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Research Article
Taxonomic and functional diversity of birds in a rural landscape of high Andean forest, Colombia
expand article infoLina P. Sarmiento-Garavito, Juan S. García-Monroy, Juan E. Carvajal-Cogollo
‡ Universidad Pedagógica y Tecnológica de Colombia, Tunja, Colombia
Open Access

Abstract

We evaluated the taxonomic and functional diversity of birds in a rural landscape in the north-eastern Andes of Colombia. We carried out seven field trips and used transects of 300 m, separated from each other by 500 m in the dominant plant cover of the rural landscape. We measured alpha (α) and beta (β) diversity at both the taxonomic and functional levels. We registered 10 orders, 21 families, 56 genera and 63 species of birds. In wooded pasture, we recorded 55 species and a relative abundance of 66% and 44 and 34% for an Andean forest fragment. The species that contributed the most to the dissimilarity between the covers were Zonotrichia capensis, Turdus fuscater, Mecocerculus leucophrys, Atlapetes latinuchus and Crotophaga ani. We identified nine functional types, where G1 was made up of small species with anissodactyl and pamprodactyl legs that were insectivorous, frugivorous and nectarivorous as the best represented. The FEve and FDiv were 0.51 and 0.74, respectively in the Andean forest fragment plant cover and, for the wooded pasture, the FEve was 0.45 and the FDiv was 0.81. Both cover types contributed to the diversity of the rural landscape and the dynamics that existed between them formed a complementary factor that favoured the taxonomic and functional richness of the characterised rural landscape.

Keywords

Colombian Andes, countryside, functional traits, species composition, species richness, transformed landscape Colombian Andes, countryside, functional traits, species composition, species richness, transformed landscape

Introduction

The transformation of landscapes by the loss and fragmentation of land-cover types results in a mosaic of native plant cover, surrounded by extensive areas of anthropogenic cover types (Collinge 2009; IPBES 2019). Agriculture and pastures, destined for livestock, form a large part of these new land covers and their unplanned extension does not allow sustainable use to be recognised as one of the current threats to biodiversity, both at the taxonomic scale (richness, composition and abundance) and at the functional level (diversity of functional traits) (Tscharntke et al. 2012; Freedman 2014). The extension of agricultural activities and livestock affect biological communities in their structure and composition and leads to functional and ecological destabilisation of natural systems (Bilenca et al. 2017). This conglomerate of effects on arable land fractions without buildings, but not containing agricultural land, crops, plantations and managed forests, as well as remnants of native vegetation, is what has been defined as rural landscape (Daily et al. 2001; Ranganathan and Daily 2008).

Rural landscapes favour positive and negative responses from biodiversity, depending on the intensity of habitat loss or fragmentation and the study group (Lawton et al. 1998; Newbold et al. 2013). For flocks of birds, studies show that they respond positively to habitat fragmentation (Villard et al. 1999; Lampila et al. 2005). In this way, when evaluating the responses of taxonomic diversity (species richness, composition and abundance) and functional variety, we understand the connection between species and how these are integrated into ecosystems (Villéger et al. 2008; Cadotte et al. 2011; López-Ordoñez et al. 2015). At the taxonomic level, the evaluation of specific diversity (alpha) through the analysis of species richness, relative abundance (structure) and species composition added to the quantification of diversity functional traits of species provides new and complementary information for the conservation of species in rural landscapes (Oldeland et al. 2010). This fact becomes relevant if we consider the changes that species undergo at the level of behavioural and functional attributes with habitat disturbance, as seen in the Andes of Colombia, where severe transformation patterns linked to human occupation have been documented (Cavelier and Etter 1995; Morante-Filho et al. 2016).

Rural landscapes modify positive and negative responses from biodiversity, depending on the intensity of the loss and/or fragmentation of the habitats and the study group (Lawton et al. 1998; Newbold et al. 2013). For many bird flocks, there are studies that demonstrate positive responses to habitat fragmentation (Villard et al. 1999; Lampila et al. 2005). In this way, when evaluating the responses of diversity from the taxonomic and functional dimensions, it allows us to understand the connection between species and the functioning of ecosystems (Cadotte et al. 2011; López-Ordoñez et al. 2015). At the taxonomic level, the evaluation of specific diversity (alpha), through species richness analysis, relative abundance (structure) and species composition added to the quantification of the diversity of functional features of species (functional dimension) provides new and complementary information for the conservation of species in rural landscapes, but especially for those that have suffered severe patterns of transformation linked to human occupation of regions like the Andean cordillera of Colombia (Cavelier and Etter 1995; Oldeland et al. 2010; Morante-Filho et al. 2016).

The landscapes of the Andean region of Colombia are the most diverse on the planet, with species that have limited ranges of distribution generating elements where the alpha and beta diversity of various taxonomic groups, such as birds, are highly expressed (Carvajal-Castro et al. 2019). Birds have been widely used as a biological model, thanks to their biological and ecological qualities (Veríssimo et al. 2009; Larsen et al. 2012); and the evaluation of different parameters of their assemblages can be used as inputs for the establishment of areas of importance or conservation strategies in each area (Westgate et al. 2014). In addition, birds have wide distribution, high taxonomic diversity and functional levels and an ability to attract attention and arouse the fascination of people making them a model for study (Veríssimo et al. 2009; Ikin et al. 2016).

We evaluated the taxonomic and functional diversity of birds in wooded grasslands and forest fragments in a rural landscape in the Colombian Andes. We started from the premise that grasslands with trees with a simple plant structure would have lower values of alpha diversity, both taxonomic and functional, in relation to forest fragments, whose plant structure is complex and stratified and provides greater availability of resources for the species. Similarly, beta diversity between assemblages will be structured by high turnover in species composition.

Materials and methods

Study area

The research was carried out in an Andean rural landscape of the Eastern Cordillera of Colombia (5°42'20"N, 73°30'35"W), at 2583 m a.s.l., in the Department of Boyacá. The study area has temperatures between 11 °C and 15 °C, relative humidity between 80% and 82% and a mean annual rainfall between 1000 mm and 1900 mm with two rainfall peaks per year, the first between March and April and the second between October and November (Galindo 2000).

