Oecologia (2009) 160:839–846 DOI 10.1007/s00442-009-1329-6

CONSERVATION ECOLOGY - ORIGINAL PAPER

Aphid biodiversity is positively correlated with human population in European countries Marco Pautasso · Glen Powell

Received: 30 August 2007 / Accepted: 10 March 2009 / Published online: 8 April 2009 © Springer-Verlag 2009

Abstract At large spatial scales, high numbers of people tend to be located in regions rich in biodiversity. This pattern has been reported for plants, some invertebrate groups, amphibians, reptiles, birds and mammals, but little is known about whether aphids conform to it. Aphids originated from temperate regions of the boreal hemisphere and are thus exceptionally species-poor in the tropics. Here, we test whether aphid species richness is related to human population variation in European countries. The number of aphid species increases signiWcantly with increasing human population size. This happens also when controlling for country area, latitude and plant species richness, which are not factors signiWcantly aVecting the response variable in the multivariate model. Given that the species–area and species–people relationships have a slope shallower than 1, small countries have a higher aphid species density relative to area and to people than large ones. There is no evidence that the speciespeople correlation for aphids in European countries arises because both variables are related to increasing tempera-

Communicated by Volkmar Wolters. M. Pautasso (&) Division of Biology, Imperial College London, Wye Campus, High Street, Wye, Kent TN25 5AH, UK e-mail: [email protected] Present Address: M. Pautasso Division of Biology, Imperial College London, Silwood Campus, Ascot, Berkshire SL5 7PY, UK G. Powell Division of Biology, Imperial College London, South Kensington Campus, London SW7 2AZ, UK

ture or precipitation. Potential mechanisms underlying the Wndings could thus be a sampling artefact or an inXuence of habitat heterogeneity. There is a need for an increase in research, public awareness and conservation of largescale aphid biodiversity. Keywords Insect biogeography · Macroecology · Spatial autocorrelation · Species–area relationship · Species-people co-existence

Introduction Human beings have a pervasive distribution on the planet Earth, yet they are not distributed evenly (Small and Cohen 2004; Ellis and Ramankutty 2008; Wittemyer et al. 2008). Several large-scale investigations have shown that there is often a spatial co-occurrence of people and biodiversity (Gaston 2005). Such a positive species-people correlation has been reported for large regions in Africa (e.g. Balmford et al. 2001; Burgess et al. 2007; Fjeldså and Burgess 2008), the Americas (e.g. McKinney 2001; Diniz-Filho et al. 2006; Vazquez and Gaston 2006; Fjeldså 2007), Asia and Australia (e.g. Hunter and Yonzon 1993; Luck et al. 2004; Ding et al. 2006; Luck 2007b), as well as Europe (e.g. Araujo 2003; Moreno-Rueda and Pizarro 2007; Knapp et al. 2008; Marini et al. 2008). Taxa analysed have included plants, fungi, stream macro-invertebrates, grasshoppers, butterXies, ants, amphibians, reptiles, birds and mammals (Luck 2007a; Pautasso and Fontaneto 2008; SchlickSteiner et al. 2008; Steck and Pautasso 2008; Pautasso and Zotti 2009). A positive species-people correlation can be puzzling, as biodiversity is traditionally thought to be at its highest in wilderness regions. Protected areas are indeed preferentially

