Bird and bat predation services in tropical forests and agroforestry landscapes

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Title
Bird and bat predation services in tropical forests and agroforestry landscapes.
Permalink
https://escholarship.org/uc/item/6qh84772
Journal
Biological reviews of the Cambridge Philosophical Society, 91(4)
ISSN
1464-7931
Authors
Maas, Bea
Karp, Daniel S
Bumrungsri, Sara
et al.
Publication Date
2016-11-01
DOI
10.1111/brv.12211

Peer reviewed
eScholarship.org Powered by the California Digital Library
University of California
Biol.Rev.(2015),pp.000–000. 1
doi:10.1111/brv.12211
Bird and bat predation services in tropical
forests and agroforestry landscapes
Bea Maas1,2,∗, Daniel S. Karp3,4, Sara Bumrungsri5, Kevin Darras1, David Gonthier3,6,
Joe C.-C. Huang7,8, Catherine A. Lindell9, Josiah J. Maine10, Laia Mestre11,12,13,
Nicole L. Michel14, Emily B. Morrison9, Ivette Perfecto6, Stacy M. Philpott15,
C¸agan H. S¸ekerciog˘lu16,17, Roberta M. Silva18, Peter J. Taylor19,20, Teja Tscharntke1,
Sunshine A. Van Bael21,22, Christopher J. Whelan23 and Kimberly Williams-Guille´n6,24
1Agroecology,Georg–AugustUniversity,Grisebachstraße6,37077Goettingen,Germany
2DivisionofTropicalEcologyandAnimalBiodiversity,DepartmentofBotanyandBiodiversityResearch,UniversityofVienna,Rennweg14,
1030Vienna,Austria
3TheNatureConservancy,201MissionStreet,4thFloor,SanFrancisco,CA94105,U.S.A.
4DepartmentofEnvironmentalScience,Policy,andManagement,UniversityofCalifornia,MulfordHall,130HilgardWay,Berkeley,CA
94720,U.S.A.
5DepartmentofBiology,FacultyofScience,PrinceofSongklaUniversity,Thailand15KarnjanavanichRd.,HatYai,Songkhla90110,Thailand
6SchoolofNaturalResourcesandEnvironment,UniversityofMichigan,440ChurchStreet,AnnArbor,MI48109,U.S.A.
7DepartmentofBiologicalSciences,TexasTechUniversity,Box43131,Lubbock,TX79409,U.S.A.
8SoutheastAsianBatConservationandResearchUnit,DepartmentofBiologicalScience,Box43131,TexasTechUniversity,Lubbock,TX
79409-3131,U.S.A.
9IntegrativeBiologyDepartment,CenterforGlobalChangeandEarthObservations,MichiganStateUniversity,288FarmLaneRM203,East
Lansing,MI48824,U.S.A.
10CooperativeWildlifeResearchLaboratory,DepartmentofZoology,CenterforEcology,SouthernIllinoisUniversity,1125LincolnDr.,
Carbondale,IL62901,U.S.A.
11CREAF,CarreteradeBellaterraal’Auto`noma,s/n,08193CerdanyoladelVall`es,Barcelona,Spain
12DepartamentdeBiologiaAnimal,deBiologiaVegetalid’Ecologia,UniversitatAuto`noma,CarreteradeBellaterraal’Auto`noma,s/n,08193
CerdanyoladelVall`es,Barcelona,Spain
13DepartmentofEcology,SwedishUniversityofAgriculturalSciences,Box7044,75007Uppsala,Sweden
14SchoolofEnvironmentandSustainability,UniversityofSaskatchewan,117SciencePlace,Saskatoon,SaskatchewanS7N5C8,Canada
15EnvironmentalStudiesDepartment,UniversityofCalifornia,SantaCruz,1156HighStreet,SantaCruz,CA95062,U.S.A.
16DepartmentofBiology,UniversityofUtah,257South1400East,Rm.201,SaltLakeCity,UT84112,U.S.A.
17CollegeofSciences,Ko¸cUniversity,Rumelifeneri,Sariyer34450,IstanbulTurkey
18ProgramadePo´s-Gradua¸ca˜oemEcologiaeConserva¸ca˜odaBiodiversidade,UniversidadeEstadualdeSantaCruz,RodoviaIlh´eus-Itabuna,km
16,45662-900Bahia,Brazil
19SchoolofLifeSciences,UniversityofKwaZulu-Natal,PrivateBagX54001,Durban4000,SouthAfrica
20SARChIChaironBiodiversityValue&ChangeandCentreforInvasionBiology,SchoolofMathematical&NaturalSciences,Universityof
Venda,P.BagX5050,Thohoyandou0950,SouthAfrica
21DepartmentofEcologyandEvolutionaryBiology,TulaneUniversity,6823St.CharlesAvenue,NewOrleans,LA70118,U.S.A.
22SmithsonianTropicalResearchInstitute,ApartadoPostal0843-03092,Balboa,Ancon,RepublicofPanama
23IllinoisNaturalHistorySurvey,c/oBiologicalSciences,UniversityofIllinoisatChicago,845WestTaylorStreet,Chicago,IL60607,U.S.A.
24PasoPacífico,POBox1244,Ventura,CA94302,U.S.A.
ABSTRACT
Understanding distribution patterns and multitrophic interactions is critical for managing bat- and bird-mediated
ecosystem services such as the suppression of pest and non-pest arthropods. Despite the ecological and economic
importance of bats and birds in tropical forests, agroforestry systems, and agricultural systems mixed with natural
* Addressforcorrespondence(Tel:[phone];E-mail:[email protected]).
