Submitted 19 April 2016Accepted 8 August 2016Published 13 September 2016

Corresponding authorEric J Fuchs ejfuchsgmailcom

Academic editorJames Roper

Additional Information andDeclarations can be found onpage 10

DOI 107717peerj2422

Copyright2016 Barrantes et al

Distributed underCreative Commons CC-BY 40

OPEN ACCESS

Effect of fragmentation on the CostaRican dry forest avifaunaGilbert Barrantes Diego Ocampo Joseacute D Ramiacuterez-Fernaacutendez and Eric J FuchsEscuela de Biologiacutea Universidad de Costa Rica San Joseacute Costa Rica

ABSTRACTDeforestation and changes in land use have reduced the tropical dry forest to isolatedforest patches in northwestern Costa Rica We examined the effect of patch area andlength of the dry season on nestedness of the entire avian community forest fragmentassemblages and species occupancy across fragments for the entire native avifaunaand for a subset of forest dependent species Species richness was independent ofboth fragment area and distance between fragments Similarity in bird communitycomposition between patches was related to habitat structure fragments with similarforest structure have more similar avian assemblages Size of forest patches influencednestedness of the bird community and species occupancy but not nestedness ofassemblages across patches in northwestern Costa Rican avifauna Forest dependentspecies (species that require large tracts of mature forest) and assemblages of thesespecies were nested within patches ordered by a gradient of seasonality and onlyoccupancy of species was nested by area of patches Thus forest patches with a shorterdry season include more forest dependent species

Subjects Biodiversity Biogeography Conservation Biology Ecology ZoologyKeywords Bird composition Nested community analysis Community similarity Forest sizepatches Habitat Habitat fragmentation

INTRODUCTIONDeforestation and change in land use are the primary factors causing habitat degradationand forest fragmentation in tropical regions (Jaeger 2000 Lambin Geist amp Lepers 2003Azevedo-Ramos De Carvalho Jr amp Do Amaral 2006 Joyce 2006 Martiacutenez et al 2009)These changes in natural landscapes may often reduce connectivity for species trying tomove between fragments embedded in a matrix that consists of anthropogenic and semi-natural habitats (Renjifo 2001Graham amp Blake 2001) Additionally the negative effects ofhabitat fragmentation may be exacerbated by increased predation and competition withinhabitat patches (Andreacuten 1992 Fahrig 2003) Thus the direct and indirect negative effectsof habitat fragmentation could cause the extinction of some species in the fragmentsparticularly of those species that rely on large tracts of mature forest for reproduction(Stiles 1985)

Bird communities undergo notable changes in composition and abundance soon afterlarge forests are reduced into smaller patches (Bierregaard amp Stouffer 1997 Oostra Gomesamp Nijman 2008) In some cases fragmentation could increase bird species richness and theabundance of bird species (Azevedo-Ramos De Carvalho Jr amp Do Amaral 2006) as birdsaggregate in the remaining available forests patches But this increase is invariably followed

How to cite this article Barrantes et al (2016) Effect of fragmentation on the Costa Rican dry forest avifauna PeerJ 4e2422 DOI107717peerj2422

by a steady reduction (Herkert 1994 Kruess amp Tscharntke 1994 Lida amp Nakashizuka1995) because the remaining habitat is insufficient to sustain either the increased abundanceor a large number of species (Fahrig 2003 Pimm amp Askins 1995) Additionally invasion ofnon-forest bird-species may increase competition for resources and increase parasite loadwhich in turn may further reduce the reproductive success and viability of populationswithin fragments (Christiansen amp Pitter 1997 Duncan 1997)

Reductions in genetic variability demographic crashes and higher susceptibility tocatastrophic events have been hypothesized for resident bird populations in forest patches(Zuidema Sayerand amp Dijkman 1996) These effects may be prevented if fragments are in-terconnected or connected to larger continuous forests (Haddad et al 2003Uezu Metzgeramp Vielliard 2005) Unfortunately due to species-specific differences in behavior corridorsare not suitable for all species (Rosenberg Noon amp Meslow 1997) Furthermore newlyfragmented habitats are often difficult to re-connect with larger forest fragments or withother small fragments in most cases continuous habitats are impossible to recover Henceisolated forest patches often become the only species reservoirs of previously widespreadavifaunas

