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Ecological Engineering 36 (2010) 1492–1496

Contents lists available at ScienceDirect

Ecological Engineering

journa l homepage: www.e lsev ier .com/ locate /eco leng

hort communication

ird community shifts related to different forest restoration efforts:case study from a managed habitat matrix in Mexico

an MacGregor-Forsa,∗, Arnulfo Blanco-Garcíab, Roberto Lindig-Cisnerosb

Laboratorio de Ecología Funcional, Centro de Investigaciones en Ecosistemas, Universidad Nacional Autónoma de México, Campus Morelia,ntigua Carretera a Pátzcuaro 8701, Morelia 58190, Michoacán, MexicoLaboratorio de Ecología de Restauración, Centro de Investigaciones en Ecosistemas, Universidad Nacional Autónoma de México, Campus Morelia,ntigua Carretera a Pátzcuaro 8701, Morelia 58190, Michoacán, Mexico

r t i c l e i n f o

rticle history:eceived 18 November 2009eceived in revised form 18 March 2010ccepted 2 June 2010

eywords:vian conservationiodiversityird communitieseotropicsurse plantupinus elegans

a b s t r a c t

Although increased attention is being paid to animals when studying restoration processes, little is knownon the effects that different restoration efforts have on birds. In this study we evaluated the variation ofbird communities in a managed landscape that includes cropfields and two different restoration strategies.To evaluate possible differential effects of both restoration strategies (plus former-state and natural-statecomparisons as controls), we compared their bird communities. After five growing seasons, bird speciesrichness was highest in native forest remnants and lowest in cropfields. Although species richness valuesfrom the restoration treatment did not show differences in relation to those from the forest treatment,values for the reforestation treatment did. Bird densities were highest in the forests and alike in crop-field, reforestation, and restoration treatments. However, bird communities recorded in the restorationtreatment were fairly even when compared to the reforestation treatment, and highest bird species com-position similarity was recorded between the restoration and forest treatments. These results suggest thatthe studied restoration treatment attracts a higher number of bird species in relation to former states andthus enhance bird richness. Also, we demonstrate that restoration efforts that include more actions canaffect more ecosystem components. In this study, nurse plants not only offered a quick growing struc-

tural vegetation component that enhanced habitat structure, but also provided abundant food resourcesfor birds. Given the scarcity of comparable habitat matrices to replicate our study, our results should betaken with caution as they are not generalizable to all Mexican temperate forest conditions. Althoughfurther studies need to address whether restoration practices using Lupinus elegans positively affect birdprimary population parameters (e.g., survival, reproduction), our results show that restoration practicesthat include nurse plants can promote rich bird communities after only 5 years from the implementation

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. Introduction

Ecological restoration has focused largely on the vegetationomponent of ecosystems. However, increased attention is beingaid to the animal component in restoration processes (Majer,009). A large proportion of the existing knowledge of the effectshat restoration activities have on wildlife has focused on birds (e.g.,assell, 2000; Gabbe et al., 2002; Hamel, 2003; Twedt et al., 2006;

aines et al., 2007).

Previous studies addressing relationships between restorationctivities and their ornithological component have drawn severalain conclusions: (1) bird species richness and abundances are

∗ Corresponding author. Tel.: +52 443 3222777x42504.E-mail address: ian@oikos.unam.mx (I. MacGregor-Fors).

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925-8574/$ – see front matter © 2010 Elsevier B.V. All rights reserved.oi:10.1016/j.ecoleng.2010.06.001

© 2010 Elsevier B.V. All rights reserved.

ften enhanced by restoration practices (Passell, 2000; Twedt et al.,002; Hamel, 2003; Gaines et al., 2007; Aerts et al., 2008; Farwigt al., 2008), (2) bird species composition can shift in restorationreatments (Brawn, 2006; Farwig et al., 2008), and (3) restorationrocesses can be accelerated by frugivore birds (Aerts et al., 2006).lthough some studies have recorded significantly higher birdpecies richness in restored areas with fast-growing tree speciesn the short-term (e.g., 3–7 years; Passell, 2000; Hamel, 2003), aecently published article reports no shifts in avian colonizationrocesses in a 5–6 year fast-growing tree restored area (Twedt,006).