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located away from regions with a high presence of human settlements (e.g. Hunter and Yonzon 1993; Luck 2007b; Virkkala and Rajasarkka 2007; Loucks et al. 2008). However, over geographic scales, both species richness and people respond positively to increasing environmental energy availability. This means that, where the climate is more favourable, there is the potential for more species to coexist, but that these are regions which also enable a stronger development of civilization (e.g. Fjeldså 2007; Luck 2007a; Pautasso 2007). A spatial correlation of people and biodiversity is of relevance to conservation biology, as there is a pressing need to make sure that the expanding world population, activity and ecological footprint of human beings do not bring endangered species to extinction (e.g. WoodroVe 2000; Turner et al. 2004; O’Dea et al. 2006; Rondinini et al. 2006). However, less attention has been paid to the spatial correlation between people and taxa which are partly antagonistic to humanity. Here, using data collated as part of the Fauna Europaea project (Fauna Europaea 2004), we test the existence of a human population-biodiversity correlation amongst European countries for aphids (Hemiptera:Aphididae), controlling for variations in country area, latitude, plant species richness, mean annual temperature and precipitation, and spatial autocorrelation. Compared with other insect families, aphids are a small taxon (Dixon et al. 1987). Some species of aphids (ca. 250 out of the known ca. 4,400 species; Blackman and Eastop 2000) cause widespread losses to agriculture in most countries of the world by combining very high rates of reproductive increase with abilities to ingest phloem sap and transmit plant viruses (Hales et al. 1997; Powell et al. 2006; Van Emden and Harrington 2007). From an evolutionary perspective, aphids are thought to have radiated from the temperate regions of the northern hemisphere, with the tropics acting as a barrier for the dispersal of these cold-adapted organisms (Ortiz-Rivas et al. 2004). This would explain the low aphid diversity observed in the southern hemisphere (Heie 1994; von Dohlen and Moran 2000). Hence, aphids are thought to be an exception to the commonly observed negative latitudinal gradient in species richness from temperate to tropical regions (Dixon et al. 1987; Gaston 1992; Qiao and Zhang 2004) and are predicted to respond in an idiosyncratic way to future climate warming (Strathdee et al. 1995; Hodkinson 2005; Harrington et al. 2007). Given their peculiar evolutionary origin and their adaptation to cold environments, it could be that aphids make an exception to the large-scale species-people correlation. On the other hand, given that many aphid species are favoured by human activities such as agriculture, they might still reXect broadscale patterns in the distribution of human beings as do other taxa.

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Materials and methods We based our analysis on the estimates of aphid species richness for European countries provided by the Fauna Europaea project (Fauna Europaea 2004). This database is the result of a collaborative project at the European Union level. The Fauna Europaea database was coordinated by the Zoological Museum of Amsterdam (The Netherlands), generated by the Zoological Museum of Copenhagen (Denmark) and validated by the Muséum National d’Histoire Naturelle in Paris (France). In total, the project involved more than 400 taxonomic experts (Fontaine et al. 2007). Human population size (EUROSTAT, referring as a rule to 2002), area, plant species richness and geographical coordinates of the European countries/regions analysed were retrieved from publicly accessible websites. Mean annual temperature and precipitation were obtained from a global 10⬘ latitude £ 10⬘ longitude dataset of mean monthly climate variables for the period 1961–1990 (New et al. 2002). Given that a reasonable estimate of aphid species richness was available for Corsica, Sardinia and Sicily, these islands were analysed separately from mainland France and Italy. However, data from groups of islands were excluded from analyses as speciation events might have increased the number of species present. Given the unreasonably low estimate (one or a few species) of aphid species richness for Albania, Bosnia Herzegovina, Croatia, Gibraltar, Iceland, Monaco, Northern Ireland, San Marino, Serbia and Vatican City, these countries were excluded from analyses. Russia was not included in analyses as only an estimate for aphid species richness in four parts of Russia and not for the whole country was available. Overall, 35 countries/regions were retained in the dataset analysed (Table 1). Aphid species richness (Table 1) varied from 55 (Cyprus) to 700 (Ukraine). Mean aphid species richness was 404, median 371 and SD 195. Across the whole of Europe, the total number of aphid species was 1,373. Human population minimum and maximum were ca. 68,400 (Andorra) and ca. 83,250,000 (Germany). Mean human population was ca. 15,970,000, median ca. 7,620,000 and SD ca. 20,860,000. Total human population across the countries analysed was slightly less than 560 million people. Country area ranged between 468 (Andorra) and 603,700 km2 (Ukraine). Mean country area was 158,430, median 78,870 and SD 169,860 km2. Overall, the analysed countries cover slightly more than 5.5 million km2, an area approximately 60% of the United States including Alaska, 65% of Brazil, and 70% of Australia. The latitudinal range analysed spanned more than 35° from Cyprus (35 N) to Norway (which extends between 58 and 71°N). For North America, this would correspond to a transect from, e.g., Albuquerque (New Mexico) to the

