Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: 51382, enero-diciembre 2023 (Publicado May. 04, 2023)

Community structure of raptors in the páramo landscape

of the Ecuadorian Andes

Santiago Barros1*; http://orcid.org/0000-0003-2647-6579

Paul Porras1; http://orcid.org/0000-0002-0428-9070

Boris Landázuri1; http://orcid.org/0000-0001-5034-124X

David C. Siddons1; https://orcid.org/0000-0003-3305-2969

Steven C. Latta2; https://orcid.org/0000-0003-3789-9470

Pedro X. Astudillo1; https://orcid.org/0000-0002-9945-9414

1. Laboratorio de Ecología, Escuela de Biología, Universidad del Azuay, Cuenca, Ecuador; jsanty.b1@gmail.com

(Correspondence*); paulporraspolo@gmail.com; borisland004@gmail.com; dsiddons@uazuay.edu.ec;

pastudillow@uazuay.edu.ec

2. National Aviary, Allegheny Commons West, Pittsburgh, Pennsylvania, USA; steven.latta@aviary.org

Received 01-VII-2022. Corrected 05-X-2022. Accepted 13-IV-2023.

ABSTRACT

Introduction: Habitat alterations result in biodiversity loss, particularly in regions with high levels of diversity

and endemism. Raptors are an essential part of the functionality and stability of ecosystems and indicators of

habitat quality. In the paramo grassland ecosystems in the high Andes of Northern South America, raptors con-

tain a high concentration of threatened species.

Objective: To describe the raptor community structure and determine the species associations.

Methods: We made monthly raptor counts in eight transects from October 2021 to September 2022 and used a

principal component analysis to determine species associations.

Results: We identified 149 individuals (seven species, three families) in two communities: abundant

(Carunculated Caracara, Variable Hawk, Andean Condor and Turkey Vulture; PCI = 47 %), and scarce

(Cinereous Harrier, Peregrine Falcon and Aplomado Falco; PCII = 27 %).

Conclusion: We provide a valid description and understanding of raptor community structure, identifying two

communities and the dynamics between them. The first is characterized by an increased abundance of general-

ist and regionally common species, when the abundance of these species decreases, the second community is

defined, characterized by an increase in the abundance of specialist and rare species at the local scale.

Key words: Macizo del Cajas biosphere reserve; protected areas; field methods; raptor census; community

analysis.

RESUMEN

Estructura de la comunidad de rapaces en el paisaje de páramo de los Andes ecuatorianos.

Introducción: Las alteraciones del hábitat provocan la pérdida de biodiversidad, especialmente en regiones con

altos niveles de diversidad y endemismo. Las aves rapaces son una parte esencial de la funcionalidad y estabili-

dad de los ecosistemas, y son indicadores de la calidad del hábitat. En los ecosistemas de páramo en los Andes

del norte de Sudamérica, hay una concentración de especies rapaces amenazadas.

https://doi.org/10.15517/rev.biol.trop..v71i1.51382

CONSERVATION

2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e51382, enero-diciembre 2023 (Publicado May. 04, 2023)

INTRODUCTION

Habitat alterations associated with glob-

al changes negatively influence ecosystems

(Hooper et al., 2012). For instance, in tropical

montane areas there is an urgent need to moni-

tor biodiversity (Rakotomalala et al., 2021;

Roach et al., 2020). For example, in regions

of high diversity and endemism, such as the

tropical high Andes, rapid land-use change

results in an increase in habitat degradation,

and this conversion of natural habitats is linked

to a biodiversity loss (Myers et al., 2000). Birds

are indicators of ecosystem health, being an

integral component of habitats and important

to ecosystem services (Hudson et al., 2014;

Sekercioglu, 2006). Raptors and scavengers

provide important services such as prey con-

trol and recycling of carcasses, which controls

the spread of diseases (Bregman et al., 2014;

Sekercioglu, 2006). Raptors are directly related

to ecosystem health and are also considered

indicator species because they have differ-

ent degrees of sensitivity as their presence or

absences indicates habitat changes (Butet et al.,

2022; Pruscini et al., 2016; Sekercioglu, 2006).

The páramo is a distinctive ecosystem of

the high Andes of Northern South America

(Neill, 1999). Here, raptors stand out as a com-

munity with a high concentration of threatened

species, whose populations are in persistent

decline due to illegal hunting and habitat

loss (Ballejo et al., 2018; Naveda-Rodríguez

et al., 2016; Plaza & Lambertucci, 2020).