However, few studies have focused on the effects that dif-erent restoration efforts have on bird communities (e.g., Hamel,003; Farwig et al., 2008). In this study we evaluated bird com-unity shifts related to different forest restoration efforts using

ropfields as former-state control and native forests as natural-

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tate control. Restoration strategies used in this study include these of a nitrogen-fixing legume (Lupinus elegans) as a nurse plantlus reforestation, and the other one only includes reforestationfforts. We predicted that bird species richness and densities wouldise gradually from cropfields to native forests, with fairly evenird communities in native forests, and highly dominated birdommunities in cropfields. Also, we expected bird composition tohange as habitat structure changed, with differences between theestoration and reforestation scenarios due to the presence of theesources offered by the legume and the plant species that estab-ished below it (e.g., flowers, fruits, perches).

. Materials and methods

.1. Study area

The study area is located in the Comunidad Indígena deuevo San Juan Parangaricutiro, Northeast Michoacán, Mexico

2750 masl). Native pine and oak–pine forests dominate the area,nd at elevations ≥2800 masl, fir (Abies religiosa) become abun-ant. The forests of the indigenous community (11,694.5 ha) areanaged for timber production under sustainable forestry prac-

ices. Our surveys were performed in a middle-slope hillside withropfields abandoned at least 8 years ago. The surrounding land-cape consists of a matrix of cropfields with dispersed pine–oak–firorest patches. Despite being abandoned almost a decade ago, ourtudy site still showed a low number of plant species, only forbsnd weeds were present, and no tree species were recorded at theeginning of the restoration and reforestation efforts in 2004.

We considered four habitat treatments for this study: (1)ative forests – natural-state control, (2) cropfields – former-stateontrol, (3) restoration – including the use of a nitrogen-fixingurse plant, and (4) reforestation. Native forests are dominatedy pine trees (i.e., Pinus pseudostrobus, P. montezumae) and, in

esser amount, oaks (Quercus crassipes) and firs (Abies religiosa).he most common plant species recorded in this treatment, otherhan trees, were: Bidens aurea, B. bigelovi, B. serrulata, Commelinauberosa, Conyza schiedeana, Crusea longiflora, Dalea touinii, Fes-uca amplisima, Gnaphalium attenuatum, G. americanum, Hypericumhilonotis, Jaegeria hirta, Lopezia racemosa, Lupinus elegans, Muh-

enbergia minutisisima, Oenothera pubescens, Phacelia platycarpa,haseolus sp., Sabazia humilis, Salvia mexicana, Tagetes micrantha,nd Tithonia tubiformis.

In June 2004, three coniferous species were used to restore a.15 ha crop-hillside, planted in equal amounts and spaced 2 mrom each other, in a 4500 m2 area: P. pseudostrobus, P. montezumae,nd Abies religiosa. An additional restoration resource was used inhis hillside: a nitrogen-fixing nurse plant (L. elegans), seeded in2 patches of 64 m × 64 m. Natural establishment of other plantpecies was allowed. This area was considered as the restorationreatment for this study. Dominant plant species that establishedn this treatment, other than the planted trees, were: Bacharis het-rophylla, Bidens aurea, B. bigelovi, B. serrulata, Commelina tuberosa,onyza coronopifolia, C. schiedeana, Crataegus mexicana, C. longiflora,. touinii, Drymaria malachioides, F. amplisima, G. attenuatum, G.mericanum, H. philonotis, J. hirta, L. elegans, Mulenbergia macroura,. pubescens, P. platycarpa, Prunella vulgaris, S. humilis, Salvia ele-ans, S. mexicana, Senecio salignus, S. stoechodiformis, T. micrantha,araxacum officinale, and T. tubiformis.