Oecologia (2009) 160:839–846

841

Spp

Area

Population dh

Andorra

160

468

68

Austria

501

83,858

8,170

Belarus

265

207,600

Belgium

364

30,510

Britain

630

230,620

Bulgaria

419

Corsica

163

Cyprus Czech Republic

da

146 342

dp 234

97 6

6

10,335

50 1.3

2.6

10,275

337 12

3.5

58,093

252 2.7

1.1

110,910

7,621

69 3.8

5

8,772

264

30 19

62

55

9,250

767

83 6

7

666

78,866

10,257

130 8

6

Denmark

452

43,094

5,369

125 10

8

Estonia

227

45,226

1,416

31 5

16

Finland

429

337,030

5,183

15 1.3

8

France (mainland)

644

538,258

59,502

111 1.2

1.1

Germany

682

357,021

83,252

233 1.9

0.8

Greece

153

131,940

10,645

81 1.2

1.4

Hungary

461

93,030

10,075

Ireland

210

70,280

4,235

60 3.0

Italy (mainland)

649

251,439

51,043

203 2.6

1.3

Latvia

371

64,589

2,366

37 6

16

Lithuania

287

65,200

3,601

55 4.4

8

Macedonia

119

25,333

2,055

81 5

6

108 5

5 5

Moldova

342

33,843

4,434

131 10

8

Netherlands

356

41,526

16,318

393 9

2.2

Norway

344

324,220

4,525

14 1.1

Poland

688

312,685

38,625

124 2.2

8 1.8

Portugal

279

92,391

10,084

109 3.0

2.8

Romania

619

238,391

21,698

91 2.6

2.9

Sardinia

173

24,090

1,656

69 7

10

Sicily

382

25,701

5,017

195 15

8

Slovakia

677

48,845

5,422

111 14

12

Slovenia

174

20,273

1,933

95 9

9

Spain

603

504,782

40,077

79 1.2

1.5

Sweden

538

449,964

8,877

20 1.2

6

Switzerland

368

41,290

7,302

603,700

48,397

Ukraine

700

Europe

1373

5,544,995 558,960

177 9 80 1.2

5 1.4

Aphid species richness (n)

Country/region

(a) 1000

100

n = 35, r2 = 0.56, y = 0.45 + 0.27x, s.s.e. = 0.04, P < 0.001

10 10,000

100,000

1,000,000

10,000,000

100,000,000

Human population size (n)

(b) 1000 Aphid species richness (n)

Table 1 Aphid species richness (spp), area (km2), human population (103 inhabitants) and density (dh; n km¡2), and aphid species density (relative to 1,000 km2: da; relative to 100,000 people: dp) in Europe

100

2

n = 35, r = 0.45, y = 1.07 + 0.26x, s.s.e. = 0.04, P < 0.001 10

100

1,000

10,000

100,000

1,000,000

2

Country area (km ) Fig. 1 The relationship between aphid species richness and a human population size (n), b area (km2) for the 35 European countries/regions analysed (log-scale); s.s.e. slope standard error

species, human population size, country area, plant species richness, mean annual temperature and precipitation were log-transformed to conform to the assumptions of statistical tests. Analyses were performed in SAS 9.1. Spatial autocorrelation was controlled for using the procedure MIXED (as, e.g., in Pautasso and Parmentier 2007). Results from nonspatial (GLMs) and spatial models are qualitatively consistent, but (apart from the proportion of variance explained, which is obtained throughout from GLMs) we present only the more conservative analyses which take into account a potential spatial non-independence of data in terms of climate, survey intensity and species presence.