BiologicalReviews(2015)000–000©2015CambridgePhilosophicalSociety
2 BeaMaasandothers
forest, a systematic review of their impact is still missing. A growing number of bird and bat exclosure experiments
has improved our knowledge allowing new conclusions regarding their roles in food webs and associated ecosystem
services.Here,wereviewthedistributionpatternsofinsectivorousbirdsandbats,theirlocalandlandscapedrivers,and
theireffectsontrophiccascadesintropicalecosystems.Wereportthatforbirdsbutnotbatscommunitycomposition
andrelativeimportanceoffunctionalgroupschangesconspicuouslyfromforeststohabitatsincludingbothagricultural
areasandforests,heretermed‘forest-agri’habitats,withreducedrepresentationofinsectivoresinthelatter.Incontrast
to previous theory regarding trophic cascade strength, we find that birds and bats reduce the density and biomass of
arthropodsinthetropicswitheffectsizessimilartothoseintemperateandborealcommunities.Therelativeimportance
ofbirdsversusbatsinregulatingpestabundancesvarieswithseason,geographyandmanagement.Birdsandbatsmay
evensuppresstropicalarthropodoutbreaks,althoughpositiveeffectsonplantgrowtharenotalwaysreported.Asboth
batsandbirdsaremajoragentsofpestsuppression,abetterunderstandingofthelocalandlandscapefactorsdriving
thevariabilityoftheirimpactisneeded.
Key words: agricultural landscapes, arthropod suppression, bird and bat ecology, cacao, coffee, ecosystem services,
exclosureexperiments,flyingvertebrates,foodwebs,pestsuppression.
CONTENTS
I. Introduction ................................................................................................ 3
II. Methods .................................................................................................... 4
(1) Datasourceandpreparation ........................................................................... 4
(2) Birdandbatspeciesrichnessandendemismperbiogeographicregion ................................ 4
(3) Mappingfeeding-guilddistributionsofbirdsandbats ................................................. 4
(4) Birdandbatspeciesrichnessandfeedingguildsperhabitat ........................................... 5
(5) Effectsizesofbird/batexclosurestudiesondifferentarthropodgroups ................................ 5
III. Zoogeographyofbirdsandbats – speciesrichnessandfunctionaldiversity ................................ 5
(1) Zoogeographyofbirdsandbats – speciesrichness .................................................... 5
(2) Zoogeographyofbirdsandbats – feedingguilds ...................................................... 5
(3) Birdsandbatsindifferentland-usesystems ............................................................ 6
IV. Effectsonfoodwebs ........................................................................................ 7
(1) Birdandbateffectsonarthropodsandplantsintropicalcommunities ................................. 8
(2) Factorsinfluencingtropicaltrophiccascadestrength .................................................. 8
(a) Insectivoreidentity ................................................................................ 8
(b) Insectivoreforagingstrategy ....................................................................... 9
(c) Insectivorediversityandabundance ............................................................... 10
(d) Presenceofmigratorybirds ........................................................................ 10
(e) Intraguildpredation ............................................................................... 10
(f) Herbivorediversity ................................................................................ 11
(g) Productivity ....................................................................................... 11
(h) Plantontogenyanddefences ...................................................................... 11
(i) Naturalversusagriculturalsystems ................................................................ 11
V. Birdandbatservicesinagriculturalsystems ................................................................ 11
(1) Birdandbatpredationintropicalagroforestry ........................................................ 11
(2) Seasonaldifferences .................................................................................... 12
(3) Zoogeographicpatterns ................................................................................ 12
(4) Effectsonleafdamageandcropyield .................................................................. 12
(5) Pollinationservicesandcropyield ..................................................................... 13
VI. Localandlandscape-managementeffects .................................................................. 13
(1) Localeffectsonpredatoryfunction .................................................................... 13
(2) Landscapeeffectsonpredatoryfunction ............................................................... 13
(3) Driversoflocalandlandscapeeffects .................................................................. 14
VII. Knowledgegapsandneedforfurtherstudies ............................................................... 14
VIII. Managementofbirdandbatecosystemservices ........................................................... 16
IX. Conclusions ................................................................................................ 16
X. Acknowledgements ......................................................................................... 17
XI. References .................................................................................................. 17
XII. SupportingInformation .................................................................................... 21
BiologicalReviews(2015)000–000©2015CambridgePhilosophicalSociety
Ecosystemservicesprovidedbytropicalbirdsandbats 3
I. INTRODUCTION precipitation; breeding cycles; presence of latitudinal
effects and migrants) and the broader landscape context.
Agricultural expansion and land-use intensification now Fortunately, community-wide manipulation experiments
typify landscapes globally (Melo etal., 2013; Laurance, (e.g. experimental exclosures) can be readily used to
Sayer & Cassman, 2014), representing a serious threat to identify the complex interactions between vertebrates and
biodiversity and ecosystem processes (Flynn etal., 2009). invertebrates that affect ecosystem services. In such studies,
Maintaining ecosystem services – the benefits that nature plants are enclosed in mesh nets that prevent access to
provides to humanity – is more important than ever as foraging birds and bats while remaining accessible to
demand for food, fuel, fibre and other biological products arthropods.Therelativeimpactsofbird-andbat-mediated
grows (Millennium Ecosystem Assessment, 2005), and predation on arthropod communities can then be isolated
Earth’s climate changes (McShane etal., 2011; Urban, through deploying exclosures either during the day (to
Zarnetske&Skelly,2013). exclude only birds), at night (to exclude only bats and
Birdsandbatsprovidemanyimportantecosystemservices night-active birds), or throughout the daily cycle to assess
such as the suppression of insect pests, seed dispersal, and jointimpactsofbirdsandbats.Untilrecently,onlythelatter
pollination (Whelan, Wenny & Marquis, 2008; Kunz etal., method was used in exclosure studies, with investigators
2011; S¸ekerciog˘lu, Wenny & Whelan, 2016). It is hard to attributing changes in arthropod density and plant damage
overstatetheeconomicimportanceoftheservicesrendered exclusively to birds (Marquis & Whelan, 1994; Greenberg
by these taxa (e.g. Cleveland etal., 2006; Boyles etal., 2011, etal.,2000b;Johnson,Kellermann&Stercho,2010)andnot
2013). In particular, the suppression of pest insects by to bats (e.g. Kalka & Kalko, 2006; Williams-Guille´n etal.,
birds and bats in tropical agroforestry systems facilitates 2008;Kunzetal.,2011).
