Birds as Predators in Tropical Agroforestry Systems Author(s): Sunshine A. Van Bael, Stacy M.

Philpott, Russell Greenberg, Peter Bichier, Nicholas A. Barber, Kailen A. Mooney, Daniel S. Gruner Reviewed work(s): Source: Ecology, Vol. 89, No. 4 (Apr., 2008), pp. 928-934 Published by: Ecological Society of America Stable URL: http://www.jstor.org/stable/27651631 . Accessed: 23/02/2012 08:12
Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact support@jstor.org.

Ecological Society of America is collaborating with JSTOR to digitize, preserve and extend access to Ecology.

http://www.jstor.org

Ecology, 89(4), 2008, pp. 928-934 ? 2008 by the Ecological Society of America

BIRDS AS PREDATORS
Sunshine A. Van Bael,1,6 Stacy M. Kailen

IN TROPICAL AGROFORESTRY
Peter Greenberg,2 Daniel S. Gr?ner5,8 Bichier,2

SYSTEMS
Nicholas A. Barber,3

Russell Philpott,2,7 and A. Mooney,4

1 Smithsonian Tropical Research Institute, Unit 0948, APO, A A 34002 USA 2Smithsonian Migratory Bird Center, National Zoological 20008 USA Park, Washington, D.C One University Boulevard, St. Louis, Missouri 63121 USA 3Department of Biology, University ofMissouri, 4Department of Ecology and Evolutionary Biology, University of California, Irvine, California 92697-2525 USA P.O. Box 247, 2099 Westside Road, Bodega Bay, California 94923-0247 5Bodega Marine Lab, University of California-Davis, reduce arthropod abundances and their damage to plants in The variation in bird pr?dation by birds has been assessed. to characteristics or quality, habitat such as plant productivity complexity, and prey assemblages. Since agroforestry and/or species diversity of predator systems vary in such characteristics, a good these systems provide when and starting point for understanding where we can expect pr?dation data from bird exclosure by birds to be important. We analyze studies in forests and agroforestry to ask whether birds consistently reduce their systems some, but not all, effects may be due studies where arthropod systems. and whether bird pr?dation differs between forests and agroforestry prey base we focus on to ask whether the magnitude of bird Further, systems agroforestry trees and understory canopy (1) differs between plants, (2) differs when migratory Abstract. Insectivorous birds

USA

pr?dation or absent, and (3) correlates birds are present with bird abundance and diversity. We found and plant damage. that, across all studies, birds reduce all arthropods, herbivores, carnivores, no difference We observed in the magnitude of bird effects between systems and agroforestry forests layer. agroforestry migratory predator structure habitat and simplified of arthropods systems, bird reduction were effects of bird pr?dation Top-down despite birds were assemblage present correlated with

in agroforestry the diversity of the systems. Importantly, the magnitude of predator the diversity of effects; where to a greater densities birds, especially birds, was greater, birds reduced migratory arthropod extent. We outline potential mechanisms for relationships between bird predator, insect prey, and habitat and we suggest future studies using tropical agroforests as a model characteristics, system to further test these areas of ecological theory. Key words: agroforestry tropical ecosystems. systems; birds; insectivory; me ta-analysis; top-down; trophic interactions;

in agroforests. Within plant diversity was in the canopy than the crop greater censuses when strong during especially

Introduction Increasingly, predators ecologists are focusing on the role of

these Linhart

factors 2006). range

(Gratton

and Denno

Insectivorous of terrestrial

and the implicationsforplants thatdirectlyor indirectly

resources Considerable control such has for the prey species in the research (Schmitz strength of et al. top 2000). variation stimulated

in reducing

the abundance

of their prey base

a broad number orous have the

and 2003, Mooney are ubiquitous across and a growing ecosystems, birds of insectiv of netting) in reductions

provide down factors,

of experimental field manipulations bird activity via exclosures (primarily and often strong

shown measurable

as variation complexity,

in nutrient or

into mitigating resource availabil condition of

crop of arthropods, standing including important of herbivores (Mols and Visser 2002). A smaller number of studies have shown in that the reduction groups herbivores sometimes, further decreases the overall herbivore and, damage growth rate or standing biomass and Whelan 1996, Van Bael and

ity, habitat

plants (Cebrian and Lartigue 2004), the diversity and

composition Schmitz of predator and 2007), temporal assemblages (Sih et al. 1998, or seasonal in variation

qualitative

28 November received 12 2006; Manuscript accepted 2 April final version received 2007. 2007; February Editor Corresponding (ad hoc): I. Perfecto. For reprints of this Special Feature, see footnote 1, p. 913. 6 E-mail: vanbaels@si.edu 7 Present address: Department of Environmental Sciences, of Toledo, Toledo, Ohio 43606 USA. University 8 Present address: Department of Entomology, University of Maryland, 20742 USA. College Park, Maryland

of plants (e.g., Marquis Brawn the wide variation in effects 2005). Considering across documented studies, a quantitative experimental to understand is needed and mecha synthesis patterns nisms of top-down systems. control across natural and managed forested

Studies Latin America have documented throughout and diversity of insectivorous birds in high abundance shaded coffee and cacao systems (Perfecto agroforestry

et al.

