The Botanist Effect Revisited: Plant Species Richness, County Area, and Human Population Size in the United States MARCO PAUTASSO∗ AND MICHAEL L. MCKINNEY† ∗ Division of Biology, Imperial College London, Wye Campus, High Street, Wye, Kent, TN25 5AH, United Kingdom, email [email protected] †Department of Earth and Planetary Sciences, 1412 Circle Drive, 306 Earth and Planetary Sciences Building, The University of Tennessee, Knoxville, TN 37996-1410, U.S.A.

Abstract: The “botanist effect” is thought to be the reason for higher plant species richness in areas where botanists are disproportionately present as an artefactual consequence of a more thorough sampling. We examined whether this was the case for U.S. counties. We collated the number of species of vascular plants, human population size, and the area of U.S. counties. Controlling for spatial autocorrelation and county area, plant species richness increased with human population size and density in counties with and without universities and/or botanical gardens, with no significant differences in the relation between the two subsets. This is consistent with previous findings and further evidence of a broad-scale positive correlation between species richness and human population presence, which has important consequences for the experience of nature by inhabitants of densely populated regions. Combined with the many reports of a negative correlation between the two variables at a local scale, the positive relation between plant species richness in U.S. counties and human population presence stresses the need for the conservation of seminatural areas in urbanized ecosystems and for the containment of urban and suburban sprawl.

Keywords: biogeography, density–area relationship, habitat heterogeneity, macroecology, native and exotic plants, North American flora, sampling effort, species–area relationship, species–energy relationship, urban ecology no de la Poblaci´ on El Efecto Bot´anico Revisado: Riqueza de Especies de Plantas, Superficie del Condado y Tama˜ Humana en los Estados Unidos

Resumen: Se piensa que debido al “efecto bot´anico” la riqueza de especies de plantas es mayor en a´ reas donde la presencia de bot´ anicos es desproporcionada y en consecuencia el muestreo es m´ as minucioso. Examinamos si este era el caso de los condados de E.U.A. Recopilamos el n´ umero de especies de plantas vasculares, tama˜ no de la poblaci´ on humana y superficie de los condados de E.U.A. Controlando la aurocorrelaci´ on espacial y la superficie del condado, la riqueza de especies de plantas increment´ o con el tama˜ no y densidad de la poblaci´ on humana en condados con y sin universidades y/o jardines bot´ anicos, sin diferencias significativas en la relaci´ on entres los dos subconjuntos. Esto es consistente con hallazgos anteriores y mayor evidencia de una correlaci´ on positiva entre la riqueza de especies y la presencia de la poblaci´ on humana, que tiene consecuencias importantes para la experiencia en naturaleza de habitantes de regiones densamente pobladas. En combinaci´ on con los numerosos reportes de una correlaci´ on negativa entre las dos variables a escala local, la relaci´ on positiva entre la riqueza de especies de plantas en los condados de E.U.A. y la poblaci´ on humana acent´ ua la necesidad de conservar a on ´ reas seminaturales en ecosistemas urbanizados y de contener la expansi´ urbana y suburbana.

Paper submitted October 31, 2006; revised manuscript accepted April 15, 2007.

1333 Conservation Biology Volume 21, No. 5, 1333–1340  C 2007 Society for Conservation Biology DOI: 10.1111/j.1523-1739.2007.00760.x

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Palabras Clave: ecolog´ıa urbana, esfuerzo de muestreo, flora norteamericana, heterogeneidad de h´abitat, macroecolog´ıa, plantas nativas y ex´ oticas, relaci´ on densidad-´area, relaci´ on especies-´area, relaci´ on especies-energ´ıa