The rest of the hillside was planted only with pine tree species

i.e., P. pseudostrobus, P. montezumae). Trees were also spaced 2 mway from each other, and natural establishment of other plantpecies was also allowed. An area of 4500 m2 was selected as theeforestation treatment. Dominant plant species that establishedn this treatment, other than the planted trees, were: Bidens aurea,

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gineering 36 (2010) 1492–1496 1493

. serrulata, C. tuberosa, Cyperus sp., Dalea touinii, H. philonotis, S.umilis, and Trifolium mexicanun.

Finally, the closest agricultural lands to both restoration andeforestation treatments were used as the cropfield treatment.ropfields are used in the study area for subsistence and are divided

n parcels smaller than 2 ha. Many were abandoned and used forattle grazing more than 10 years ago but several are still plantedith corn (Zea mays).

By 2009, the restored/reforested hillside was covered by aanopy of young trees. A random sample of 100 trees at both treat-ents showed that the height of P. montezumae pines, the most

bundant tree species in both treatments, was statistically highern the restoration treatment (F1,98 = 31.7, P < 0.0001). Also, totallant species richness increased from 18 to 60 in a four-year period2004–2008) in the restoration treatment, while the reforestationreatment still had low plant species richness (n = 19) by 2008.

.2. Bird surveys

We surveyed bird communities from August 2008 to June 2009sing point counts (5-min, 25 m radius; following Ralph et al.,993), recording all birds seen or heard, from 0700 to 1000 h. Wesed limited-radius point counts for assuring that all birds recordedere actively using the surveyed area and not nearby sites with dif-

erent habitat attributes. To calculate bird densities, we measuredhe distance from the observer to the recorded birds inside theoint counts using a rangefinder (Bushnell Yardage Pro). We sur-eyed two point counts replicates in the four described treatments.oint counts were established in the restored plot and adjacentropfields, reforestation plots, and a nearby native forest patch.n order to assure the independence of point count replicates, weocated them at least 200 m away from each other (as recom-

ended by Huff et al., 2000). Thus, we surveyed eight point countstwo replicates per treatment), during the same day and under sim-lar weather conditions, in August and October 2008, and January,

arch, April, and June 2009 in order to record year-round seasonalariations.

.3. Data analysis

To contrast bird species richness values, we used a rarefactionnalysis. For this we computed the statistical expectation of birdpecies richness for each treatment using EstimateS (Sobs [Maoao] ± 95% confidence intervals; Colwell, 2005). Such expectation isalculated based on the repeated re-sampling of all pooled samplesGotelli and Colwell, 2001), allowing the comparison of the statisti-ally expected species richness of the bird community recorded atach treatment using a comparable computed accumulated abun-ance (Moreno, 2001; Magurran, 2004).

To calculate bird densities, we computed bird individuals/hamean ± 95% confidence intervals) using Distance 5.0 (Thomas etl., 2005). This software calculates the probability of detectionf individuals at increasing distances from the observer, consid-rs detection rates by concentric surveyed area, and estimateshe number of bird individuals that exist within a surveyed areaBuckland et al., 2001). To determine if species richness and birdensity values were statistically different among the surveyedreatments, we compared their 95% confidence intervals. If con-dence intervals did not overlap, we considered the data to betatistically different with an ˛ < 0.01 (following Payton et al., 2003;

. Payton pers. com.).To assess differences in the evenness/dominance of the bird

ommunities recorded at the different studied treatments, we usedspecies rank/abundance plot approach (=Whittaker plot; as rec-mmended by Magurran, 2004). Rank/abundance plots are often

1494 I. MacGregor-Fors et al. / Ecological Engineering 36 (2010) 1492–1496

Table 1Bird species recorded in the studied treatments.