1996, Rice

and Greenberg 2000). Although

share some qualities with native

agroforestry

systems

928

April 2008
Table 1. Review

AGROFORESTS AS MODEL
of effect sizes from bird exclosure studies

SYSTEMS FOR ECOLOGY

systems of Central America. Effect sizesf All arthropods Large arthropods

929

in agroforestry

Focal plant and location Coffee crops

Duration Habitat description (months)

-.-: Insecticides

Plant damage

Guatemala^ Mexico?

Puerto Ricof Cacao crops Panama# Inga spp. Guatemala] Mexicoff Various species |

shaded monoculture unshaded monoculture traditional polyculture commercial polyculture commercial polyculture shaded monoculture commercial polyculture traditional polyculture 12 shade shade shade

1 2

2 2 24 24 24 24 4

yes yes no no no no

-0.13 -1.93 -0.14 0.06 -0.10 0.21 -0.16

-1.05 -1.75 0.15 0.33 -0.17 -0.29 -1.32

-0.17 -0.25 0.17 -0.63 -0.18 -0.34 NA

-0.11 no no no

-0.64

-0.37

trees over coffee 2 trees over coffee 1 trees over coffee 2

2 2

-0.55 -0.47 -0.89

-1.09 -1.54 -1.07

-0.08 NA NA

MexicoJJ

tree patch

in pasture

-1.36

NA

NA

f Effect sizes are calculated as ln(response ratios), i.e., ln(control mean/exclosure mean). More negative effect sizes indicate a stronger effect of birds. et al. (2000). Unshaded monoculture Data from Greenberg coffee from this study was excluded from the agroforest vs. forest % analysis, as itwas not grown in an agroforest. P. Bichier, C. E. Gordon, A. Garcia-Ballinas, and G. Lopez Bautista (unpublished ? I. Perfecto, R. Greenberg, G. Ibarra-Nu?ez, manuscript). This study examined bird effects in four farms, under three different shade management regimes. At time of exclosure establishment, site 1 had slightly higher density and diversity of shade trees, and site 2 had relatively less density and diversity of on the two farms became more similar. shade trees. During the two years exclosures were maintained, management et al. (2006). % Borkhataria # Van Bael et al. (2007). et al. (unpublished data), same site and authors as Greenberg et al. (2000). II Greenberg ff Philpott et al. (2004); treated as two separate studies because different exclosures were used on different trees in the dry (1) and wet (2) seasons. and Ortiz (1994). ?t Greenberg are both structur habitats ordinarily agroforest are and than forests and ally floristically simpler in and homogeneous relatively species composition structure with tropical forests. The interme compared forest, of agroforestry systems hence provides complexity a potential model system for understanding ecological in terrestrial control of top-down aspects systems. Recent have exclosure studies used in experiments diate shaded to quantify agroforests on arthropod densities insectivory and the and effects plant of bird damage our tropical results in temperate systems in order place a larger ecological context. We then focus on agrofor to ask whether the magnitude of bird estry systems trees between and under differs canopy pr?dation (1) birds are present story plants, (2) differs when migratory or absent, and with bird abundance and (3) correlates how from agrofor discuss this research diversity. We estry systems suggests approaches future studies. broader ecological theory and

(Table 1). Many of these studies are notable in thatbird

abundance ly: a rarity diversity were documented in the literature from natural studies regimes across quantitative forests. This a range agrofor of We criteria: ed and were Literature

Methods search, effect size and meta-analysis database exclosure calculations,

of exclosure replication and management locations estry systems allows studies studies agroforestry exclosure often been biological complexity

in tropical

tropical forest studies. Although

in shaded to evaluate

for a comparative among analysis and between and agroforestry

lished studies that fulfilled all three of the following

(1) netted paired with the dominant rather were experiments were construct (2) trees open controls, appropriate strata vegetation upper than shrublands in the shrub were the focal

compiled

of published

and

unpub

the impetus for

has

systems agroforestry the potential of bird pr?dation for we use of vegetative this range control, structure natural forests and and among

landscapes (3)-exclosures A). In all

(forested or grasslands), and and/or canopy

layer (not theunderstoryherb/seedlinglayer) (Appendix

studies, some and birds vertebrate of leafThe All . interest, but excluded experiments necessarily lizards concomitantly with birds. and forests,

placed

to address basic We agroforests ecological questions. studies to of data from exclosure present a meta-analysis assess effect size of insectivo and compare the overall rous birds we in forests compare and forests, agroforestry bird effects systems. Within in tropical and

final data set consisted of 48 studies,with 11 and 37

studies in agroforests respectively.

gleaning

bats

930
Table 2. Comparison

SUNSHINE

A. VAN

BAEL

ET AL.

