Journal of Applied Ecology

doi: 10.1111/j.1365-2664.2012.02120.x

Landscape simplication and altitude affect biodiversity, herbivory and Andean potato yield
Katja Poveda1*, Eliana Mart nez2, Monica F. Kersch-Becker3, Maria A. Bonilla2 and Teja Tscharntke1
ttingen, Agroecology, Department of Crop Sciences, Georg-August University, Griesbachstrae 6, 37077 Go Germany, and Department of Entomology, Cornell University, 4142 Comstock Hall, Ithaca, NY 14853. USA; 2Biology , Department, Universidad Nacional de Colombia, Bogota Colombia; and 3Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY, USA
1

Summary 1. The simplication of agricultural landscapes through the increase in cropped area has caused the loss of habitats for many species that full important ecosystem services such as pest control and production. Evidence for detrimental eects on ecosystem services is scarce, particularly in tropical regions. 2. We studied the eect of the percentage of cropped land in the landscape and altitude in tropical agro-ecosystems in relation to crop pest regulation and yield. In the Colombian Andes, we established potato Solanum tuberosum plots along gradients of altitude and increasing proportion of cropped area to assess the eects on herbivores, their natural enemies, potato production and overall biodiversity. 3. Increasing altitude and percentage cropped land reduced the richness and abundance of herbivores and their natural enemies, except for the specialist Guatemalan potato moth Tecia solanivora, which showed the opposite response. 4. Potato yield was negatively aected by the presence of the Guatemalan potato moth, which increased in density as the percentage of cropped land and altitude increased. Other herbivores and natural enemies did not aect yield. 5. Synthesis and applications. Tropical landscapes at lower altitude or with smaller areas of cropped land suered less from the presence of the potato moth, which had a negative eect on yield. Our results suggest that conservation of natural habitats like the endangered Andean ecosystems would benet farmers through ecosystem services such as reduced pest damage, higher yield and increased functional biodiversity. Key-words: altitudinal gradient, arthropod richness, crop production, land use intensication, landscape complexity

Introduction
Agro-ecosystems have faced great changes in the last decades owing to increased conversion of natural habitat to cropped lands and through the intensication of agriculture, both of which are drivers of biodiversity loss (Krebs et al. 1999; Sala et al. 2000; Tilman et al. 2001). Changes may occur at dierent spatial scales including increased agrochemical inputs at a local scale and a reduction in landscape complexity at a wider
*Correspondence author: Department of Entomology, Cornell University, 4142 Comstock Hall, Ithaca, New York 14853. USA. E-mail: kap235@cornell.edu These authors contributed equally to this work.

scale as more land is cultivated (Tscharntke et al. 2005). As agro-ecosystems rely heavily on ecosystem services such as pollination and natural pest control, landscape simplication and the loss of functionally important biodiversity are of major global concern (United Nations 2005). For example, natural pest control has been positively associated with the diversity of natural enemies (Wilby & Thomas 2002; Gurr, Wratten & Luna 2003; Snyder & Ives 2003). However, the role of biodiversity in maintaining natural pest control, decreasing herbivore pressure and increasing productivity is less well understood (but see Cardinale et al. 2003; Ostman, Ekbom & Bengtsson 2003; Finke & Denno 2004). At a landscape scale, structurally complex landscapes with small areas of cropped land interspersed between natural habitat have been found to