Northwestern Costa Rican dry-forest has been reduced to a series of small patchessurrounded by large cultivated areas (eg sugar cane rice field cattle haciendasQuesada ampStoner 2004) which cover only 01 of its original extension (Janzen 1988) Consequentlythe original terrestrial avifauna is now confined to these isolated small forest patches someof which are protected but with little if any chance of reconnection As a first approach toestimate the importance of these forest fragments for the dry forest avifauna we tested theeffect of natural habitat fragmentation (Fahrig 2003 Fahrig 2013) on species compositionin dry forests of northwestern Costa Rica at two different levels the entire bird communityand the assemblage of forest dependent species Most dry forest birds occupied originallynearly the entire northwestern region of Costa Rica and even species that now occur atmiddle elevations were reported at lower elevations (Wetmore 1944 Slud 1980) Thusit is likely that the distribution of most species has been affected by fragmentation dueto habitat loss We use nestedness analyses to test whether fragmentation or the lengthof the dry season (ie seasonality gradient) produce a nested species pattern Testing ifforest patches nest along a seasonal gradient provides information on the potential effectof climate changes predicted for the region (Sheffield amp Wood 2008) A nested pattern isexpected when species assemblages in species-poor sites are a subset of those assemblagespresent in species-rich sites (patch nestedness) or when species occupying few sites are asubset of those species occupying a large number of sites (species nestednessNovak Mooreamp Leidy 2011) Hence nestedness may be the result of variation in rates of colonizationand extinction among sites (Lomolino 1996) or among species (Atmar amp Patterson 1993)We also test whether extinction (the likely cause of species richness reduction acrossforest fragments) is caused by either a reduction in patch size an increase in the distancebetween forest fragments as consequence of habitat deterioration or if the nested pattern isassociated with a climatic gradient (ie seasonality) (Lomolino 1996Wright et al 1998)

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Table 1 Area location and number of native species recorded in five dry forest fragments in north-western Costa RicaDry season includes the length of dry season in months and is based on meteorologi-cal stations located in the same or nearby sites

Locality Dry season Area (ha) Location No of species

Santa Rosa 6ndash65 37117 1050primeN 8537primeW 123Palo Verde 5ndash55 11970 1020primeN 8520primeW 135Rincoacuten de laVieja 2ndash3 8411 1049primeN 8521primeW 127Diriaacute 45ndash5 5426 1010primeN 8535primeW 109Cabo Blanco 3ndash4 1172 0933primeN 8506primeW 104

MATERIALS AND METHODSData collectionWe gathered information on species composition from five forest fragments innorthwestern Costa Rica that varied in size and connectivity (Table 1 and Fig 1) ParqueNacional Diriaacute (Dir) Reserva Natural Absoluta Cabo Blanco (CB) Parque Nacional PaloVerde and the Reserva Bioloacutegica Lomas Barbudal (PV) Parque Nacional Santa Rosa (SR)and Parque Nacional Rincoacuten de la Vieja (RV) These forest patches are surrounded bylarge agricultural fields and human communities (Joyce 2006) and the distance betweenthe nearest two forest patches included in this study is 589 km There are some isolatedtrees and small tracts of early successional vegetation in the matrix that surround forestpatches but they are likely inadequate as corridors between patches The fragmentation inthe region has been the result of a progressive loss of natural habitats due to transformationof these habitats into agricultural fields (Boucher et al 1983 Joyce 2006) We visited (GBDO and JDRF) each site from 8 to 20 times to compile a comprehensive bird list of eachsite during the last 15 years starting in 2002 We sampled 3ndash4 days during each visit andsearched for birds from 8 to 12 walking hoursday In sites in which access is difficult (egRV) we extended the sampling period of each visit to 5ndash8 days to reduce the numberof visits Particularly during the breeding period of most dry forest birds (May throughJuly) we focused our efforts in detecting those elusive rare species (eg some nightjarsand cuckoos) We complemented our survey data with information from Stiles (1983)checklist of SR and OTS (PV) Julio Saacutenchez and Luis Sandoval provided us additionaldata for PV and RV respectively

