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Journal of Forestry Research ISSN 1007-662X J. For. Res.DOI 10.1007/s11676-015-0043-y

Natural enemies depend on remnanthabitat size in agricultural landscapes

Mainara Xavier Jordani, Érica Hasui &Vinícius Xavier da Silva

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ORIGINAL PAPER

Natural enemies depend on remnant habitat size in agriculturallandscapes

Mainara Xavier Jordani • Erica Hasui •

Vinıcius Xavier da Silva

Received: 13 April 2013 / Accepted: 21 June 2013

� Northeast Forestry University and Springer-Verlag Berlin Heidelberg 2015

Abstract In recent decades, the consequences of habitat

fragmentation have been of growing concern, because it is

particularly important to understand how fragmentation

may affect biodiversity, an ecological service. We tested

two hypotheses: (1) that natural fragment size in agricul-

tural landscapes indirectly affects the herbivore through

effects on natural predator populations; and (2) predator

activity into the crop reduces along the distance from the

natural fragment edge. From 2008 and 2009, we conducted

our study in seven forest remnants and in surrounding

coffee plantations (fragments ranged from 6 to 105 ha,

mean 49.28 ± 36.60 ha) in Southern Minas Gerais, Brazil.

Birds were sampled by point counts, and insect predation

was evaluated by using an artificial insect model (Koh and

Menge 2006). Our results suggest that although there were

many potential predators (e.g., wasps, ants, birds, and

mammals), birds were the most important taxon unit. The

covariance analysis supported the hypothesis that patch

size affected the number of larvae predation by overall taxi,

but there was no support for a distance effect. These

findings suggest that natural enemies’ ecological service

(mainly from birds) declined with remnant reduction,

which has implications not only for human welfare, but

also in strengthening the economic justifications for con-

serving the remaining natural habitats and biodiversity in

agricultural landscapes.

Keywords Ecosystem service � Fragmentation �Isolation � Insectivore � Predation

Introduction

Increasing human population size and food consumption

per person have resulted in an expansion in agricultural

landscapes and a concurrent reduction of natural habitats to

smaller, isolated fragmented patches. These changes in

land use are the major drivers of biodiversity loss, because

these patches become too small to support particular spe-

cies or too far apart to ensure regional persistence of

metapopulation dynamics (Tilman et al. 2001; Fahrig 2003;

Tscharntke et al. 2005).

Although most people give little thought to how

dependent they are on biodiversity, crucial services for

humanity are disappearing or becoming inefficient (Daily

1997; Tscharntke et al. 2005; Whelan et al. 2008). If

conserved and managed appropriately, biodiversity can

contribute to agricultural productivity and sustainability of

ecosystem services (such as pest control, crop pollination,

soil fertility, protection against soil erosion in waterways,

Project funding: This work is financially supported from Fundacao de

Amparo a Pesquisa do Estado de Minas Gerais FAPEMIG-VALE S/A

(Process #RDP-00104-10) and Conselho Nacional de

Desenvolvimento Cientıfico e Tecnologico (CNPq) (Process #

472250/2010).

The online version is available at http://www.springerlink.com

Corresponding editor: Chai Ruihai

M. X. Jordani

Laboratorio de Ecologia Animal, Departamento de Zoologia e

Botanica, Universidade Estadual Paulista - UNESP, Rua

Cristovao Colombo, 2265, Jardim Nazareth,

Sao Jose Do Rio Preto, SP CEP 15054-000, Brazil

E. Hasui (&) � V. X. da Silva

Laboratorio de Ecologia de Fragmentos do Sul de Minas

Gerais – ECOFRAG, Instituto Ciencias da Natureza,

Universidade Federal de Alfenas - UNIFAL – MG, Rua Gabriel

Monteiro da Silva, 700, Centro,

Alfenas, MG CEP 37130-000, Brazil

e-mail: ericahasui@yahoo.com

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J. For. Res.

DOI 10.1007/s11676-015-0043-y

Author's personal copy

and the removal of excessive nutrients). Natural pest reg-

ulation is an important service with economic and human

health benefits.