2012 The Authors. Journal of Applied Ecology 2012 British Ecological Society

2 K. Poveda et al. increase natural enemy populations and reduce pest pressure on crops in 74% and 45% of cases, respectively (based on a review by Bianchi, Booij & Tscharntke 2006). Based on the resource concentration hypothesis, this pattern would be expected, given that a higher percentage of cropped land could be of benet to herbivores feeding on crops (Root 1973). However, none of the studies reviewed the eect on crop yield (Bianchi, Booij & Tscharntke 2006), and we are not aware of any more recent investigations on landscape complexity and the eects on crop productivity. Although there is evidence that landscape structure can inuence crop damage (Thies & Tscharntke 1999), it remains unclear whether the eect on natural enemies and pests cascades down to crop yield. Apart from the study by Parsa, Canto & Rosenheim (2011), we are not aware of any other study carried out in the highly diverse tropical ecosystems; most studies examining the relationship between landscape complexity and diversity have been performed in less diverse temperate regions. Although temperate regions undergone landscape transformation over long periods of time, tropical ecosystems have faced this change increasingly in the last decades (Sodhi, Brook & Bradshaw 2007). The relationship between landscape complexity and ecosystem functions such as natural pest control and productivity in those highly biodiverse ecosystems could provide some insights into the functional importance of biodiversity in changing tropical environments. Biodiversity is aected by natural factors as well as by human activities. Environmental gradients such as altitude are also known to aect biodiversity and may interact with anthropogenic forces that shape ecosystem function. Higher altitudes are associated with a decline in species richness in many groups of animals, including insects (Lawton, Macgarvin & Heads 1987; Hodkinson 2005). However, in the Andes, the evidence for a reduction in pest pressure with altitude is not based on eld data, but on observations of the preference shown by farmers to grow crops at higher elevations to avoid the negative eects of herbivores and pathogens (Montaldo 1984). The tendency to convert high-elevation natural areas to cropped land has led to widespread clearance of endangered ecosystems such as the paramos in Colombia, where 60% of the total area has been converted to agricultural use such as cattle farming and potato elds (Monasterio, Smith & Molinillo 2006; Rangel 2006). In the higher Colombian Andes, potato Solanum tuberosum, L. is the most important crop. Approximately 170 000 ha distributed in 250 municipalities between 2000 and 3500 m are planted with potato, employing directly more than 110 000 families (Osorio, Espitia & Luque 2001; Lopez 1980). In this study, we focused on the eect of percentage cropped land and altitude on functional arthropod diversity, including herbivores and their natural enemies, in Andean potato elds. We tested the direct and indirect eects of landscape variables, herbivores and natural enemies on potato yield. We proposed three alternative hypotheses for the mechanism behind this pattern: (i) Altitude and the percentage of cropped land in a 1-km-radius landscape area are directly related to potato yield; (ii) Following the natural enemies hypothesis, both increased cropped land and altitude negatively aect the diversity and abundance of natural enemies, releasing herbivores from topdown predation pressures and decreasing yield; (ii) Following the resource concentration hypothesis, increased cropped land positively aects herbivore abundance and potato herbivory, which has a negative impact on potato tuber yield.

Materials and methods

STUDY AREA AND PLANTING

We planted a total of 17 potato S. tuberosum cv Pastusa Suprema plots in the Cundinamarca Department of Colombia (Fig. S1). We established six 20 12 m plots between July and December 2006 and 11 plots between March and July 2007. The plots were situated along a gradient from landscapes with intensive land use (94% agricultural area) to more complex landscapes with a high percentage of natural habitats (37% agricultural area). Plots were also established along an altitudinal gradient between 2584 and 3227 m above sea level, unrelated to the landscape complexity gradient (r = 034, P = 017, n = 17). Distance between plots ranged from 12 to 661 km with a mean distance (SE) of 303 16 km. Each plot consisted of 20 furrows, 12 m in length and separated by 1 m. Seed tubers were planted every 35 cm. Potato seed tubers were planted between June and July 2006 and in March 2007. Plants were fertilized twice. During establishment, they were fertilized with N : P : K 12 : 34 : 12 (Ecofertil S.A., Bogota, Colombia). At the time of ridging (also known as hilling) 8 weeks after establishment, they were fertilized with N : P : K 10 : 10 : 10 (Ecofertil S.A., Bogota, Colombia). Seedlings of potato plants are normally attacked by ea beetles (Coleoptera: Chrysomelidae) that can cause complete defoliation and death of the plants in the rst weeks after emergence (Poveda K. & E. Martinez personal observation). To control for this initial stages of foliar herbivory but without compromising the survivorship of the organisms associated with the potato crops, we sprayed the plants weekly with a commercial garlic pepper extract (Agrisan, Cundinamarca, Colombia; 120 mL per 20 L) for the rst 8 weeks and before the plant started producing tubers. We favoured garlicpepper extract over any commercial insecticide, as its main way of action is insect repellence and not toxicity. Our previous work has shown that spraying garlicpepper extract does not aect the predator community in comparison with unsprayed plots, while insecticide treatments reduce predator and overall arthropod abundance (Gomez-Jimenez & Poveda 2009). Insects were rst sampled 4 weeks after the last garlicpepper spray. We controlled late blight Phytophthora infestans (Mont.) de Bary through biweekly spraying of Dithane M-45 (Dow Agrosciences de Colombia, Bogota, Colombia; active compound: Mancozeb 80%), alternated with Fitoraz WP 76 [Bayer CropScience S.A. Bogota, Colombia; active compound: Propineb (70%) and Cymoxanil (6%)].
LANDSCAPE DATA