Ecology, and forests.

Vol.

89, No.

of effect sizes (response Agroforest

ratios) from bird exclosure Forest

studies in agroforests Comparison

Overall Mean 0.41 0.19 0.99 0.31 25 41 40 34 -0.32 -0.61 -0.60 -0.71 effect size (CL) (-0.45, (-0.86, (-0.90, (-0.95, -0.20) -0.37) -0,30) -0.49)

Variable Plant damage All arthropods Herbivores Carnivores 7 11 11 11

Mean -0.23 -0.33 -0.60 -0.53

effect size (CL) (-0.04, -0.06) (-0.63,-0.09) (-0.89,-0.36) (-0.81,-0.29) 18 30 29 23

Mean effect size (CL)

-0.35 -0.72 -0.60 -0.79 (-0.51, -0.19) (-1.05,-0.42) (-1.0,-0.22) (-1.09,-0.48)

Q
0.078 1.191 0.001 0.497

df
1, 23 1,39 1,38 1,32

Notes: Effect sizes were calculated as ln(response ratios), i.e., ln(control mean/exclosure mean). Bootstrap confidence intervals, representing a 95% confidence limit, are used throughout this table; n is the number of studies in the calculation of mean effect size. The Q statistic partitions the total heterogeneity into variance explained by the model and the residual error not explained by the for resampling details. model (Q is similar to F in an ANOVA test). See Methods and For six of the forest studies we were classified in detectable but tests are more intervals forest, were conservative around and mean overall 999 with

agroforest

studies

of each site using tree canopy of the shade (i.e., descriptions to assign tree density) tree diversity, cover, percent and Toledo of Moguel (1999). systems to the categories informa The studies are listed in the online supporting author

systems. agroforestry tropical the level of management intensity

studies,

to type I error [Hedges et al. 1999]). We

bootstrap estimates (Metawin confidence for agroforest, 2.0). The data to generate lowest 2.5% lower 95%

calculated
effect effect size sizes the

respect

replacement and highest upper and

resampled a distribution, values were limits.

times with to represent

from which

used

tion (Appendix B).

For studies, comparisons which effects

confidence data

among

the similar

tropical

employed

agroforestry we methodologies, reduc

Bird

census

and predatory

effects

describe tion

in arthropod

intuitively using numbers due studies

compare

agroforestry

simple percent to bird pr?dation. To with the larger and more set of forest study using studies, we log response

heterogeneous methodologically effect sizes for each calcLilated

= 9 studies exclosure (n sites), we agroforest tropical effects and between tested for relationships pr?dation of rarefied bird richness of species per number (number and abundance. individuals) site consisted of between minute conducted R. point by counts, the same Bird 38 and

With bird point count data provided by authors of the

ratios (In R) where

ln(exclosure mean) (this

In R =

ln(control mean)
to -[ln(treatment

in each study sampling 10 410 25 m radius, of which were and (P. Bichier observer bias among

mean/control mean)]

[Hedges et al.

is equivalent

1999]). Where

the majority two observers

we calculated effect sizes for bird pr?dation possible, on all arthropods, herbivo (>5 mm), large arthropods rous arthropods and the and carnivorous arthropods, For all damaged by herbivores. a larger more effect sizes indicate variables, negative to and zero corresponds reduction due to bird pr?dation no effect. We to calculate effect values used endpoint percentage sizes when studies of leaf area

S. Greenberg), thereby lessening to only studies. We limited the bird data sets for analysis found in the strata in insectivores omnivores) (including exclosures (and were percentage when were further limited point placed. We to data in arthropods) reduction were and present (2) (1) migrants

which count the dry resident point

season, birds data

dix A).
Differences and were forests (and calculated

reported

repeated

measures

(Appen agroforests

count

in mean

effect

size between

the dry only activities of resident alter

not breeding. We these compared to predatory effect data also limited to season. and in the behaviors Changes

summary Sinauer

between and tropical forests) temperate using a fixed-effects model (categorical with the Q 2.0, statistic; Metawin analysis Sunderland, Massachusetts, and effect all the residual sizes studies within as USA).

uals at the study siteswere 66% ? 5% and 34% ? 5%

(mean ? correlations abundance residents) for the data examined SE), respectively. We and richness between six bird variables (the of and all insectivorous birds, reduction the percentage migrants, in total and and

season may in the breeding birds on their effects (Greenberg significantly arthropods individ of migrant and resident 1995). The proportions

Associates,

The Q
variance ANO VA

statisticpartitions the total heterogeneity into

explained test). by the model error

not explained by themodel

To compare we treated between systems,

(Q is similar to F

in an
and equal

large (>5 mm) arthropods (Appendix A).