Pests, particularly herbivorous insects, destroy 37 per-

cent of the potential crop yield (Pimentel et al. 1997).

Despite millions of tons of synthetic pesticides used

annually, farmers frequently failed to combat pests because

many have evolved resistance to them. To avoid immunity

to specific chemicals, farmers need to maintain as many

weapons in the pest control arsenal as possible and alter-

nate these strategies (Sodhi and Ehrlich 2010). However,

these chemical compounds can also kill beneficial species

(such as pollinators, or natural predators of the pest) and

also put human health at risk through food and water

contamination.

Achieving success in natural pest control depends on

many factors and can easily be disrupted (Bianchi et al.

2006). There is increasing evidence that landscape struc-

ture and composition can interfere with this service

(Tscharntke et al. 2005; Bianchi et al. 2008). Several

studies have shown that species richness and abundance of

natural enemies are affected by the proximity of a natural

habitat patch (Tscharntke et al. 2007). In this case, preda-

tors cross natural habitat edges into neighboring crops,

where they significantly reduce prey populations (Cronin

2003). Thus, managing action on natural habitats in agri-

cultural ecosystems assumes that significant predator

incursions will across natural habitat edges and result in

enhanced biological control (Denno et al. 2005).

The question of the optimal size and distance of natural

habitats to enhance natural enemies, and consequently

maximize ecosystem service, is not well understood. For

example, Puckett et al. (2009) showed higher foraging

habits of insectivorous birds within 20 m of the edge, but

other studies also found a foraging distance pattern at least

1 km apart from a natural habitat (Jonsson et al. 2010). The

distance pattern depends on the biology of individual

species, mainly related to habitat specialization and dis-

persion ability in the crop.

We test the hypothesis of incremental predator activity

into the crop along natural patch-size gradients. From a

natural enemies’ perspective, increasing natural patch size

can result in higher abundance and diversity of food

resource (MacArthur and Wilson 1967; Connor et al.

2000). If predator populations exhibit positive response to

food availability, then higher predator abundance and

greater predator effects are likely to be found in larger

patches (With 2002; Langellotto and Denno 2004). This

increment in predator abundance can be propagated into

the crops, if predators can disperse freely across natural

habitat edges (Cronin 2003).

Alternatively, the opposite hypothesis of the relationship

between patch size and foraging activity can be expected

due edge-related phenomena. In this case, in small natural

patches with high edge-to-area ratio, prey mortality will

increase as a result of predator incursion into the crops

(Cronin et al. 2004). There are data to support both sce-

narios of increasing and decreasing impacts across a patch

gradient (Denno et al. 2005). In this study, we tested two

alternative hypotheses and also evaluate the distance effect

from the natural habitat patch in the agricultural landscape.

Materials and methods

Study area

Fieldwork was conducted in fragments in the southern

Brazilian state of Minas Gerais, Brazil (21�25048.0300S,

45�56051.7600W, Fig. 1). Altitude in this area averages

880 m asl, with a mean annual temperature of 23 �C and

annual rainfall of 1,413 mm (Costa 1998). The original

vegetation is classified as seasonal semideciduous forest

(Oliveira Filho and Fontes 2000). However, now the

landscape is highly fragmented, with only four percent of

native forest remaining in various successional stages

(Fundacao SOS Mata Atlantica and INPE 2009). The

landscape matrix is mainly composed of pastures and

coffee and sugar cane plantations.

The landscape analysis was conducted using satellite

images (CBERS), with a 20 m resolution, using ArcGIS

9.2TM software to visually classify mature forest remnants

in a 30 km radius of the municipality of Alfenas, Brazil.

The patch size was then calculated to select seven forest

remnants in a size gradient ranging from 6 to 105.9 ha

(mean 49.28 ± 36.60 ha, Fig. 1). The matrix surrounding

forest remnants was composed by coffee plantation.

Fig. 1 Location of the study area in the State of Minas Gerais, Brazil,

showing the location of the sample sites (dark gray)

M. X. Jordani et al.

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Bird sampling

In each sample site, six points were chosen: two points

inside the fragment (located at 100 m from the nearest

forest edge), two in the forest edge (located at one meter

from the nearest forest edge) and two inside the coffee

plantation (located at 100 m from forest edge). Each point

was at least 100 m apart from the other (Fig. 2). Each

fragment was sampled three times in the wet season in the

years of 2008 and 2009, always in the morning.