At the landscape scale, we mapped dierent land use types (potato, pasture and other crops) and dierent natural habitats (exotic forest, native forest and hedgerows) through eld visits and inspection of aerial photographs and ocial topographic maps [Instituto Geograco Agustin Codazzi (IGAC) scale 1 : 10 000 for aerial photographs and 1 : 5000 for cartographic material] using the program gis arcview 3.2 (ESRI 1999). We used the percentage cropped land (crops and heavily grazed pastures dominated by the tropical grass species Pennisetum clandestinum Hoechst Ex Chiov.) in a circular area of 1 km radius surrounding each study site as a measure of landscape

2012 The Authors. Journal of Applied Ecology 2012 British Ecological Society, Journal of Applied Ecology

Landscape aects potato pests and yield 3

simplicity (see Tscharntke et al. 2005). This measure was correlated with the Shannon habitat-type diversity (r = )087 P < 00001 n = 17: calculated from the six types of habitats measured) and marginally correlated with the percentage area of potato elds (r = 046, P = 0058, n = 17). We chose to measure percentage cropped land over the percentage area of potato elds because potatoes are usually rotated with pastures and potato pests that nish their development in the soil can easily move from recent pastures to potato elds. To correct for the eect of the relief on the area estimation, we topographically corrected all aerial photographs through the program erdas imagine (Leica Geosystems 2001) using 20 control points. There was a gradient in land use intensity from 37% to 94% cropped area with a mean SE of 74 176% across the 17 plots (for more details see Appendix S1).
SOIL FACTORS POTATO YIELD

To quantify potato yield, we harvested 20 plants from the centre of each plot, when plants began to senesce. We determined the number and weight of undamaged (marketable) and damaged (unmarketable) tubers per plant by visual inspection after cutting open each tuber. Damage was mainly caused by T. solanivora, larvae, although we found evidence of damage by two other pests, Premnotrypes vorax Hustache (Coleoptera: Curculionidae) and Naupactus sp (Coleoptera: Curculionidae). To estimate pest pressure, we calculated the percentage of tubers damaged by dividing the number of damaged tubers by the total number of tubers per plant.
DATA ANALYSIS

We determined local soil chemistry in each eld by taking ve soil cores of 10 cm depth during the potato harvesting period (December 2006 and August 2007). Samples were analysed for percentage nitrogen and organic carbon by the soil laboratory of the Agronomy Faculty of the Universidad Nacional de Colombia, Bogota.
ARTHROPOD SAMPLING

We caught epigeic fauna using four pitfall traps (7 cm in diameter and 10 cm height) arranged at the four corners of a 8-m square. We opened the traps for two 1-week sampling periods during potato owering and 2 weeks before harvesting. Sampling dates were chosen based on the previously reported increased attraction to herbivores of the potato plants at the moment of tuberization (Nino 2004), which starts with the owering period. The trapping uid was an alcohol: water dilution (2 : 1) with some added detergent to break surface water tension. Arthropods were separated by order and identied to family. We sampled ying and leaf-dwelling arthropods between two central furrows on the days that pitfall traps were opened and emptied. We took sweep-net samples the day pitfall traps were opened and the day those traps were collected. We summed the four pitfall trap and four sweep-net subsamples to obtain the total number of arthropods for each of the sampling dates. According to previous reports that emphasize the importance of assigning arthropods to dierent functional groups (i.e. Clough, Kruess & Tscharntke 2007b; Tscharntke et al. 2007), we divided the arthropod families found into predators, parasitoids, herbivores, saprophages and omnivores (based on what is reported by Carrejo & Gonzalez 1992; Triplehorn & Johnson 2005; Wolf 2006). Organisms that could not clearly be assigned to a trophic group were included in the analysis of total number of families and total abundance, but not the analysis of the dierent functional groups. All analyses were conducted at a family level because of the lack of identication keys to identify insects to a more precise level. The Guatemalan potato moth Tecia solanivora Povolny (Lepidoptera: Gelechiidae) is one of the main potato insect pests in Latin America (OEPP & EPPO 2005), so we estimated its presence in 2007 by setting up pheromone traps in the centre of each plot. These traps are eective up to a distance of 30 m and capture only males; this underestimates the actual population size (Nino 2004) but is adequate for performing comparisons between plots. We left traps in the eld for 7 days at the end of the cultivation period (August 2007), when the population should be at its highest peak. Data are reported as the number of individuals captured per day.