Introduction Human beings exert a pervasive influence on biodiversity (e.g., Vitousek et al. 1997). We have increased the rate of species extinctions (e.g., Kerr & Currie 1995) through habitat loss following land use and climate change (e.g., Schlesinger 2006), the appropriation of an increasing part of the Earth’s primary productivity (e.g., Imhoff et al. 2004), and species introductions, especially on islands (e.g., Manne et al. 1999). These processes reach areas far from regions of preferential human settlement (e.g., Gregg et al. 2003), but are worsened by the spatial cooccurrence at coarse resolutions of high numbers of human beings and species (e.g., Gaston 2005; Pautasso 2007). Such a broad-scale correlation has been documented for plants (in Africa, Balmford et al. 2001; in Europe, Ara´ ujo 2003; in North America, McKinney 2001; on islands of the Southern Oceans, Selmi & Boulinier 2001), amphibians, birds, and mammals (in Africa, Balmford et al. 2001; in Asia [birds only], Ding et al. 2006; in Australia and North America, Luck et al. 2004; in Europe, e.g., Ara´ ujo 2003; in South America [anurans only], Diniz-Filho et al. 2006). Other researchers report such a correlation for these and other taxa and regions, and their findings are reviewed in Gaston (2005). Mechanisms that have been suggested as potential causes of this correlation are of two kinds. On the one hand, people have historically tended to settle in higher numbers in regions of medium to high productivity (e.g., Balmford et al. 2001; Gaston 2005; McKinney 2006a), and these regions are also those where, other things being equal, species richness of most taxa tends to be at its highest (e.g., Rosenzweig 1995; K¨ uhn et al. 2004; Williams et al. 2005). Similarly, it has been shown that global hotspots of biodiversity tend to be located in regions of high population size and growth rate (although this is to be expected when definitions of hotspots include species’ threat status due to habitat conversions; Cincotta et al. 2000; Fisher & Christopher 2007) and that species extinction risk is related to measures of human impact for birds globally (Davies et al. 2006) and for plants regionally (Britain, Thompson & Jones 1999). On the other hand, where people have settled, they have made habitats more diverse and introduced species, either consciously or inadvertently (e.g., Hope et al. 2003; Williams et al. 2005); thus, people not only drive many species to extinction, but also raise the number of species present (e.g., McKinney 2002a; Wania et al. 2006). For example, for plants, herptiles, and mammals the number of exotic species per nation is positively related to a nation’s

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human population size (McKinney 2006a); the number of exotic plant species in U.S. parks is positively related to the human population size of neighboring counties (McKinney 2002b); and the number of exotic plant species per unit area in U.S. counties is positively related to native plant species richness and human presence (Stohlgren et al. 2005). Similarly, the number of exotic insect and plant species on islands in the Southern Ocean is positively related to energy availability and frequency of human visitors (Chown et al. 2005); the number of exotic plant species on islands off the coast of eastern North America is positively related to human population size of these islands (McMaster 2005); and species richness of exotic plants of roadside communities on the Canary Islands, Spain, is positively related to native richness and proximity to urban centers along an elevational gradient (Arevalo et al. 2005). The first mechanism is a major worry for conservationists because parks and nature reserves have historically tended to be located in wilderness areas, hence at a distance from human settlements, and, paradoxically enough, where many species of conservation interest are absent or rare (e.g., Ando et al. 1998; Luck et al. 2004; V´azquez & Gaston 2006). In this context if important parts of biodiversity are located in regions where the pace of urbanization is increasing (e.g., Vaha-Piikkio et al. 2004; Canova 2006; Hope et al. 2006), then a successful conservation strategy of these biotic resources should enable the coexistence between people and nature (e.g., Bryant 2006; Miller 2006). In this way urban ecology becomes a key element of conservation biology (e.g., Moskovits et al. 2004; Pauchard et al. 2006). The second mechanism is somewhat at odds with current ecological thinking about invasive species and their threat to natural ecosystems (e.g., Mack et al. 2000; Genovesi 2005). Nevertheless, even if densely populated regions show a higher number of species than surrounding areas (for plants, e.g., Klotz 1990; this is in part due to the presence of exotics, Pyˇsek 1993; Stadler et al. 2000; Deutschewitz et al. 2003), measures aimed at reducing species introductions in a framework of biodiversity protection can still be justified because they favor nativespecies preservation and curb regional biotic homogenization (e.g., Lockwood et al. 2000; Olden et al. 2006). Another explanation of the human-biodiversity correlation might be the sampling effect recently suggested by Moerman and Estabrook (2006). In 30 of the 37 cases they examined, the number of plant species reported in U.S. counties where universities and/or botanical gardens (UBG) are present is higher than the plant species