Birds were sampled using the point count method with

limited distance (30 m, Develey 2003). The time for

sampling in each point was 10 min. All birds were recor-

ded, but only insectivorous (including omnivores) under-

story birds were considered in this study, because they are

potential predators of caterpillars. The classification of

foraging behaviour and vertical stratification followed

Willis (1979), Fitzpatrick (1980), Ridgely and Tudor

(1994, 1997), Remsen and Robinson (1990), Stotz et al.

(1996), Sick (2001) and Gomes et al. (2008). The taxo-

nomic classification of the bird species followed CBRO

(Comite Brasileiro de Registros Ornitologicos 2011).

Caterpillar predation

An experimental approach was used to compare the num-

ber of caterpillars found in the fragments. Using modeling

clay, an oil-based and nontoxic compound, artificial cat-

erpillars were constructed to capture the bite marks of

potential predators. The artificial caterpillars had a standard

size (30 mm 9 7 mm), shape (cylindrical) and color

(green). Due to malleability of model and the type of

impression upon its retrieval, the predator taxa can be

identified using a method successfully employed in other

studies (Freitas and Oliveira 1996; Koh and Menge 2006).

The artificial caterpillars were randomly distributed along

five parallel trails (20 caterpillars per trail, length = 5 m)

per fragment: two inside the fragment, two inside the coffee

plantation, and one on the edge forest (Fig. 2). Each trail was

at least 25 m from the other. Each caterpillar was secured on

the top of leaves at 1.5 m above ground using plastic glue.

After five days, the caterpillars were collected and examined

under a stereomicroscope in order to determine the nature of

the bite marks inflicted by potential predators (e.g., mam-

mals, birds, ants and wasp; Fig. 3).

Data analysis

The relative importance of predators was determined using

a two-way ANOVA with habitat and predator type as the

categorical predictors. A subsequent Tukey’s test was done

to assess where there was a difference. In this analysis we

excluded the edge-collected data.

Through an analysis of covariance (ANCOVA), three

models were established, representing all possible n-way

combinations of the two predictor variables: patch size and

predator type. Later these models were compared and

selected by Akaike information criterion (AIC—Akaike

Information Criterion) and then adjusted for small samples

(AICc) (Burnham and Anderson 2002). This highlighted

the most plausible models to explain the variation in the

number of caterpillars. The Akaike criterion is defined by

likelihood AICc = -2 ? 2 * K * (n/(nk - 1)), where

maximum likelihood is the likelihood of the data, K is the

number of parameters in the model, and n is the size of

sample. This generates a ranking of the best to worst

model, and AICc differences C2 are considered great, and

the best support is given to the model with lowest AICc.

The plausibility of the models was evaluated through the

values of DAIC (difference between a determined and the

lowest value of AIC among all models tested) and wi,

which is the Akaike weight, which varies between 0 and 1,

and estimates the weight of evidence in favor of a model

i given the set of models compared.

To assess whether the distance from the fragment affects

the amount of caterpillars attacked by predators, we also

conducted an analysis of covariance to determine the best

model relating the number of attacked caterpillars to the

distance from fragment and type of predator. So we explore

the gradient interior-edge-coffee plantation. Our study did

not have a control area for absolute lack of forest fragments

with more than 500 hectares within 100 km radius.

Furthermore, a Spearman correlation was used to eval-

uate the relationship between the abundance index of

insectivorous bird and the number of artificial caterpillars

predated by birds.

Fig. 2 Sampling unit design of seven sites in Minas Gerais, Brazil.