The study area (Fig. 1A–D) was a landscape dominated by two types of cover, namely Andean forest fragments and wooded grasslands. The forest fragments are remnants of the original vegetation, composed of Quercus humboldtii or oak, with arborescent elements that have colonised the spaces made available by logging, giving space to Pinus patula plantations, Acacias melanoxylon and Acacia decurrens (Rangel-Ch et al. 1997). The second dominant cover of wooded grasslands are defined as open areas with isolated Melastomataceae and Clusiaceae trees, with herbaceous and shrub elements (70%), dedicated to cattle grazing (Rangel-Ch. et al. 1997).

Figure 1. 

Location of the study area, an Andean rural landscape of the Eastern Cordillera of Colombia. The sampled landscape units are highlighted A, B wooded pasture C, D Andean Forest.

Research design and sampling

We established transects in an Andean forest fragment of 17.57 ha and a wooded pasture of 12.13 ha, both at an altitude of 2527 m above sea level. For each of the sampled covers (fragment of Andean forest and wooded pasture), we carried out two free travel transects with a length of 300 m each, separated from each other by 500 linear m, a distance documented as optimal for data collection in linear transects and that for the study area guaranteed the independence of samples, due to the topography of the area with steep slopes that spatially increased the real distance across the land surface (Gale et al. 2009). Each transect was replicated in space and time and represented the minimum sampling unit. The order of sampling of each transect was carried out randomly to eliminate the correlation between the observations and avoid overestimations in the richness and abundance of the species (Ralph et al. 1996). In each transect, all bird species that were visually detected within an unlimited radius, for 10 minutes in the morning sampling and eight minutes in the evening sampling, for a total of 18 minutes per point/day (Howe et al. 1997; Leach et al. 2016).

We carried out seven field trips between June and December 2017. During this period, we registered the birds for the climatic seasons that characterise the area and a migration peak, to obtain real estimates of alpha diversity. During each field trip, we walked a daily transect two times, one in the morning from 5:30 h to 10:30 h and another in the mid- to late afternoon between 15:00 h and 17:30 h. We rotated these schedules throughout the field trips to obtain records of most species, given their activity peaks (Ralph et al. 1996). For bird watching, we used 10 × 50 binoculars and reflex cameras with a 150–600 mm super telephoto lens and a 75–300 mm lens. The sampling effort was 420 hours/person.

For recording information, formats were used daily during each field trip. In these formats, we recorded the data of the coordinates of the place of each observation, the altitude, the date and the time of the sighting, the foraging stratum and the social behaviour (López-Ordoñez et al. 2015). In addition, the number of individuals observed (detections) made up the basic input for the analysis of alpha and beta diversity.

Taxonomic determination was carried out with specialised pictorial keys for neotropical and Colombian birds (Restall et al. 2007; Ridgely and Tudor 2009; McMullan and Donegan 2014). The taxonomic arrangement followed Remsen et al. (2020).

Analysis of data

We evaluated the alpha diversity (α) of each vegetation type (cover type) from data of relative richness and abundance. We used the sample´s completeness method (Chao and Jost 2012) that measures the proportion represented by the individuals of each species in the sample with respect to the total number of individuals with which the expected species could be quantified through accumulation curves. Sampling coverages were evaluated through accumulation curves (rarefaction and extrapolation) and with the Hill numbers and the evaluation of q = 0 that measured the total species richness (true diversity), the q = 1 that expressed the exponential of the Shannon Entropy Index and q = 2, corresponding to the inverse of the Simpson Index (Chao et al. 2014). For each analysis, we used the procedure of Chao and Jost (2012) in the iNEXT programme (Hsieh et al. 2013). In addition, we applied non-parametric estimators of Chao 1 and bootstrap for a better approach to the structure of the bird assemblage (Chao and Lo 1994), since there were species that were represented by few individuals. We quantified the values ​​of singletons and doubletons and of any unique and duplicate samples using the programme EstimateS version 9.0 (Colwell et al. 2019).

The structure of the bird assemblage, expressed by the relative abundance of the species, was obtained from the division of the number of individuals counted for each species and the total numbers per cover type taken as a percentage (Pettingill 1985; Issa 2019). We applied analysis of similarity of the abundance matrix (ANOSIM) to determine if there were differences in the composition of birds between cover types and a SIMPER analysis to identify the taxa that contributed to the differentiation or similarity between the groups through the percentages of contribution (PC) and accumulation (AC) of the detections in each of the vegetation cover types (Clarke 1993). Beta diversity (β) was analysed by means of the turnover of species between the two vegetation cover types with the complementarity index. Exclusive and shared species between both cover types were also identified (Colwell and Coddington 1994).

For the functional diversity analyses, we considered four ethological functional traits related to the ecological role of nutrient and energy flow within the ecosystem (Stotz et al. 1996; López-Ordoñez et al. 2015): 1. Type of diet (carnivore, scavenger, folivore, frugivore, granivore, insectivore, nectarivore) (Stotz et al. 1996; Wilman et al. 2014); 2. Feeding strategy (catcher, forager, robber) (López-Ordoñez et al. 2015), 3. Foraging stratum (arboreal, shrub, herbaceous and soil) (Rangel-Ch and Lozano-C 1986); and 4. Social behaviour (mixed flock, monospecific flock and solitary). Furthermore, we took into account four morphometric traits, related to the selection of foraging sites and seed dispersal (Sekercioglu 2006): 1. Type of legs (anissodactyls, pamprodactyls, sydactyls, totipalmos, zygodactyls); 2. Beak shape (tall and compressed, conical, short and robust, recurved, curved, fine and pointed, hooked, slightly curved, pointed, straight, straight and fine, straight and pointed) and 3. Body size (large, medium, small) (Herrel et al. 2005; López-Ordoñez et al. 2015). The values ​​of the functional traits were obtained in the field and supplemented by secondary information.