101 0.25 0.25

Results northern-most regions in Alaska. For Asia, a corresponding transect would start, e.g., in Osaka (Japan) and end on the Siberian coast of the Arctic Ocean. The mean and median latitude of the analysed countries was 48.3°N (SD 7°). The correlation of aphid species richness with human population size was Wrst analysed on its own with linear models. We then built general linear models (GLMs) of aphid species richness as a function of human population size controlling for variations in area, latitude and plant species richness amongst countries. Number of aphid

Aphid species richness signiWcantly increased with increasing human population (Fig. 1a) and with increasing area (Fig. 1b). This followed from the positive relationship between human population and country area [n = 35, r2 = 0.74, log10(population) = 2.27 + 0.92 log10(area), slope standard error (s.s.e.) = 0.07, P < 0.0001]. Aphid species richness also signiWcantly increased with increasing human population when controlling for variations in area [n = 35, r2 = 0.57, log10(species richness) =

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Oecologia (2009) 160:839–846

(a) 1000 Aphid species richness (n)

Aphid species richness (n)

(a) 1000

100

2

n = 35, r = 0.13, y = 1.75 + 0.015x, s.s.e. = 0.007, P = 0.04

10 30

40

50

60

100

2

n = 35, r = 0.04, y = 2.60 - 0.17x, s.s.e. = 0.18, P = 0.36

10 0.1

1.0

10.0

100.0

Mean annual temperature (C)

70

Latitude (N)

(b) 1000

100

2

n = 35, r = 0.05, y = -0.35 + 0.72x, s.s.e. = 0.18, P = 0.003

10 2.8 10

10

3.0

10

3.2

10

3.4

10

3.6

10

3.8

10

4.0

Plant species richness (n)

Aphid species richness (n)

Aphid species richness (n)

(b)

1000

100

2

n = 35, r = 0.00, y = 4.01 - 0.65x, s.s.e. = 0.41, P = 0.12

10 2.6

10

2.8

10

3.0

10

3.2

10

Mean annual precipitation (mm)

Fig. 2 The relationship between aphid species richness (log-scale) and a latitude, b plant species richness (log-scale) for the 35 European countries/regions analysed; s.s.e. slope standard error

Fig. 3 The relationship between aphid species richness and a mean annual temperature (C), b mean annual precipitation (mm) for the 35 European countries/regions analysed (log-scale); s.s.e. slope standard error

0.45 + 0.27 log10(population) + 0.00 log10(area), s.s.e. = 0.09, 0.09, P = 0.006, 0.96]. This result was conWrmed when controlling also for variations in latitude amongst countries [n = 35, r2 = 0.64, log10(species richness) = ¡0.15 + 0.31 log10(population) ¡ 0.04 log10(area) + 0.01 latitude, s.s.e. = 0.09, 0.10, 0.01, P = 0.003, 0.66, 0.13]. The last model showed that aphid species richness did not vary signiWcantly as a function of area and latitude. On its own, latitude was signiWcantly positively related to aphid species richness (Fig. 2a). This was conWrmed by a model including plant species richness as an independent variable [n = 35, r2 = 0.70, log10(species richness) = ¡1.42 + 0.37 log10(population) ¡ 0.19 log10(area) + 0.02 latitude + 0.35 log10(plant species richness), s.s.e. = 0.10, 0.13, 0.01, 0.22, P = 0.001, 0.15, 0.01, 0.11], where there was no signiWcant association of species richness with area, but a signiWcant increase of aphid species richness with increasing latitude. Remarkably, plant species richness was not signiWcantly associated with aphid species richness when controlling for population, area and latitude, whereas, on its own, plant species richness was positively correlated with aphid species richness (Fig. 2b). These results were conWrmed when replacing latitude with climatic variables (mean annual temperature and