Climatically the northwestern region of Costa Rica is characterized by a long dryseason fromDecember throughMay (Mata amp Echeverriacutea 2004) followed by a rainy seasonHowever the local conditions affect the length of the dry season across sites (Saacutenchez-Murilloet al 2013) and thismakes it possible to order sites along a gradient of seasonality (Table 1)Precipitation patterns influence vegetation in the region which is dominated by deciduousvegetation with evergreen species along rivers and seasonal and permanent streams(Hartshorn 1983) We obtained the area of each patch for statistical analyses from the Sis-temaNacional de Areas de Conservacioacuten de Costa Rica (httpwwwsinacgocr) For PVweexcluded the area covered by wetlands and included the area of the Reserva Bioloacutegica LomasBarbudal because it is connected with PV and excluded the area on the Caribbean slope ofRV because this area is covered with rain forests rather than dry forests (Hartshorn 1983)

Barrantes et al (2016) PeerJ DOI 107717peerj2422 314

Figure 1 Dry forest fragments and land use in northwestern Costa Rica The inset shows the map ofCosta Rica

We excluded fresh water (eg Anatidae Ardeidae) and marine birds (eg Fregatidae)from our analyses because they are restricted to habitats that are not present in all sites Wealso excluded migratory birds Occasional native species far from their normal geographicbreeding distribution ranges were also excluded Thus the dry-forest bird-communitywas composed of resident breeding species with terrestrial habits Each bird specieswas classified into one of three forest dependency categories following Stiles (1985) withmodifications by Sandoval amp Barrantes (2009) 1 = species that live and reproduce inextensive mature forest 2 = species that require habitats with 40ndash50 of forest cover 3= species that inhabit open areas Species in categories 1 and 2 are likely more affected byhabitat fragmentation than those species included in category 3

Statistical analysesWe evaluated similarity of bird species composition among sites using Soslashrensen Index andtested for a relationship between species composition and geographic distances between sitesusing aMantel test We also determined whether composition of resident species across dryforest patches follows a nested distribution or if each patch contains an independent subsetof species using the Vegan package (version 117 httpcranr-projectorg) implemented inthe R Statistical Language (version 300 R Core Team 2013) A nested species distribution

Barrantes et al (2016) PeerJ DOI 107717peerj2422 414

occurs when species richness in smaller fragments is a subset of the richness of largerfragments To test for species nestedness in the dry forest patches we used presenceabsencematrices in which rows and columns were patches and species respectively and then sortedrows (assemblages) and columns (species) by a gradient of patch sizes and a gradient ofrainfall seasonality We calculated the NODF metric (Almeida-Neto et al 2008 UlrichAlmeida-Neto amp Gotelli 2009 Moreira amp Maltchik 2012) and used 999 permutationswith the lsquoquasiswaprsquo algorithm to construct a null distribution of NODF values (Mikloacutes ampPodani 2004)During eachpermutation the lsquoquasiswaprsquo algorithm randomly shuffles valuesof rows and columns butmaintains constantmarginal frequencies (total frequencies of rowsand columns) We then estimated the probability that the calculated nestedness differedsignificantly from the generated null distribution lsquoQuasiswaprsquo in addition to retainingrow (sites) and column (species) frequencies does not increase Type I or Type II errors(Gainsbury amp Colli 2003) We used the NODF metric because it independently estimatesnestedness of species assemblages among sites (NODF rows) and nestedness for occupancyor presence among species (NODF columns) and for the entire matrix that we refer toas community (Almeida-Neto et al 2008) NODF for instance calculates the nestednessof sites by comparing the occurrence of each species in each site (ie fill or empty cells)with the marginal values corresponding to all sites and then ranking the sites by a previousdetermined gradient (eg area of fragments) (Almeida-Neto et al 2008) NODF is reportedin values ranging from 0 (not nested) to 100 (maximum nestedness) These models do notincorporate the probability of detection of each species but require that all (or nearly so)species from each fragment are included