Results Overall The and Discussion and habitat bird comparison exclosure

replicates and did not weight the individual effect sizes

that variance Besides the fact their variance. by were unavailable for some studies, weighting estimates but well replicated the influence of small-scale increases studies realistic overall power relative studies. effect (i.e., to large-scale but Excluding sizes, but may differences variance result between more potentially the does not bias statistical are less

effects of bird pr?dation overall mean suggest effect that

sizes birds

from

experiments arthropods systems

in reduced systems

and plant damage recent meta-analyses 2).- Three reported (Table on herbivores in effect sizes for pr?dation comparable

reduce consistently in forests and agroforestry

real

terrestrialsystems (Schmitz et al. 2000, Halaj andWise

April 2008
100

AGROFORESTS AS MODEL

SYSTEMS FOR ECOLOGY 931 Vegetation (Schmitz et al. 2000, Halaj

Shurin et al. on impact Accordingly, than arthropods and forest 2002). birds on

and Wise
had a

2001,

C/) "? O Q. o ti 05 "cC _c c g o 0) rr

80 -]

60 J 40 20 H OH
-20 100-n = 10.029Xy R2 = 0.6435,

agroforestry most studies effect sizes

plant 1 and 2). In (Tables was the where measured, plant damage some damage birds show reduction where systems are small (Table on plant damage to -0.20, -0.45

greater in damage

but the effect size magnitudes foraged, effect size for pr?dation 2). Our overall = CL -0.32, (plant damage log ratio Table et al. 40.785 P - 0.009 2) was much (2000) (plant These lower damage than

to ?0.72). common, comprise larger directly plant

suggesting the majority relative

analyses that invertebrate in Schmitz on plant

that reported by Schmitz = CL -1.18 -0.95, log ratio two studies in have only (which predators et al. 2000) may have than they do damage because the effects of

effects accumulate

on herbivores.

However,

c/)

damage

^ 8. O s_ -C c CO 0 O) i_
_?0 C c g o D "? O rr

tory growth may trees, the impacts damage across 50 (Schmitz Based stronger 25 = 8.7336X y R2 = 0.6824, 5 10 8.3759 P= 0.011 systems

occur

through time, and compensa within individual shrubs and

as measured

systems et al. 2000). on theoretical impacts in than are of

on tree or shrub pr?dation by leaf area are difficult to compare is also unless biomass reported plant of bird we would expect predictions, in agroforestry bird pr?dation forests. Generally tropical speaking, versions less at all of complex forests, tropical and containing

agroforests both being reduced

simplified

structurally

15

No. migrant species

Fig. 1. Bird effects on (a) all and (b) large (>5 mm) arthropods as a factor of migrant bird diversity. Each point and insectivorous represents bird data for only omnivorous birds that primarily forage in the strata inwhich bird exclosures were placed. Species numbers were rarefied to the maximum number of individuals observed in the site with the lowest bird were A for details). Correlations abundance (see Appendix determined

suggests be more (Polis we found and and

biodiversity that strong likely where

top-down

levels. Theory trophic will effects of pr?dation

and diversity are lower complexity et al. 2000). In contrast, Hulot 1996, Strong no significant differences between agroforests in the extent or plant compared and to which bird pr?dation affected true 2). This was (Table damage to all forest the agroforest studies

forests

arthropods when we

(Table 2) and to tropical forest studies (P > 0.05 for all

were No studies damage). plant the systems, and temperate agroforestry small sizes for tropical forests were sample relatively to temperate the forests. Thus, we increased compared of these comparisons power temperate by aggregating arthropods available for because (mean -0.15] low effect

with the percentage linear regressions using reduction of all or large arthropods as the dependent variable and species diversity as the independent variable. Panel (b) contains one less data point because one study did not separate large arthropods. et al. 2002). All were dominated analyses were and invertebrates,

2001,

Shurin

and tropical forest studies inTable 2. This was justified

similar in the two forest types sizes were on to effect size -0.36 [CL] [?0.57 plant damage, to -0.06], These and -0.33 [-0.60 respectively). gaps highlight the effects of in bird the ecological in pr?dation

the predators by studies where two included systems agricultural

Halaj

and Wise

2001). Halaj

and Wise

(Schmitz

et al.