Adequacy of sampling eort was validated by calculating species accumulation curves and the Incidence-based Coverage Estimator (ICE) using estimates, Version 8.2.0 (Colwell 2006) with 500 randomizations. The degree of saturation at a family level was indicated by the percentage of observed arthropod families relative to the estimated family richness and was 831% for all samples. These results suggest that sample size and sampling eort were sucient. To evaluate the eects of cropped area and altitude on arthropod abundance and richness at a family level, as well as potato yield, we used generalized linear models with a stepwise backward simplication to comply with the principle of parsimony (Crawley 2003). The analysis was performed with the program statistica (Statsoft 2003), and all variables not signicant at P < 005 were excluded from the model. The percentage of cropped land was used as a measure of landscape simplicity, and altitude was included as a measure of the altitudinal gradient. Year of sampling was used as a random factor, and soil nitrogen and soil organic matter were included as covariates in the analysis. To adjust to normal distribution of residuals and heteroscedasticity, we ln-transformed the variables herbivore and parasitoid family richness, total number of arthropods, herbivores, predators, parasitoids and T. solanivora. We plotted the standardized residuals and tted to a normal curve to determine adjustment to normal distribution. The inspection of plots showing standardized residuals against tted values showed us which data were more homogeneous in variance (Crawley 2003). The percentage of potatoes that were damaged was arcsin square-root-transformed. Model assumptions about spatially independent and identically distributed residuals were checked by Mantel tests and diagnostic plots in R (The R project for statistical computing, version 2.10, http://www.rproject.org/). No spatial autocorrelation was found for any models reported in Table 1 ()031 < r < 018; P > 014). Given that we had data on the Guatemalan potato moth abundance for 2007 but not for 2006, we investigated the eect of potato moth abundance on percentage tubers damaged and on marketable tuber weight through Spearmans correlations. We also analysed how altitude, percentage cropped area and previous plot use aected potato moth abundance through a generalized linear model (glm) with a stepwise backward simplication. These analyses were all done with the program statistica (Statsoft 2003).
DIRECT AND INDIRECT EFFECTS OF LANDSCAPE AND ARTHROPOD VARIABLES ON POTATO YIELD

To investigate whether percentage cropped land or altitude aected nal marketable potato yield and whether it was a direct or an indirect eect driven through herbivores or natural enemies, we used path analysis to test our hypotheses. In our path model, we included

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4 K. Poveda et al.
Table 1. Results of generalized linear models with a stepwise backward simplication of the percentage cropped land in a 1 km radius around the plot, altitude and year of study in relation to the family richness and abundance of arthropod fauna associated with potatoes Solanum tuberosum and potato production Response variable Arthropod family richness Percentage cropped land F1,14 = 805 P = 0013 F1,15 = 883 P = 0009 ns Altitude of plot F1,14 = 2434 P < 0001 ns Year of study ns Model t R2 = 077 F2,14 = 2398 P < 0001 R2 = 032 F1,15 = 883 P = 0009 R2 = 048 F2,14 = 867 P = 0004 R2 = 067 F2,14 = 1782 P < 0001 R2 = 058 F1,15 = 2301 P < 0001 R2 = 056 F2,14 = 111 P = 0001 R2 = 034 F1,15 = 941 P = 0008 R2 = 049 F1,15 = 1652 P = 0001 R2 = 059 F2,14 = 1268 P < 0001 R2 = 021 F1,15 = 537 P = 003 R2 = 020 F1,15 = 506 P = 0039

Herbivore family richness

ns

Predator family richness

F1,14 = 1067 P = 0006 F1,14 = 137 P = 0002 F1,15 = 2301 P < 0001 F1,14 = 786 P = 0014 F1,15 = 941 P = 0008 F1,15 = 1652 P = 0001 F1,14 = 795 P = 0013 ns

