaping and gardening (Walker et al. 2009). Also, both species types are able to occupy the diverse habitats available in cities, with their heterogeneous landscapes, compared with more homogeneous agriculture-dominated rural areas (Rebele 1994; Wania, Kuhn & Klotz 2006; Godefroid & Koedam 2007; McKinney 2008).
In addition to spatial patterns, it is important to investigate how urbanization has affected floras through time. Several studies examining temporal effects of urbanization on flora have used transect data that document changes that span the rural–urban gradient (e.g. Sukopp 2003; Lawson, Lamar & Schwartz 2008; Walker et al. 2009). With this approach, contemporaneous spatial patterns are surrogates for change with development over time. A few studies have examined the relationship between plant species’ functional traits and their success at persisting in urban areas (e.g. Godefroid 2001; Chocholouškovà & Pyšek 2003; Knapp et al. 2009, 2010). However, additional information describing changes in urban floras through time is still needed to better guide sound ecological restoration and management (e.g. Godefroid 2001; Tait, Daniels & Hill 2005; Pavao-Zuckerman 2008) and to predict future changes.
The paucity of studies that directly compare historical floras in formerly less urbanized areas with the current flora present in the same area (Stehlik et al. 2007) is due to lack of comprehensive historical data for most cities. In this article, we compare vouchered historical records from 1905 to 1940 of plant species occurring outside of cultivation in Marion County, Indiana, USA, with contemporary inventories to document changes in the flora. Using herbarium specimens, collections of pressed and dried plants that document flora of a region, we provide a record of floristic changes through time in response to urbanization. We hypothesized that land use changes would be reflected in: (i) an increase in the total number of species due primarily to an increase in non-natives resulting from spread of weedy species and escapees from gardens and landscaping; (ii) the loss of species with preference for high-quality natural habitat (due to direct effects of habitat destruction and indirect effects of fragmentation and alteration of natural disturbance regimes; (iii) shifts in physiognomy due to changes in habitat availability and community composition and (iv) possible phylogenetic shifts in species composition in response to landscape pattern changes and changing evolutionary selective pressures with urbanization.
Materials and methods
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- Materials and methods
The Friesner Herbarium of Butler University (BUT) was founded in 1919 and contains over 42 000 specimens collected in Indiana. Over 2800 of these were collected in Marion County, home to the university and the city of Indianapolis, which has served as the state capital since 1831. Marion County has the largest population of any county in the state, an estimated 900 000 people. There are an estimated one million more in the surrounding counties that make up the greater Indianapolis metropolitan area. Marion County is currently one of the 20 most populated counties in the United States with a total area of approximately 1050 km2, its human-population density of 857 inhabitants km−2 is considered very high (http://www.citydata.com) by United States standards.
Marion County is located in central Indiana, in the Central Till Plain Section of the Central Till Plain Natural Region (Homoya et al. 1985). General Land Office Survey records witness trees from 1820 to 1822 and soil survey records indicate that Marion County was 98% forested in pre-European settlement times (Barr et al. 2002), with remaining land cover being open water or prairie. Mesic beech–maple upland forest covered 76% of the county, with small areas of oak–hickory forest on drier ridges. Wet–mesic depressional forests were scattered throughout the county with floodplain forests along major rivers and tributaries. Wetlands including ponds, bogs, marshes and fens are estimated to have made up approximately 1% of the original land cover (Barr et al. 2002). Barr et al. (2002) reported recent forest cover in Marion County reduced to 13% by the late 1900s. In 1922, an estimated 80% of land use was agriculture (http://www.savi.org). Agricultural use remained consistent through 1953 at 72%, but rapid urbanization in the 1960s and 1970s reduced the amount of farmland by half; by 1990, only 18% remained.
Published historical records for Marion County were compiled and nomenclature was updated to follow the USDA Plants Database (http://plants.usda.gov). Deam’s authoritative 1940 Flora of Indiana (Deam 1940) reports records by county for species for which he confirmed vouchers in herbaria. These records were checked against 2820 specimens deposited at BUT and additional sheets in the Deam Herbarium at Indiana University (IND). Historical collection localities within the county were also gathered from specimens in each collection.
While herbarium specimens provide a concrete and reviewable record of plants growing in a particular place at a particular time, there are caveats to be aware of when using them to establish historical floras. They tend not to be uniform in location and habitat description, as noted by Fuentes et al. (2008). However, in the label convention used at BUT, all sheets have county of collection specifically listed, and county boundaries have been in place in central Indiana since 1816. Level of collection effort can bias data gleaned from herbarium specimens and presents particular challenges when, for example, using herbarium specimens to track the spread of non-native species across landscapes by decade (e.g. Delisle, Lavoie & Lachance 2003 or Lavoie, Dufresne & Delisle 2005). We categorize our species into just two groups, historical (pre-1940) and recent (since 1996), reducing the likelihood of bias. Marion County specimens at BUT were not collected in a systematic method and may not cover all habitats and geographic regions in the county. However, they represent the efforts of 28 different collectors, beginning in 1905. We assume this broad coverage reduces chances of pseudo-absences, where species were present but either not encountered or collected and therefore not documented.