We also inferred whether nestedness was either caused by extinction due to a reductionin patch size or by rainfall seasonality (Cutler 1991 Lomolino 1996 Patterson 1990Patterson amp Atmar 1986) conducting the statistical analyses described by Lomolino (1996)PN= 100times(RminusD)R where PN= of perfect nestedness R = mean number ofdepartures from random simulations and D= number of species that depart from perfectnestedness To estimate the probability associated with the D statistic we took the ratio ofspecies that depart from perfect nestedness between the original matrix and those obtainedfrom 999 randomly generated matrices (scripts for running these analyses are included asSupplemental Information 1) Lomolinorsquos statistics were calculated for a presenceabsencespecies matrix in which sites were first ordered by decreasing area and then along a gradientof seasonality (Fig 1) Analyses were conducted for all the species and for forest dependentspecies (categories 1 and 2 of forest dependence)With thesematrices we tested if nestednessis caused by extinction due to area reduction or rainfall seasonality

RESULTSWe registered a total of 187 resident species in all study sites (Table S1) PV had themost resident species while CB and Dir had the fewest but the number of species didnot differ significantly across sites (x2 = 551 df = 4 p= 0239 Table 1) RV was leastsimilar in species composition with all other sites and CB and Dir were most similar(Table 2) Species richness was independent of both geographic distance (Mantel test= 042 p= 0185 Table 2) and fragment area (r = 041 p= 0494)

Barrantes et al (2016) PeerJ DOI 107717peerj2422 514

Table 2 Soslashrensen similarity index and the number of species shared between sites in parentheses (be-low the diagonal) and distance (km) (above the diagonal) between five forest patches in northwesternCosta Rica Larger values of the Soslashrensen similarity index indicate greater similarity in species composi-tion between sites

Distance

S Rosa P Verde Diria C Blanco R Vieja

S Rosa 779 726 715 636P Verde 080 (116) 689 694 589Diria 082 (92) 071 (97) 706 613C Blanco 081 (88) 067 (94) 085 (86) 646

Similarity

R Vieja 073 (88) 062 (90) 070 (80) 076 (84)

Patch size and rainfall were not correlated (Spearman = 070 p= 0180) but bothfactors affected similarly the nested pattern at three different levels bird community(entire matrix) bird assemblages and species occurrence among dry forest patches Thevalue of NODF (overlap and decreasing fill statistics) indicated that the community wassignificantly nested by size of dry forest patches (NODF = 316 p= 0001) Furthermorespecies occupancy was nested among patches (NODF columns= 316 p= 0001) but birdassemblages were not nested by size of patches (NODF rows= 656 p= 0099) though thisprobability may imply nestedness with the possibility of an outlier The entire communityalso nested within forests ranked by length of dry season (NODF = 316 p= 0001)The bird assemblages showed a weak tendency to be nested in patches ordered along thisgradient of rainfall seasonality (NODF rows= 320 005lt plt 01) and species occupancywas strongly nested along such gradient (NODF columns= 316 p= 0001) The similarityof these results indicate that both factors affected the nestedness of species in dry forestpatches (Fig 2) but the small sample size (N = five patches) prevented us from testing theinteraction of both factors on species nestedness

The subset of forest dependent species (categories 1 and 2) was nested when consideringarea (NODF = 2417 p= 0001) or seasonality (NODF = 2415 p= 0001) of dry forestfragments Bird assemblages of forest dependent species nested among forest fragmentsranked along a seasonality gradient (NODF rows = 4215 p= 0005) but not by area offragments (NODF rows = 5768 p= 0397) The species occupancy nested along bothgradients seasonality (NODF columns = 2413 p= 0001) and area (NODF columns= 2413 p= 0001) According to Lomolinorsquos test reduction in species richness for theentire community was not due to habitat loss (D= 121 R= 1279 p= 0386 PN =69) distance between fragments (D= 120 R= 1289 p= 0336 PN = 69) nor rainfallseasonality (D= 118 R= 1287 p= 0276 PN = 83) Results are similar for forestdependent species (Table S1)