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richness in neighboring counties without these institutions. They argue that this finding is neither random nor likely to be caused by differences in area or other environmental factors and conclude that the database they used (and possibly many others) is biased inasmuch as counties where botanists are present have been sampled more thoroughly. In their view, U.S. counties with higher species richness and botanists’ presence are thus only artifactually species rich. This “botanist effect” had already been invoked as one potential explanation possibly contributing to the higher plant species richness reported in the urbanized area of Nairobi compared with other regions of northwestern Kenya (Stadler et al. 2000). It has been repeatedly pointed out that, other things kept constant, the number of species of a given taxon recorded from different areas of equal size depends on the effort invested in sampling that area (e.g., Colwell & Coddington 1994). We examined the issue of plant species richness in U.S. counties with or without UBG more thoroughly. Variation in area and population size among counties does not seem to have been addressed properly by Moerman and Estabrook (2006). A positive species–area relationship is widely reported in the ecological literature (e.g., MacArthur & Wilson 1967; Connor & McCoy 1979), and a positive relationship between species richness and human presence at coarse scales, possibly mediated by primary productivity and habitat heterogeneity, is being documented increasingly.

Methods We based our analyses on the data set of vascular plant species in U.S. counties used by Moerman and Estabrook

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(2006), the Synthesis of the North American Flora (Version 2.0, Kartesz & Meacham 2005), which can be freely downloaded from the Web. Using this software, we manually noted the number of flowering plant species for each county in the coterminous United States (n = 3072). We then obtained data on the area (square kilometers) and resident human population for each of these counties from the U.S. Census Bureau Web site. County area and human population data refer to 1990. To control for spatial autocorrelation, we recorded the geographical coordinates for each county seat. We then subdivided the data into two subsets: counties with universities, other institutions of higher education (University of Austin 2006), and botanical gardens (Botanical Gardens Conservation International 2006) and counties without any of these institutions. We did not include data from Ohio and Virginia in analyses because in Ohio species richness values were remarkably low compared with counties in neighboring states (average species richness of Ohio counties, 42; Kentucky, 435; Indiana, 717; Pennsylvania, 1081) and in Virginia patterns may be biased by the presence of counties that are towns. Urban counties in states other than Virginia were not excluded from analyses because counties in Virginia that are towns have an average area of 37 km2 , whereas the most densely populated counties in the United States (those, e.g., with a density higher than 1000 inhabitants/km2 ) have an average area of 540 km2 . Given their markedly larger area, urban counties in U.S. states other than Virginia tended to include habitats other than towns and did not represent an incongruity in the data set as did counties in Virginia. This left a set of 692 counties with UBG and a set of 2187 counties without these entities (Fig. 1). We did not assess the influence on recorded plant species richness of varying numbers of UBG in

Figure 1. Geographical distribution (Albers projection) of U.S. counties where universities and/or botanical gardens are present ( filled circles; n = 692) and without such institutions (empty circles; n = 2187). Counties in Ohio and Virginia were excluded (see Methods).

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different counties because it is probably not the density of institutions with potential presence of botanists, but the number of botanists that could be of direct relevance in this issue, and appropriate weighting of UBG of different sizes could be problematic. We thus conducted analyses on a basis of presence or absence of UBG. We performed analyses in SAS 9.1 (Littell et al. 1996). We log transformed county species richness, population, and area prior to analysis to conform to the assumptions of statistical tests. Because neighboring data points may not be spatially independent (e.g., Legendre 1993), we ran mixed models to control for spatial autocorrelation within six main geographic regions (southeast, southcentral, southwest, northwest, north-central, northeast). For further details on the methodology we used to control for spatial autocorrelation, see Pautasso and Gaston (2005). Because results from nonspatial models are less reliable than those controlling for spatial autocorrelation, only the latter are given. Nevertheless, we conducted analysis of variance and determined the proportion of variance in the response variable explained by the dependent variables without controlling for spatial autocorrelation. We assessed differences in the slope and if slopes were not significantly different in the intercept of regressions for the two subsets of data on the basis of the 84% confidence intervals (Payton et al. 2003). In addition, the effect in models of the presence or absence of UBG was tested with a categorical factor.