To quantify functional diversity, we performed a cluster analysis to identify functional types of birds in each of the sampled habitats (Petchey and Gaston 2002; Casanoves et al. 2011). We also calculated two multidimensional-multifunctional indices, functional equity (FEve) and functional dispersion (FDis) (Mouillot et al. 2005; Laliberté and Legendre 2010). For these analyses, we used the statistical packages infoStat and FDiversity that connects to the statistical programme R with an interface written in Delphi with DCOM-R (Di Rienzo 2009; Casanoves et al. 2011).

Results

Richness and composition of bird assemblages

We registered 10 orders, 21 families, 56 genera and 63 species of birds (Table 1). In the wooded pasture, the richness was 55 species, followed by the Andean forest fragment with 44 species. The families with the highest abundances were Passerellidae with 282 individuals, followed by Parulidae with 185 and Trochilidae with 179. The genera with the highest number of individuals were Atlapetes (183), Myioborus (103) and Coeligena (103). In the Andean forest fragment, the two best represented families were Trochilidae with eight genera and Passerellidae with four and, in the wooded pasture, they were Trochilidae with seven genera and Tyrannidae with five.

Table 1.

Composition and richness of birds and their respective absolute and relative abundances in an Andean rural landscape of the Eastern Cordillera of Colombia. The five most abundant species for each cover are highlighted in bold.

Taxon name English name Code Absolute Abundance (AA) Relative abundance (RA%) Functional group
Fragments of Andean forest Wooded pasture Fragments of Andean forest Wooded pasture
Galliformes
Cracidae
Penelope montagnii Andean Guan Pem 3 0 0.718 0 G9
Columbiformes
Columbidae
Patagioenas fasciata Band-tailed Pigeon. Paf 0 15 0 1.789 G4
Zenaida auriculata Eared Dove Zea 0 3 0 0.358 G4
Cuculiformes
Cuculidae
Crotophaga ani Smooth-billed Ani Cra 0 33 0 3.938 G8
Piaya cayana Squirrel Cuckoo Pic 4 0 0.957 0 G8
Coccyzus americanus Yellow-billed Cuckoo Coa 2 5 0.478 0.597 G8
Apodiformes
Trochilidae
Adelomyia melanogenys Speckled Humming-bird Adm 18 6 4.307 0.716 G1
Chaetocercus heliodor Gorgeted Woodstar Chh 1 1 0.240 0.120 G1
Chaetocercus mulsant White-bellied Woodstar Chm 0 8 0 0.955 G1
Campylopterus falcatus Lazuline Sabrewing Caf 10 0 2.393 0 G1
Chlorostilbon poortmani Short-tailed Emerald Chp 1 1 0.240 0.120 G1
Coeligena prunellei Black Inca Cop 30 40 7.177 4.773 G1
Colibri coruscans Sparkling violet-ear Coc 2 4 0.479 0.478 G1
Colibri cyanotus Lesser Violetear Coy 18 14 4.307 1.671 G1
Heliangelus amethysticollis Amethyst-throated Sunangel. Hea 11 2 2.632 0.239 G1
Metallura tyrianthina Tyrian Metaltail. Met 3 9 0.718 1.074 G1
Pelecaniformes
Ardeidae
Ardea alba Great White Egret Ara 0 1 0 0.120 G9
Cathartiformes
Cathartidae
Coragyps atratus Black Vulture Cga 2 2 0.479 0.239 G9
Cathartes aura Turkey Vulture Caa 0 2 0 0.239 G9
Accipitriformes
Accipitridae
Rupornis magnirostris Roadside hawk. Rum 3 7 0.718 0.836 G4
Coraciiformes
Alcedinidae
Megaceryle torquate Ringed Kingfisher Meq 0 2 0 0.239 G9
Piciformes
Picidae
Colaptes rivolii Crimson-mantled Woodpeck-er. Cor 6 1 1.436 0.120 G7
Melanerpes formicivorus Acorn Woodpeck-er Mef 0 2 0 0.239 G7
Ramphastidae
Aulacorhynchus prasinus Emerald Toucanet Aup 0 2 0 0.239 G6
Passeriformes
Passerellidae
Arremon brunneinucha Chestnut-capped Brush-finch Arb 4 0 0.957 0 G3
Atlapetes albofrenatus Moustached Brush-finch Ata 26 54 6.221 6.444 G2
Atlapetes latinuchus Yellow-breasted Brush-finch Atl 32 71 7.656 8.473 G2
Chlorospingus canigularis Ashy-throated Chloro-spingus Chc 13 5 3.111 0.597 G2
Chlorospingus flavopectus Common Chloro-spingus Chf 17 2 4.067 0.239 G2
Zonotrichia capensis Rufous-collared Sparrow Zoc 2 56 0.479 6.683 G2
Turdidae
Catharus ustulatus Swainson’s Thrush Cau 0 4 0 0.478 G3
Turdus ignobilis Black-billed Thrush Tui 0 3 0 0.358 G3
Turdus fuscater Great Thrush Tuf 8 65 1.914 7.757 G4
Thraupidae
Diglossa albilatera White-sided Flower-piercer Dia 18 31 4.307 3.701 G4
Diglossa caerulescens Bluish Flower-piercer Dgc 0 1 0 0.120 G3
Diglossa cyanea Masked Flower-piercer Dic 5 8 1.197 0.955 G1
Stilpnia heinei Black-Capped Tanager Tah 4 7 0.957 0.836 G2
Sporathraupis cyanocephala Blue-capped Tanager Spc 13 35 3.111 4.177 G1
Tyrannidae
Elaenia frantzii Mountain Elaenia Elf 2 18 0.479 2.148 G1
Mecocerculus leucophrys White-banded Tyrannulet Mel 11 51 2.632 6.086 G1
Pitangus sulphuratus Great Kiskadee Pis 0 6 0 0.716 G4
Pyrrhomyias cinnamomeus Cinnamon Flycatcher Pyc 1 0 0.240 0 G3
Tyrannus melancholicus Tropical Kingbird Tym 0 10 0 1.194 G1
Zimmerius chrysops Golden-faced Tyrannulet Zic 3 5 0.718 0.597 G1
Troglodytidae
Troglodytes aedon House Wren Tra 0 13 0 1.552 G1
Henicorhina leucophrys Grey-breasted Wood Wren Hel 9 10 2.154 1.194 G1
Pheugopedius mystacalis Whiskered Wren Phm 1 0 0.240 0 G3
Icteridae
Icterus chrysater Yellow-backed Oriole Icc 26 44 6.221 5.251 G1
Sturnella magna Eastern Meadow-lark Stm 0 6 0 0.716 G4
Furnariidae
Lepidocolaptes lacrymiger Montane Wood-creeper. Lel 2 0 0.479 0 G5
Synallaxis azarae Azara´s Spinetail Sya 12 44 2.871 5.251 G1
Xenops rutilans Streaked Xenops Xer 2 1 0.479 0.120 G5
Parulidae
Mniotilta varia Black-and-white Warbler Mnv 1 2 0.240 0.239 G5
Myioborus miniatus Slate-throated Redstart Mym 39 45 9.331 5.370 G1
Myioborus ornatus Golden-fronted Whitestart Myo 13 6 3.111 0.716 G1
Myiothlypis coronate Russet-crowned Warbler Myc 9 0 2.154 0 G1
Setophaga fusca Blackburn-ian Warbler Sef 20 49 4.785 5.848 G1
Parkesia noveboracensis Northern Waterthrush Pan 0 1 0 0.120 G3
Fringillidae
Spinus psaltria Lesser Goldfinch Spp 1 2 0.240 0.239 G3
Spinus spinescens Andean Siskin Sps 1 1 0.240 0.120 G3
Virionidae
Vireo leucophrys Brown-capped Vireo Vil 9 19 2.154 2.268 G4
Vireo olivaceus Red-eye Vireo Vio 0 2 0 0.239 G3
Cardinalidae
Piranga rubra Summer Tanager Pir 0 1 0 0.120 G3