In general the proportion of species included in the three categories of forest dependencywas similar for all sites (x2 = 77 df = 8 p= 0468 Table 3) The number of forestdependent species (category 1) did not differ across sites (x2 = 51 df = 4 p= 0167Table 3) From this category 18 species were detected in only one site and 72 of themwere exclusively detected in RV (Table 3) Similarly for species in category 2 we detected58 only in RV From category 3 only four species were detected in only one site

Barrantes et al (2016) PeerJ DOI 107717peerj2422 614

Figure 2 Relationship between area of fragments and seasonality estimated as the length of dry seasonin months

Table 3 Species included in each category of forest dependence The first row includes the total numberof species in each category and the number of species detected in a single sampling site The other rows in-clude the number of species of that particular category detected in each site and the number of species de-tected only in that particular site The percentage of restricted species of each category per site is shown inparentheses

Site Category 1 Category 2 Category 3

No species Restricted No species Restricted No species Restricted

Total 33 18 101 26 53 4Santa Rosa 10 0 (0) 71 1 (4) 42 0 (0)Palo Verde 14 2 (11) 74 4 (15) 47 1 (25)Diriaacute 14 3 (17) 58 2 (8) 37 2 (50)C Blanco 10 0 (0) 61 4 (15) 33 0 (0)R Vieja 22 13 (72) 70 15 (58) 35 1 (25)

Barrantes et al (2016) PeerJ DOI 107717peerj2422 714

DISCUSSIONArea did not explain the number of species found in these forest patches which suggeststhat other factors such as environmental heterogeneity influenced the number andorcomposition of species in fragments For instance patches with complex topography (egaltitudinal gradient mountains) often have higher species richness or at least a differentsubset of species when compared with patches with relatively homogeneous topographies(Primack 1998 Fernaacutendez-Juricic 2000Mayr amp Diamond 2001) The characteristics of thematrix surrounding fragments connectivity between fragments edge effect and humaninterventions may also influence species richness within fragments (Bierregaard amp Stouffer1997Whitmore 1997)

In this study nestedness of the dry forest avifauna and forest dependent species isinfluenced by a gradient of seasonality (length of dry season) and by fragment area (Fig 2)Sites with a shorter dry season maintain a larger number of dry forest and forest dependentspecies From a conservation perspective forest dependent species are likely moresusceptible to global climatic changes particularly to the changes expected to occur as aconsequence of the increasing frequency of ENSO events (Cai et al 2014) and the predictedintensification in the severity of droughts in the region (Sheffield amp Wood 2008) Dry forestdependent species require large mature forest tracts to maintain reproductive populations(Stiles 1985) However both factors ENSO events and severe droughts result in longer andmore severe dry seasons which consequently increase the frequency of wild fires (Janzen1986) affecting the physiognomy of the dry forest changing its composition and structure(Barlow amp Peres 2004) and thus affecting the avifauna associated to mature forest tracts

Fragmentation did not appear to cause a reduction in species richness (based onLomolinosrsquo test) among forest patches In systems in which nestedness is caused by theinteraction of different factors as seems to be the case here Lomolinosrsquo test is likely tofail to detect the causes of nestedness This test has several assumptions (eg correlationbetween nestedness and area of fragments extinctions are not correlated with isolation)and incorrect assumptions may influence its sensitivity (Lomolino 1996) In this studyseveral factors may obscure the signature of habitat fragmentation (or distance betweenfragments) on nestedness For instance the high resilience apparently inherent to dryforest birds (Barrantes amp Saacutenchez 2004) Many dry forest birds are presumably capable ofmaintaining small reproductive populations in suboptimal habitats (eg small patches ofsecondary vegetation pastures Barrantes amp Saacutenchez 2004) Other species (eg Callocittaformosa and Campylorhynchus rufinucha) are capable of moving between distant forestfragments along linear vegetation corridors or flying between isolated trees or bushes(Harvey et al 2005) Thus habitat use and behavioral features of some dry forest birdspecies reduce the probability of detecting the proximal causes of nestedness (eg habitatreduction and geographical isolation)

Species composition across sites may be more related to vegetation features than to areaof fragments or geographic isolation The area of the patches included in this study does notpredict the number of species present in each fragment For instance while having similarspecies richness SR is nearly three times the area of PV Likewise species richness is