F1,14 = 496 P = 0042 ns

Parasitoid family richness (log)

F1,14 = 96 P = 0008 ns

Arthropod abundance (log)

ns

Herbivore abundance (log)

F1,14 = 66 P = 0022 ns

ns

Predator abundance

ns

Parasitoid abundance (log)

ns

ns

Pests abundance (log)

F1,14 = 859 P = 001 ns

ns

% damaged tubers (arcsin sqrt)

F1,15 = 536 P = 0035 F1,15 = 506 P = 0039

Weight undamaged potatoes (log)

ns

ns

Statistics for each signicant variable (ns, not signicant) and the t of the whole model for each variable are presented. Arthropod fauna was divided into three major functional groups: herbivores, predators and parasitoids. Total arthropod fauna included saprophages and omnivores.

percentage cropped land, as a measure of landscape simplication, altitude, natural enemies (richness and abundance), herbivores (richness and abundance) excluding the potato moth, as well as T. solanivora abundance. Using our data on the abundance of the potato moth in 2007, we plotted the regression line between the percentage tubers damaged (arcsin square-root-transformed for a better t) and T. solanivora abundance in 2007 (T. solanivora abundance = )958 (% tubers damaged) +1239; R2 = 043, F19 = 689, P = 0027) from which we estimated our predicted T. solanivora abundance. We used percentage of tubers damaged as a proxy for T. solanivora abundance in 2006. Although the percentage of tubers damaged in 2006 was much lower than in 2007, the data points were still within the range of data used to calculate the regression between percentage of tubers damaged and T. solanivora abundance in 2007. To ensure that the damage on potato tubers reected T. solanivora abundance alone and not the abundance of other pests in general, we correlated the abundance of potato pests with the percentage of tubers damaged and with potato yield. In both cases, we found no correlation between the variables (Spearmans correlations: r = )029, P = 025, n = 17: r = 012, P = 063, n = 17). Although there is some information about the

natural enemies of T. solanivora (Lopez-Avila & Espitia-Malagon 2000) including both parasitoids and predators, we only made identications to the family level. In addition, our results show that predators and parasitoids are similarly aected by percentage cropped land and altitude. Therefore, we decided to pool data on predators and parasitoids together in a natural enemy category, reducing the number of paths in our model and increasing our statistical power. Herbivore abundance, natural enemy abundance and richness as well as potato yield were ln-transformed prior to the path analysis to meet parametric assumptions. The path analysis was calculated in the program systat (Systat Software Inc, Chicago, IL, USA 2004).

Results
EFFECTS ON ARTHROPODS

A total of 25 892 individuals from 16 orders and 113 families (See Appendix S2) were captured. Most of the arthropods were saprophages (641%), followed by herbivores (248%), predators (61%) and parasitoids (44%). We sampled a total

2012 The Authors. Journal of Applied Ecology 2012 British Ecological Society, Journal of Applied Ecology

Landscape aects potato pests and yield 5 of 9270 herbivores and their natural enemies, classied into 13 orders and 69 families. Both altitude and percentage cropped land within a 1 km radius around the plot had a negative relationship with both arthropod and parasitoid family richness and nearly all functional groups (Table 1, Fig. 1). Only predators did not respond to changes in the percentage cropped land, while herbivore family richness did not vary along the altitudinal gradient (Table 1, Fig. 1). The abundance of all arthropod groups was negatively correlated with altitude, but only herbivores were negatively aected by an increasing percentage of cropped land (Table 1, Fig. 2).
POTATO YIELD

Percentage cropped land and altitude had no direct eect on potato production, but there was an eect of year on the per-

Total arthropod family richness

65 60 55 50 45 40 35 30 30

Total arthropod family richness

(a)

65 60 55 50 45 40 35 30

(b)

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2006 2007

Predator family richness

% Cropped land Parasitoid family richness Parasitoid family richness

20 16 12 8

Predator family richness

Altitude (m)
20 16 12 8

(g)

(h)

Fig. 1. Family richness of total arthropods (a & b), herbivores (c & d), predators (e & f) and parasitoids (g & h) collected on potato elds in the Colombian Andes in relation to the cropped land area in a circular area of 1 km radius around the plot (a, c, e & g) and the altitude at the site of each plot (b, d, f & h).