substantialincreasesincrop yields(Karp etal.,2013; Maas, In recent years, however, several exclosure experiments
Clough & Tscharntke, 2013) and may serve as a viable have demonstrated that both birds and bats significantly
alternative to pesticides and other chemical compounds constrainarthropodpopulations,yetmajorknowledgegaps
(e.g. Bianchi, Booij & Tscharntke, 2006; Clough, Faust persist.Forexample,fewstudieshaveaddressedtheinfluence
& Tscharntke, 2009b). Biodiversity-friendly management oflocalandlandscapemanagementonpestcontrol,aswell
of tropical farming landscapes thus provides a promising astheultimateeffectofbirdandbatpredationoncropyields
conservation strategy while enhancing human well-being (Kellermann etal., 2008; Johnson etal., 2010; Karp etal.,
through support of food security and ecosystem resilience 2013; Maas etal., 2013), hampering the design of targeted
(Fischer, Lindenmayer & Manning, 2006; Tscharntke etal., service management. In addition, study sites have been
2012a). biased, with the Paleotropics underrepresented (Maas etal.,
However, the impact of insectivorous birds and bats on 2013)comparedtotheNeotropics(e.g.VanBael&Brawn,
arthropodcommunities,plantproductivityandyieldaswell 2005; Kalka, Smith & Kalko, 2008; Williams-Guille´n etal.,
as the underlying taxonomic and functional drivers, are 2008;Morrison&Lindell,2012;Karpetal.,2013).
highlyvariableandtheexistingknowledgeisstillunbalanced Here, we compare arthropod suppression services of
and limited. Insectivorous birds and bats consume a wide insectivorous birds and bats in tropical forest, agroforestry
variety of arthropods: not only herbivorous pests (e.g. systems, and agricultural systems mixed with natural forest
S¸ekerciog˘lu, 2006a; Whelan etal., 2008; Kunz etal., 2011; (herereferredtoasforest-agrisystems),focusingonagrowing
Morrison & Lindell, 2012; Taylor etal., 2013a) but also numberoflandscape-scaleexclosureexperiments.Through
predatoryarthropods,suchasantsandspiders(e.g.Mooney comprehensive review and discussion of previous results,
&Linhart,2006;Gunnarsson,2007).Therefore,whilebirds we describe trophic interactions among birds, bats and
and bats often improve crop yields directly by consuming arthropods, the importance of environmental factors and
herbivorous insects, they may at times depress crop yields biogeographic patterns in relation to vertebrate ecosystem
through feeding as intraguild predators (consuming both functions,andaddressexistingresearchgaps.Weconducted
intermediate predators and herbivores). Whether birds and a comprehensive literature search as well as a focused
bats will ultimately suppress herbivores and contribute to solicitationfromcolleaguesforstudiesfocusingontheroleof
yieldproductivitylikelydependsonspecificfunctionaltraits birdsand/orbatsinregulatingarthropodcommunities.Our
(Philpottetal.,2009)aswellasonfactorssuchasgeographic search yielded 32 publications in which exclusions of birds
distribution (Olson etal., 2001), seasonality (e.g. Erickson andbatswereusedtoquantifytheeffectsofflyingvertebrate
& West, 2002; Williams-Guille´n, Perfecto & Vandermeer, predationondifferentarthropodgroups.Thesepublications
2008;Singeretal.,2012;Taylor,Monadjem&Steyn,2013b), provide the basis for our discussions of birds and bats in
landscapecontext(e.g.Fahrigetal.,2011),andlocalhabitat tropical agroforestry systems (i.e. coffee, cacao, and mixed
structure or management regimes (e.g. Rice & Greenberg, fruit orchard) and forests, combining both prominent and
2000; Loeb & O’Keefe, 2006; Bhagwat etal., 2008; Maas newpublicationsonbirdandbatecosystemservices.
etal.,2009). In Section III, we provide an overview of zoogeographic
Managing bird- and bat-mediated ecosystem services patterns of bird and bat species and their functional
thus requires thorough understanding of multitrophic diversity (feeding guilds, habitat affiliations). Section IV
interactions, seasonal patterns (e.g. resource availability; unravels general effects of birds and bats on arthropod
BiologicalReviews(2015)000–000©2015CambridgePhilosophicalSociety
4 BeaMaasandothers
food webs and plants via trophic cascades and discusses the (3) Mappingfeeding-guilddistributionsofbirds
factors modulating these top-down effects. The importance andbats
of predation services in diversely managed agricultural
Bird data were taken from a database with standardized
landscapes and tropical communities, with particular
entries on the ecology of the bird species of the world. See
focus on the economic importance of birds and bats, is
S¸ekerciog˘lu etal. (2004) and S¸ekerciog˘lu (2012) for further
discussed in Section V. Existing evidence for local and
details.BatdatawerebasedondietdatamainlyfromIUCN
landscape-management effects on bird and bat predatory
andtheAnimalDiversityWeb(bothretrievedinMay2014),
functions is described in Section VI. Finally, in Sections
except for 14 species whose diet was retrieved from other
VII and VIII, we point out existing knowledge gaps
scientificpublications.