precipitation). Aphid species richness increased signiWcantly with increasing human population size, did not vary signiWcantly with variations in country area and plant species richness, and signiWcantly declined with increasing mean annual temperature and precipitation [n = 35, r2 = 0.67, log10(species richness) = 1.88 + 0.38 log10(population) ¡ 0.19 log10(area) ¡ 0.42 log10(temperature) ¡ 0.68 log10(precipitation) + 0.30 log10(plant species richness), s.s.e. = 0.10, 0.12, 0.16, 0.28, 0.19, P = 0.001, 0.12, 0.01, 0.02, 0.12]. However, on their own, both mean annual temperature (Fig. 3a) and mean annual precipitation (Fig. 3b) were not signiWcantly associated with aphid species richness. Human population size of the countries/regions analysed was signiWcantly positively correlated with mean annual temperature in a model including country area as an explanatory variable [n = 35, r2 = 0.85, log10(population) = ¡0.57 + 1.00 log10(area) + 0.67 log10(temperature) + 0.66 log10(precipitation), s.s.e. = 0.06, 0.17, 0.41, P < 0.001 for area and temperature, p = 0.11 for precipitation]. The same model shows that mean annual precipitation was not signiWcantly associated with human population size. When controlling for variations in country area, human population size was negatively related to latitude [n = 35, r2 = 0.78,

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log10(population) = 2.99 + 1.00 log10(area) ¡ 0.025 latitude, s.s.e. = 0.06, 0.012, P < 0.001, P = 0.04].

Discussion Reported aphid species richness in European countries conforms to the positive species-people correlation reported from many recent regional studies (see “Introduction”). For insects, this pattern has been documented for butterXies in Australia and North America (Luck et al. 2004; Luck 2007b), and for ants, grasshoppers and stream macro-invertebrates in Europe (Pautasso and Fontaneto 2008; SchlickSteiner et al. 2008; Steck and Pautasso 2008), but little is known about whether or not a higher number of species of other insect families is found in regions where there are more human beings. There is a need to redress a taxonomic imbalance biased towards charismatic taxa such as plants and vertebrates (Colwell and Coddington 1994; Dobson 2005; Lonsdale et al. 2008) in relation to analyses of the species-people correlation. For aphids, we show here that there is indeed a positive species-people correlation for European countries, with more than half of the variance in aphid species numbers explained by variations in human population. Aphid species richness may positively correlate with higher human population because the latter increases with environmental productivity, which has been shown in turn to relate positively to species richness over regional scales (e.g. Kaspari et al. 2000; Whittaker and Heegard 2003; Araujo and Rahbek 2007; Ulrich et al. 2007). Other things being equal, and at a broad scale of analysis, both human beings and other species tend to increase in numbers with increasing energy availability (e.g. Luck 2007a; Pidgeon et al. 2007; Fjeldså and Burgess 2008). There is no evidence that this is an explanation for the observed aphid species-people correlation in European countries. In models controlling for variations in country area, whilst human population size increases with mean annual temperature, aphid species richness decreases with mean annual temperature. Similarly, in the same multivariate models, whereas human population size is not correlated with mean annual precipitation, aphid species richness decreases with increasing mean annual precipitation. Moreover, again when controlling for variations in country area, we observe a negative latitudinal gradient in human population size, but not in aphid species richness. For aphid species richness, there is even a positive latitudinal gradient when including in models variations in plant species richness. This runs counter to the widely documented negative latitudinal gradient of species richness (for insects, e.g. Godfray et al. 1999; Andrew and Hughes 2005; Novotny et al. 2006; Baselga 2008). This exception may be