Recent records were compiled from surveys of 16 sites conducted by the authors and students from BUT from 1996 to 2009, covering over 8.5 km2, along with a few surveys provided by other botanists. Most locations inventoried were parks with significant natural area remaining, but habitats of all disturbance levels are included. Three are State Dedicated Nature Preserves. The areas recently inventoried cover approximately 8% of the county’s non-mowed vegetated area and approximately 80% of forested remnants (Barr et al. 2002). Vouchers documenting recorded species for four sites are deposited at BUT. Recent records for non-native species include the observational records of Overlease & Overlease (2007). It is difficult to know how comprehensive these recent studies are compared with historical records and collections. There is less remnant natural habitat remaining, which would tend to concentrate effort, but there are also more second-growth woods in the county where agriculture has been abandoned.
We used coefficients of conservatism (C-values) to quantify species’ fidelity to high-quality habitats and therefore, tolerance of disturbance, as an indicator of overall floristic quality. C-values were chosen for analysis of our data because they are comprehensive for the plants in our study area, provide a numerical value for species’ behaviour, and can be used to make statistical comparisons between sites and through time. C-values, originally devised for the flora of the Chicago region by Swink & Wilhelm (1994), rank native species from 0 to 10 based on fidelity to high-quality habitats, with higher numbers indicating greater preference for high-quality habitat and less tolerance of disturbance. Because habitat characteristics and species behaviour often vary geographically, C-values must be assigned at a regional scale. In 2004, C-values were assigned to all the species known to grow in Indiana by a panel of nine experts with great familiarity with the state flora (Rothrock 2004). C-values are now available for at least six state floras and one Canadian province and their use is gaining wide acceptance among land managers and restoration ecologists (Rothrock 2004). They have been used to identify high-quality remnant habitat (e.g. Rothrock & Homoya 2005; Ruch et al. 2007) and to quantitatively track the habitat quality of restorations through time (usually several years) based on the species they support (e.g. Taft, Hauser & Robertson 2006; McIndoe et al. 2008). To our knowledge, ours is the first study to use C-values to track floristic changes over decades.
C-values for species present in Marion County historically and those seen in recent surveys were compiled and analysed, along with species’ nativity, physiognomy and wetland type indicator using Floristic Quality Assessment software developed by the Conservation Research Institute (Wilhelm & Masters 2004). The software assigns each species a regional numeric ‘wetness’ value corresponding to U.S. Fish and Wildlife Wetland Category type (http://plants.usda.gov/wetinfo.html). Obligate wetland species score −5, obligate upland species 5. Plants listed as native are those considered to have been present in Indiana at the time of western European settlement. We include only plants growing spontaneously, outside of cultivation (native and naturalized).
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Comparison of the contemporary flora of Marion County with historical records shows both reporting about 700 species (Table 1). The percentage of non-native species has increased from slightly more than 20% to over 27%. Mean C-value for native species did not change with time, but there has been a significant decline in mean C-values with non-natives included (given C-values of zero) (Table 1).
Table 1. Floristic quality data comparing historical records of Marion County, Indiana, USA, with recent inventories
|No. native species||563||509|
|Native mean C||4.2||4.0|
|Native mean C with non-natives||3.4*||2.9*|
|Native mean wetness||0.2||0.4|
Although there has not been much of a change in overall species richness, there has been considerable species turnover. Thirty-one percent of all species reported historically have not been seen during recent studies. Eighty-eight percent of these are native species, which equates to a loss of 2.4 native species per year. Additions to the flora almost balance losses. Two hundred and eleven species have been seen in recent studies that were not reported by Deam (1940), representing 30% of the current flora. Almost half of these, 96 of 211, are non-native plants. This equates to a rate of non-native species gain of 1.4 per year.
Historical records report 54 more species of native plants than have recently been seen (Table 2). Native perennial forbs are the most common physiognomic group for both time periods, accounting for almost 50% of species. Recent inventories show notable decreases in annual forbs, perennial and annual grasses and perennial sedges. More native trees and shrubs have been reported in recent years than were reported historically.
Table 2. Comparison of the physiognomic breakdown of species of native and non-native plants reported historically with contemporary inventories in Marion County, Indiana, USA
| ||Native species||Non-native species|
|Total||(%) Total*||(%) Native†||Total||(%) Total*||(%) Native†||Total||(%) Total*||(%) Non-native‡||Total||(%) Total*||(%) Non-native‡|
The distribution of species with different C-values (range 0–10) indicates a loss of species indicative of high-quality remnant habitat based on C-value (C-values 8–10) (Fig. 1). Losses of species with C-values of 10 and 9 were most dramatic, with shifts from 14 to two and seven to one respectively (Table 3). Almost all of these plants are obligate wetland species with wetness values of −4 or −5.