2000,

(2001) used

d as their effect size statistic, and their results Hedges our measure could not be compared directly. However, ment to bird of herbivore response pr?dation (overall herbivore Table natural 2) log ratio = -0.60, to ratios 95% CL -0.90 predator to -0.30, removal is similar invertebrate

sizes sample literature regarding forest

tropical Bird

systems. in the canopy of agroforestry vs. understory systems coffee farms suggest in the Latta We layers

effects

reported (herbi previously vore to -0.35, CL -0.63 sign reversed for comparison log ratio [Schmitz et al. 2000]; herbivore = et al. [2002]: to -0.20, from Shurin CL -0.70 -0.45, Fig. 1). food webs, to be large the impact tends relative on of predators to their effects on In terrestrial herbivores

log response = -0.49, log ratio

Previous

observations and than bird

in shaded abundances

that arthropod rather canopy

the crop 1997,

et al. 1996, Greenberg bird pr?dation compared for three agroforestry

layer Jedlicka

are greater and (Wunderle et al. and 1) crop

2006).

in the canopy studies (Table

layers in Mexico

(Philpott et al. 2004, Perfecto et al. 2007) and

in

932 SUNSHINE

A. VAN

BAEL

ET AL.

Ecology, the "winter" result

Vol.

89, No. we

Guatemala

et al. Birds reduced (Greenberg 2000). ? ? abundance 11.4% and 4.5% by 46.1% arthropod / in canopy 6.4% and coffee layers, respectively (paired = = The trend was marginally test, t2 4.7, P 0.02).

migratory

that the relatively high density of birds and

tional of arthropods will reductions in arthropod we would expect because a

birds. During

months

expect

low

abundance

vs. 24.3% ? 36.7% t test, i2= 2.10, [mean ? SD], paired = P recent studies in tropical forests 0.08). Similarly, on have demonstrated that bird effects pr?dation than canopy are Bael and (Van 2005) greater understory on reproductive trees than saplings and Marquis (Boege the small number of studies in agroforestry 2006). Thus, conspecific greater and Brawn systems bird and forests and (e.g., of show a consistent pattern of greater effects in the canopy. layers differ in plant understory/crop structural suit productivity, complexity, for trees are in the

for large (>5 mm) arthropods (70.7% ? 7.0% significant

in large propor the abundance. During reduced birds are proportional less common the

"summer" reduction and

of arthropods, are more arthropods studies

abundant. systems support

Exclosure

in agroforestry

>5 that the standing crop of arthropods proposition mm are present in length is reduced more when migrants than when significant reflecting arthropods: they are absent. We interpret the larger and as effect in the larger size class of arthropods the fact that birds may not prefer very small

Canopy qualities ability

and environmental herbivores) We that birds suggest (e.g., qualities light, moisture). their foraging in the canopy be focusing because may result greater levels of plant productivity and/or quality et al. in greater abundances arthropod (e.g., Oksanen foliage in agroforestry systems, the canopy example, or one a consists of few pioneer layer generally species rates and productivity selected for their high growth 1981). For coffee 1997), while (Pennington derived from forest understory have slower growth rates, output, and tough, long-lived These life-histories contrasting abundances greater arthropod crop and cacao or cultivars shrubs are that saplings low photosynthetic et al. 2001). foliage (Matta lead to the expectation in the canopy than

those that constitute the largest share of to 5 mm total arthropods (Gr?ner 2004). The restriction on the range of prey and above focuses the analyses taken by birds, but should not be confused commonly an analysis For allowing six of the very we studies, direct for largest prey used had data from both comparisons. The

with

breeding. seasons,

reduction (mean ? SD) of large (>5 mm) arthropods by

were when greater significantly migrants were ? to relative when absent present (35.8% they = = ? 25.3%, vs. 23.8% 25.9% i5 3.39, P 0.0\). However, no significant difference was found for percent reduction birds was with for the season 12.0% ? 24.1% arthropods ? and the season 10.8% 19.9% for migrants = = to without migrants P If the 0.16, (/5 0.44). degree of total with which crop of arthropods standing indicator of the potential for food from is a season by is reduced limitation, is a good then the

pair-wise

relatively

of the

be ideal settings systems would layer. Agroforestry to for future exclosure fertilization experiments using to and quality in order manipulate plant productivity further canopy. Seasonality Insectivorous double with in the magnitude of bird pr?dation effects may at a explore why bird effects are greater in the

prediction the winter is supported

the breeding currency of greater potential these comparisons. between and bird effects,