Each sample site was composed of six point counts (white circles) and

five transects (white lines). White circles represent the locations where

birds were sampled by point counts and the white transects where

predation models were distributed

Natural enemies depend on remnant habitat size

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Results

Relative importance of predators

Birds, insects, and mammals were the main predators of

caterpillars in the study site. After five days, they attacked

21.7–60.3 % of the artificial caterpillars. After excluding

mammal predations from the statistical analysis due to an

insufficient sample size (only two occurrences), there were

significant differences between predators (i.e., birds, ants,

and wasps). The birds preferentially attacked in the forest

(two-way ANOVA: F2, 46 = 4.1; p = 0.02), but even so,

their attacks in the coffee plantation were higher than those

from wasps and ants (Tukey test: p \ 0.05) (Fig. 4).

Interaction between predator type and patch size effects

The best-supported model constructed in the analysis of

covariance (GLM–ANCOVA) indicated that the predations

were affected only by the combination of predator type and

patch size (Table 1). There was no support for the indi-

vidual prediction models (DAICc C 2). Specifically, this

model showed a positive relationship between patch size

and number of predation, but the intensity of those attacks

was conditioned by the predator type (Fig. 5a). Birds

attacked more with an increase in patch size. The same

thing happened with ants and wasps, but at lower levels.

Distance from remnants effect on predations in the

coffee plantations

There was no support for the effect of distance from

remnants according to the analysis of covariance (GLM–

ANCOVA). The most plausible model included only the

predator type (Table 2). The contribution of distance as

predictor variable was very low (predictor weight = 0.03),

mainly when wasp and ant predations were considered

(Fig. 5b).

Potential bird predators

From a total of 23 insectivorous understory bird species in

the sample sites, five may be potential candidates for pest

Fig. 3 Examples of different bite marks found on artificial caterpillars: a mammals, b birds and c ants

Birds Wasps Ants0

5

10

15

20

25

30

Num

ber o

f pre

datio

ns

Predators

ForestCoffee plantataion

Fig. 4 Number of artificial larvae attacked by birds, wasp and ants in

the interior of the forest fragments and in the coffee plantation. Points

represent mean ± SE

Table 1 GLM–ANCOVA model results compared with the null model,

ranked by Akaike’s Information Criterion corrected for small sample

size (AICc), predicting the number of artificial caterpillar predations

Models K AICc DAICc wi

Predation * Size ? Predator 4 777.24 0.00 1.00

Predation * Predator 3 926.03 148.79 0.00

Predation * Size 3 878.46 101.22 0.00

Null model 2 1,034.25 257.01 0.00

Two predictor variables were used in the models: Patch size (size) and

Predator type (Predator)

K number of parameters, DAICc difference in AICc between the best

and present model, wi Akaike’s weight

M. X. Jordani et al.

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predators, because they mainly attack prey on foliage and

stems and also occur in the coffee plantations (Table 3). In

particular, Basileuterus leucoblepharus (Spearman corre-

lation: rs = 0.82 and p = 0.02) and Dysithamnus mentalis

(Thamnophilidae, Spearman correlation: rs = 0.89 and

p = 0.006) showed a significant correlation between the

number of caterpillars attacked and the number of bird

contacts.

Discussion

Influence of natural habitat patch on pest regulation

service

The economic reasons for saving and restoring natural

habitats are growing increasingly influential for politicians

and resource managers. It is of utmost importance to

identify strategies that generate positive co-benefits for

production, biodiversity, and local people. This experi-

mental study found evidence that the size of natural habitat

patches in the agricultural landscape interfered with natural

predators. The predator service increases with the

increasing size of the adjacent natural habitat, being able to

reduce larvae by 21.7–60.3 % after five days.

These percentages may be higher since we studied

predation in small-sized patches (ranging from 6 to

105.9 ha), and therefore higher percentages may be

expected in larger natural patches. For example, Greenberg

et al. (2000) found that birds reduced the abundance of

large arthropods ([5 mm) in a coffee plantation by

64–80 % and also with lower levels of leaf damage.

Borkhataria et al. (2006) expanded the insect size classes,

demonstrating that birds can also reduce small-sized insect

populations in a coffee plantation. Furthermore, pest con-

trol services in the crops were not influenced by the dis-

tance from natural habitats, at least 100 m apart from the

edge.

Potential pest predators

Due to the study design, we only have indirect evidence

about the type of predators. Our results indicated that

predation intensity is species specific, where bird species

were more effective control agents than ants or wasps,

although birds were more affected by patch-size variation.