Important threatened species in this commu-

nity include Vultur gryphus (Andean Condor),

Falco peregrinus (Peregrine Falcon), Falco

femoralis (Aplomado Falcon) and endemics

such as Phalcoboenus carunculatus (Caracara

Curiquingue) (Fjeldsa & Krabbe, 1990; Freile

& Restall 2018; Freile et al., 2019; Ridgely &

Greenfield, 2001; Stattersfield et al., 1998).

Therefore, to improve monitoring efforts for

the high Andean raptor community, formal

descriptions of field methods and data analy-

sis of the community assemblage is crucial in

order to improve management and conserva-

tion plans in the region.

In the páramo landscape of the Southern

Andes of Ecuador, preliminary monitoring

efforts have focused on intensive searches and

ecological modelling at a species scale (i.e.,

species-by-species manner), notably include

threatened species such as V. gryphus (e.g.,

Astudillo et al., 2011; Astudillo et al., 2016;

Naveda et al., 2016). However, no efforts have

concentrated on the entire raptor community.

Furthermore, the raptor community is charac-

terised by low population densities across large

areas (Newton, 1979; Pruscini et al., 2016),

resulting in limited efforts to monitor the entire

raptor community, as well as complications in

data analyses due to low detections, evidencing

the need for robust monitoring and analysing

protocols. In this context, the present study

assesses the high Andean raptor community in

Objetivo: Describir la estructura de la comunidad de aves rapaces y determinar las asociaciones entre las

especies.

Métodos: Hicimos conteos mensuales de rapaces en ocho transectos, de octubre 2021 a setiembre 2022 y usamos

un análisis de componentes principales para determinar las asociaciones entre especies.

Resultados: Identificamos 149 individuos (siete especies, tres familias) en dos comunidades: abundantes (e.g.,

Caracara Curiquingue, Gavilán Variable, Cóndor Andino y Gallinazo Cabecirrojo; PCI = 47 %), y poco abun-

dantes (e.g., Caracara Curiquingue, Gavilán Variable, Cóndor Andino y Gallinazo Cabecirrojo; PCII = 27 %).

Conclusiones: Nuestro enfoque proporciona una descripción y comprensión válida de la estructura de la comu-

nidad de rapaces. Identificamos dos comunidades y la dinámica entre ellas. La primera se caracteriza por una

mayor abundancia de especies generalistas y regionalmente comunes, cuando la abundancia de estas especies

disminuye, se define la segunda comunidad, caracterizada por un aumento de la abundancia de especies espe-

cialistas y raras a escala local.

Palabras clave: reserva de la biosfera Macizo del Cajas; áreas protegidas; métodos de campo; monitoreo de

rapaces; análisis de la comunidad.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: 51382, enero-diciembre 2023 (Publicado May. 04, 2023)

the páramo grassland ecosystem of Southern

Andes of Ecuador through annual monitoring

across transects. Community structure is then

explored by means of multivariate analysis (i.e.,

principal components) to determine the species

associations that comprise the community.

MATERIALS AND METHODS

Study area: Our study was carried out the

core area of the Macizo del Cajas biosphere

reserve in 31 761 ha (3 % of the biosphere

reserve) of protected páramos in the province

of Azuay, Southern Ecuador (Fig. 1). The

study boundaries include the Quimsacocha

National Recreation Area and buffer zone (i.e.,

10 km radius; 3°3’16” S & 79°14’ 56” W). The

monitoring encompassed around 7 434 ha (i.e.,

monitoring area influence; Fig. 1). The land-

scape is characterized by an irregular topogra-

phy composed of deep, U-shaped valleys, steep

slopes, with rivers on the valley floors and rock

mounds at mountain tops (Rodríguez et al.,

2014). The elevational range in the study area

is 3 430 m.a.s.l. to 3 900 m.a.s.l. The monthly

average temperature is 5.4 °C with a maximum

of 13.8 °C and a minimum of -0.9 °C. Annual

rainfall varies from 1 000 mm to 1 250 mm. The

highest precipitation occurs between December

and May (Campozano et al., 2016; Ochoa-Sán-

chez et al., 2018). The vegetation is dominated

by páramo grassland (90 % of the vegetation

cover), an open habitat with herbaceous plants

(mainly of the genus Calamagrostis) aggre-

gated in tussocks, and associated with shrubby

plants of the genera Chuquiraga, Gynoxys,

Monticalia, Valeriana and Loricaria (Baquero

et al., 2004; Neill, 1999).

Bird monitoring: Raptor monitoring fol-

lowed the protocols described by Astudillo et

al., (2011) adapted from Ralph et al., (1996) for

the Southern Andes of Ecuador. In total, eight

Fig. 1. Map showing the study area and location of eight transects for raptor monitoring in the páramo ecosystem, high Andes

of Southern Ecuador. The grey shaded polygon represents the Quimsacocha National Recreation Area. The monitoring area

influence is 7 434 ha. The secondary map shows the province of Azuay (grey polygon) in Ecuador.

4Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e51382, enero-diciembre 2023 (Publicado May. 04, 2023)

transects of 2 km in length separated by at least

700 m were established. The distance between

transects was defined to ensure data indepen-

dence. All transects were located in wide-open

sites to ensure an observation radius of at least

1 km. To avoid double counting, censuses were

carried out by two observers who walked each

transect at a constant speed and recorded all

raptor individuals seen, including those flying

overhead. Transects were surveyed only on

days with good weather conditions, avoiding

periods of rain, fog, and low visibility. Each

transect was conducted for three hours once a

month from October 2021 to September 2022,

with surveys occurring between the hours

of 07:00 to 17:00. The total surveying effort

was 288 hours of observation. The transects

were walked in a random order each month.

Taxonomic identification of species follows the

classification of the South American Classifi-

cation Committee (Remsen et al., 2021).

Data analysis: Total abundance was con-

sidered as the sum of all individuals per species

and per transect (Nur et al., 1999). Community

structure was described by principal compo-

nent analysis (PCA) (Gewers et al., 2021;

Huettmann & Diamond, 2001). This technique

is one of the most widely used approaches for

the analysis and description for biological com-

munity data (Vaughan & Ormerod, 2005). The

PCA is effective in solving problems associ-

ated with different numbers of variables (e.g.,

species), multicollinearity and small sample

sizes (Graham, 2003; Jankowski et al., 2009).

Therefore, we used a PCA ordination, based

on a correlation matrix of species abundances

against sites. The most important components

of this ordination were then chosen via the

broken-stick method (Jackson, 1993). Sites and

species were projected onto a two-dimensional

space defined by the chosen components (i.e.,

biplot), sites closer to each other within the

two-dimensional space are considered more

similar (Jankowski et al., 2009; Palacio et

al., 2020); this graphical visualization of the

biological data allows us to make a global

description of the variation in the community

data (i.e., species and sites).

We used the loadings of PCA to interpret

the model (correlation coefficient between the

species abundance and the principal component

scores), which utilizes the relative contribution

of each variable to each component (Palacio

et al., 2020). To define the raptor community

as a species set, we considered only loadings

with values ≥ 0.25 as a conservative threshold

(i.e., 75 % of the data is retained) to summarise

each component.

In order to identify the species that inte-

grate each raptor community, we explored an

additional graphical option. We created scat-

terplot with PCI and PCII scores for each site

versus the abundance of each species per site

to visualise the importance of species com-

prising each community component (i.e., PCI

and PCII). Species within each community

were identified via establishing cut-off points;

these points are limits of a given graph section

where changes in the abundance of species can

be easily identified (i.e., through an increase

or decrease in the abundance of species, and/

or the appearance or disappearance of other

species) (Ballance et al., 1997; Huettmann &

Diamond, 2001). In other words, the scatterplot

allows us to visualise a dramatic or evident

change in abundance of species associated with

PCI and PCII.

RESULTS

In total, 149 individuals were recorded

associated with seven species and three fami-

lies (Table 1). The most abundant species was

P. carunculatus (51.7 % of records), followed

by Geranoaetus polyosoma (Variable Hawk)

(27.5 % of records) and Cathartes aura (Tur-

key Vulture) (12.7 % of records). The least

abundant was V. gryphus (Andean Condor) (4

% of records), F. femoralis (Aplomado Falcon)

(2 % of records), Circus Cinereus (Cinereous

Harrier) (1.7 % of records) and F. peregrinus

(Peregrine Falcon) (< 1 % of records).

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: 51382, enero-diciembre 2023 (Publicado May. 04, 2023)

Community structure: The first three

components of our PCA explain 91 % of the

total variance in the occurrence of seven raptor

species in eight transects in the páramo grass-

land ecosystem (Table 2). However, through

the broken-stick method, only the first two

components were retained (74 %). The first

component (PCI = 47.4 %) reflects a gradient

of change from lower abundance to increased

abundance of P. carunculatus, G. polyosoma,

V. gryphus and C. aura; while the second com-

ponent (PCII = 27 %) reflects a gradient of

change from lower to higher abundance of C.

cinereus (Cinereous Harrier), F. peregrinus and

F. femoralis (Table 2).

The community ordination (2D solution)

showed that PCI is represented by transects

composed of more abundant or common spe-

cies (e.g., P. carunculatus and G. polyosoma)

and are located towards the right side of the

biplot (Fig. 2). The PCII axis is represented by

transects that are composed of the less abun-

dant or rare species (e.g., C. cinereus and F.

peregrinus) and are located towards the upper

side of the biplot (Fig. 2).