Barrantes et al (2016) PeerJ DOI 107717peerj2422 814

similar in CB and Dir but the area of CB is only one 20 of the area of Dir SR and PVare primarily deciduous forest and small tracts of evergreen vegetation (Hartshorn 1983)and both sites have similar species compositions Dir and CB share many species andboth have more humid conditions than SR and PV and larger tracts of evergreen forest asa result of a shorter dry season (Janzen 1986 Saacutenchez-Murillo et al 2013) In contrast RVshares fewer species with other dry forest patches and populations of many of these speciesarewell isolated by topographic barriers fromother populations (Barrantes 2009BarrantesIglesias amp Fuchs 2011) The topography of RV is more complex and includes an altitudinalgradient covered by forests with different structure (Janzen 1986) The differencesin species composition across sites highlight two important aspects first that speciescomposition should be analyzed at a finer scale taking forest structure and compositioninto account and second that to preserve the rich dry forest avifauna it is necessary topreserve ecosystem diversity eg through habitat restoration and fragments connection

Results in Table 3 indicate that between 5 and 12 of all native species in dry forestpatches require large areas of mature forests and more than 40 of the species in eachforest patch require at least 50 of forest cover for feeding and reproduction (Stiles 1985)Hence forest patches in northwestern Costa Rica support a large number of species thatrequire large tracts of mature tropical dry forests in the most threaten forest ecosystem inMesoamerica (Janzen 1988) These patches are then an important reservoir for the richdry forest Mesoamerican avifauna (Stotz et al 1996) including four endemic species to thePacific slope of Middle America dry forest region (Lesser Ground Cuckoo Pacific ScreechOwl Long Tailed Manakin White Throated Magpie-Jay) but habitat destruction theremoval of isolated trees and forest patches reduce connectivity and may drastically reducethe viability of populations in remnant forest fragments In these isolated small patchesgenetic variability may decrease rapidly (Evans amp Sheldon 2008 but see Fuchs amp Hamrick2010) and the recurrent catastrophic events caused primarily by intentional fires (Quesadaamp Stoner 2004) seriously threaten the long-term maintenance of bird populations

In conclusion forest patches in northwestern Costa Rica are reservoirs of a large portionof bird species of the Pacific slope of Central American dry forests However speciescomposition varies widely across fragments possibly as a consequence of differences invegetation climatic and topographic conditions In northwestern Costa Rica the reductionof the original dry forest into small isolated patches resulted in a nested pattern of bothbird assemblages and species The lack of connectivity between these fragments and therecurrent intentional fires in the region and the predicted global climatic changes threatenthe long-term population-viability of many bird species Nestedness analyses proved tobe an important tool to evaluate the consequences of habitat fragmentation of naturalenvironments Most important this method can be used periodically to evaluate the effectof changes in climate and land use on the avifuna (or other animals) in forest patches

ACKNOWLEDGEMENTSWe thank Julio Saacutenchez and Luis Sandoval for providing the data for Palo Verde andRincoacuten de la Vieja respectively We also thank John Blake and two other anonymousreviewers for their critical and useful comments

Barrantes et al (2016) PeerJ DOI 107717peerj2422 914

ADDITIONAL INFORMATION AND DECLARATIONS

FundingThe authors received no funding for this work

Competing InterestsThe authors declare there are no competing interests

Author Contributionsbull Gilbert Barrantes conceived and designed the experiments performed the experimentsanalyzed the data wrote the paper prepared figures andor tables reviewed drafts of thepaper bird surveysbull DiegoOcampo and Joseacute D Ramiacuterez-Fernaacutendez conceived and designed the experimentsperformed the experiments prepared figures andor tables reviewed drafts of the paperbird surveysbull Eric J Fuchs analyzed the data prepared figures andor tables reviewed drafts of thepaper

Data AvailabilityThe following information was supplied regarding data availability

The raw data has been supplied as a Supplemental Dataset

Supplemental InformationSupplemental information for this article can be found online at httpdxdoiorg107717peerj2422supplemental-information

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