843

the consequence of the evolutionary origin of aphids at temperate latitudes of the Northern hemisphere (Dixon et al. 1987; Kouki et al. 1994). The absence of a negative latitudinal gradient in aphid species richness raises the question of which other mechanism(s) may be behind the observed aphid species richnesspeople relationship for European countries. Is this a sampling artefact, due to a more thorough knowledge of aphid diversity in more populated countries? This is unlikely, given the quality of the Fauna Europaea project (Fontaine et al. 2007), and given the generality of the species-people relationship for many other taxa and regions. Moreover, it has been shown for birds in Britain and vascular plants in USA that such a sampling argument may not explain observed positive species-people relationships (Evans et al. 2007; Pautasso and McKinney 2007), although the available data do not allow similar analyses for aphids. Sampling eVort might actually be greater in smaller countries, but these are the countries with lower human population size, and this eVect might compensate any higher survey eVort in countries with higher human population size due to a larger presence of taxonomists. Further work is needed to assess whether the rate of new aphid species descriptions diVers in diVerent European countries. For dung beetles, Cabrero-Sanudo and Lobo (2003) argue that taxonomic activity has been biased towards northern and western Europe. But if this is the case also for aphids, it is unlikely that any such increase in taxonomic activity could be associated with a larger human population size, as many countries in northern Europe have a relatively low number of inhabitants. Whilst we know that the presence of taxonomists and sampling eVort tend to be higher in species-poor bioregions (e.g. Gaston and May 1992; Kim and Byrne 2006; Wilson et al. 2007; Hendriks and Duarte 2008), there is less knowledge on this issue at a smaller scale at the level of single countries, thus making it diYcult to assess whether numbers of currently reported aphid species in the Fauna Europaea database correlate artefactually with human population size. Another explanation could be that higher human population is concurrent with a higher number of species introductions, or a more diverse presence of habitats (Araujo 2003; Koh et al. 2006; Luck 2007a). The data available do not provide evidence that countries with higher human populations have higher aphid species richness because they have a higher number of plant species, although this would be a reasonable biological explanation (e.g. Dixon and Kindlmann 1990; MacKenzie et al. 1994; Hawkins and Porter 2003; Huang et al. 2008). It would be interesting to test whether aphid species richness is related to ant species richness, given the array of ant-aphid interactions present in European ecosystems (e.g. Stadler et al. 2003; Lewinsohn et al. 2005; Stadler and Dixon 2005). At the level of European

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countries, the Fauna Europaea data (for the countries of this analysis) show a weak correlation between aphid and ant species richness (r2 = 0.20), which disappears when controlling for country area (n = 35, r2 = 0.47, log aphidspp = 1.01 + 0.10 log antspp + 0.23 log area, s.s.e. = 0.20, 0.07, P = 0.61, 0.004), but it is possible that at a Wner resolution a signiWcant correlation may appear. An additional mechanism which could provide a link between human population size and aphid species richness may be that more populated countries have a larger area devoted to agriculture, which might in turn lead to a higher number of aphid species present in a country. For the countries for which we could Wnd an estimate of utilized agricultural area (27 out of the 35 countries for which an estimate of aphid species richness was available), there is no evidence that aphid species richness increases with increasing utilised agricultural area in a model of species richness as a function of human population size, total country area and utilised agricultural area (agricultural area is positively correlated both with human population size and with country area; our unpublished result). However, for the same subset of countries, there is evidence that the proportion of agricultural land of a country is positively associated with aphid species richness, again controlling for human population size, country area and latitude (our unpublished result). Little is known about a potential inXuence of agriculture intensity and pesticide use on regional aphid species richness. Interestingly, for the European countries analysed, there is no signiWcant association of country area with aphid species richness when controlling for human population. This is consistent with the analysis of Dixon et al. (1987), who investigated the ratio of aphid species relative to plant species in various countries of the world (from Svalbard to New Zealand) as a function of the number of plant species (incidentally, this is a relation of the form a/b f(b), as for density–area relationships; Pautasso and Weisberg 2008). They assumed in their model that the number of aphid species increased with increasing country area according to a power law with exponent 0.25, but their data do not actually show a signiWcant inXuence of area on aphid species richness (n = 23, r2 = 0.02, log spp = 1.65 + 0.17 log area, s.s.e. = 0.09, P = 0.08). This is conWrmed when controlling for absolute latitude and human population (n = 23, r2 = 0.87, log spp = ¡0.78 + 0.56 log pop ¡ 0.29 log area + 0.02 abslat, s.s.e. = 0.06, 0.07, 0.003, P < 0.001 for all factors). In such a model, species richness actually tends to decrease with increasing area, possibly as a consequence of including in the data set small islands with a high population such as Madeira and the Azores. A positive species– area relationship is believed to be a very general pattern in ecology (e.g. Lawton 1999), and has in fact been reported for various groups of insects (Connor and McCoy 1979;