We obtained a high proportion of avian species richness from the two cover types. The percentage of representativeness was 94.39% and 94.38%, for the wooded pastureland and the Andean forest fragment, respectively (Fig. 2A–C).

Figure 2. 

A Sampling coverage by number of bird individuals in a rural Andean landscape of the Eastern Cordillera of Colombia. Rarefaction (solid lines), and extrapolated (dotted lines). B Diversity of species by number of individuals in a rural Andean landscape of the Eastern Cordillera of Colombia. Interpolation (solid line) and extrapolation (dashed line). C Sampling coverage by number of bird species in a rural Andean landscape of the Eastern Cordillera of Colombia. Interpolation (solid line) and extrapolation (dashed line). The shadows on the curves correspond to the 95% confidence intervals.

Structure of the bird assemblage

In the wooded pasture, we obtained a relative abundance of 66% (838 individuals), with nine species represented by only one individual and 10 species with two (Table 1). In the Andean forest fragment, the relative abundance was 34% (418), represented by seven unique individuals and seven species with two individuals (Table 1). The hierarchical distribution of the species abundance was different between the two vegetation covers (Fig. 3). For the wooded pasture, the species with the highest relative abundances were Atlapetes latinuchus, Turdus fuscater, Zonotrichia capensis, Atlapetes albofrenatus and Mecocerculus leucophrys and, for the Andean forest fragment, they were Myioborus miniatus, Atlapetes latinuchus, Coeligena prunellei, Atlapetes albofrenatus and Icterus chrysater. The species Atlapetes latinuchus and Atlapetes albofrenatus had high relative abundances in both plant cover types (Fig. 3).

Figure 3. 

Range-abundance curve of the bird species for two covers evaluated in a rural landscape an Andean rural landscape of the Eastern Cordillera of Colombia. The green line corresponds to the cover of wooded grassland. Reference the codes in relation to Table 1.

The species that contributed the most to the dissimilarity between the vegetation covers were Zonotrichia capensis (SIMPER: 7.865%), Turdus fuscater (SIMPER: 7.445%), Mecocerculus leucophrys (SIMPER: 5.605%) and Atlapetes latinuchus (SIMPER: 5.132%), as well as species Crotophaga ani (SIMPER: 4.944%), Synallaxis azarae (SIMPER: 4.788%), Setophaga fusca (SIMPER: 4.627%), Diglossa albilatera (SIMPER: 3.957%) and Atlapetes albofrenatus (SIMPER: 3.935%).

Beta diversity

Of 63 species found, 19 were exclusive to the wooded grassland cover and eight were exclusive to the plant cover type of the Andean forest fragment (Table 1). The dissimilarity between the coverages was 43%. The transects of each cover was also a high dissimilarity, 48% amongst the transects of the Andean forest fragment and 43% amongst those of the wooded pasture. We did not find differences between the richness and composition of the Andean forest fragment and the wooded pasture (ANOSIM: R = 1, p = 0.32).

Functional diversity

We identified nine functional types: Group 1 (G1) was the best represented, made up of mainly small species, with anissodactyl and pamprodactyl legs and diets based on the ingestion of insects, fruits, nectar or both. Group 2 (G2) was represented by species of small size, trappers and foragers with anissodactyl and pamprodactyl legs that can occupy the shrub and herbaceous strata (Table 2). In the Andean forest fragment, we recorded eight of the nine groups identified in the entire study and, in the wooded pasture, all nine groups were represented. The functional equity (FEve) was 0.51 in the Andean forest fragment cover and differences are shown between the roles played by the dominant species (FDiv = 0.74). In the wooded pasture, we obtained a lower functional equity (FEve = 0.45) than in the Andean forest fragment. Similarly, role differentiation was presented by the dominant functional species (FDiv = 0.81).

Table 2.

Groups or functional types of birds in a rural Andean landscape of the Eastern Cordillera of Colombia. Each group was generated from cluster analysis for coverage type.