that hypothesis food limitation

Relationships

richness,

abundance agroforests showed that

bird populations the influx of migrants

in the Neotropics from the North

A the

comparison effects of were and

of two coffee birds greater than on

time of year when

abundance is thought to be arthropod low (September-April; late rainy and dry seasons). Both the diversity and abundance of insectivorous is migrants

herbivores density fewer birds

experimentally in a farm with in a neighboring

introduced bird higher farm with

diversity (Perfecto

them systems, making particularly high in agroforestry ideal locations for assessing food limitation for migra resources are in tropical If food tory birds systems. in tropical then from communities, limiting breeding to support where does the surplus arise this influx of The breeding holds that currency hypothesis migrants? birds are limited by the abundance of specific breeding food types (large herbivorous insects such as Lepidop tera and Orthoptera, 1 cm or greater in length) usually required Johnson birds food with of are for et al. successful 2005). 1995, breeding (Greenberg the nonbreeding season, During total arthropod abundance. The to migrants two limits, insects, support are such set by the that habitats

et al. 2004). Comparing pr?dation limited evidence only in two farms, however, provides for the importance of predator in predatory diversity our gradient function. Across of nine sites, we found that species richness correlation and large strongest of migratory with percent arthropods birds showed of the all reduction

arthropods were weaker reduction percentage 0.07), and 0.05). and

(Fig. 1). Correlations for species richness of all birds (vs. percent ? vs. in all arthropods, R2 = 0.55, P 0.02; reduction in large arthropods, R2 = 0.44, P = correlations between were resident not bird richness (P > reductions significant

arthropod

limited

resources

by available

difference

between

these

few large herbivorous total arthropods should

but high abundance a greater influx of

of all, per Species density (species sample) or resident bird species did not correlate with migrant, total or large arthropod reductions (P > 0.05); nor did or bird density of all, migrant, per (individuals sample) resident bird species.

April 2008
These ship bird results

AGROFORESTS AS MODEL
of a relation striking evidence provide and migrant bird effects on arthropods this but the mechanisms underlying further study. The influence of diversity the top-down the levels, but are matters of

SYSTEMS FOR ECOLOGY 933

number arthropod differences omnivores differences of species, reductions? but Future not density, correlate that to

between richness,

relationship

deserve

analyses in the proportion of vs. in migrant resident and or

incorporate and insectivores assemblages, or of birds

may assemblages predator on lower effects of predators trophic direction and intensity of these effects 2007). For

may

active debate in the literature(Sih et al. 1998, Schmitz

by a suite of predator example, pr?dation at decreased herbivore densities natural popula species than a single tions and increased yields more plant et al. 2003).

energy requirements the observed relationships. change in agroforestry studies systems Carefully replicated and the effects of diversity could isolate potentially influence habitat complexity Conclusions Agroforestry and systems to examine and these hypotheses.

in sizes

recommendations

Other alone (Cardinale species of predator can that predator demonstrated diversity examples of increased control because reduce top-down intraguild and Denno and interference pr?dation (e.g., Finke studies of predator 2004). Most diversity experimental a very small number in of arthropod involve species or series small-scale additive replacement designs an important contri 2007). Our study makes (Schmitz bution to this literature a suite focused includes in at least on three ways. predators First, we past investigate work has our data than past arthropod birds do providing diversity of vertebrate exclusively where

complexity to conduct

predator recent work where

of habitat gradients and provide the ability that manipulate large-scale experiments areas effects and nutrient input. We highlight present species diversity, in coffee and cacao systems can be

to basic the impor about applied ecological questions season tance of vegetation habitat strata, complexity, multi of and for the diversity strength ably, predator could interactions. Coffee and cacao systems trophic also be exploited to address additional concerning plant To interactions. examined nutrients coffee the and plants and the and cacao of quality, productivity our knowledge, no effects pr?dation systems prey as both It has of factorial in these questions and multi-trophic have experiments combinations systems. Moreover, of

V /7/" /

a greater range diversity where studies Finally, (from 3 to 11 species). consume each other, commonly predators thus clearer se. a and dynamics simplifying trophic view of the effects of predator

arthropods. in predator

Second,

V/

not, per

provide

diversity introduced crops, new world. may

to study opportunities on and native assemblages crops are grown in the old that exotic hypothesized lower specialist