Results Plant species richness was significantly higher (ANOVA: F 1,2877 = 278, p < 0.0001) for counties with UBG (mean [SD] = 896 [411]) than for those without (595 [327]). Although area was not significantly different (F 1,2877 = 0.23, p = 0.63) between counties with UBG (mean [SD] = 2,781 km2 [4,370]) and those without (2,523 km2 [3,139]), human population was significantly higher (F 1,2877 = 1,361, p < 0.0001) in the former (234,098 [506,231]) than in the latter counties (29,957 [67,226]). Counties with UBG may have had higher species richness than those without such institutions because of higher human population in the first set of counties. Thus, we investigated the relationship between species richness and human population size. Species richness increased significantly with increasing human population both in counties with UBG (r2 = 0.13, log species richness = 2.15 + 0.15 [log population], intercept SE = 0.08, slope SE = 0.01, p < 0.0001; Fig. 2) and in those without (r2 = 0.10, log species richness = 2.18 + 0.15 [log population], intercept SE = 0.05, slope SE = 0.01, p < 0.0001; Fig. 2). Both slopes and intercepts of the relation between species richness and human population were not significantly different in the two subsets. An overall

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Figure 2. Regression of logarithmically transformed species richness (number of species) in U.S. counties against human population size (number of people). Symbols defined in Fig. 1.

model of species richness for all data as a function of human population and of a categorical factor reflecting the presence or absence of UBG showed that the latter factor was not significant ( p = 0.85). Although average county area did not vary significantly between the two subsets, the area of individual counties may still have been an important factor in the regression of species richness against human population. Thus we investigated how species richness and human population varied with county area. Species richness significantly increased with increasing county area both in counties with UBG (r2 = 0.08, log species richness = 2.23 + 0.20 [log area], slopes SE = 0.03, p < 0.0001) and in those without (r2 = 0.06, log species richness = 1.51 + 0.38 [log area], slope SE = 0.02, p < 0.0001). A categorical factor in a model of the whole data set showed that the presence or absence of UBG was a significant factor ( p = 0.02). The slope of the relationship between species richness and county area was significantly steeper for counties without UBG than for those with them, which means their intercepts could not be meaningfully compared. As for human population, it did not significantly vary with increasing county area in counties with UBG (r2 = 0.00, log population = 4.58 + 0.10 [log area], slope SE = 0.06, p = 0.13) but significantly increased (albeit less than proportionately, i.e., with a slope significantly <1) in counties without UBG (r2 = 0.01, log population = 2.01 + 0.67 [log area], slope SE = 0.04, p < 0.0001), although the proportion of variance explained was negligible. Thus, human population density significantly declined with increasing county area both in counties with UBG (r2 = 0.30, log density = 4.58 − 0.90 [log area], slope SE = 0.06, p < 0.0001) and in those without (r2 = 0.37, log density = 2.01 − 0.33 [log area], slope SE = 0.04, p < 0.0001), although the latter case had a slope that was significantly less steep than the former. A categorical

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factor revealed that the presence or absence of UBG was a significant factor in these models ( p < 0.0001). We then modeled species richness as a function of human population controlling for variations in county area. County area influenced species richness in both subsets and human population in counties without UBG. Species richness significantly increased with increasing human population when controlling for county area both in counties with UBG (r2 = 0.21, log species richness = 1.53 + 0.15 [log population] + 0.19 [log area], slope SE respectively = 0.01, 0.03, p < 0.0001 in both cases) and without UBG (r2 = 0.18, log species richness = 1.32 + 0.09 [log population] + 0.32 [log area], slope SE respectively = 0.01, 0.02, p < 0.0001 in both cases). The increase of species with human population was significantly steeper in counties with UBG, but the increase in species with county area was significantly steeper in the other subset of counties. Nevertheless, a categorical factor revealed that the presence or absence of UBG was not a significant factor in these models ( p = 0.45). This result was confirmed by an overall model for all data of species richness as a function of human population, country area, a categorical factor for the presence or absence of UBG, and the interactions between these three explanatory variables, where the p for the presence or absence of UBG was even higher ( p = 0.77). Combining human population size and county area, human population density provided a way to simplify models while still taking into account both variables. Although in both cases the proportion of variance explained was not substantial, species richness significantly increased with increasing human population density both in counties with (r2 = 0.02, log species richness = 2.79 + 0.07 [log density], intercept SE = 0.03, slope SE = 0.02, p < 0.0001) and without UBG (r2 = 0.01, log species richness = 2.76 + 0.04 [log density], intercept SE = 0.03, slope SE = 0.01, p < 0.0001). Neither slopes nor intercepts of the relationship between species richness and human population were significantly different in the two subsets. This was confirmed by a model of the whole data set with the addition of a categorical factor, which showed that the presence or absence of UBG was not a significant factor in these models ( p = 0.09).