Group Number of species Characteristics Coverage
G1 23 Mainly small, anisodactyl and pamprodactyl legged species, with diets based mostly on insects, fruits and/or nectar. Fragment of Andean forest and wooded pasture.
G3 12 Species of small size, of trapping and foraging habits, with anisodactyl and pamprodactyl legs, which can occupy the arboreal, shrubby and herbaceous levels. Fragment of Andean forest and wooded pasture.
G4 8 Small and medium-sized species, which present anisodactyl legs, are mostly catchers and scavengers, with straight beaks dominating, followed by hooked ones. Fragment of Andean forest and wooded pasture.
G2 6 Species of small size, with anisodactyl legs, this group is dominated by species with a not very specific diet, which includes fruits, seeds, insects and leaves, most of the species in this group presented conical beaks. Fragment of Andean forest and wooded pasture.
G9 5 Large species, almost all of which occupy mainly the arboreal stratum, their diets include the ingestion of carrion, meat and fruits. Fragment of Andean forest and wooded pasture.
G5 3 Small species, with insectivorous diet of curved beak, that occupy the shrub and sapling levels. Fragment of Andean forest and wooded pasture.
G8 3 Medium-sized, curved-billed, zygodactyl, trappers or foragers, living in monospecific and/or solitary flocks. Fragment of Andean forest and wooded pasture.
G7 2 Species of various sizes, of foraging habits, insectivorous, with zygodactyl legs, with straight beaks, they mainly occupy the arboreal and shrub levels. Fragment of Andean forest and wooded pasture.
G6 1 A single, medium-sized, foraging species with zygodactyl legs and a high, compressed beak that occupies the arboreal stratum and bases its diet on fruit and insects. Wooded pasture.

Discussion

Taxonomic diversity of birds

The diversity of birds in the rural landscape for each of their representative cover types was low in relation to other fragmented landscapes in Colombia, such as those found in the tropical and sub-Andean region of the Las Quinchas Mountain range in the Eastern Cordillera of Colombia (García-Monroy et al. 2020). Although the rural landscape of our study was completely in the Andean life region, for these sectors, there are records of a higher number of species (Córdoba-Córdoba and Echeverry-Galvis 2006; Jiménez 2010). In this regard, Trzcinski et al. (1999) hypothesise that the presence of bird species in the landscape is more related to the amount of habitat present than to the degree of fragmentation. Our rural landscape, despite being in areas bordering a protected area, has had a history of transformation in the last century, where most of the original coverage has diminished to critical points or has even disappeared (Etter 1993). This fact shows a configuration of the current landscape made up mostly of pastures for livestock, crops and small fragments of intervening forest, many of them the product of natural regeneration in the last four decades (Chavarro 2005).

The fact that, in the wooded pasture, the highest species richness value was recorded compared to the Andean forest fragment shows several ecological aspects of landscapes, as documented by Tabarelli et al. (2010), for fragmented landscapes of the Atlantic Forest. First, the greater heterogeneity of the wooded pastures gives rise to various areas that offer more resources, both for specialist species and generalists in choice of habitat. Second, the greatest amount of edge habitats are found for the wooded grasslands, facilitating edge effects: higher richness and higher detection values ​​for the ecotonal area (e.g. for the study area the forest edges, areas around roads or living fences), as documented in multiple studies (García-Romero et al. 2019). Third, the structure of vegetation in Andean forests with the presence of foreign species, such as Pinus radiata (Don, 1836) and Eucalyptus globulus (Labill, 1800), limits food resources and nesting sites for many bird species (Zurita et al. 2006); and this is directly related to the alpha diversity for these plant cover types.

Another ecological aspect that has a direct effect on the species richness values ​​in the sample cover types and that is often not considered because of inferences towards a specific taxonomic group is the detection capacity. This can be managed with other methodologies. However, for the purpose of this study and that of observing the functional attributes, direct observation of the species was necessary. This fact together with the fact that the wooded grassland area had more heterogeneity than the Andean forest fragment and given the complex plant structure and homogeneous nature of the latter, the type of plant cover limited observations, while they were facilitated in areas of wooded grasslands with open areas (Enríquez-Lenis et al. 2007).

In terms of composition and structure, the differences recorded between the plant cover types are due, like the species richness, to the structural complexity in terms of the vegetation of each of the plant cover type. This is a general pattern identified in rural landscapes (Cook et al. 2002). In contrast, the conjunction of remnant vegetation, living fences and production areas with isolated trees in wooded pastures creates suitable locations for the establishment and occupation of sites corresponding to species with a wide spectrum of habitat, generalists in the choice of resources, such as Turdus fuscater, Zonotrichia capensis and Tyrannus melancholicus (Ocampo-Peñuela and Pimm 2015). In the case of the Andean forest fragment, the assemblage has generalist species, but also there are others with some degree of specialisation, for example, Pyrrhomyias cinnamomeus and Colaptes rivolii (Avendaño et al. 2013). This is a pattern like that recorded in other fragmented natural systems (Zurita et al. 2006; Tabarelli et al. 2010; Hadley et al. 2018).

The contrasting plant cover in the landscape contributes to the turnover of species within the types of cover observed in the wooded pasture, as it is the dominant cover in the north-eastern Andean landscapes after grasslands (Etter 1998). In this way, wooded grasslands serve as a transition zone between the open areas and the Andean forest fragment. However, it is important to bear in mind that both plant covers have a different structure and contribute unique species to the assemblage of birds in the landscape. This is a basic input when taking conservation actions in this type of region since this contrast of areas contributes greatly to the maintenance of biodiversity in these transformed landscapes (Lôbo et al. 2011).

The exchange of species found in the study area can be linked to the heterogeneity that is present in tropical landscapes altered by changes in land use. The land-use changes directly affect the composition of birds within the landscape vegetation coverage; and according to the spatial scale of the analysis, it can generate variations within the analysed coverage, together with other filters and biotic variables of each landscape (Morante-Filho et al. 2016).