a natural in systems provide gradient Agroforestry to examine the relative impact of predatory which guilds of The downside with varying diversity and abundance. this natural manipulation, however, at the sites may also of insectivores complexity. data from between sion. There are several and reduc relationship positive suite tion of arthropod abundance. First, a more diverse more consume kinds of prey of predator species may or by microhabitats or in species. Alternatively, consuming more diverse bird assemblages, is greater that the chance et al. very efficient insectivores will be present (Perfecto species, either by foraging more individuals are are abundances baseline arthropod larger where to a and a greater diversity of birds is attracted for this found no evidence base. We larger resource and relationships possibility: density (for all birds, migrants, at abundance baseline arthropod between and the bird rich residents) sites were to be in more possible between explanations bird richness for this Without each examining site, we cannot bird diversity co-vary is that the diversity with habitat

been

but greater initially have but that herbivore generalist species after introduction, more exotics accumulate species eventually specialist et al. 1984, Andow and Imura 1994). Finally, (Strong our

that habitat complexity is driving the tightrelationship

migrant and arthropod suppres

comparable vegetation rule out the possibility

between and forests tropical agroforests comparison a gap future in the ecological literature: highlights exclosure of studies can be strengthened by replication in complex, systems. tropical experiments Acknowledgments authors thank E. Herre, E. G. Leigh, Jr., and two and I. reviewers for comments on the manuscript, anonymous Perfecto for sharing unpublished data. This work was to S. A. Van IRFP Grant # OISE-0401957 supported by NSF to I. Perfecto, R. S. Green Bael, NSF Grant #DEB-9981526 to and EPA STAR #FP91648501 berg, and G. Ibarra-Nu?ez, The

I?77
r tr

4"'

N.

2004). An additional possibility is thatpr?dation effects

greater,

A. Barber. K. A. Mooney received support from the Sciences. School of Biological University of California-Irvine This is contribution number Marine Lab, 2376, Bodega University of California-Davis. Literature Cited

Andow,

alternative ness and

(P > 0.05 for all correlations). nonsignificant additional Our stimulates questions analysis approached with but not more resident reductions? data. bird For migrant with arthropod

example, why does richness correlate species why does the

Furthermore,

115:559-572. for herbivores and plants. Oikos R. R., J. A. Collazo, J. Groom. 2006. and M. Borkhataria, Additive effects of vertebrate predators on insects in a Puerto Rican coffee plantation. Ecological Applications 16:696-703. B. J., C. T. Harvey, K. Gross, and A. R. Ives. 2003. Cardinale, emergent impacts of a multi Biodiversity and biocontrol:

1994. Specialization of phytophagous arthropod communities on introduced plants. Ecology 75:296-300. and R. J. Marquis. and 2006. Plant quality Boege, K., risk mediated pr?dation by plant ontogeny: consequences A.,

D.

and

O.

Imura.

934 SUNSHINE

A. VAN

BAEL

ET AL.

Ecology,

Vol.

89, No.

on pest suppression and crop yield in an enemy assemblage agroecosystem. Ecology Letters 6:857-865. J., and J. Lartigue. 2004. Patterns of herbivory and Cebrian, in aquatic and terrestrial ecosystems. decomposition ical Monographs 74:237-259. Ecolog

D. L., and R. F. Denno. 2004. Predator diversity dampens trophic cascades. Nature 429:407-410. and R. F. Denno. shift from 2003. Seasonal Gratton, C, to top-down insect bottom-up impact in phytophagous 134:487-495. populations. Oecologia Finke,

Mooney, K. A., and Y. B. Linhart. 2006. Contrasting cascades: insectivorous birds increase pine but not parasitic mistletoe growth. Journal of Animal Ecology 75:350-357. 1981. and P. Niemela. L., S. Fretwell, J. Arruda, Oksanen, ecosystems in gradients of primary productivity. Exploitation 118:240-261. American Naturalist 1997. The genus Inga. Continental Printing, Pennington, T. D. Brussels, Belgium. S. M. Philpott, L. Soto-Pinto, and Perfecto, I., I. Ambrecht, T. V. Dietsch. 2007. Shaded coffee and the stability of in Latin America. in T. rainforest margins Pages 227-264 and A. Tscharntke, C. Leuschner, M. Zeller, E. Guhadja, Bidin, editors. The stability of tropical rainforest margins, economic, and social constraints of land linking ecological, use and conservation. Springer, New York, New York, USA. Perfecto, Voort. and M. I., R. A. Rice, R. Greenberg, 1996. Shade coffee: a disappearing 46:598-608. biodiversity. BioScience G. L. Bautista, Perfecto, I., J. H. Vandermeer, E. Van refuge

Greenberg, R. 1995. Insectivorous migratory birds in tropical the breeding currency hypothesis. Journal of ecosystems: Avian Biology 26:260-263. R. Perez, Greenberg, R., P. Bichier, A. C. Ang?n, C. MacVean, and E. Cano. 2000. The insectivory on impact of avian in some Guatamalan and leaf damage coffee arthropods plantations. Greenberg, Ecology 1997. Bird and J. Sterling. R., P. Bichier, in rustic and planted shade coffee plantations populations 29:501-514. of eastern Chiapas, Mexico. Biotropica 81:1750-1755.

der for

Greenberg, pasture 682.