Figure 1. Numbers of species for each C-value reported for the Marion County, Indiana, USA, flora in historical and recent studies.
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Table 3. Species in the Marion County, Indiana, USA, flora with C-values of 9 and 10
|Acorus americanus||10||−5||x|| |
|Carex bromoides||10||−5||x|| |
|Carex lupuliformis||10||−4||x|| |
|Cornus amomum||10||−4||x|| |
|Deschampsia caespitosa||10||−4||x|| |
|Dryopteris cristata||10||−5||x|| |
|Dulichium arundinaceum||10||−5||x|| |
|Eleocharis erythropoda||10||−5||x|| |
|Lysimachia hybrida||10||−5||x|| |
|Melanthium virginicum||10||−5||x|| |
|Sagittaria rigida||10||−4||x|| |
|Saxifraga pensylvanica||10||−5||x|| |
|Symphyotrichum laeve||10||5|| ||x|
|Ulmus thomasii||10||−1||x|| |
|Carex careyana||9||5||x|| |
|Comarum palustre||9||−5||x|| |
|Cystopteris bulbifera||9||−2||x|| |
|Filipendula rubra||9||−4||x|| |
|Helianthus microcephalus||9||4||x|| |
|Triphora trianthophora||9||4||x|| |
Perennial forbs and grasses are the largest groups of non-native plants in both historical and recent records (Table 2). The most notable shifts in the physiognomy of non-natives with time are very large increases in woody species (Table 4). The number of trees increased from three to 11 and the number of shrubs increased from one to 23. There was also a large decrease in the percentage of annual forbs and grasses.
Table 4. Woody non-native species reported in recent studies of the Marion County, Indiana, USA, flora
| ||Scientific name|
|Rubus idaeus var. idaeus§|
|Viburnum opulus var. oplulus‡|
|Woody vines||Celastrus orbiculatus¶|
The number of non-native herbaceous invasive species in Marion County has increased only slightly since the time of Deam (1940) (Table 5). Fourteen species considered ‘most unwanted’ invasive plants by the Indiana Cooperative Agricultural Pest Survey Program (http://extension.entm.purdue.edu/CAPS/) based on the threats they pose to cultivated and natural plant communities have been seen in recent surveys. Only two of these are new to the flora: Alliaria petiolata (M. Bieb.) Cavara & Grande and Humulus japonicus Siebold & Zucc. were not reported by Deam for Indiana in 1940. Phalaris arundinacea L. was known from elsewhere in Indiana but not reported for Marion County by Deam, indicating it is not new to the region. Dipsacus laciniatus L., Glechoma hederacea L. and Melilotus officinalis (L.) Pall. were known for the county as early as 1895 (Wilson 1895).
Table 5. Invasive non-native herbaceous species found in historical and recent floristic survey in Marion County, Indiana, USA
|Alliaria petiolata|| ||x|
|Humulus japonicus|| ||x|
The plants historically known from Marion County are from 106 families. Recent inventories have identified plants from 113 families. Nearly a third of the flora during both inventory times belongs to one of three families. For both historical and contemporary inventories, Asteraceae are the most common family comprising about 12.6 and 13.6% of plants respectively. Poaceae (11.0 and 7.3%) and Cyperaceae (8.6 and 5.5%) are second and third in abundance during both sample times. The distribution of species among plant families, an indicator of taxonomic evenness, did not change appreciably with time (Fig. 2).
Figure 2. Distribution of species among families for plants reported for the Marion County, Indiana, USA, flora in historical and recent studies.
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Williams et al. (2009) present a framework for understanding floristic changes in response to urbanization based on factors that influence habitat availability, spatial arrangement of habitats, the pool of plant species and evolutionary selective pressures on population persistence. They identify four filters: (i) habitat transformation, (ii) fragmentation, (iii) the urban environment and (iv) human preferences. Our data indicate urbanization in Marion County has clearly been influenced by two of these filters. High-quality wetland species have been locally extirpated due to habitat loss and changing patterns of land use have shifted the physiognomic composition of plant communities and species that comprise them. The species pool has also been greatly influenced by human preference for non-native landscape shrubs, which have now escaped from cultivation.
Urbanization can also be seen as a local extinction filter (Williams et al. 2005). Our finding of loss of high-quality wetland plants adds to a small set of urban flora studies that document this connection. Larger and more representative studies are needed to help determine the strength of different filters, to further identify plant and habitat traits that are favoured or lost through urbanization (Williams et al. 2005; Thompson & McCarthy 2008; Knapp et al. 2010) and to determine the degree to which there are common characteristics of urban floras that override regional habitat differences and past land use. Herbarium collections, with their documentation of species’ historical presence, will continue to be an important resource for future studies in urban ecology.