Differential responses among taxa may be due to differ-

ences in their biological traits, such as ecological special-

ization, matrix use, and organism dispersal capacity (Henle

et al. 2004).

However, interactions of species traits and landscape

structure must be considered. These predators are

0 20 40 60 80 100 120

Fragment size (ha)

-5

0

5

10

15

20

25

30

35

40

45N

umbe

r of p

reda

tions

B i rds Wasp Ants

-75 -50 -25 0 25 50 75

Distance from edge (m)

-5

0

5

10

15

20

25

30

35

40

45

A B

Fragment size (ha)

-5

0

5

10

15

20

25

30

35

40

45N

umbe

r of p

reda

tions

B i rds Wasp Ants

Distance from edge (m)

-5

0

5

10

15

20

25

30

35

40

45

A B

Fig. 5 Number of artificial larvae attacked by birds, wasps and ants in different forest fragment sizes (a) and different distance from the edge of

forest fragments (b)

Table 2 GLM–ANCOVA model results compared with the null

model, ranked by Akaike’s Information Criterion corrected for small

sample size (AICc), predicting the number of artificial caterpillar

predations

Models K AICc DAICc wi

Predation * Predator 3 926.03 0.00 0.97

Predation * Predator ? Distance 4 932.81 6.78 0.03

Predation * Distance 3 1,034.03 108.00 0.00

Null model 2 1,034.25 108.22 0.00

Two predictor variables were used in the models: Distance from edge

(Distance) and Predator type (Predator)

K number of parameters, DAICc difference in AICc between the best

and present model, wi Akaike’s weight

Natural enemies depend on remnant habitat size

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dependent on resources not contained within a single

habitat type and are likely influenced by the landscape

structure of all required patch-habitat types. The ability to

use resources in different habitats is dependent on biolog-

ical traits of species and is influenced both by the charac-

teristics of the patch (food supply, predation risk,

competition pressure) and the characteristics of landscape

(habitat complexity, diversity, quality, and patchiness).

This spatial association of required habitat patches influ-

enced the distribution patterns of predation across the crop-

natural habitat interface (Tscharntke et al. 2005).

Our results suggest, at least two distribution patterns of

predator attacks. The first pattern, represented by ant and

wasp predators, showed homogeneous distribution of

attacks in the crop-natural habitat interface without specific

preference for one habitat type or the other. The second

pattern, described for bird predators, showed heteroge-

neous distribution of attacks with higher attacks in the

natural habitats than in the crops.

Five insectivorous bird species occurred in the matrix

and are possible candidates of these attacks. However,

Basileuterus leucoblepharus and Dysithamnus mentalis

had a strong positive correlation between the number of

larvae attacks and the number of individual bird contacts.

Thus, they were potentially the most important pest pred-

ator in the study area. The positive effect of bird attacks

with the natural patch size was explained by the addition of

bird species of higher sensitivity to human disturbances

(sensus Stotz et al. 1996), such as Hemitriccus orbitatus

and Drymophila ferruginea, which are restricted to larger

fragments. This work supports an earlier suggestion that

insectivorous birds were important in the reduction of

herbivorous insect pests (Altegrim 1989; Strong et al.

2000) or plant damages in both natural habitats and coffee

plantation (Greenberg et al. 2000; Borkhataria et al. 2006;

Kellermann et al. 2008; Van Bael et al. 2008; Johnson et al.

2009). For example, they are able to reduce the population

of the forest pest Lepidoptera, which the birds feed on, by

20–100 % (Barbaro and Battisti 2011).