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6 K. Poveda et al.
Total arthropod abundance Total arthropod abundance
(a) (b)
2981

2981

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403

403

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Predator abudance

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Fig. 2. Abundance of total arthropods (a & b), herbivores (c & d), predators (e & f) and parasitoids (g & h) collected in potato elds in the Colombian Andes in relation to the percentage of cropped land in a circular area of 1 km radius around the plot (a, c, e & g) and the altitude at the site of each plot (b, d, f & h).

centage of potatoes damaged and the weight of marketable potatoes (Table 1). In 2007, the mean (SE) percentage of potato tubers damaged (mainly by the Guatemalan potato moth) was 50% (8%), whereas in 2006, it was around 16% (11%). At the same time, the mean (SE) marketable potato yield in 2006 was 1324 (215) g compared to 337 (159) g in 2007. The damage caused to the potato tubers was mainly inicted by the Guatemalan potato moth Tecia solanivora. Data on T. solanivora abundance for 2007 showed a strong relationship between the abundance of male moths in the region and the damage to tubers (r = 062; P = 0039, Fig. 3a) and a nega-

tive relation to marketable potato yield (ln-transformed; r = )070; P = 0015, Fig. 3b). Abundance of T. solanivora was positively aected by the percentage agricultural area (Fig. 4a) and by altitude (Fig. 4b) and was higher when the plot was previously cultivated with potatoes compared with plots previously put to a dierent use (Table 2, Fig. 4c). Altitude and percentage cropped land were not correlated with each other (r = 045, P = 016). The path analysis of how dierent variables aected potato yield showed that it was strongly reduced as the abundance of T. solanivora increased (Fig. 5). The t of the model did not dier between the two models (richness

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Landscape aects potato pests and yield 7

(a) (a)
10

% Tubers damaged/plant

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Tecia solanivora abundance

Fig. 3. Relationship between the abundance of Tecia solanivora and the percentage of tubers damaged (a) and the yield (weight of marketable potato tubers) (b) for 2007 data.
10

Altitude (m)
(c)

Tecia solanivora abundance

and abundance) (RMSEArichness < 0001, P = 0800; RMSEAabundance < 0001, P = 0722). Altitude and per cent cropped land did not aect potato yield directly, but both variables indirectly decreased production by increasing the incidence of potato moth. Higher densities of T. solanivora were recorded at higher altitudes and in landscapes with higher percentages of cropped land. At higher altitudes, the abundance and species richness of natural enemies decreased, but they were not aected by the percentage of cropped land. Landscapes with a higher percentage of cropped land harboured lower abundance and lower species richness of herbivorous insects (excluding T. solanivora), but the abundance of these herbivores did not alter potato yield. Both path diagrams showed a positive relationship between the abundance and species richness of natural enemies and the incidence of T. solanivora, but natural enemies did not aect the abundance and richness of herbivores.

01

Other

Potato

Previous land use

Fig. 4. Mean number of Tecia solanivora moths captured per day in relation (a) to the percentage of cropped land in a circular area of 1 km radius around the plot, (b) to the altitude and (c) to the previous use of the plots (ve plots previously planted with potatoes; six plots previously pastures).

Discussion
Both the percentage of cropped land in the landscape and altitude directly inuenced the abundance of herbivores and their natural enemies. Our results showed that a decline in diversity at a landscape scale can increase pest abundance and consequently can have a negative eect on crop production. Potato yield decreased with increased potato moth abundance. Tecia solanivora populations increased with percentage cropped land, suggesting that low-diversity, simplied landscapes

encouraged the presence of the moth, while natural enemies did not reduce its abundance. This nding supports the resource concentration hypothesis over the natural enemies hypothesis as the most plausible mechanism for the variation found in T. solanivora abundance. These results are the rst eld data to support the commonly claimed notion that high-diversity crop habitats are more resilient to pest species outbreaks and this potentially can have an indirect positive inuence on crop yield. The long-term sustainability of ecosystems and the services they generate depend on the conservation of biodiversity at scales beyond the local scale (Bengtsson et al. 2003; Loreau, Mouquet & Holt 2003). Landscapes with a low incidence of cropped lands (with a large arthropod species pool) should

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8 K. Poveda et al.
Table 2. Eects of the percentage of cropped land in a 1 km radius around the plot, altitude and previous potato cover on the abundance of the potato moth Tecia solanivora Variable assessed Log (Tecia solanivora abundance +1) Percentage cropped land F1,7 = 233 P = 0002 Altitude of plot F1,7 = 2499 P < 0001 Previous cover F1,7 = 2438 P < 0001 Model t R2 = 097 F3,7 = 1353 P < 0001

F, P and R2 values as well as the degrees of freedom for each response variables are reported after performing a generalized linear model.