and highlight the potential for bird- and bat-mediated
Feeding-guilddataforbirdsandbatswereadaptedtobe
arthropod suppression to contribute to food security and
comparablebetweenthetwogroups.Allbatdietdatawere
improved landscape management in the tropics, with
enteredintoanAccessdatabase.Forbatspecies-richgenera,
important implications for future biodiversity conservation
when diet was unequivocal and consistent for multiple
and research. Together, our conclusions contribute to both
species, the remaining species were assigned the same diet
a practical and theoretical framework for the study and
(e.g.Rhinolophusinsectivores).Forty-twospecieshadunknown
management of tropical landscapes affected by ongoing
diets. Each bat was then assigned to one feeding guild (see
agriculturalexpansionandbiodiversityloss.
below), depending on its main diet, which could comprise
multiple items (e.g. insects and fruits). Bats were classified
into the omnivorous guild whenever their diet comprised
II. METHODS plantandanimalmatter.
Bird feeding guilds from S¸ekerciog˘lu etal. (2004) were
(1) Datasourceandpreparation adaptedtobecomparablewithbats:thevertebrate-feeding
guild was obtained by merging vertebrate-, scavenger, and
Quantum Gis 2.6 (QGis) was used for all Geographic
fish-feeding guilds, the plant-feeding guild was obtained
Information System (GIS) operations. Bird data were
by merging the fruit- and plant-feeding guilds (see below).
taken from a database with standardized entries on the
Note that omnivorous birds only belonged to that guild
ecology of the bird species of the world. See S¸ekerciog˘lu,
when no clear main diet could be found, which is different
Daily & Ehrlich (2004) and S¸ekerciog˘lu (2012) for further
from bats. Therefore the omnivorous bird guild is slightly
details. For bats, the terrestrial mammals shapefile was
underestimated in birds – or the bat omnivorous guild
downloadedfromtheInternationalUnionforConservation
overestimated – andbotharenotdirectlycomparable.
of Nature and Natural Resources (IUCN) Red List website
Feeding guilds were defined as follows: (i)
(in May 2014); records not pertaining to Chiroptera were
invertebrate-feeding guild (only arthropods for bats).
deleted. Records with presence codes different from 1
(ii)Vertebrate-feedingguild(includingavianscavengers,fish
and 2 (extant and probably extant, respectively), and with
predators and blood-feeding bats). (iii) Omnivorous birds
seasonalcodes differentfrom1, 2 and3 (resident,breeding
andbats[seeS¸ekerciog˘luetal.(2004)andS¸ekerciog˘lu(2012)
seasonandnon-breedingseason,respectively),weredeleted.
fortheomnivorousguilddefinitionofbirds;omnivorousbats
The separate bat distribution polygons were merged into
were defined as feeding on both plant and animal matter].
multipart polygons for each species, to yield our bat
(iv) Seed-feeding guild (only birds). (v) Fruit-, leaf-, flower-
distributionlayer.Thelandmasspolygonlayerwasobtained
and bark-feeding birds and bats. [This class was largely
fromhttp://www.naturalearthdata.com.Thebiogeographic
dominated by fruit-feeding species. Eighty percent of the
realms were drawn by hand in QGis based on the realms
world’splant-feeding(nectarandseedsexcluded)birdsfeed
defined by Olson etal. (2001). The tabular IUCN Red List
on fruit; the remaining 20% feed on plant parts other than
dataonChiroptera,incorporatingfulltaxonomicdata,were
seeds, fruit, or nectar. Ninety-two percent of plant-feeding
downloadedandimportedintoaMicrosoftAccessdatabase.
bats (nectar excluded) feed on fruit, the remaining 8% feed
onleaves,flowers,andbark].(vi)Nectar-andpollen-feeding
(2) Birdandbatspeciesrichnessandendemismper
birdsandbats.
biogeographicregion
To generate the world map for both birds and bats (see
Bird data were updated from S¸ekerciog˘lu etal. (2004) and Fig. 1), we calculated percentage proportions of feeding
S¸ekerciog˘lu (2012), with new ornithological data published guildsandtotalrichnessnumbersforeachrealm.Forbirds,
until 2014. For bats, spatial queries between the IUCN bat thelatterwereexportedfromthebirddatabase.Togenerate
distributiondata(IUCN,2015)andthebiogeographicrealms these numbers for bats, the table from the bat database
layers(followingOlsonetal.,2001)weremadetodetermine (containingfeedingguilddata)wasjoinedwiththeattribute
batspeciesrichnessandnumberofendemicspeciesineach table of the terrestrial mammals shapefile (IUCN, 2015),
region: each realm’s polygon was intersected with the bat linkedbySpeciesID.Thebatlayerwasthenspatiallyjoined
distribution layer to find the total species richness, and the with the realms layer, and the sum was output, allowing us
number of bat polygons contained exclusively within each tocountthenumberofbatspeciesperfeedingguildineach
realmwascountedtoderivetheendemicspeciesrichness. realm. Finally, feeding guilds and total species richness of
BiologicalReviews(2015)000–000©2015CambridgePhilosophicalSociety
Ecosystemservicesprovidedbytropicalbirdsandbats 5
birdsandbatswererepresentedaspiechartswiththeirarea transport of nutrients and energy (Whelan etal., 2008;
proportionaltothespeciesrichnessineachrealm. Kunz etal., 2011). Many studies of both birds and bats
also demonstrate significant arthropod-suppression services
in natural and human-modified habitats. Nevertheless, we
(4) Birdandbatspeciesrichnessandfeedingguilds
know substantially less about the ecological functions and
perhabitat
services of birds and bats in the tropics than we do in the
Species lists of bats were downloaded from the IUCN Red temperatezone.Thereisparticularurgencyinunderstanding
List website (in May 2014), singly for each habitat type, howhuman-drivenchangesintherichness,abundanceand
and imported into the Access database. Forest bats were proportionsofvariousspecieswillaffectecosystemfunctions.
identified as species found in forest. Agricultural bats were Inthissection,wesummarizepatternsofbirdandbatspecies
identifiedasspeciesfoundinagriculturalsystems(arableland, richness and functional diversity in different zoogeographic
pastureland,andplantations).Forest-agribatsweredefined regionsandhabitats.