Functional diversity

From the results, we observe that there is higher functional diversity in the wooded pasture with respect to the Andean forest cover. There is also a marked relationship between functional equity and the distribution of wealth between functional attributes (Luck et al. 2013). However, the fact that functional diversity does not decrease with the degree of simplification of the structure of the plant cover reflects a result that is observed infrequently in fragmented landscapes, when the biodiversity values ​​are congruent with the complexity of the structure of the vegetation that is evaluated. It also provides information on the response of the assemblages to these new landscapes, where the greater heterogeneity of the wooded landscapes could provide a greater number of resources for the maintenance of the bird assemblage and the history of disturbances of the fragments clearly reflects the composition and structure of current assemblages. In this way, the fragments of secondary forests that form the rural landscapes of the north-eastern Andes of Colombia are the product of regeneration, restoration or both during the last three decades, where the vegetation has reached structural maturity, but perhaps the faunal groups that occupy these areas do not follow the same maturity line (Etter 1993). This fact represents a priority topic for evaluation in this type of rural landscape.

Regarding functional divergence, the values ​​obtained for the two vegetation types reflect high niche differentiation, allowing better use of the resources that the plant cover type provides and reduces the levels of competition (Ding et al. 2017). In addition to this, we found a higher abundance of frugivorous and nectarivorous birds in the plant cover of the wooded grasslands. These species may be closely related to the passive restoration of the site since they influence pollination and seed dispersal, like that documented by Tscharntke et al. (2012). In addition, the absence of group G6 in the Andean forest fragment cover, represented only by Aulacorhynchus prasinus (Gould, 1833) in wooded pasture, may be attributed to the scarcity of fruits in the forest. This scarcity of food could generate a differential effect on the distribution of the functional attributes and, therefore, a functional contrast between the coverages.

Implications for landscape management and bird conservation

Although the wooded pasture presented a better state at a taxonomic and functional level, it is important to maintain the remnants of Andean forests, since they contribute to the functional richness of the area, in general and to an increase in the diversity of a landscape with contrasting hedges. The heterogeneity of the landscape generated a differential effect on the patterns of species richness and also on the patterns of species turnover and positively affected birds, along with the effect of a system that included semi-natural habitats, low-intensity agriculture and various mosaics of small-scale land-use types.

The contrast of cover allowed the birds´ greater mobility with fewer interruptions within the landscape since bird assemblages tended to avoid clearly-defined forest edges and completely open areas. A strategy for the study area is the enrichment of living fences and wooded pastures that, due to their high heterogeneity, provide good resource availability for birds in the rural landscape.

Acknowledgements

Roberto Chavarro Chavarro, owner of the Natural Reserve of the Civil Society “Rogitama Biodiversidad”, partially financed this research and provided logistical support for the mobilisation between the different sampling coverages. The Biodiversity and Conservation research group of the Pedagogical and Technological University of Colombia provided tutorials for the statistical analyses of this research. This article is published as a product of the Project “The biodiversity of Boyacá: Complementation and synthesis through altitudinal gradients and implementations of its incorporation in projects of social appropriation of knowledge and the effects of climate change, Boyacá” BPIN 2020000100003.