(a)
% Cropped land
0433

0034
*

0
04

Herbivores richness
16 1
00 03

Natural enemies richness 0711*

**

Yield

12

75

41

3*

0696
Altitude

T. solanivora abundance

0176

(b)
% Cropped land
0
0409

0066
**

Herbivores abundance
1 33

0
0352

19

Natural enemies abundance 0631*

*

Yield

0 24 4 0 7 21 ** *

7 0

83

**

0625
Altitude

T. solanivora abundance

0275

Fig. 5. Path diagram for the model of the eect of percentage of cropped land in a circular area of 1 km radius around the plot, altitude, natural enemies, herbivores and T. solanivora abundance on potato yield. Path diagram including a) species richness for natural enemy families and herbivores and b) the abundance of natural enemies and herbivores. Solid lines denote signicant eects, and dashed lines denote non-signicant eects. Width of each line is proportional to the strength of the relationship. *P < 005, **P < 001, ***P < 0001.

support a more diverse and abundant natural enemy community thus maximizing natural pest control and crop productivity (Tscharntke et al. 2007). Our data show that as the percentage of cropped land in the landscape surrounding the

plot increased, there was a negative eect on parasitoid richness. Landscape simplication (high percentage of cropped land and low habitat-type diversity) is a result of agricultural intensication causing loss of the natural habitats that provide resources for the arthropod fauna (Kruess 2003; Schmidt & Tscharntke 2005; Tscharntke et al. 2005). Parasitoid longevity and fecundity, for example, are dependent on the availability of food resources like pollen and nectar as well as their hosts in the environment (Baggen & Gurr 1998; Tylianakis, Didham & Wratten 2004; Wackers 2004). In complex habitats, these types of resources are normally found adjacent to the main crops in non-cropped vegetation where they support benecial organisms (Freeman Long et al. 1998). Altitude had a negative eect on the overall arthropod family richness. The linear reduction or hump-shaped distribution of arthropod species richness along an altitudinal gradient has been reported previously, and several hypotheses have been proposed to explain this phenomenon (reviewed by Hodkinson 2005). Lower plant diversity at higher altitudes can limit the abundance and species richness of herbivores and therefore also the abundance of natural enemies (Hodkinson 2005). Moreover, a series of abiotic factors such as lower temperatures and increased UV-B radiation can directly or indirectly aect insect richness and abundance (Coulson & Whittaker 1978; Ro 1980; McCloud & Berenbaum 1994; Bird & Hodkinson 1999). According to the resource concentration hypothesis (Root 1973), we would expect that plots surrounded by simple landscapes (higher percentage cropped land) would have high abundance of herbivores. However, in temperate regions, it has been reported that simplied landscapes have a lower abundance of herbivores (Roschewitz et al. 2005; Thies, Roschewitz & Tscharntke 2005; Clough, Kruess & Tscharntke 2007a; Rand & Tscharntke 2007). Similarly, in our study, we found that a higher percentage of cropped land reduced the abundance and richness of herbivores. This may be due to high levels of disturbance in agro-ecosystems and increased use of insecticides. The potato moth is a specialist potato pest whose larvae can only feed on potato tubers (OEPP & EPPO 2005), yet it had a dierent impact on yield in successive years. Damage caused to the potatoes by the potato moth was 16% in 2006 and 50% in 2007. In 2007, we found more moths in plots surrounded by a high percentage of cropped land, suggesting that landscape simplication had a positive eect on potato moth abundance. The results from the path analysis showed that the abundance