asspeciesfoundbothinforestandagriculturalsystems.Bird
data are from a database with standardized entries on the
(1) Zoogeographyofbirdsandbats – species
ecology of the bird species of the world, see S¸ekerciog˘lu
richness
etal. (2004) and S¸ekerciog˘lu (2012) for further details. We
classified 6093 tropical bird species based on their most More than a third (3564) of the world’s approximately
preferredthreehabitatslistedinpublishedspeciesaccounts. 10300birdspeciesarefoundonlyintheNeotropics,andan
Thehabitatpreferencesconsideredforthisanalysiswere(i) additional320speciesmigratethereformostoftheyearafter
only natural forest or woodland habitats (‘forest specialists’, breeding in the Nearctic region (S¸ekerciog˘lu etal., 2004).
4574 species), (ii) agricultural areas including agroforests The highest endemic species richness in the Neotropics
but not natural forest or woodland habitats (‘agriculture is followed by the Afrotropics (1671 species), Indomalaya
specialists’303species),and(iii)bothagriculturalareasand including Wallacea (1242 species), Australasia (Australia,
forests/woodlands(‘forest-agribirds,’1216species). PapuaNewGuinea,andsurroundingislands:1019species),
andtemperateandpolarregions(Nearctic,Palearctic,New
Zealand,Antarctica,andsub-Antarcticislands:757species)
(5) Effectsizesofbird/batexclosurestudieson
(Table 1). Only 1% of the world’s bird species (98 species)
differentarthropodgroups
are truly cosmopolitan, found on all continents except
We collected data from 32 exclosure studies on birds Antarctica. Another 150 species are found on most of the
and bats from tropical agroforestry systems (i.e. cacao, continentsintheeasternhemisphere.
coffee, mixed fruit orchard) and forests (seven tropical According to the IUCN Red List data on Chiroptera
countries) to compare effects of predatory birds and bats (IUCN,2015),morethan80%oftheworld’s1232batspecies
on the abundance of herbivorous insects, ants, spiders and (Kunz etal., 2011) are found in the tropics (Australasia,
arthropods in general (see online Table S1). We compare Oceania, Afrotropics, Indomalaya, and Neotropics). Of
mean arthropod abundances in unmanipulated control these, 785 [spatial data from IUCN (2015) for 1133
treatments to experimental exclosures of birds, bats and bat species] occur only in the tropics. The Neotropics
birds+bats. Effect sizes were calculated as the logarithm harbourthemostbatspecies(337),followedbyIndomalaya
of the ratio of insect abundance in the control versus (282), Australasia (270) and the Afrotropics (237, Table 1).
the exclosure, then graphed in R (3.1) with the package No bat species is found in the Antarctic and no bat
ggplot2. species is cosmopolitan (found in all biogeographic realms).
Tropical realms have high percentages of endemic species
(approximately 68–89%), though Indomalaya falls notably
short (approximately 44%), as a consequence of being
III. ZOOGEOGRAPHYOFBIRDSANDBATS –
situatedattheconvergenceofmanyrealms.
SPECIESRICHNESSANDFUNCTIONAL
DIVERSITY
(2) Zoogeographyofbirdsandbats – feedingguilds
As flying vertebrates, bats and birds share several Most avian feeding guilds (often used as a proxy for
characteristics that allow them to provide important functional groups; cf. Philpott etal., 2008) reach their peak
ecosystem services (Fujita & Tuttle, 1991; S¸ekerciog˘lu, richness in the Neotropics (Kissling, S¸ekerciog˘lu & Jetz,
2006a,b; Muscarella & Fleming, 2007; Whelan etal., 2008; 2012; Fig. 1). However, proportionate representation of
Kunz etal., 2011; S¸ekerciog˘lu etal., 2016). Many bat avian feeding guilds varies across biogeographic realms.
and bird species, owing to their capacity for flight, are Insectivores and frugivores have the highest representation
highly vagile and thus capable of moving across complex in the tropics, with frugivores and insectivores being
landscapes, allowing both opportunistic tracking of shifting proportionally lower in the Afrotropics and in Australasia,
food resources (Barber, Marquis & Tori, 2008; Richter & respectively. Seed-eaters are well-represented in drier parts
Cumming, 2008; McCracken etal., 2012) and the linkage of the world, especially in Australasia, the Afrotropics and
of distinct geographic areas through seed dispersal and temperate regions. Nectarivores, on the other hand, reach
BiologicalReviews(2015)000–000©2015CambridgePhilosophicalSociety
6 BeaMaasandothers
Fig.1. Birdandbatspecies’proportionsinthesixlargestfeedingguilds(seeSectionII.3)indifferentbiogeographicrealms(following
Olsonetal.,2001).Thesizeofthepiechartsisproportionaltobird(right)andbat(left)speciesrichnessineachrealm.
Table1. Totalandendemicspeciesrichnessofbirdsandbatslivingonlyinoneregion,foreachbiogeographicrealm(following
Olsonetal.,2001)
Biogeographic Totalbat Endemicbat Totalbird Endemicbird
realm speciesrichness speciesrichness speciesrichness speciesrichness
Afrotropics 237 211(89%) 2079 1671(80%)
Australasia 270 185(68%) 1399 1019(73%)
Indomalaya 282 124(44%) 1982 1242(63%)
Neotropics 337 255(75%) 3996 3564(89%)
Nearctic 94 12(13%) 689 173(25%)
Oceania 14 10(71%) 375 261(70%)
Palearctic 155 41(26%) 1160 349(30%)
BirddatafromS¸ekerciog˘luetal.(2004)andS¸ekerciog˘lu(2012),updatedwithnewornithologicaldatapublisheduntil2014.Batdatafrom
IUCNRedListmammaldata(IUCN,2015).