Species Forest Restoration Reforestation Cropfield

Hylocharis leucotis • •Archilochus alexandri •Selasphorus platycercus • •Trogon mexicanus •Melanerpes formicivorus •Picoides villosus •Mitrephanes phaeocercus •Contopus pertinax •Colaptes auratus •Tyrannus vociferans • • •Pachyramphus aglaiae •Cyanocitta stelleri •Aphelocoma ultramarina •Tachycineta thalassina •Stelgidopteryx serripennis • •Poecile sclateri •Psaltriparus minimus • •Troglodytes aedon • •Regulus calendula •Myadestes occidentalis •Sialia sialis •Turdus migratorius • • •Ptilogonys cinereus • •Peucedramus taeniatus •Vermivora celata •Vermivora ruficapilla • •Dendroica coronata • • •Dendroica nigrescens •Dendroica townsendi •Dendroica occidentalis •Wilsonia pusilla •Cardellina rubrifrons •Ergaticus ruber •Myioborus miniatus •Basileuterus belli • •Piranga rubra •Pipilo ocai •Pipilo maculatus • • •Pipilo fuscus • •Aimophila ruficauda • • •Oriturus superciliosus •

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sed to represent species abundance distribution in a community.hey highlight differences in dominance/evenness amongst com-unities, where steep curves represent assemblages with high

ominance of a few set of species, and shallower slopes implyommunities with higher evenness where species share similarbundances. Thus, the steepness of the slope of rank/abundancelots allows to infer the processes determining the diversity of aommunity, and reflects the success of the implied species to com-ete for limited resources (Magurran, 2004). To test differences inhe slopes of both rank/abundance regression lines, we performedNCOVA.

Finally, we evaluated bird community composition shifts amonghe studied treatments using ˇsim (Lennon et al., 2001). This dissim-larity index quantifies the relative magnitude of species gains andosses in relation to the sample with less unique species, allowinghe identification of species loss or shift in relation to the sampleith more unique species (Koleff et al., 2003; Gaston et al., 2007).

. Results

We recorded at total of 45 bird species of 39 genera (Table 1).o contrast bird species richness among the studied treatments,e used a comparable abundance of 41 individuals (lesser abun-

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ance recorded at the reforestation treatment). This analysishowed forests to comprise highest bird species richness (19.6 ± 3.8pecies), being statistically higher than that from the reforestationreatment (10 ± 4.9 species), but not different in relation to theestoration treatment (14.9 ± 3.4 species). However, bird speciesichness expectations for restoration and reforestation treatmentsid not differ (Fig. 1). Regrettably, we could not compare thepecies richness expectation for the cropfield treatment with thether three treatments due to the low species richness and birdbundance recorded in that treatment. However, total bird speciesichness recorded in the cropfield treatment was very low (6pecies), being twofold lower than the species richness recordedt the reforestation treatment (12 species).

Bird densities recorded in the forest treatment were signifi-antly higher (129 ind/ha; confidence intervals: 78, 210) than thoserom the other treatments. Although bird densities from the crop-eld treatment were low (9 ind/ha; confidence intervals: 5, 18),heir confidence intervals overlapped with the bird density confi-

ence intervals for the restoration (24 ind/ha; confidence intervals:2, 46) and reforestation (29 ind/ha; confidence intervals: 17, 51)reatments (Fig. 1).

Bird abundance distribution among the recorded bird commu-ities differed gradually, with fairly even communities in the forest

I. MacGregor-Fors et al. / Ecological Engineering 36 (2010) 1492–1496 1495

Fig. 1. Bird species richness and den

Fig. 2. Regression lines for the rank/abundance plots of the studied bird communi-ties. While bird communities recorded at the forest treatment showed a significantlyshallower slope in relation to the other studied treatments (regression equation:f(x) = −0.29x + 9.13), bird communities from the restoration treatment (regressionequation: f(x) = −0.45x + 7.31) showed a significantly more even community thantmL

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ogeneralizable to all Mexican temperate forest conditions. Although

he reforestation (regression equation: f(x) = −1.04x + 10.61) and cropfield treat-ents (regression equation: f(x) = −0.74x + 4.93), while the latter did not differ.

etters besides the symbology represent statistical differences from ANCOVA.

reatment and highly dominated communities in the cropfield andeforestation treatments. The forest treatment had significantlyess dominated bird communities than the rest of the treatments.he restoration treatment showed a significantly more even birdommunity than that from the reforestation and cropfield treat-ents. Finally, the rank/abundance regression line of reforestation

nd cropfield treatments did not differ (Fig. 2).Bird community composition differed among the studied treat-

ents. Species turnover rates show that, when compared tohe forest treatment, cropfields had the highest dissimilarityalue (ˇsim = 0.8), followed by the reforestation (ˇsim = 0.6), andestoration treatments (ˇsim = 0.4). These results show that speciesomposition changed gradually in relation to the forest treatment,s follows: restoration–reforestation–cropfield.