0234

**
04 19 *

49 *

2012 The Authors. Journal of Applied Ecology 2012 British Ecological Society, Journal of Applied Ecology

Landscape aects potato pests and yield 9 of the potato moth is more strongly aected by bottom-up eects providing support for the resource concentration hypothesis, as opposed to top-down eects where natural enemies would be controlling the moth. Simpler landscapes contain a higher percentage of potato crops, which makes the landscape more attractive for specialized pests and provide more food resources for larger pest population. Moreover, the abundance of traditional, relatively open potato shelters, where potato farmers store the tubers, is higher in areas with more intensive potato production. Potato shelters oer optimal conditions for moth development (Keasar et al. 2005) and could be the main source of potato moth infestation in the eld. Although our regression data suggest that the potato moths encounter fewer natural enemies in landscapes with higher percentage of cropped land, the path analysis illustrates that the natural enemies recorded in this study are not controlling T. solanivora abundance, thus providing no support for the natural enemy hypothesis. The adaptation of T. solanivora to higher altitudes parallels the adaptation of its host plant, the potato, to high altitudes in the Andes (Lopez 1980). However, it has been shown that temperature can limit the development of T. solanivora under laboratory as well as under eld conditions (Dangles et al. 2008). Along an altitudinal gradient from 2550 to 3650 m in Ecuador, lower temperatures at higher altitudes reduced the abundance of T. solanivora (Dangles et al. 2008). This eect was not observed in our study probably because our altitudinal gradient reached a maximum of 3227 m rather than the 3650 m recorded in Dangles et al. (2008). This suggests that the abundance of T. solanivora may peak at mid-elevations and that abiotic factors such as temperature could constrain its upper distribution. Finally, when analysing the eects of altitude and percentage of cropped land on potato tuber damage and marketable yield, we did not detect a general eect of either factor on productivity, yet we found a clear dierence between study years. The percentage of tubers damaged diered between the 2 years, indicating dierences in abundance of the potato moth. In 2007, we found a strong correlation between the percentage of cropped land and the abundance of potato moths, as well as between the abundance of potato moths and the percentage of tubers damaged at harvest and the nal marketable yield of the potato plants. Nevertheless, there was no signicant direct eect of the percentage of cropped land on yield. Instead, our analysis showed a pest-mediated reduction in potato yield as the percentage of cropped land and altitude increased. In conclusion, we found the landscape context and altitude to be important in shaping the arthropod community richness and abundance. Increased percentage of cropped land and altitude led to a decrease in arthropod species richness and abundance, and the eect was similar in all feeding guilds (except for T. solanivora), contrary to what would be expected by functional-group-specic responses. We provide the rst eld data showing how a decline in tropical landscape diversity owing to increased percentage of cropped land is related to an increased pest abundance, which in turn has an eect on crop production. Tecia solanivora is the main potato pest causing high tuber damage and reducing crop productivity. We suggest that the conservation of natural habitats like the endangered high-altitude Andean ecosystems is not only important to conserve biodiversity per se but also to conserve the ecosystem functions provided by natural biodiversity.

Acknowledgements
We thank A. Ramirez, C. Nustez, E. Torrado, E.A. Pedraza, P.A. Diaz, J. Jacome, Y. Ospina, P. Gonzalez, D. Campos, H. Aguirre, O. Dix, J.M. Vargas and the 17 farmers who collaborated with the project for assistance with eld or laboratory work and advice. We specially thank the Laboratorio de Entomolog a and the Grupo de Investigacion en Papa of the Agronomy Faculty Universidad Nacional de Colombia for logistical support. We thank S. Mc Art, D. Gabriel, S. Parsa, J. Cepeda and O. Dangles for their helpful comments on the manuscript. This research was funded by the German Research Foundation (DFG) through grants PO 1215_21 and PO 1215_31 to K. P.

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Supporting Information
Additional Supporting Information may be found in the online version of this article: Fig. S1. Overview of the location of all the potato plots used in the years 2006 and 2007. Appendix S1. Description of the variables of the 17 potato plots established in the year 2006 and 2007. Appendix S2. Arthropod community composition associated with potatoes in 17 potato plots in the Cundinamarca Region, Colombia. As a service to our authors and readers, this journal provides supporting information supplied by the authors. Such materials may be re-organized for online delivery, but are not copy-edited or typeset. Technical support issues arising from supporting information (other than missing les) should be addressed to the authors.

2012 The Authors. Journal of Applied Ecology 2012 British Ecological Society, Journal of Applied Ecology