their highest proportions in the Neotropics (home of the Australasia. Overall, herbivorous bats, the great majority
hummingbird radiation), the Pacific Ocean islands, and of which are frugivorous, outweigh nectar-feeding bats
Australia. Scavengers (vertebrate-feeding guild) reach their in species number. The Neotropics represents the most
highest species richness in the savannas of eastern Africa. speciose realm (Table 1), and harbours by far the majority
Finally,piscivores(fish-eaters),carnivores(birdsofprey),and ofomnivorousbatspecies(56)andthelowestproportionof
herbivoresarebetterrepresentedinthetemperatezonethan invertebrate-feedingbats(approximately56%,species-poor
Oceania excluded). Bats overall have fewer feeding guilds
inthetropics.
thanbirds,withnoplant,seed,non-arthropodinvertebrate,
All bat communities are dominated by the invertebrate-
orcarrionspecialists.
feeding guild, comprised almost exclusively by insectivores
(Fig. 1). The Palearctic has the highest proportion of
insectivores but not the highest number of insectivorous (3) Birdsandbatsindifferentland-usesystems
species. As with birds, the species richness of fruit and Although few bird species prefer agricultural areas for
nectar-feeding bats peaks in the tropics. Indomalaya and feeding, breeding, and other activities, nearly a third of all
the Afrotropics have higher proportions of nectar and birdspeciesoccasionallyusesuchhabitats(S¸ekerciog˘luetal.,
fruit-feeding guilds than temperate realms, but distinctly 2007), especially in combination with forests (S¸ekerciog˘lu,
belowtheproportionsfoundintheNeotropics,Oceania,and 2012;Fig.2).Comparedtoprimaryforests,speciesrichness
BiologicalReviews(2015)000–000©2015CambridgePhilosophicalSociety
Ecosystemservicesprovidedbytropicalbirdsandbats 7
reservesandforestfragmentsweredetectedatleastoncein
agriculturalhabitats(Mendenhalletal.,2014).
Across all habitat types, bat communities are dominated
by insectivores (more than 60% of species) and frugivores
(morethan20%).Itshouldbenoted,however,thatthereare
very few agricultural-specialist bats (bats using agricultural
habitatsbutnotforest;11species),makingitdifficulttodetect
shiftsinfeeding-guildstructureacrosshabitatsanalogouslyto
thoseweobservedforbirds.Apartfromthelossofvertebrate
feeders, bat feeding guilds in forest-agri systems remain
similartoforestbatfeedingguilds.Notethatevidencefrom
the Paleotropics on the representation of different feeding
Fig.2. Feeding-guildcompositionofbirdandbatcommunities guilds in forests and agricultural habitats is limited (e.g.
indifferenthabitats.Totalnumberofspeciesineachhabitatis Furey, Mackie & Racey, 2010; Phommexay etal., 2011; in
indicatedbelowthebars.Forestspecialistsarebirdsthatoccur this review: 26 reports from the Neotropics versus 6 reports
only in forest or woodland habitats. Agriculture specialists are from the Paleotropics listed in Table S1), and additional
birds that occur in agricultural areas including agroforests but investigations are needed to clarify if these results based
notnaturalforestorwoodlandhabitats.Forest-agribirdsoccur
largelyontheNeotropicscanbeappliedelsewhere.
in both agricultural areas and forests/woodland. See Sections
II.3 and II.4 for details of the classification of feeding guilds
andhabitats.ThegraphforbirdsisadaptedfromS¸ekerciog˘lu
(2012),withpermissionofSpringer-Verlag.
IV. EFFECTSONFOODWEBS
In temperate zones, predators affect plant communities
oflargefrugivorousandinsectivorousbirdsoftendeclinesin by consuming herbivores, indirectly influencing plant
agroforests (i.e. coffee, cacao, and mixed fruit orchard), communitycomposition,agestructure,diversity,cropyield,
particularly among terrestrial and understorey species. productivity, and even nutrient cycling (Letourneau etal.,
By contrast, nectarivores, small-to-medium insectivores 2009). Such trophic cascades occur through a decrease in
(especially migrants and canopy species), omnivores, and herbivorous arthropod abundance, reducing their negative
some granivores and small frugivores have higher species effects on plants. Until recently, trophic cascades were
richness in agroforests compared with forest habitats thought to be rare in tropical terrestrial communities as
(S¸ekerciog˘lu,2012). a result of high species richness, including remarkable
Theseglobaltrendsaresupportedbyfieldresearchresults densitiesofinsectivorousbirdsandbats(Polis&Holt,1992;
from Afrotropical (Waltert etal., 2005), Indomalayan (Peh Strong, 1992; Polis & Strong, 1996). In theory, diverse and
etal., 2006), Australasian (Marsden, Symes & Mack, 2006), complexpredator–preyinteractionnetworksshouldcontain
and Neotropical (Leyequien, de Boer & Toledo, 2010) redundancysuchthatthelossofanyindividualpredatorguild
regions. In general, these field studies suggest that the would be compensated by functionally redundant species,
replacement of forests with agricultural systems results in thus preventing a trophic cascade. However, exclosure
ashifttowardsless-specializedbirdcommunities,comprised experimentshavedocumentedthepresenceofinsectivorous
of more-widespread and relatively common species, and bird-andbat-initiatedtrophiccascadesinbothnaturaland
with altered proportions of functional groups (Karp etal., human-dominatedtropicallandscapes(VanBaeletal.,2008;
2011; S¸ekerciog˘lu, 2012; Fig. 2). Specifically, agricultural Mooneyetal.,2010;Ma¨ntyla¨,Klemola&Laaksonen,2011).