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SteVan-Dewenter 2003; Drakare et al. 2006; Finlay et al. 2006, but see Hof et al. 2008), but our analyses and the data reported by Dixon et al. (1987) suggest that aphids may be an exception. More work is needed for other regions and at diVerent scales to conWrm or dismiss this exception. Table 1 shows the ratio of aphid species richness and country area. This is a way to standardise species richness to a common unit of area (in this case, 1,000 km2), i.e. a measure of species density. However, given that the aphid species–area relationship has a slope shallower than 1, smaller countries have a higher aphid species density than larger ones. This pattern is similar to the negative density– area relationship reported for abundances, i.e. number of individuals (e.g. Pautasso and Weisberg 2008). As a consequence, these aphid species densities can only be meaningfully compared amongst countries with similar area. For example, Britain and Romania have a similar number of aphid species per unit area (2.7 vs 2.6 species per 1,000 km2), and this is not an artefact of diVering areas, as the two countries have a similar area and a similar total number of aphid species (Table 1). Conversely, Belgium and Switzerland have a similar total number of aphid species, but the species density is slightly higher in Belgium (12 vs 9 species per 1,000 km2) as this country is slightly smaller than Switzerland. Table 1 also shows the ratio of aphid species and human population, i.e. a species density referred to 100,000 people (this number of people results in a human density of 100 inhabitant per km2 from the two units used to calculate the aphid species density relative to area and to people, and was chosen as this average human density is also obtained for the whole of the 35 countries analysed). Also in this case, smaller countries tend to have a higher aphid species density relative to population, as small countries have a lower population and as the aphid species-people relationship is less than proportionate. As Britain is more densely populated than Romania, it has a lower aphid species density relative to population (ca. 1 vs 3 species per 100,000 people). This is also the case for Belgium and Switzerland (3.5 vs 5 species per 100,000 people), because Belgium is more densely populated than Switzerland. All these densities are much higher than the average value for all the countries analysed (0.25 aphid species per 1,000 km2 and per 100,000 people). Given the detrimental local eVects of human activities, a large-scale co-existence of species and people can easily turn into a conservation challenge. In many cases, this problem is worsened by the location of human settlements in sensitive ecosystems, such as, e.g., lake shores (Gonzalez-Abraham et al. 2007). More populated European countries have a lower aphid species density than less populated ones, but they still have a higher absolute number of aphid species. Given that not all aphid species are detrimental to

Oecologia (2009) 160:839–846

humanity, and given that many aphid species have an important role in natural ecosystems, where, for example, they provide a signiWcant Xow of energy from forest canopies to the soil (e.g. Stadler et al. 2001; Michalzik and Stadler 2005), it is important that both small and large countries (1) improve the conservation of their aphid biodiversity, (2) make the public more aware of it, and (3) increase our knowledge about the distribution and abundance of diVerent aphid species, functional groups and endemic areas. Acknowledgments Many thanks to the many people involved in the compilation of the Fauna Europaea database, to I. Currado, D. Fontaneto, K. Gaston, O. Holdenrieder, M. Jeger, M. McKinney, A. Rodrigues, B. Schlick-Steiner, C. Steck, F. Steiner and P. Weisberg for insights and discussions, to H. Kreft and A. Romanowicz for providing data, and to K. West and two anonymous reviewers for helpful comments on a previous draft.

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