1994. Interspecific defense of R., and J. S. Ortiz. trees by wintering Yellow Warblers. Auk 111:672

of top-down and bottom-up Gr?ner, D. S. 2004. Attenuation forces in a complex terrestrial community. Ecology 85:3010 3022. 2001. Terrestrial J., and D. H. Wise. Halaj, trophic cascades: how much do they trickle? American Naturalist 157:262-281. Hedges, L. V., J.Gurevitch, and P. S. Curtis. 1999. The meta analysis of response ratios in experimental ecology. Ecology 80:1150-1156. and M. Hulot, F. D., G. Lacroix, F. O. Lescher-Moutoue, re Loreau. 2000. Functional diversity governs ecosystem sponse to nutrient enrichment. Nature 405:340-344. I. Perfecto, S. M. Philpott, and Jedlicka, J. A., R. Greenberg, T. V. Dietsch. 2006. Seasonal shift in the foraging niche of a at work? resident: resource competition tropical avian

140-149. Polis, G. A., and D. R. Strong. 1996. Food web complexity and 147:813-846. community dynamics. American Naturalist 2000. Cacao cultivation and the Rice, R. A., and R. Greenberg. conservation of biological diversity. Ambio 29:167-173. Schmitz, O. J. 2007. Predator diversity and trophic interactions. Ecology 88:2415-2426. 2000. and A. P. Beckerman. Schmitz, O. J., P. A. Hamback, Trophic cascades in terrestrial systems: A review of the effects 155: of carnivore removals on plants. American Naturalist 141-153. Shurin, J. B., E. T. Borer, E. W. Seabloom, K. Anderson, C. A. and B. S. Halpern. Blanchette, B. Broitman, S. D. Cooper, 2002. A cross-ecosystem of the strength of comparison trophic cascades. Ecology Letters 5:785-791. 1998. Emergent impacts Sih, A., G. Englund, and D. Wooster. on prey. Trends and in Ecology of multiple predators

G. Ibarra 2004. P. Bichier, and S. Langridge. Nunez, R. Greenberg, Greater pr?dation in shaded coffee farms: the role of resident neotropical birds. Ecology 85:2677-2681. Philpott, S. M., R. Greenberg, P. Bichier, and I. Perfecto. 2004. Impacts of major predators on tropical agroforest arthro 140: pods: comparisons within and across taxa. Oecologia

Journal of Tropical Ecology 22:385-395. Johnson, M. D., T. W. Sherry, A. M. Strong, and A. Medori. 2005. Migrants in Neotropical bird communities: an assess ment of the breeding currency hypothesis. Journal of Animal Ecology 74:333-341.

R. J., and C. Whelan. 1996. Plant morphology, Marquis, recruitment of the third trophic level: subtle and recognized defenses? Oikos 75:330-334.

and little

F. M., R. A. Loos, R. Rodriguez, and R. S. Barros. Matta, rates of tropical 2001. Actual and potential photosynthetic 13:24-32. crop species. Revista Brasileira Fisiolog?a Vegetal 1999. Biodiversity conservation P., and V. M. Toledo. Moguel, in traditional coffee systems of Mexico. Conservation

13:11-21. Biology Mols, C, and M. Visser. 2002. Great tits can reduce caterpillar in apple orchards. Journal of Applied Ecology 39: damage 888-899.

forests. Oecologia 143:106-116. J.M., and S. C. Latta. in 1996. Avian abundance Wunderle, sun and shade coffee plantations and remnant pine forest in the Cordillera Central, Dominican Ornithologia Republic. 7:19-34. Neotropical

Evolution 13:350-355. 1984. Insects Strong, D. R., J. H. Lawton, and R. Southwood. on plants: community patterns and mechanisms. Harvard USA. University Press, Cambridge, Massachusetts, 2007. Van Bael, S. A., P. Bichier, I. Ochoa, and R. Greenberg. Bird diversity in cacao farms and forest fragments of western Panama. Biodiversity and Conservation 16:2245-2256. Van Bael, S. A., and J.D. Brawn. 2005. The direct and indirect effects of insectivory by birds in two contrasting Neotropical

APPENDIX A
Supplementary methods diversity effects (Ecological for literature search, Archives E089-053-A1). study selection, effect size calculations, and analyses of bird pr?dation and

APPENDIX B
A table describing bird exclosure studies included inmeta-analysis (Ecological Archives E089-053-A2).