systems harbour fewer insectivores and other invertebrate Most exclosure experiments have been conducted in
pest consumers but more seed predators (Tscharntke etal., the Neotropics and the Caribbean (Van Bael etal., 2008),
2008;S¸ekerciog˘lu,2012). although top-down effects on arthropods by birds and bats
Like birds, most bat species live in forests (Fig. 2), and have also been documented in Hawaii (Hooks, Pandey &
about one quarter (246 species) occur exclusively there, yet Johnson,2003;Gruner,2004,2005;Gruner&Taylor,2006),
batsarealsowelladaptedtohumanlandscapes.According Asia(Koh,2010;Maasetal.,2013),Australia(Loyn,Runnalls
toIUCNRedListdata,almostaquarteroftheworld’sbats & Forward, 1983), and Africa (Dunham, 2008). Moreover,
(271 species) use agricultural habitats such as arable land, tropicaltrophiccascadeshavesimilareffectsizesasthosein
pastureland,andplantations(IUCN,2015).Forest–agribat temperateandborealsystems(Mooneyetal.,2010;Ma¨ntyla¨
communities(whichwedefineasbatsoccurringbothinforest etal.,2011;Morrison&Lindell,2012).However,thespecific
andagriculturalhabitats)arealsowellrepresentedwith253 effects of birds and bats on arthropod communities might
species,andhavepreviouslybeenshowntobesuccessfulin notbethesameindifferentregionsbecauseofdifferencesin
coffeeandcacaoagroforestrysystems(Harvey&Villalobos, species richness and specialization, necessitating additional
2007; Williams-Guille´n & Perfecto, 2010). In Costa Rica, research from underrepresented tropical areas such as the
for example, approximately 60% of bats surveyed in forest Paleotropics.
BiologicalReviews(2015)000–000©2015CambridgePhilosophicalSociety
8 BeaMaasandothers
(1) Birdandbateffectsonarthropodsandplantsin Through preventing outbreaks and consuming herbivo-
tropicalcommunities rousarthropods,birdsandbatsoftenindirectlyaffectplants,
although these effects on plants are generally weaker than
Birds and bats generally reduce total arthropod abundance
effectsonarthropodabundances(VanBaeletal.,2008).Plant
and biomass in the tropics (Van Bael etal., 2008; Mooney
damagegenerallyshowsastrongerresponsetobirdandbat
etal.,2010;butseeVanBael,Brawn&Robinson,2003;Van
exclusion than leaf biomass, plant growth, or reproductive
Bael&Brawn,2005;Michel,2012;Fig.3),buttheygenerally
output (e.g. fruit yield; Schmitz, Hamba¨ck & Beckerman,
do not affect arthropod diversity (Mooney etal., 2010; but
2000; Van Bael etal., 2008; Mooney etal., 2010; Ma¨ntyla¨
seeGruner&Taylor,2006).
etal., 2011; Morrison & Lindell, 2012). However, birds and
Bird and bat top-down effects often differ by arthropod
bats do not always protect plants, for reasons that remain
size,withsomeindicationsthatbirds – particularlybreeding
unclear(see,e.g.VanBael&Brawn,2005;Williams-Guille´n
birds – consumelargerarthropodsthanbats.Threestudies
etal., 2008; Morrison & Lindell, 2012; Maas etal., 2013).
have found that the effects of birds and bats combined
reduced large arthropods (>5 or ≥3mm) but not small Notably, leaf damage was actually greater in the presence
of birds and bats outside experimental mammal exclosures
arthropods (<2mm; Greenberg etal., 2000b; Borkhataria,
at La Selva Biological Station in Costa Rica (Michel etal.,
Collazo & Groom, 2006; Van Bael, Bichier & Greenberg,
2014).
2007a). Conversely, Karp & Daily (2014) found that birds
Apotentiallimitationofexclosureexperimentsisthatthey
reducedlargeandsmallarthropodswhilebatsreducedonly
likely underestimate bird and bat effects on arthropods, as
small arthropods, which they attributed to consumption of
many species capture insects in flight, distant from plants
large arthropod larvae by birds but not bats. In Mexico,
(orexclosures)(Kunzetal.,2011).Inaddition,theexclosure
both birds and bats (separately and together) reduced both
mesh size may potentially introduce a bias by hindering
large and small arthropods (Williams-Guille´n etal., 2008).
movement of larger arthropods (e.g. adult lepidopterans);
In Jamaica, birds and bats reduced large arthropods in
fewstudieshaveanalysedsuchcage-inducedsizebiases(Van
summerandautumn,butonlyreducedsmallarthropodsin
Bael & Brawn, 2005; Gunnarsson, 2007; Maas etal., 2013).
thesummer(Johnsonetal.,2009).Thismaybeexplainedby
Nevertheless, studies to date indicate that birds and bats
thebreedingcurrencyhypothesis(Greenberg,1995),which
have strong and pervasive – although variable – effects on
states that breeding resident birds take large arthropods
arthropodsandplantsintropicalcommunities.
suitable for nestlings (‘breeding currency’) during the
breedingseason(springandsummer),whereasintheautumn
Nearcticmigrantsandnon-breedingresidentsconsumemore (2) Factorsinfluencingtropicaltrophiccascade
smallprey. strength
Birdsandbatsoftenreducetheabundanceofleaf-chewing Thestrengthoftop-downeffectsofbatsandbirdsontropical
and phloem-feeding insects (Van Bael etal., 2008; Mooney arthropods and plants can vary substantially. Below, we
etal., 2010), but the extent of limitation of these dominant review insectivore, arthropod, plant, and community traits
pests often varies among study sites (Van Bael etal., 2003; thatcouldaffecttrophiccascadestrengthinthetropics.