Despite the lower level of attacks by wasps and ants,

previous studies have demonstrated the importance of these

taxa as natural enemies of coffee plantation pests such as

Table 3 Bird species recorded in point count observations of seven forest remnants and surrounding coffee matrix in Alfenas, MG

Family Species Forest Edge Matrix Foraging Substrate

Cariamidae Cariama cristata (Linnaeus 1766) X X Ground leaf-litter

Conopophagidae Conopophaga lineata (Wied 1831) X X Ground leaf-litter

Cuculidae Guira guira (Gmelin 1788) X Ground

Piaya cayana (Linnaeus 1766) X X Foliage or stem surfaces

Dendrocolaptidae Lepidocolaptes angustirostris (Vieillot 1818) X Bark

Sittasomus griseicapillus (Vieillot 1818) X Bark

Furnariidae Automolus leucophthalmus (Wied 1821) X X Foliage or stem surfaces

Synallaxis cinerascens (Temminck 1823) X Foliage or stem surfaces

Synallaxis frontalis (Pelzeln 1859) X Foliage or stem surfaces

Synallaxis ruficapilla (Vieillot 1819) X X X Foliage or stem surfaces

Synallaxis spixi (Sclater 1856) X X Foliage or stem surfaces

Parulidae Basileuterus culicivorus (Deppe 1830) X Foliage or stem surfaces

Basileuterus flaveolus (Baird 1865) X X Foliage or stem surfaces

Basileuterus leucoblepharus (Vieillot 1817) X X X Ground leaf-litter andfoliage

or stem surfaces

Picidae Picumnus cirratus (Temminck, 1825) X X Bark

Rynchocyclidae Hemitriccus orbitatus (Wied 1831) X X Foliage or stem surfaces

Thamnophilidae Drymophila ferruginea (Temminck 1822) X Foliage or stem surfaces

Dysithamnus mentalis (Temminck 1823) X Xa Foliage or stem surfaces

Pyriglena leucoptera (Vieillot 1818) X Ground leaf-litter

Thamnophilus caerulescens (Vieillot 1816) X X Foliage or stem surfaces

Tyrannidae Elaenia flavogaster (Thunberg 1822) X X Foliage or stem surfaces

Lathrotriccus euleri (Cabanis 1868) X X Foliage or stem surfaces

Platyrinchus mystaceus (Vieillot 1818) X X Foliage or stem surfaces

Bird species were classified by foraging behaviour (specifically the substrate on which birds attack their preys) followed Sick (2001), Stotz et al.

(1996), Fitzpatrick (1980) and Remsen and Robinson (1990)a Bird species occurrence in the coffee plantation came from another study, which used the same methods (M. T. P. Coelho unpublished data)

M. X. Jordani et al.

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leafminer, Leucoptera coffeellum (Guerin-Meneville)

(Lepidoptera: Lyonetiidae), which causes great economic

losses in some New World coffee-producing countries,

such as Brazil, Colombia, Cuba, Guatemala, Peru, and

Puerto Rico (Parra 1985; Reis et al. 2000; Fragoso et al.

2001). A study in Brazil on population dynamics of this

species demonstrated that wasps could reduce pest popu-

lations by 69 % (Reis et al. 2000). A collection of wasp

predator species from prior studies documented, at least,

six genera and 11 species—including Protonectarina syl-

verae Saussure, Polybia paulista Ihering, Polybia occi-

dentalis Olivier, Polybia scutellaris White, Brachygastra

lecheguana Latreille, and Synoeca surinama cyanea Lin-

naeus—that feed on coffee leafminers (Fragoso et al. 2001;

Lomeli-Flores 2009). However, the findings of Reis et al.

(2000) contrast to Lomeli-Flores (2009), who found that

ants were the principal coffee leafminer predators in

Mexico. At least 12 species were observed preying on

eggs, larvae, or pupae, from the Camponotus, Pseudo-

myrmex, and Azteca genera. Lomeli-Flores (2009) sug-

gests that the differences in the relative importance of

predator species between countries could be due to dif-

ferences in coffee-farm microclimatic conditions and/or

management regimes. Brazilian coffee production is

mainly under sunny conditions and farms are intensively

managed, while in Mexico, production is under shady

conditions and farms are traditionally managed, but this

difference needs to be further tested and verified.