By visually identification of the species

composing the raptor community (Fig. 3), cut-

off points were determined for each component.

In the community represented by the PCI, the

abundance of more common species increases

at PCA-derived scores greater than 2.86 (Fig.

3A); while in the community represented by the

PCII, the abundance of rare species increases at

scores greater than 2 (Fig. 3B); these changes

show a gradient of variation in the abundance

of the raptor community.

DISCUSSION

The patterns of raptor diversity observed

during the surveys are consistent with the gen-

eral patterns reported for the páramos in the

TABLE 1

List of raptor species and their total abundances recorded at eight transects in the páramo grassland ecosystem, high Andes

of Southern Ecuador from October 2021 to September 2022.

Order Family Common name Species Code Abundance

Cathartiformes Cathartidae Turkey Vulture Cathartes aura CAAU 19 (mean = 2.38; ± SD = 1.60)

Andean Condor Vultur gryphus VUGR 6 (mean = 0.75; ± SD = 1.16)

Accipitriformes Accipitridae Variable Hawk Geranoaetus polyosoma GEPO 41 (mean = 5.13; ± SD = 4.22)

Cinereous Harrier Circus Cinereus CICI 2 (mean = 0.25; ± SD = 0.46)

Falconiformes Falconidae Aplomado Falcon Falco femoralis FAFE 3 (mean = 0.38; ± SD = 0.74)

Peregrine Falcon Falco peregrinus FAPE 1 (mean = 0.13; ± SD = 0.35)

Carunculated Caracara Phalcoboenus carunculatus PHCA 77 (mean = 9.63; ± SD = 9.29)

TABLE 2

Loadings of the first three components of the principal component analysis (PCA) for seven raptor species recorded at eight

transects in the páramo grassland ecosystem, high Andes of Southern Ecuador

Species PCI (47.4 %) PCII (27 %) PCIII (16 %)

Turkey Vulture (Cathartes aura)0.421 0.253

Andean Condor (Vultur gryphus)0.438 -0.413

Variable Hawk (Geranoaetus polyosoma)0.448 -0.267

Cinereous Harrier (Circus cinereus)0.683

Aplomado Falcon (Falco femoralis)0.339 -0.736

Peregrine Falcon (Falco peregrinus)0.326 0.491 0.343

Carunculated Caracara (Phalcoboenus carunculatus)0.531

The first two PCA components were chosen to determine community structure, no loadings < 0.25 are shown (see methods).

6Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e51382, enero-diciembre 2023 (Publicado May. 04, 2023)

Southern Andes of Ecuador (e.g., Astudillo et

al., 2015). Our analysis of the occurrence of

seven raptor species in eight transects in the

páramo grassland ecosystem of the Macizo del

Cajas biosphere reserve revealed two distinct

raptor communities. Differences in these two

communities as revealed by a PCA are related

to species abundance. One community is char-

acterized by a higher abundance of generalist

as well as regionally common or uncommon

species. However, when the abundance of these

common species decreases, the raptor com-

munity is characterised by an increase in the

abundance of specialist and rare species at the

local scale. Competition among species for the

limited resources in this ecosystem is probably

a potential factor that may explain the varia-

tions in the raptor community.

The first community is comprised of spe-

cies that are more typical of the páramo land-

scape, particular across the study area. Species

associations including G. polyosoma and P.

carunculatus are expected, as these raptors are

common and widely distributed in páramo eco-

system (Astudillo et al., 2015; Freile & Restall,

2018). However, our results also show that the

common species that integrate the community

may also be associated with species such as

V. gryphus and C. aura. The former species is

reported as rare in the páramos due to its low

population densities (Freile & Restall, 2018;

Naveda-Rodríguez et al., 2016), while the lat-

ter is generally rare in the páramo (Astudillo et

al., 2015; Olmedo, 2019). On the other hand, V.

gryphus and C. aura are both scavengers and

their occurrence has been previously linked to

Fig. 2. Ordination biplot of the raptor community recorded in eight transects (green circles) in the páramo grassland

ecosystem, high Andes of Southern Ecuador. The ordination shows the first two components of the principal component

analysis (PCA). The arrows describe the loadings of the species that integrate the raptor community. Blue lines represent

the vectors associated with species whose greatest contribution is to the first component of the PCA (PCI) and those in red

for the second component of the PCA (PCII). For species codes refer to Table 1.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: 51382, enero-diciembre 2023 (Publicado May. 04, 2023)

the presence of more common species, such as

P. carunculatus (Astudillo et al., 2011; Stuc-

chi & Figueroa, 2010). Peisley et al., (2017)

and Sekercioglu, (2006) mention that raptors

indirectly lead other species to prey or food

sources. In this context, in our study area, espe-

cially when G. polyosoma and P. carunculatus

were sighted together, the presence of V. gry-

phus tended to be more frequent. Our findings

demonstrate that a community dominated by

common species may also be integrated by less

common species important for conservation

(e.g., V. gryphus) and is therefore a characteris-

tic community of the regional páramo.