Van Bael & Brawn, 2005; Michel, 2012; Michel, Sherry
& Carson, 2014) and insect orders (Van Bael etal., 2007a;
(a) Insectivoreidentity
Williams-Guille´n etal., 2008; Maas etal., 2013). Given the
importance of herbivorous arthropod suppression for plant Early exclosure experiments in tropical communities
communities, including crops, further research into the attributed arthropod suppression and plant effects to
factorsunderlyingspatialandphylogeneticvariationinbird insectivorousbirds,overlookingorminimizingthepotential
and bat predation is encouraged. Moreover, birds and bats effects of gleaning bats, which are abundant in tropical
alsofrequentlylimitnumbersofarthropodpredatorssuchas areas and eat similar types of arthropod prey (Kalka
ants and spiders (Van Bael etal., 2008; Mooney etal., 2010; & Kalko, 2006; Whelan etal., 2008; Kunz etal., 2011).
Mestre etal., 2013; Karp & Daily, 2014; but see e.g. Hooks Nevertheless, the relative impact of birds versus bats on
etal.,2003;Borkhatariaetal.,2006;Maasetal.,2013;Michel the densities of arthropods in general and of specific
etal.,2014;Fig.3),potentiallyreducingtop-downeffectson arthropod groups could vary as a result of differences in
herbivorousinsectdensities(Martinetal.,2013). anatomy,behaviour,andrelativeabundance.Forexample,
While rarely reported, birds and bats may suppress manytropicalherbivorousarthropodsarelargelynocturnal,
arthropodoutbreaksintropicalcommunities.Birdsandbats presumablymakingthemmorevulnerabletobatpredation
inhibitedinvasionbyanintroducedspider(Achaearaneariparia) (Kalka & Kalko, 2006). In Panama, gleaning bats have a
in Hawaii (Gruner, 2005), and were observed consuming larger impact on arthropod abundances and leaf damage
largequantitiesofcaterpillarsduringanoutbreakinPanama than do birds, saving an estimated 52000kg of leaves from
(VanBaeletal.,2004).Moreover,duringanexperimentally herbivoryannually(Kalka&Kalko,2006;Kalkaetal.,2008).
simulatedoutbreak,birdsandbatssubstantiallyreducedthe Other studies have demonstrated broadly similar impacts
abundanceoflepidopteranlarvaeinaMexicanshadedcoffee of birds and bats on arthropods and plants, although
plantation(Perfectoetal.,2004).Theseisolatedexperiments with sometimes differing effects by arthropod clade and
introducethepotentialforwidespreadoutbreaksuppression. season (Williams-Guille´n etal., 2008; Morrison & Lindell,
BiologicalReviews(2015)000–000©2015CambridgePhilosophicalSociety
Ecosystemservicesprovidedbytropicalbirdsandbats 9
Fig.3. Effectsizesofbirdandbatsuppressionofarthropodabundancefordifferentgroupsandstudiesincacaoandcoffeeplantations,
tropical forests and mixed fruit orchards. Effects on arthropods were calculated using log response ratios [LRR=ln(control
mean/exclosuremean)].AmorenegativeLRRindicatesastrongernegativeeffectofpredatoronpreyabundance.Notethatants
werenotsampledinallstudies(nodatadisplayedforrespectivestudyID).Originaldata,studyIDnumbersandadditionaldetails
aregiveninTableS1.
2012). In the Caribbean lowland forest of Costa Rica, Symondson, Sunderland & Greenstone, 2002; Borer etal.,
bat predation effects on herbivorous arthropods exceed the 2005).
effects of birds in areas where insectivorous birds have Thus far we have discussed how birds and bats benefit
declined, suggesting that bats may functionally compensate plants by reducing the density of herbivorous arthropods,
fordecreasingtop-downlimitationofarthropodsprovidedby knownasdensity-mediatedeffects.However,birdsandbats
birds(Michel,2012). may also benefit plants by inducing effects on phenotypic
traits of prey such as mobility, dispersal propensity and
feeding activity (trait-mediated effects; Werner & Peacor,
(b) Insectivoreforagingstrategy
2003). Indeed, trait-mediated effects can involve changes
Batsandbirdspossessuniqueforagingtraitsthatmayaffect in the foraging habits of herbivorous prey, potentially
herbivore suppression, indirect effects on plants, and the causing host shifts that differentially affect plant species
strength of trophic cascades in predator–herbivore food (Calcagno etal., 2011). Even though systematic research
webs(Ke´fietal.,2012).Batstendtobegeneralistpredators, about trait-mediated effects of birds and bats on their
although different foraging strategies (e.g. gleaners versus prey is lacking, it seems that both bats and birds impose
hawkers) might result in different effects on arthropod trait-mediatedeffectsonarthropodswithvaryingimportance
densities (e.g. Kunz etal., 2011). By contrast, gleaning forarthropodsuppressionindifferentsystems.Forexample,
insectivorous birds often have specialized diets and/or ultrasonic bat calls invoke behavioural responses in insects
foraging strategies (Sherry, 1984; Whelan etal., 2008). that alter insect infestation rates, mating behaviour, and
For example, specialized guilds such as bark-probers, reproductivesuccess(Kunzetal.,2011),whilebirdscanaffect
leaf tossers, and ant followers are found only among the foraging pattern of aphid-tending ants in tree canopies
birds. These specialists can have important effects on (Mooney & Linhart, 2006). The relationship between bird
limiting arthropods unavailable to generalist predators and bat foraging strategies and the abundance of certain
(e.g. bark-probing birds such as woodpeckers suppress arthropodgroupsthatdifferinabundanceandoverallimpact
wood-boring pests in temperate forest; see Fayt, Machmer on plant productivity might explain their different relative
&Steeger,2005;Koenigetal.,2013;Floweretal.,2014).On impactsonpestcontrol,plantgrowthandcropyieldsinthe
theotherhand,generalistpredatorssometimeshavestronger differentland-usesystemsandtropicallandscapesthathave
top-downeffectsthanspecialists(Halaj&Wise,2001;butsee beeninvestigatedtodate.
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