References

  • Avendaño JE, Cortés-Herrera JO, Briceño-Lara ER, Rincón-Guarín DA (2013) Crossing or bypassing the Andes: A commentary on recent range extensions of cis-Andean birds to the west of the Andes of Colombia. Orinoquia (Universidad Tecnologica de los Llanos Orientales) 17(2): 207–214. https://doi.org/10.22579/20112629.18
  • Bilenca DN, Abba AM, Corriale MJ, Carusi LCP, Pedelacq ME, Zufiaurre E (2017) De venados, armadillos y coipos: Los mamíferos autóctonos frente a los cambios en el uso del suelo, los manejos agropecuarios y la presencia de nuevos elementos en el paisaje rural. Mastozoología Neotropical 24(2): 277–287.
  • Carvajal-Castro JD, Ospina-L AM, Toro-López Y, Pulido-G A, Cabrera-Casas LX, Guerrero-Peláez S, Vargas-Salinas F (2019) Birds vs. bricks: Patterns of species diversity in response to urbanization in a Neotropical Andean city. PLoS ONE 14(6): e0218775. https://doi.org/10.1371/journal.pone.0218775
  • Cavelier J, Etter A (1995) Deforestation of montane forests in Colombia as a result of illegal plantations of opium (Papaver somniferum). In: Churchill SP, Balslev H, Forero E, Luteyn JL (Eds) Biodiversity and Conservation of Neotropical Montane Forests, Proceedings of the Neotropical Montane Forest Biodiversity and Conservation Symposium, The New York Botanical Garden, 21–26 june 1993, 541–550.
  • Chao A, Jost L (2012) Coverage‐based rarefaction and extrapolation: Standardizing samples by completeness rather than size. Ecology 93(12): 2533–2547. https://doi.org/10.1890/11-1952.1
  • Chao MT, Lo SH (1994) Maximum likelihood summary and the bootstrap method in structured finite populations. Statistica Sinica: 389–406.
  • Chao A, Gotelli NJ, Hsieh TC, Sander EL, Ma KH, Colwell RK, Ellison AM (2014) Rarefaction and extrapolation with Hill numbers: A framework for sampling and estimation in species diversity studies. Ecological Monographs 84(1): 45–67. https://doi.org/10.1890/13-0133.1
  • Chavarro R (2005) Ilustraciones y fotografías de aves-Coeligena prunellei Inca Negro-Black Inca (Príncipe de Arcabuco). Boletín SAO 15(2): 118–122.
  • Collinge SK (2009) Ecology of fragmented landscapes. Johns Hopkins University Press, Baltimore, 341 pp.
  • Colwell RK, Coddington JA (1994) Estimating terrestrial biodiversity through extrapolation. Philosophical Transactions of the Royal Society of London – Series B, Biological Sciences 345(1311): 101–118. https://doi.org/10.1098/rstb.1994.0091
  • Colwell RK, Chao A, Gotelli NJ, Lin S-Y, Mao CX, Chazdon RL, Longino JT (2019) Models and estimators linking individual-based and sample-based rarefaction, extrapolation, and comparison of assemblages. Journal of Plant Ecology 5(1): 3–21. https://doi.org/10.1093/jpe/rtr044
  • Córdoba-Córdoba S, Echeverry-Galvis MÁ (2006) Diversidad de aves de los bosques mixtos y de roble del Santuario de Flora y Fauna de Iguaque, Boyacá. I Simposio Internacional de Roble y Ecosistemas Asociados, Memorias, 119–128.
  • Di Rienzo JA, InfoStat versión (2009) Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Argentina. http://www.infostat.com.ar
  • Ding N, Weifang Y, Zhou Y, González-Bergonzoni I, Zhang J, Chen K, Vidal N, Jeppesen E, Liu Z, Wang B (2017) Different responses of functional traits and diversity of stream macroinvertebrates to environmental and spatial factors in the Xishuangbanna watershed of the upper Mekong River Basin, China. The Science of the Total Environment 574: 288–299. https://doi.org/10.1016/j.scitotenv.2016.09.053
  • Enríquez-Lenis ML, Sáenz JC, Ibrahim M (2007) Richness, abundance and diversity of birds and their relationship with tree cover in an agricultural landscape dominated by cattle in the sub-humid tropics of Costa Rica. Agroforestería en las Américas 45: 49–57. [CATIE]
  • Etter A (1993) Diversidad ecosistémica en Colombia hoy. Nuestra Diversidad Biológica, 43–61.
  • Etter A (1998) Bosque húmedo tropical. Informe nacional sobre el estado de la diversidad. Instituto de Investigación de Recursos Biológicos Alexander von Humboldt, PNUMA, Ministerio del Medio Ambiente. Bogotá, Colombia, 106–133.
  • Gale GA, Round PD, Pierce AJ, Nimnuan S, Pattanavibool A, Brockelman WY (2009) A field test of distance sampling methods for a tropical forest bird community. The Auk 126(2): 439–448. https://doi.org/10.1525/auk.2009.08087
  • Galindo R (2000) Esquema de Ordenamiento Territorial del Municipio de Arcabuco-Boyacá. Planificación económica, social, dimensión territorial y aprovechamiento sostenible (Ley 388 de 1997). Gobierno municipal de Arcabuco, Boyacá, Colombia, 321 pp.
  • García-Monroy JS, Morales-González ÓE, Carvajal-Cogollo JE (2020) New bird records for the Serranía de Las Quinchas, Colombia: Inventory update and comments on distributions in an altitudinal gradient. Check List 16(6): 1475–1518. https://doi.org/10.15560/16.6.1475
  • García-Romero A, Vergara PM, Granados-Peláez C, Santibañez-Andrade G (2019) Landscape-mediated edge effect in temperate deciduous forest: Implications for oak regeneration. Landscape Ecology 34(1): 51–62. https://doi.org/10.1007/s10980-018-0733-x
  • Hadley AS, Frey SJ, Robinson WD, Betts MG (2018) Forest fragmentation and loss reduce richness, availability, and specialization in tropical hummingbird communities. Biotropica 50(1): 74–83. https://doi.org/10.1111/btp.12487
  • Herrel A, Podos J, Huber SK, Hendry AP (2005) Bite performance and morphology in a population of Darwin’s finches: Implications for the evolution of beak shape. Functional Ecology 19(1): 43–48. https://doi.org/10.1111/j.0269-8463.2005.00923.x
  • Howe RW, Niemi GJ, Lewis SJ, Welsh DA (1997) A standard method for monitoring songbird populations in the Great Lakes region. The Passenger Pigeon 59(3): 183–194.
  • Ikin K, Yong DL, Lindenmayer DB (2016) Effectiveness of woodland birds as taxonomic surrogates in conservation planning for biodiversity on farms. Biological Conservation 204: 411–416. https://doi.org/10.1016/j.biocon.2016.11.010
  • IPBES (2019) Summary for policymakers of the global assessment report on biodiversity and ecosystem services of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services. IPBES Secretariat, Bonn, Germany, 56 pp.
  • Issa MAA (2019) Diversity and abundance of wild birds species’ in two different habitats at Sharkia Governorate, Egypt. Journal of Basic & Applied Zoology 80(1): e34. https://doi.org/10.1186/s41936-019-0103-5
  • Laliberté E, Legendre P (2010) A distance‐based framework for measuring functional diversity from multiple traits. Ecology 91(1): 299–305. https://doi.org/10.1890/08-2244.1