Natural habitat influence on predation in crops

Potential mechanism behind patch size

The positive relationship between the amount of predation

in crops and the size of adjacent forest is consistent with

the resource-concentration hypothesis (Root 1973). This

hypothesis conjectures that population density should be

positively correlated with patch area. Previous work found

evidence for this relationship in bird and insect species

(Connor et al. 2000). Several potential mechanisms, such

as demographic effect, may be responsible for this pattern,

and differences among species (Connor et al. 2000). In the

demographic effect, smaller patches should have lower

density, due to greater vulnerability to stochastic conditions

or the higher probability of an Allee effect (Vergara and

Hahn 2009). Therefore, a denser population in larger pat-

ches could increase prey consumption in resource-rich

habitats (Bianchi and Wackers 2008).

Distance effect from remnant

Based on theoretical predictions (Strong 1992; Polis and

Strong 1996), we would expect a stronger impact of

predators on herbivorous prey near natural habitats. How-

ever, our results did not support this prediction for all taxa.

The absence of the distance effect may be due to the fine

spatial scale used in the experimental designs, considering

the high mobility of the natural enemies in the crops.

Future analyses that incorporate larger distance ranges may

influence or change the observed relationships. Klein et al.

(2006) found a significant distance effect in wasps, work-

ing with distances as far as 1,400 m to the nearest natural

forest.

Conservation and management implications

Arthropod pests have been estimated to cause around 14 %

losses in the gross domestic product (GDP) in developed

countries and 38 percent in developing countries (Zambolim

et al. 2008). For example, considering that the GDP of Bra-

zilian agribusiness reached R$ 822.9 billion in 2011

(National Confederation of Agriculture and Cattle Breeding

of Brazil), an estimated R$ 312.7 billion was lost in the year

due to arthropod pests. Chemical pesticides are still the

dominant form of control for many of these pests, but they

also imply additional costs in the form of human health and

degraded environment. On the other hand, the management

and conservation of natural habitats can increase production,

without these negative additional costs, due the conservation

and enhancement of natural enemies (Jonsson et al. 2010).

These methods can provide natural enemies with a favorable

microclimate condition and place for shelter, dormancy, and

alternative food sources (Landis et al. 2000). Several studies

showed that density and diversity of natural enemies tend to

be higher in landscapes with a high proportion of non-crop

vegetation (Bianchi et al. 2006). Generally, the percentage of

habitat area in a given landscape has a strong correlation with

the mean patch size and the size of largest patch (Fahrig

2003). Therefore, landscapes with higher percentages of

habitat areas often correspond to landscapes to where pat-

ches are large.

Our studies support these previous predictions, showing

a positive relationship between the size of natural habitat

patches and the amount of predation predators. However,

some questions about this relationship and other landscape

ecology issues remain. For example, what is the optimal

size of a natural habitat to provide natural pest control and,

the same time, to maximize the crop production? Should

landscape restoration efforts focus on enlarging existing

natural patches or building new patches? Will restored or

managed landscape really restore the natural enemy’s

composition and consequently the ecological process?

What is the minimum distance between natural patches to

facilitate natural enemy’s species migration in a managed

landscape? What is the optimal spatial scale to which the

predation process mainly responds?

Natural enemies depend on remnant habitat size

123

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Future research addressing these questions can facilitate

biological conservation associated with crop production

increases. Concluding, our results suggest that the natural

enemies’ service (mainly from birds) declined with natural

habitat reduction in the agricultural landscape. This has

implications not only for human welfare, but also in

strengthening the economic justifications for conserving

remaining natural habitats.

Acknowledgments We wish to express our gratitude to M. Raniero,

M. F. V. Silva, E. Pessoni, and other members of the Laboratorio de

Ecologia de Fragmentos Florestais (ECOFRAG), who have been

valuable friends, assisted in fieldwork, and made essential comments

at different phases of this study. This manuscript also greatly bene-

fited from the comments of Alberto Jose Arab Olavarrieta. We also

thank several private landowners who permitted access to their

properties. Universidade Federal de Alfenas provided logistical sup-

port. We received financial support from Fundacao de Amparo a

Pesquisa do Estado de Minas Gerais FAPEMIG-VALE S/A (Process

#RDP-00104-10) and Conselho Nacional de Desenvolvimento

Cientıfico e Tecnologico (CNPq) (Process # 472250/2010). We

appreciated the improvements in English language made by Jim

Hesson of http://www.AcademicEnglishSolutions.com

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