. Discussion

After five growing seasons, bird communities recorded atestoration and reforestation treatments differed significantly. Asxpected, bird species richness was highest in native forests rem-ants and lowest in cropfields. However, although bird species

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sity in the studied treatments.

ichness values from the restoration treatment did not show differ-nces in relation to those recorded at the forest treatment, valuesrom the reforestation treatment did. These results: (1) strengthenhe idea that restoration efforts can attract a higher number ofird species in relation to former states (e.g., cropfields), and thusnhance bird species richness (Passell, 2000; Hamel, 2003; Gainest al., 2007; Aerts et al., 2008; Farwig et al., 2008); and (2) demon-trate that restoration efforts that include more actions (e.g., usef nurse plants) affect a wider array of ecosystem components, asredicted by the restoration spectrum model (Zedler, 1999). The

atter was also recorded by Hamel (2003) in the US, who found aigher number of birds species in a Populus deltoides nurse cropnderplanted with Quercus nuttallii seedlings.

Contrary to our expectations, bird densities were highest in theorest treatment and not different in cropfields, reforestation, andestoration treatments. However, bird communities recorded inhe restoration treatment were fairly even when compared to theeforestation treatment, and lowest bird species composition dis-imilarity was recorded between restoration and forest treatments.hese results suggest that the use of nurse plants in restorationfforts not only changes vegetation structure (Rey et al., 2009), butlso allows a higher number of forest-dwelling birds to use it. Asoted by others, some bird species benefit from forest restorationctivities and some do not because restoration changes several eco-ogical functions and processes (Brawn, 2006; Farwig et al., 2008).amel (2003) found that bird community composition among dif-

erent restoration treatments differed, recording a higher numberf forest-related bird species in a nurse plant treatment. This is sim-lar to our bird community composition results. We believe thatn our case, L. elegans did not only offer a quick growing struc-ural vegetation component that enhanced habitat structure (A.lanco-García, unpublished results), but also provided abundant

ood resources for birds (flowers, nectar, and seeds; USDA-NRCS,002). In fact, we only recorded nectar feeding birds (i.e., hum-ingbirds) in two treatments: (1) forest, where Salvia elegans, an

bundant flowering species, is recurrently visited by humming-irds; and (2) restoration, where several flowering plants attractedwo of the three hummingbird species recorded in the forestreatment.

Given the scarcity of comparable habitat matrices to replicateur study, our results should be taken with caution, as they are not

urther studies are needed to address how avian primary pop-lation parameters respond to forest restoration practices thatse L. elegans as nurse plants, our results suggest that restorationtrategies of this nature offer conditions that a higher number of

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(USDA-NRCS), 2002. United States Department of Agriculture—NaturalResources Conservation, 2002. Elegant Lupine Lupinus elegans Kunth.,

496 I. MacGregor-Fors et al. / Ecologi

orest-related bird species can use, even after only 5 years from themplementation of the restoration efforts. L. elegans is particularlybundant in abandoned cropfields throughout our study area ands removed by landowners before re-foresting (Lindig-Cisneros etl., 2007). Thus, we strongly suggest that this legume should note removed when natural succession and/or forest restoration are

ntended.

cknowledgments

We thank Roberto Sáyago for help with fieldwork and the Comu-idad Indigena de Nuevo San Juan Parangaricutiro for their support.esearch funds were granted to R.L-C. by the Mexican Sciencend Technology Council (CONACYT–SEMARNAT-2002-C01-0760).M-F, being part of the Posgrado en Ciencias Biológicas of theniversidad Nacional Autónoma de México, received a Ph.D. schol-rship from CONACYT (175447).

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