Discussion The increasing plant species richness with larger U.S. county human population size documented here is consistent with results from previous studies at broad scales reporting higher species richness in more populated regions. Together with that independent evidence, our results argue for a reconsideration of the botanist effect in U.S. counties (Moerman & Estabrook 2006). If plant species richness increases when there are more people

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without significant differences in intercept and slope of the relationship for counties with UBG and for those without, it is likely that U.S. counties with high plant species richness really have more species than those that show fewer species in the database used. This follows all the more so given that such a positive correlation between species richness and human population presence at coarse scales has been documented independently in other regions. Therefore, U.S. counties where botanists are disproportionately present have more plant species not because they have been sampled more thoroughly, but because they are regions of preferential human settlement, possibly because these regions have in turn higher primary productivity. It is also possible that human presence may correlate with a relatively high presence of species introductions, as has been shown for plants in U.S. states (McKinney 2002a) and U.S. and Canadian provinces (Qian & Ricklefs 2006), although both the role of productivity and of exotic species needs to be tested in further investigations at a finer scale. An additional factor is habitat heterogeneity, which is often reported as enhanced in urbanized ecosystems, particularly at coarse scales. Higher habitat heterogeneity may in turn lead to increased niche opportunities for both native and exotic species (Rebele 1994; Niemel¨a 1999; Davies et al. 2005). Because our analyses controlled for variations in area among counties, there was no evidence that area was a factor in the increase of plant species richness with an increase in human population. Incidentally, the density–area relationship was negative (there was a less than proportionate individuals–area relationship) for human beings. This relationship is well known for birds and mammals when sampling units are not delimited randomly (e.g., Pautasso & Gaston 2006) and is reported also for trail length in parks of different areas (McKinney 2005). Whatever the mechanisms are that are making human population and plant species richness positively covary in U.S. counties, our results suggest that this co-occurrence may be real and need not be a consequence of more thorough sampling in regions with higher presence of botanists. From an applied point of view, the finding that counties with high human population presence also host more species than other counties is good and bad news. It is good news for people because it means there is the potential for town dwellers to experience a higher number of species in their neighborhoods (Miller 2005). Thus people need not travel to see many different species of plants (Hope et al. 2003; Zerbe et al. 2003; Turner et al. 2004). If populated areas have more species, people are more apt to see that nature is already around them and that preserving seminatural areas in urbanized landscapes is important from aesthetic and educational perspectives (Bolund & Hunhammar 1999; Savard et al. 2000). Nevertheless, the broad-scale coincidence of people and species richness is bad news for biodiversity because

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urbanization is a major cause of biotic homogenization (e.g., Clergeau et al. 2006; McKinney 2006b). Species richness may be higher in urbanized counties, but these species could often be the same common and unthreatened species. Moreover, human presence is a negative factor for biodiversity at local scales. For plants a decrease in species richness with increasing human impact is reported at a local scale in Europe (e.g., for bryophytes in Wroclaw, Poland [Fudali 2001] and Vienna, Austria [Hohenwallner & Zechmeister 2001] and for the flora of Rome [Ricotta et al. 2001]). A similar effect of urbanization is reported in other continents (e.g., for tree species in Guangzhou City, China [Jim 2002], plants in lowland riparian areas in Colorado, United States [Miller et al. 2003], and the woody vegetation in forests in Rajasthan, India [Yadav & Gupta 2006]). Analogous findings have been documented extensively for invertebrates and birds. Results from these studies imply that the evidence reported here of a broad-scale correlation between plant species richness and human population is no justification for further urban sprawl. This is confirmed by Evans et al. (2006), who studied the relation between avian and anuran species richness and human population in South Africa at two time points. Despite a marked increase in human population, there was no significant variation in the species–human population relationship. Although the time lag chosen for the analyses (1996–2001) may be too short, this result would speak against a direct causal link between the two variables. Such an absence of causality is substantiated by Ding et al. (2006), who showed that in Asia bird species richness is related positively to human population density; but when taking into account net primary productivity, this relationship becomes negative. Further analyses should aim to unravel the mechanisms behind broad-scale positive and local-scale negative species richness-human population relationships (e.g., Hansen et al. 2005; Schochat et al. 2006). Nevertheless, given the current unrelenting population growth in urbanized areas (Calcagno 1996; Broggi 1999) and continued sprawl of development (Bassand et al. 2000; Hill et al. 2002), the conservation of seminatural patches and green corridors in urbanized areas needs to become a priority on the agenda of nature-preservation institutions.

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