  • Larsen FW, Bladt J, Balmford A, Rahbek C (2012) Birds as biodiversity surrogates: Will supplementing birds with other taxa improve effectiveness? Journal of Applied Ecology 49(2): 349–356. https://doi.org/10.1111/j.1365-2664.2011.02094.x
  • Lawton JH, Bignell DE, Bolton B, Bloemers GF, Eggleton P, Hammond PM, Hodda M, Holt RD, Larsen TB, Mawdsley NA, Stork NE, Srivastava DS, Watt AD (1998) Biodiversity inventories, indicator taxa and effects of habitat modification in tropical forest. Nature 391(6662): 72–76. https://doi.org/10.1038/34166
  • Leach EC, Burwell CJ, Ashton LA, Jones DN, Kitching RL (2016) Comparison of point counts and automated acoustic monitoring: Detecting birds in a rainforest biodiversity survey. The Emu 116(3): 305–309. https://doi.org/10.1071/MU15097
  • Lôbo D, Leão T, Melo FP, Santos AM, Tabarelli M (2011) Forest fragmentation drives Atlantic Forest of northeastern Brazil to biotic homogenization. Diversity & Distributions 17(2): 287–296. https://doi.org/10.1111/j.1472-4642.2010.00739.x
  • López-Ordoñez JP, Stiles FG, Parra-Vergara JL (2015) Protocolo para la medición de rasgos funcionales en aves. In: Salgado-Negret B (Ed.) La ecología funcional como aproximación al estudio, manejo y conservación de la biodiversidad: protocolos y aplicaciones. Instituto de Investigación de Recursos Biológicos Alexander von Humboldt. Bogotá, D. C. Colombia, 80–126.
  • Luck GW, Carter A, Smallbone L (2013) Changes in bird functional diversity across multiple land uses: Interpretations of functional redundancy depend on functional group identity. PLoS ONE 8(5): e63671. https://doi.org/10.1371/journal.pone.0063671
  • McMullan M, Donegan TM (2014) Field Guide to the Birds of Colombia, 2nd edn. Fundación ProAves, Bogotá.
  • Morante-Filho JC, Arroyo-Rodríguez V, Faria D (2016) Patterns and predictors of β diversity in the fragmented Brazilian Atlantic Forest: A multiscale analysis of forest specialist and generalist birds. Journal of Animal Ecology 85(1): 240–250. https://doi.org/10.1111/1365-2656.12448
  • Newbold T, Scharlemann JP, Butchart SH, Şekercioğlu ÇH, Alkemade R, Booth H, Purves DW (2013) Ecological traits affect the response of tropical forest bird species to land-use intensity. Proceedings of the Royal Society B: Biological Sciences 280(1750): 2012–2131. https://doi.org/10.1098/rspb.2012.2131
  • Oldeland J, Wesuls D, Rocchini D, Schmidt M, Jürgens N (2010) Does using species abundance data improve estimates of species diversity from remotely sensed spectral heterogeneity? Ecology 10: 390–396. https://doi.org/10.1016/j.ecolind.2009.07.012
  • Pettingill OS (1985) Ornithology in Laboratory and Field. 5th edn. Academic Press, London, 409 pp.
  • Ralph CJ, Geupel GR, Pyle P, Martin TE, DeSante DF, Milá B (1996) Manual de métodos de campo para el monitoreo de aves terrestres. Gen. Tech. Rep. PSW-GTR-159. Albany, CA: US Department of Agriculture, Forest Service, Pacific Southwest Research Station, 159 pp. https://doi.org/10.2737/PSW-GTR-159
  • Ranganathan J, Daily GC (2008) La biogeografía del paisaje rural: oportunidades. Evaluación y conservación de biodiversidad en paisajes fragmentados de Mesoamérica, 15 pp.
  • Rangel-Ch JO, Lozano-C G (1986) Un perfil de vegetación entre La Plata (Huila) y el volcán del Puracé. Caldasia: 503–547.
  • Rangel-Ch JO, Lowy-C PD, Aguilar-P M, Garzón-C A (1997) Tipos de vegetación en Colombia. Una aproximación al conocimiento de la terminología fitosociológica, fitoecológica y de uso común. In: Rangel-Ch JO, Lowy-C P, Aguilar-P M (Eds) Diversidad Biótica II. Tipos de Vegetación en Colombia. Universidad Nacional de Colombia-Instituto de Ciencias Naturales, Instituto de hidrología, Meteorología y estudios Ambientales (IDEAM)-Ministerio del Medio Ambiente, Comité de Investigaciones y Desarrollo Científico-CINDEC.U.N, Academia Colombiana de Ciencias Exactas, Físicas y Naturales. Bogotá, 304–382.
  • Remsen JV, Areta JI, Bonaccorso E, Claramunt S, Jaramillo A, Pacheco JF, Robbins MB, Stiles FG, Stotz DF, Zimmer KJ (2020) A classification of the bird species of South America. American Ornithological Society Version [2020]. http://www.museum.lsu.edu/~Remsen/SACCBaseline.htm
  • Restall RL, Rodner C, Lentino M (2007) Birds of Northern South America: Plates and maps (Vol. 2). Yale University Press, 880 pp.
  • Ridgely RS, Tudor G (2009) Field Guide to the songbirds of South America: the passerines. University of Texas Press, 748 pp.
  • Stotz DF, Fitzpatrick JW, Parker TA, Moskovits DK (1996) Neotropical birds: ecology and conservation. University of Chicago Press, 293–377.
  • Tabarelli M, Aguiar AV, Ribeiro MC, Metzger JP, Peres CA (2010) Prospects for biodiversity conservation in the Atlantic Forest: Lessons from aging human-modified landscapes. Biological Conservation 143(10): 2328–2340. https://doi.org/10.1016/j.biocon.2010.02.005
  • Tscharntke T, Tylianakis JM, Rand TA, Didham RK, Fahrig L, Batary P, Bengtsson J, Clough Y, Crist TO, Dormann CF, Ewers RM, Fründ J, Holt RD, Holzschuh A, Klein AM, Kleijn D, Kremen C, Landis DA, Laurance W, Lindenmayer D, Scherber C, Sodhi N, Steffan-Dewenter I, Thies C, van der Putten WH, Westphal C (2012) Landscape moderation of biodiversity patterns and processes‐eight hypotheses. Biological Reviews of the Cambridge Philosophical Society 87(3): 661–685. https://doi.org/10.1111/j.1469-185X.2011.00216.x
  • Villard MA, Trzcinski MK, Merriam G (1999) Fragmentation effects on forest birds: Relative influence of woodland cover and configuration on landscape occupancy. Conservation Biology 13(4): 774–783. https://doi.org/10.1046/j.1523-1739.1999.98059.x
  • Villéger S, Mason NWH, Mouillot D (2008) New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89(8): 2290–2301. https://doi.org/10.1890/07-1206.1
  • Westgate MJ, Barton PS, Lane PW, Lindenmayer DB (2014) Global meta-analysis reveals low consistency of biodiversity congruence relationships. Nature Communications 5(1): 1–8. https://doi.org/10.1038/ncomms4899
  • Wilman H, Belmaker J, Simpson J, de la Rosa C, Rivadeneira MM, Jetz W (2014) EltonTraits 1.0: Species‐level foraging attributes of the world’s birds and mammals: Ecological Archives E095‐178. Ecology 95(7): 2027–2027. https://doi.org/10.1890/13-1917.1
  • Zurita GA, Rey N, Varela DM, Villagra M, Bellocq MI (2006) Conversion of the Atlantic Forest into native and exotic tree plantations: Effects on bird communities from the local and regional perspectives. Forest Ecology and Management 235(1–3): 164–173. https://doi.org/10.1016/j.foreco.2006.08.009