A second community consists of locally

rare species such as C. cinereus, F. femoralis

and F. peregrinus. These species forage rela-

tively close to páramo ground level, flying at

medium altitude and with a more localized

distribution (Freile & Restall, 2018; Ridgely &

Greenfield, 2001). Within this context, we con-

sider that competition between species of the

first community against. species of the second

community could play a fundamental role in

determining the structure of this second raptor

community (Ballejo et al., 2018; Donázar et

al., 2016; Han et al., 2021), where competitive

exclusion of certain species may occur when

they share a similar role (Sergio & Hiraldo,

2008; Vrezec & Tome, 2004). For example, C.

cinereus was observed more frequently when

P. carunculatus decreased in abundance at

transects, perhaps because both species have

similar ground-level foraging habits (Fjeld-

så & Krabbe, 1990; Freile & Restall, 2018;

Ridgely & Greenfield, 2001). However, more

Fig. 3. Scatterplot of abundance by species and their relationship to scores derived from principal component analysis (PCA)

for the raptor community surveyed at eight transects in the páramo grassland ecosystem, high Andes of Southern Ecuador.

A. corresponds to the community described within the first component of the PCA (PCI) and B. is the second community

described within the second component of the PCA (PCII). Grey arrows show cut-off points: > 2.86 for PCI and > 2 for

PCII (see methods). For species codes refer to Table 1.

8Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e51382, enero-diciembre 2023 (Publicado May. 04, 2023)

studies are required to clarify this relationship.

For example, phylogenetic diversity could be

employed to understand whether competition

is an important factor in species assemblages

(e.g., Han et al., 2021).

Our method of characterizing raptor com-

munities through intensive walking transects

surveys and principal component analysis

proved to be valid for describing and helping

to understand páramo raptor community struc-

ture. The determination of cut-off points in the

analysis is appropriate to interpret and identify

changes in the raptor community. Huettmann &

Diamond, (2001), for example, mention that this

approach can be used when species abundances

are very low. Therefore, this approach is espe-

cially relevant in habitats where raptors have

been little studied due to their low densities and

wide distribution ranges such as high Andean

ecosystems. In addition, we have shown that

this approach represents a more comprehensive

monitoring protocol that encompasses the over-

all community assemblage rather than the more

common species-by-species assessment, which

fails to take into account possible interactions

between species. Furthermore, the approxima-

tion of principal components and their cut-off

points (based on PCA scores and the relation-

ship with their abundances) can be seen as an

alternative for understanding the importance

of species even when records are scarce. The

páramo regional application of the methods

described in this study could help to determine

species associations, its turnover and overlap

at a landscape scale. It can also be used as a

tool for recognising conservation priorities for

threatened species.

Ethical statement: the authors declare

that they all agree with this publication and

made significant contributions; that there is

no conflict of interest of any kind; and that we

followed all pertinent ethical and legal proce-

dures and requirements. All financial sources

are fully and clearly stated in the acknowled-

gements section. A signed document has been

filed in the journal archives.

ACKNOWLEDGMENTS

We thank the constant support to our

research activities of Jacinto Guillén, Raffaella

Ansaloni, and Andrés López, from Universidad

del Azuay. We thank Eduardo Barnuevo and

Bruno Timbe for their field assistance. We

also acknowledge Vicente Jaramillo, Soledad

Avendaño, Fernando Carrión and Scott Camp-

bell from Dundee Precious Metals, Ecuador

(DPMECUADOR S.A.) as well as Mark Thorpe

and Jorge Barreno for their continued support

to our research. The logistical support came

from Hari González and park manager staff of

Quimsacocha National Recreation Area, as well

as to Empresa Pública de Telecomunicaciones,

Agua Potable, Alcantarillado y Saneamiento de

Cuenca (ETAPA-EP). This study was funded

by Vicerrectorado de Investigaciones, Uni-

versidad del Azuay (under grant 2017-0131;

2018-003; 2022-0054), DPMECUADOR S.A.,

ETAPA-EP (under grant 78010200001) and

the Avian Conservation Endowment of the

National Aviary (USA).

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